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Issues Concerning Survival of Viruses on Surfaces

Issues Concerning Survival of Viruses on Surfaces Food Environ Virol (2010) 2:24–34 DOI 10.1007/s12560-010-9025-6 REVIEW PAPER • • • P. Vasickova I. Pavlik M. Verani A. Carducci Received: 24 November 2009 / Accepted: 17 January 2010 / Published online: 4 February 2010 Springer Science+Business Media, LLC 2010 Abstract Viruses are the causative agents of an estimated were not related to microbial contamination of surfaces, the 60% of human infections worldwide. The most common Centre for Disease Control (CDC) and the American Hos- viral illnesses are produced by enteric and respiratory pital Association focussed only on patient diagnosis up to viruses. Transmission of these viruses from an infected 1987. Over the years studies have changed perspectives on person or animal to a new host can occur via several routes. viral transmission and have integrated a more complex Existing studies strongly suggest that contaminated fomites multifactorial model of disease spreading including the or surfaces play an important role in the spreading of viral contaminated environment (Boone and Gerba 2007). diseases. The potential of viral spreading via contaminated Viral transmission from an infected person or an animal surfaces depends particularly on the ability of the virus to to a new host can occur by direct or indirect routes. During maintain infectivity whilst it is in the environment. This is indirect transmission, contaminated surfaces can play an affected by a combination of biological, physical and important role. This kind of transmission is dependent on chemical factors. This review summarises current knowl- several factors, which include the quantity of viral particles edge about the influence of environmental factors on the excreted by an infected organism, their stability in the survival and spread of viruses via contaminated surfaces. environment, the potential to spread within a closed envi- ronment, as well as interaction of the virus and the host Keywords Pathogenic viruses  Environmental factors  organism. Large numbers of viral particles can be shed via Surveillance  Biofilms various body fluids including blood, faeces, vomit, saliva, urine, and respiratory secretions from infected individuals or carriers. The more viruses are shed, the greater their Introduction chance is to survive and reach a new host organism (Rzezutka and Cook 2004). A critical factor of viral transmission is its ability to Viruses are causative agents of an estimated 60% of human infections worldwide (Barker et al. 2001). For centuries it survive in the environment. Previous studies have shown was assumed that these viral diseases were spread primarily that viral particles can persist for extended periods on through direct patient contact or by the airborne route, and surfaces such as medical devices, fomites or human skin surrounding environment played little or no role in disease (Abad et al. 2001; Sattar et al. 1986, 1987; Todd et al. transmissions. Due to the opinion that nosocomial infections 2009). Even if some viruses survive relatively poorly in the environment, the low infective dose suggests that these viruses are able to persist in sufficient numbers to act as a P. Vasickova (&)  I. Pavlik source of infection for several days, week or in some cases Veterinary Research Institute, Hudcova 70, 621 00 Brno, Czech Republic months (Barker et al. 2001; Boone and Gerba 2007). e-mail: vasickova@vri.cz Surfaces can be contaminated directly by their contact with body secretions and fluids or indirectly through virus M. Verani  A. Carducci contaminated aerosol or other contaminated fomites. Once a Department of Biology, University of Pisa, Via S. Zeno, surface is contaminated, the transfer of infectious viral 35-56127 Pisa, Italy 123 Food Environ Virol (2010) 2:24–34 25 particles may easily occur between inanimate or animated Coxsackievirus), hepatitis A virus (HAV) and hepatitis objects, or vice versa, e.g. hands and work surfaces with the E virus (HEV). Infection by enteroviruses is often potential of subsequent transfer to food or direct hand- subclinical but they may induce signs and symptoms of to-mouth transfer (Goldmann 2000; Marks et al. 2000; disease in not related with intestinal tissue. The infections caused by hepatitis viruses affect liver Rzezutka and Cook 2004). Rapid spread of viral infections through contaminated surfaces is common particularly in tissue (Carter 2005). crowded indoor establishments such as schools, day-care Recent epidemiological studies have shown that noro- facilities, nursing homes, business offices, hospitals or virus is one of the most frequent cause of acute non-bac- transport systems (Barker et al. 2001). The influences of terial gastroenteritis. Additionally, it is responsible for environmental factors on the stability and spread of bacte- almost all foodborne outbreaks, where viruses are identi- rial infections are well documented, especially in hospitals. fied (Goodgame 2006; Koopmans and Duizer 2004). A The comparable knowledge concerning the role of surfaces study by Barker et al. (2004) demonstrated that noroviruses or fomites in viral transmission is still lacking and further could be transferred from contaminated surfaces to clean investigation is needed (Boone and Gerba 2007; von Rhe- hands. It was also found that norovirus-contaminated hands inbaben et al. 2000). could cross-contaminate a series of seven types of clean The objective of this review is to summarise current surfaces. Wu et al. (2005) tested ten environmental samples knowledge about influences of environmental factors on taken during the norovirus outbreak at a long-term-care survival and spread of viruses via contaminated surfaces. facility. Positive swabs were obtained from toilet seats used by case-residents, bed rails from case-residents’ bed, a dining room tabletop and an elevator button. Viruses Spread Via Contaminated Fomites Worldwide, rotavirus is probably the most important pathogen causing diarrhoeal disease in infants. Rotaviruses Nearly one thousand different types of viruses are known to are shed in large numbers from infected person with faeces infect humans, whilst the most common viral illnesses are 8 11 often containing 10 –10 virions per gram (Bajolet and produced by enteric and respiratory viruses (Barker et al. Chippaux-Hyppolite 1998; Leung et al. 2005). It has been 2001). In developed countries, viruses are responsible demonstrated that infective viral particles can survive on approximately for 30–40% of infectious gastroenteritis human hands and be transferred to animate and non-porous cases. Estimates indicate that adults have two to five colds surfaces (Ansari et al. 1988; Sattar et al. 1986). Ward et al. per year and infants or preschool children four to eight colds (1991) examined the transmission of rotavirus from a per year. Existing studies prove that contaminated fomites contaminated surface to the mouth and from surface to play an important role in the spreading of these diseases hands and mouth. All the volunteers who licked rotavirus- (Barker et al. 2004; Winther et al. 2006; Wu et al. 2005). contaminated plates became infected. Whereas, only about half of individuals touching the virus contaminated plates Viral Gastroenteritis and Hepatitis with their fingers and then their mouth became infected. Infections caused by HAV are endemic throughout the Viruses that infect a host organism via the gastrointestinal world. Transfer of infectious viral particles from contam- tract are excreted in faeces and may be also present in vomit inated to clean surfaces was also reported. The persistence (Seymour and Appleton 2001). Normally they are shed in of HAV on surfaces and the ability of the virus to be high numbers and exhibit great particle stability outside the interchanged from animate and inanimate environments organism and on passage through the stomach. There are confirm that surfaces present important epidemiological two types of viruses infecting gastrointestinal tract: factors in the indirect transmission of HAV (Croci et al. 2002; Bidawid et al. 2000; Mbithi et al. 1992). Mbithi et al. 1. Capable of primarily multiplying in the intestine. These agents cause gastroenteritis, and include members of (1992) presented that considerable amounts of HAV genus: Rotavirus, Norovirus, Astrovirus and Adenovi- remained infectious on finger pads after 4 h, even though rus. Viral gastroenteritis is usually relatively mild 68% of viruses lost their infectivity during the first hour. disease, which has a short incubation period (1–4 days) Astroviruses or adenoviruses exhibited shorter survival depending on the virus species. Specific symptoms are time than rotaviruses and HAV. Despite this, they were diarrhoea and vomiting. Most infected people do not able to survive on inert surfaces long enough to suggest consult a medical practitioner. Therefore, the majority that contaminated surfaces may have a relevant role in the of cases is not reported and subsequently investigated. secondary transmission of these viruses (Abad et al. 2001). 2. Capable of multiplying elsewhere in the body. These Information about the survival of HEV in environment is viruses include enteroviruses (e.g. poliovirus or still lacking. 123 26 Food Environ Virol (2010) 2:24–34 Respiratory Infections particles could be transferred from hands and fingers to surfaces and back again (Brady et al. 1990; Gwaltney and Respiratory viral infections are a major health burden Hendley 1982; Hendley et al. 1973; Winther et al. 2007). (Winther et al. 2006). Although these diseases are often regarded as trivial, hospital admission and mortality rates in infant or elderly are considerable. For instance, respi- Factors Affecting Virus Survival on Surfaces ratory viruses cause more than 400,000 hospitalizations per year in children less than 18 years of age in the United The potential of viral spreading via contaminated surfaces States (Henrickson et al. 2004). Viral agents that primarily depends particularly on the ability of the viruses to maintain infect the upper or lower respiratory tract include influenza infectivity whilst they are in the environment (Boone and and parainfluenza viruses, adenoviruses, respiratory syn- Gerba 2007). Their survival in the environment is affected by cytial virus (RSV), coronaviruses, human metapneumovi- a combination of biological, physical and chemical factors rus, rhinoviruses and enteroviruses (Kesson 2007). (Fig. 1). To date, complete information regarding the influ- It is generally accepted that respiratory viruses are ence of the environment on all viruses and their stability in spread from person to person by aerosol transmission due external conditions does not exist. Most studies have used to sneezing or coughing (Goldmann 2000). Additionally, only few target viruses or their surrogates. Since experi- there is evidence to suggest that a significant proportion of mental condition and methods vary, it is difficult to draw flu viruses and other respiratory viruses are spread via conclusions from these studies (Carter 2005). contaminated hands and fomites (Hall et al. 1980; Tiwari Once the surface is contaminated, it can be source of et al. 2006; Winther et al. 2007). contamination for other animate or inanimate objects, e.g. RSV was recovered from counters for up to 6 h, from contaminated door handles and hands were found to be an rubber gloves for up to 1.5 h, from clothing gowns and efficient vector of viruses. At least 14 persons could be paper tissue for 30–45 min, and from skin for up to 20 min. contaminated or infected by touching a polluted door Additional experiments demonstrated that infectious RSV handle. Successive transmission of virus from one person could be transferred to hands by touching these contami- to another could be followed up to the sixth contact person nated surfaces and could be further recovered from these (von Rheinbaben et al. 2000). It was also found that con- hands for up to 25 min (Hall et al. 1980). A study done by taminated fingers could subsequently transfer a virus from Winther et al. (2007) was designed to assess rhinovirus up to seven clean surfaces (Barker et al. 2004). contamination of surfaces and rhinovirus transfer from these surfaces to fingertips during normal daily activities of Virus Characterisation and Classification adults. Common virus-positive sites were door handles, pens, light switches, TV remote controls, faucets and The most important aspects affecting virus survival are telephones. Rhinovirus was transferred from surfaces to biological factors like the presence of the envelope and fingertips in 60% trials 1 h after contamination and in 33% virus type. These basic characteristics influence and help to after 18 h after contamination. predict virus survival in the environment and behaviour in Influenza viruses, and parainfluenza viruses are also able a host organism. to survive on hands long enough to permit self-inoculation. Persistence of a virus in the environment is primarily It has been demonstrated that these infectious viral affected by the presence of a viral envelope. The non- Fig. 1 Factors affecting virus survival on surfaces 123 Food Environ Virol (2010) 2:24–34 27 enveloped viruses have higher resistance to drying or des- was kept either low or high than when RH has medium iccation methods and therefore are spread more easily than range. Sattar et al. (1986) reported that human rotavirus enveloped viruses (which are less stable in the environment). survived for a shorter period of time at high RH. Abad et al. The non-enveloped enteric viruses like HAV, rotavirus or (1994) also observed that human rotavirus and poliovirus astrovirus are able to remain infective on surfaces for at least exhibited greater persistence at high RH on non-porous 2 months. In contrast, enveloped respiratory viruses usually material. The survival of adenovirus was not affected by remain infectious for several hours to several days (Duizer RH. At 5C RH had a little effect on survival time of et al. 2004). Reovirus, non-enveloped virus, when dried in an norovirus, but its survival was longest at 20C and low RH. organic matrix can survive for a period of 30 days, whereas Sattar et al. (1987) investigated rhinovirus on surfaces. the enveloped Sindibis virus dies rapidly (Howie et al. 2008). Humidity was used as a variable factor. The study found Variation in virus survival occurs within a viral family that rhinovirus exhibits optimum survival at 50% RH. or even genus. Feline calicivirus (FCV) and norovirus belong to the same family. Their physicochemical prop- Temperature erties and genome organisation are similar. Therefore, FCV is used as a surrogate model, e.g. to determine the efficacy However the degree of virus survival on surfaces is affected of disinfectants against norovirus on fresh produce or by temperature, it depends also on the virus type and RH. surfaces (Gulati et al. 2001). Duizer et al. (2004) reported Viral particles are able to persist from days to months over a that norovirus is profoundly more resistant to low and high range of temperatures in the environment, and being pre- pH than FCV and canine calicivirus, which are members of served by refrigeration or freezing (Cliver 2009). the same family. Hewitt and Greening (2004) mentioned Temperature is one of the most important of determining that in comparison to norovirus, FCV is more sensitive to norovirus survival in the environment. Recent studies indi- environmental factors in general. Examples of survival cate that noroviruses can survive for a prolonged period of variation within the genus are coronaviruses OC43 and time at a low temperature and can be transmitted to a sus- 229E. After drying, coronavirus 229E infectivity was ceptible population via different environmental media detectable after 3 h on various surfaces (aluminium, sterile including surfaces (Mattison et al. 2007). Doultree et al. latex surgical gloves and sterile sponges), whilst corona- (1999) found that FCV dried onto glass and stored at 4C virus OC43 survived 1 h or less (Sizun et al. 2000). displays a 4.75 log reduction over 56 days. FCV survival was lower at room temperature, but still prolonged. The number Relative Humidity of infectious FCV declined to undetectable levels by 21– 28 days. FCV was not detected at 37C after 1 day. Com- Effect of relative humidity (RH) varies within virus type. It parative analyses indicated that FCV survival was greater at is believed that the survival of enveloped viruses on 4C than at room temperature. Therefore, outbreaks caused inanimate surfaces is better when RH levels are below by noroviruses are much more prevalent in the winter than in 50%. On the other hand, RH levels higher than 80% are the summertime (Doultree et al. 1999; Mattison et al. 2007). considered to be more beneficial to the survival of non- Rotavirus particles are able to survive storage in ambient enveloped viruses. In general, viruses with higher lipid tropical temperatures for more than 2 months (Fischer et al. content tend to be more persistent at a lower RH, whilst 2002). Moe and Shirley (1982) reported that rotavirus viruses with lesser or no lipid content are more stable at a infectivity decreases more rapidly under all RH at 37C higher RH (Assar and Block 2000; Moce-Llivina et al. than at 4 or 20C. According to a study done by Sattar et al. 2006). However, there are exceptions. (1986), rotaviruses can persist longer at a lower tempera- Studies have shown that HAV is able to survive better at ture (4C) and RH (25–50%), with approximately 10% low levels of RH, which is in contrast to the behaviour of infectious virus remaining after 10 days, in comparison to other enteroviruses (Mbithi et al. 1991; Stine et al. 2005). less than 1% after 2 days at 22C and 85% RH. Abad et al. When its persistence in high and medium RH (85.7–90.3% (2001) investigated the survival of an astrovirus at 4 and and 45.1–48.4%) was compared, HAV survived longer on 20C with a high RH (90 ± 5%). At 4C, the virus was lettuce in dry conditions. Based on the calculated inacti- able to persist for 60 days desiccated on non-porous vation rates, a 99.9% reduction in HAV could take material and for 90 days on porous material. Faster decay 822 days in pre-harvest conditions of contaminated vege- was observed at 20C. Short-term survival of astrovirus tables (Stine et al. 2005). In contrast, Abad et al. (1994) was compared to that observed for other enteric viruses found that survival of HAV was enhanced at high RH. significant for health, such as rotavirus, adenovirus, Data regarding rotavirus survival was determined to be poliovirus and HAV. Overall, astrovirus persisted better contradictory. Moe and Shirley (1982) showed that a field than poliovirus and adenovirus, although they exhibited a strain of human rotavirus could survive longer when RH shorter survival than the rotavirus and HAV. 123 28 Food Environ Virol (2010) 2:24–34 Amongst other factors, the effect of freezing on enteric depends especially on fragment size of viral nucleic acid. viruses in berries and herbs was tested by Butot et al. Nevertheless, it also shows that the viral capsid structure (2008). This study revealed that freezing does not signifi- has an important protective role against UV radiation cantly reduce the viability of norovirus, HAV and rotavi- (Simonet and Gantzer 2006). rus. Only infectivity of FCV on strawberries can be decreased. Freezing for 3 months had a limited effect on Type of Surface HAV and rotavirus in all tested food products. A higher decay rate was observed in frozen raspberries and straw- Several studies have compared the survival of different berries contaminated with FCV due to the acidic pH (Butot types of viruses on porous and non-porous surfaces. The et al. 2008). No reduction of MNV-1 PFUs was observed majority of viruses remain viable for a longer period of on frozen onions or spinach during storage for 6 months time on non-porous materials, although there are excep- (Baert et al. 2008). Kurdziel et al. (2001) reported a tions (Abad et al. 1994; Boone and Gerba 2007; Lam- reduction of \2 log units of poliovirus on frozen straw- houjeb et al. 2009; Tiwari et al. 2006); e.g. higher berries after 15 days of storage. So far, no data about persistence of poliovirus and adenovirus was observed on survival of other viruses during freezing are available. porous materials (paper and cotton cloth) compared to non- porous materials: aluminium, china, glazed tile, latex, and Sunlight and UV polystyrene (Abad et al. 1994). The enteric viruses reveal exhibited inactivation rates (at least 2 logs lower) than Ultraviolet radiation is the crucial virucidal agent, which respiratory viruses, with the exception of adenovirus and primary targets viral nucleic acid but also modifies capsid influenza virus (Boone and Gerba 2007). Tiwari et al. proteins. Virus resistance to UV exposure also appears to (2006) studied survival of avian metapneumovirus and vary according to virus type. Viruses with single-stranded avian influenza virus on 12 different porous and non-por- nucleic acid (ssDNA and ssRNA) are more susceptible to ous materials. Both viruses persisted longer (up to 6 days) UV inactivation than viruses with double-stranded nucleic on non-porous surfaces than on porous ones. acid: dsDNA and dsRNA (Gerba et al. 2002; Hijnen et al. Survival times for enteric viruses have been determined 2006; Tseng and Li 2007). on a range of different fruit and vegetable commodities According to Hijnen et al. (2006), adenoviruses are (Seymour and Appleton 2001). Mattison et al. (2007) sug- classified as the most resistant virus type to UV. The gested that smooth surfaces, such a lettuce leaf, might pro- obtained k-values, which characterise UV-sensitivity of the vide less protection to the virus than coarse surfaces like ham microorganism, are similar for FCV, rotavirus, poliovirus has. Results of other studies indicated that on plant surfaces, and Coxsackievirus. HAV is more sensitive then the above- viruses are exposed to potentially toxic compounds, such as mentioned viruses. The correlation between low and high phenols, ethanol, and acetaldehyde, which could accelerate solar virucidal radiation and high and low influenza prev- the inactivation process (Lamhoujeb et al. 2009). alence suggest that inactivation of viruses in the environ- Some specific chemical surfaces (e.g. heavy metals) are ment by solar UV radiation has a stronger effect than virucidal. Influenza virus particles (2 9 10 ) were inocu- expected and can play a role in seasonal occurrence, e.g. lated onto cooper and stainless steel surfaces in a study by influenza pandemics (Sagripanti and Lytle 2007). Noyce et al. (2007). After incubation for 24 h on stainless Duizer et al. (2004) exposed surrogate caliciviruses steel, 500,000 virus particles were still infectious in com- (enteric canine calicivirus and respiratory FCV) to UV-B parison with cooper, where only 500 viral particles were radiation as a factor affecting environmental survival. active after incubation for 6 h. Other recent studies also Results were comparable to enteroviruses (Gerba et al. suggest the antimicrobial properties of cooper-based sur- 2002), less effective than for vegetative bacteria, but more faces (Barker et al. 2004; Faundez et al. 2004; Iriarte et al. effective than for phage MS2 (Husman et al. 2004), ade- 2007; Noyce et al. 2006, 2007). It has been reported that noviruses (Gerba et al. 2002; Nwachuku et al. 2005), and aluminium also has virucidal activity. Adenovirus, polio- Baccilus subtilis spores (Chang et al. 1985). Parallel virus and the B40-8 phage persist for a shorter time on analysis of four RNA virus models (poliovirus 1, phage aluminium than on other non-porous material (Abad et al. MS2, phage GA and phage Qb) showed that the least 1994; Thurman and Gerba 1988). resistant virus to UV radiation was poliovirus 1. Qb phage had intermediate sensitivity, whilst MS2 and GA phages Adsorption State and Organic Matter were the most resistant. The rate of RNA degradation increased linearly with increasing fragment size, except The extent and state of virus adsorption on surfaces has an viruses with a similar size of genome (poliovirus 1 and important influence on virus survival. Studies have shown MS2). Based on these results, viral resistance to UV that the survival of viruses is increased with increased 123 Food Environ Virol (2010) 2:24–34 29 adsorption to the surfaces and that immobilized (adsorbed) The viral adsorption to the surfaces can be influenced by viral particles most often keep their infectious potential ionic strengths; therefore, salts are commonly used to after desorption. Interactions that take place between favour the attachment of viruses to different types of sur- viruses and surfaces are determined by their characteristics faces. Theoretically, adsorption of viral particles is better in and involve electrostatic, hydrophobic interactions, and/or high ionic strength. Enteric viruses are destabilized and 2? ionic strength (Hurst et al. 1980; Lacroix-Gueu et al. 2005). inactivated by water lacking salt ions, e.g. Mg . On the Vega et al. (2008) compared the relative contributions of contrary, increased concentrations of salts (e.g. NaCl) are these interactions with the nonspecific attachment of antiviral for many viruses. echovirus 11, FCV, MS2, and uX174 to butterhead lettuce. The results imply that electrostatic forces play a major role in controlling virus adsorption to lettuce. Interaction of Pathogenic Viruses with Other Many viruses can be stabilized and protected by dis- Microorganisms During their Presence on Surfaces solved, colloidal and solid organic matter; including faecal and humic material. Organic matter has a low isoelectric Data about the influence of other microorganisms on virus point, and thus carries a negative surface charge at most survival are contradictory. Virus survival may increase or naturally occurring pH levels (Boone and Gerba 2007). decrease with the number of microbes present on the sur- Kiseleva (1971) reported that strains of poliomyelitis virus, face. Bacteria or microscopic fungi are able to attack and echovirus and coxsackievirus remained infectious from two inactivate infectious viral particles. Some bacteria can to more than 12 days on the surface of substances used in produce low molecular weight substances that apparently various household objects. The greater survival was inactivate viruses. Others appear to use viral capsid proteins observed, if the inoculum also contained coliform bacteria, as substrates (Deng and Cliver 1995a, b; Cliver 2009; proteins, fats and dust particles, but no precise results or Herrmann et al. 1974). By contrast increasing amount of experimental details were given (Kiseleva 1971 as quoted by microbes can protect viruses from desiccation and disin- Rzezutka and Cook 2004). Lee et al. (2008) found that fection. Interactions of pathogenic viruses with bacterial murine norovirus is more stable in a stool suspension than on biofilms have been reported (Lacroix-Gueu et al. 2005; different types of surfaces. After 30 days of incubation at Skraber et al. 2005). As biofilms can form on a wide spectra 18C, there was a 2.7-log reduction in the stool suspension, of surfaces (Davey and O’toole 2000), their influence on compared to the maximum reduction of 5.3-log on a gauze virus survival is also discussed in this review. or diaper surface. A study by Abad et al. (1994) showed that on non-porous surfaces, poliovirus and adenovirus persist Negative Influence of Other Microorganisms better in the presence of faeces. However, on porous fomites on Virus Survival the presence of faecal material has a negative influence on the survival of these viruses. HAV and human rotavirus One proposed mechanism of viral loss in the environment is persistence is not affected by the presence of faeces. inactivation by the direct or indirect action of microorgan- isms. Environmental isolates of bacteria with antiviral pH and Presence of Salts ability have been found on several occasions. These microbes are able to produce metabolites, which adversely In general, pH has a minimal effect on virus survival in an affect viral particles, or can use the viral capsid as a nutrient indoor environment. Hurst et al. (1980) measured the source (Deng and Cliver 1995a, b; Ward 1982). The inac- effects of several environmental conditions on virus per- tivation of viruses by bacterial cultures is temperature sistence in soil. They found that the temperature and virus dependent. The lower the temperature of the mixed waste, adsorption to soil is more important for virus survival than the longer the virus is able to persist. Moreover temperature the effect of pH. Enteric viruses are able to survive severe could strongly influence microbial activity, and thus influ- conditions in the gastrointestinal tract, such as low pH in ence viral persistence (Deng and Cliver 1992). stomach or high bile concentration. They are generally most Ward (1982) investigated the influence of mixed-liquor stable near pH 7, but prefer low pH’s (3–5) rather than suspended solids (MLSS) of inactivated sludge on a alkaline pH’s (9–12). It was shown that noroviruses are able poliovirus 1 survival. The first experiment was conducted to persist at pH 2.7 and room temperature more than 3 h in order to determine the effect of MLSS on the recovery of (Duizer et al. 2004). As the surface charge of viral particles poliovirus after a different period of time. The second varies depending on the pH, disruption of electrostatic experiment was designed to find out the role of different interactions between viral particles and environmental MLSS components in virus loss. Results of these studies surfaces commonly consists of changing the pH, and thus indicate that MLSS contain a component(s) which can affect viral persistence in the environment (Gerba 1984). inactivate poliovirus 1. These components were pelleted 123 30 Food Environ Virol (2010) 2:24–34 during centrifugation, destroyed by autoclaving, and during biofilms erosion or sloughing, protected immobilised removed by filtration. Consecutively, residual activity of an viral particles may be released in the environment, and then MLSS supernatant fraction was also studied to confirm the contact their target host commencing the viral infectious absence of antiviral activity in non-living heat-sensitive cycle (Briandet et al. 2008; Helmi et al. 2008; Lacroix-Gueu material in the MLSS. Subsequent increasing activity of et al. 2005; Lehtola et al. 2007; Quignon et al. 1997). Viral this supernatant, coupled with the previous results, strongly attachment rates to biofilms vary greatly and may depend on indicates the antiviral activity of some microbial species. many factors such as the biofilm or viral characteristics Deng and Cliver (1992) demonstrated the antiviral effect of (size, shape, isoelectric point), and concentration of viral several bacterial cultures from swine manure slurry and particles (Helmi et al. 2008). mixed septic tank effluent. These cultures were identified Helmi et al. (2008) reported that poliovirus 1 adsorption as Micrococcus luteus, Staphylococcus epidermidis, was higher in wastewater biofilm than in drinking water Bacillus sp. and Streptococcus sanguis group. A compari- biofilm. Infectious viral particles were detected in the son of poliovirus 1 inactivation in raw mixed waste, drinking water biofilm for up to 6 days after inoculation, autoclaved mixed waste, and bacterium-free filtrate of raw whilst the viral genome was still detectable at day 34. Hock mixed waste demonstrated that virus inactivation is related, and Botzenhart (2002, 2003) injected phages MS2, uX174 at least in part, to microbial activity in similar environ- and poliovirus 1 at comparable concentrations into a lab- mental conditions. Inhibition of poliovirus 1 inactivation oratory reactor containing approximately 100 ml of by protease inhibitors suggested that antiviral activity of drinking water. After the contact time of 1 h, concentra- mixed waste was partially due to proteolytic enzymes tions of 0.04, 0.13 and 0.27% were recovered from the produced by bacteria in wastes. biofilm. MS2 showed less adsorption to the biofilm than Bacteria may also produce substances that inactivate uX174 and poliovirus 1 (Hock and Botzenhart 2002; Hock viruses by processes other than enzymatic ones, e.g. and Botzenhart 2003 as quoted by Skraber et al. 2005). Pseudomonas aeruginosa can produce substances with These results can be explained by the fact that MS2 is more molecular weights below 500 Da which appear to inacti- negatively charged than other tested viruses. In contrast, vate viral particles. Substances with such low molecular Storey and Ashbolt (2003a, b) estimated that the attach- weights cannot act enzymatically and they are referred to ment rates of MS2 and uX174 were similar: 1% of the as virolytic substances (Cliver and Hermann 1972; Deng initial input. The efficiency of viral recovery was prede- and Cliver 1992). Deng and Cliver (1995a) studied the role termined for MS2, but not for uX174 or poliovirus in the of the microbial activity of animal wastes in inactivation of mentioned studies. Due to this fact, differences or simi- HAV. Ten out of 31 bacterial isolates were able to effi- larities between apparent attachments can be explained by ciently inactivate HAV. The inactivation capacity of four variation between efficiencies of viral recovery. of the nine culture filtrates was significantly reduced by Results published by Quignon et al. (1997) showed that incubation with selected protease inhibitors before the water biofilm can protect viruses form inactivation. This virus was added. These inhibitors did not affect the activ- hypothesis is supported by the study of Storey and Ashbolt ities of the other five culture filtrates. Fractions prepared by (2001). Phages MS2 and B40-8 were recovered from biofilm ultrafiltration (nominal molecular weights \1,000 Da) in the presence of the average concentration of 0.2 mg free from two of these cultures inactivated HAV suggested that chlorine/l during a 30-day period. In comparison, Duran et al. their mode of action was not enzymatic. (2003) reported that phages MS2 and B40-8 showed 3.2 and 1.7 log -units reduction after only ten min in groundwater Viruses Within Biofilms containing 0.5 mg free chlorine/l. Storey and Ashbolt (2003b) compared the inactivation of two phages (B40-8 and From a public health point of view, biofilms have been MS2) within biofilms. Results indicated that the subpopu- already regarded as a common cause of bacterial infections. lation of approximately 0.01% of phages had the potential to It has also been hypothesised that produced exopolymeric persist over 100 days for B40-8 and almost 10 times longer substances (EPS) may protect biofilms from viruses, espe- for MS2 in the presence of free chlorine. The level of viral cially phage penetration (Sutherland et al. 2004). Recent protection may depend on parameters such as the composi- studies have revealed that, even in the absence of specific tion, thickness, or structure of biofilms. enzymatic reactions, viral particles are able to penetrate Various studies have suggested that biofilms may trap inside the EPS structure of mucoid biofilms. After pene- and accumulate virus-sized particles and produce a poten- tration inside the polymeric matrix, the viruses may take tial reservoir of human or bacterial pathogens. In natural advantage from the specific ‘biofilm lifestyle’, and benefit environments, biofilms are mixed microbial cultures nor- from protection against environmental stress, such as des- mally consisting of predominantly prokaryotes with some iccation or other actions of antimicrobial agents. Moreover eukaryotes (Sutherland et al. 2004). Although virus 123 Food Environ Virol (2010) 2:24–34 31 attachments to biofilms have been observed experimentally It is obvious that physical properties of the surface could and contamination of natural biofilms with pathogenic further reduce recovery of viral particles form surfaces. viruses can be very low, biofilms should be considered as a Viruses can be trapped within the matrix, especially if the protective reservoir for pathogenic viruses, and could be surface is porous (Scherer et al. 2009). Therefore, sampling responsible for numerous persistent viral infections (Lac- and detection methods must be sensitive enough to detect roix-Gueu et al. 2005). low levels of viral particles. Cell culture methods are sensitive and can determine infectivity of isolated viral particles, but these methods are time consuming. More- Specific Antiviral Chemicals over, there is a problem of interference amongst viruses, which are able to grow on the same cell line (e.g. reovirus Due to the importance in preventing the spread of viruses and enterovirus) or can allow chronic infections without a in healthcare settings and food establishments, the effect of visible cytopathic effect (e.g. HAV or reovirus). Even if chemical disinfectants on contaminated surfaces has been this cytopathic effect is evident, the identification of iso- extensively studied. Some studies demonstrated that sus- lated agents requires additional techniques for confirmation pension tests performed with the same disinfectants of virus strain or type. Finally, cultivation methods cannot showed different virus inactivation rates, thus failing to be used for non-cell culture viruses (e.g. HEV). For enu- provide a reliable indication of the extent of virus disin- meration of infectious viruses it is necessary to use cell fection on surfaces. The activity of disinfectants is strongly culture in a quantitative format, e.g. plaque assay. The related to RH and temperature (Casella and Schmidt-Lor- number of infectious viruses remaining in the sample is enz 1989; Theilen et al. 1987). compared with the number which was introduced, and a Viruses without envelope are more resistant to desic- statistical procedure can be performed to calculate any cation. Biocides that have activity against both enveloped degree of decline. and non-enveloped viruses include chlorine- and iodine- Molecular methods are an alternative which can be used releasing agents, peracids and ozone. Their effectiveness for virus detection. PCR and NASBA techniques represent depends on the nature of the virus, the surface carrier, the high sensitive and specific methods. They can be used for presence of interfering substances such as organic soil or all types of viruses, require a short time for execution, can hard water salts, and contact time. However, some cleaning determine different agents in the same sample, and allow products or disinfectants are ineffective against viruses, identification of non-cultivable virus. Nevertheless, analy- and can result in viral spread or cross-contamination of ses may be hindered by inhibitory substances present in the surfaces (Boone and Gerba 2007). environment, so there is a risk of occurrence of false negative results. Due to this fact it is necessary to imple- Chemical disinfection on food contact surfaces and rising food items with sanitizers is generally relied on ment internal amplification controls. Moreover viruses prevention and control food-borne outbreaks. Numerous detected by these techniques are not necessary infectious. authors have reported on the efficacy of disinfectants for Molecular methods can reveal nucleic acid originating the inactivation of cultivable viruses using standard sus- from partially denatured viral particles. Thus, viral capsid pension tests, but data for gastroenteritis viruses and HAV is still capable of protecting nucleic acid, but the viral are lacking (Seymour and Appleton 2001). This is partially particle is not infectious. Therefore, the combination of due to the lack of methods for propagation of these viruses molecular techniques and cell culture methods should be in vitro (Gulati et al. 2001). used for the detection of viruses (Cliver 2009; Cook 2003). Detection of Viruses on Surfaces Conclusion Sufficient detection of infectious viral particles in the In conclusion, there is strong evidence to suggest that transmission of viruses via contaminated surfaces is a environment is affected by several obstacles such as: virus size, the large variability amongst and within viral genera, significant factor contributing to the spread of disease. the low concentration, the presence of substances which Virological monitoring of surfaces can be very useful in can interfere with analysis procedures, the limits of risk analysis to identify ways of viruses spreading, to detection of proposed techniques, and absence of reliable monitor environmental pollution, and thus assess the risk of controls. Therefore, appropriate sampling and sensitive infection. Moreover detection of viral contamination of the detection methods are necessary to help better under- environment allows molecular epidemiologic and phylo- standing of viral transmission routes. genetic data for virus surveillance and circulation. 123 32 Food Environ Virol (2010) 2:24–34 Acknowledgments This study was supported by Grants No. effectiveness of gaseous formaldehyde and level of residues in MZE0002716202 (Ministry of Agriculture of the Czech Republic), dependence on concentration, temperature and relative humidity. OC08045 (support of the Cost Action 929) and AdmireVet (Ministry International Journal of Hygiene and Environmental Medicine, of Education, Youth and Sports of the Czech Republic), Cost Action 188(6), 533–549. 929 ENVIRONET of Brussels, EC and the Italian National Institute Chang, J. C. H., Ossoff, S. F., Lobe, D. C., Dorfman, M. H., Dumais, of Occupational Safety and Prevention. The authors wish to thank C. M., Qualls, R. G., et al. (1985). 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Originale B, Hygiene, Infection Control and Hospital Epidemiology, 26, 802–810. 184(3–4), 229–252. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Food and Environmental Virology Pubmed Central

Issues Concerning Survival of Viruses on Surfaces

Food and Environmental Virology , Volume 2 (1) – Feb 4, 2010

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© Springer Science + Business Media, LLC 2010
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1867-0334
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Abstract

Food Environ Virol (2010) 2:24–34 DOI 10.1007/s12560-010-9025-6 REVIEW PAPER • • • P. Vasickova I. Pavlik M. Verani A. Carducci Received: 24 November 2009 / Accepted: 17 January 2010 / Published online: 4 February 2010 Springer Science+Business Media, LLC 2010 Abstract Viruses are the causative agents of an estimated were not related to microbial contamination of surfaces, the 60% of human infections worldwide. The most common Centre for Disease Control (CDC) and the American Hos- viral illnesses are produced by enteric and respiratory pital Association focussed only on patient diagnosis up to viruses. Transmission of these viruses from an infected 1987. Over the years studies have changed perspectives on person or animal to a new host can occur via several routes. viral transmission and have integrated a more complex Existing studies strongly suggest that contaminated fomites multifactorial model of disease spreading including the or surfaces play an important role in the spreading of viral contaminated environment (Boone and Gerba 2007). diseases. The potential of viral spreading via contaminated Viral transmission from an infected person or an animal surfaces depends particularly on the ability of the virus to to a new host can occur by direct or indirect routes. During maintain infectivity whilst it is in the environment. This is indirect transmission, contaminated surfaces can play an affected by a combination of biological, physical and important role. This kind of transmission is dependent on chemical factors. This review summarises current knowl- several factors, which include the quantity of viral particles edge about the influence of environmental factors on the excreted by an infected organism, their stability in the survival and spread of viruses via contaminated surfaces. environment, the potential to spread within a closed envi- ronment, as well as interaction of the virus and the host Keywords Pathogenic viruses  Environmental factors  organism. Large numbers of viral particles can be shed via Surveillance  Biofilms various body fluids including blood, faeces, vomit, saliva, urine, and respiratory secretions from infected individuals or carriers. The more viruses are shed, the greater their Introduction chance is to survive and reach a new host organism (Rzezutka and Cook 2004). A critical factor of viral transmission is its ability to Viruses are causative agents of an estimated 60% of human infections worldwide (Barker et al. 2001). For centuries it survive in the environment. Previous studies have shown was assumed that these viral diseases were spread primarily that viral particles can persist for extended periods on through direct patient contact or by the airborne route, and surfaces such as medical devices, fomites or human skin surrounding environment played little or no role in disease (Abad et al. 2001; Sattar et al. 1986, 1987; Todd et al. transmissions. Due to the opinion that nosocomial infections 2009). Even if some viruses survive relatively poorly in the environment, the low infective dose suggests that these viruses are able to persist in sufficient numbers to act as a P. Vasickova (&)  I. Pavlik source of infection for several days, week or in some cases Veterinary Research Institute, Hudcova 70, 621 00 Brno, Czech Republic months (Barker et al. 2001; Boone and Gerba 2007). e-mail: vasickova@vri.cz Surfaces can be contaminated directly by their contact with body secretions and fluids or indirectly through virus M. Verani  A. Carducci contaminated aerosol or other contaminated fomites. Once a Department of Biology, University of Pisa, Via S. Zeno, surface is contaminated, the transfer of infectious viral 35-56127 Pisa, Italy 123 Food Environ Virol (2010) 2:24–34 25 particles may easily occur between inanimate or animated Coxsackievirus), hepatitis A virus (HAV) and hepatitis objects, or vice versa, e.g. hands and work surfaces with the E virus (HEV). Infection by enteroviruses is often potential of subsequent transfer to food or direct hand- subclinical but they may induce signs and symptoms of to-mouth transfer (Goldmann 2000; Marks et al. 2000; disease in not related with intestinal tissue. The infections caused by hepatitis viruses affect liver Rzezutka and Cook 2004). Rapid spread of viral infections through contaminated surfaces is common particularly in tissue (Carter 2005). crowded indoor establishments such as schools, day-care Recent epidemiological studies have shown that noro- facilities, nursing homes, business offices, hospitals or virus is one of the most frequent cause of acute non-bac- transport systems (Barker et al. 2001). The influences of terial gastroenteritis. Additionally, it is responsible for environmental factors on the stability and spread of bacte- almost all foodborne outbreaks, where viruses are identi- rial infections are well documented, especially in hospitals. fied (Goodgame 2006; Koopmans and Duizer 2004). A The comparable knowledge concerning the role of surfaces study by Barker et al. (2004) demonstrated that noroviruses or fomites in viral transmission is still lacking and further could be transferred from contaminated surfaces to clean investigation is needed (Boone and Gerba 2007; von Rhe- hands. It was also found that norovirus-contaminated hands inbaben et al. 2000). could cross-contaminate a series of seven types of clean The objective of this review is to summarise current surfaces. Wu et al. (2005) tested ten environmental samples knowledge about influences of environmental factors on taken during the norovirus outbreak at a long-term-care survival and spread of viruses via contaminated surfaces. facility. Positive swabs were obtained from toilet seats used by case-residents, bed rails from case-residents’ bed, a dining room tabletop and an elevator button. Viruses Spread Via Contaminated Fomites Worldwide, rotavirus is probably the most important pathogen causing diarrhoeal disease in infants. Rotaviruses Nearly one thousand different types of viruses are known to are shed in large numbers from infected person with faeces infect humans, whilst the most common viral illnesses are 8 11 often containing 10 –10 virions per gram (Bajolet and produced by enteric and respiratory viruses (Barker et al. Chippaux-Hyppolite 1998; Leung et al. 2005). It has been 2001). In developed countries, viruses are responsible demonstrated that infective viral particles can survive on approximately for 30–40% of infectious gastroenteritis human hands and be transferred to animate and non-porous cases. Estimates indicate that adults have two to five colds surfaces (Ansari et al. 1988; Sattar et al. 1986). Ward et al. per year and infants or preschool children four to eight colds (1991) examined the transmission of rotavirus from a per year. Existing studies prove that contaminated fomites contaminated surface to the mouth and from surface to play an important role in the spreading of these diseases hands and mouth. All the volunteers who licked rotavirus- (Barker et al. 2004; Winther et al. 2006; Wu et al. 2005). contaminated plates became infected. Whereas, only about half of individuals touching the virus contaminated plates Viral Gastroenteritis and Hepatitis with their fingers and then their mouth became infected. Infections caused by HAV are endemic throughout the Viruses that infect a host organism via the gastrointestinal world. Transfer of infectious viral particles from contam- tract are excreted in faeces and may be also present in vomit inated to clean surfaces was also reported. The persistence (Seymour and Appleton 2001). Normally they are shed in of HAV on surfaces and the ability of the virus to be high numbers and exhibit great particle stability outside the interchanged from animate and inanimate environments organism and on passage through the stomach. There are confirm that surfaces present important epidemiological two types of viruses infecting gastrointestinal tract: factors in the indirect transmission of HAV (Croci et al. 2002; Bidawid et al. 2000; Mbithi et al. 1992). Mbithi et al. 1. Capable of primarily multiplying in the intestine. These agents cause gastroenteritis, and include members of (1992) presented that considerable amounts of HAV genus: Rotavirus, Norovirus, Astrovirus and Adenovi- remained infectious on finger pads after 4 h, even though rus. Viral gastroenteritis is usually relatively mild 68% of viruses lost their infectivity during the first hour. disease, which has a short incubation period (1–4 days) Astroviruses or adenoviruses exhibited shorter survival depending on the virus species. Specific symptoms are time than rotaviruses and HAV. Despite this, they were diarrhoea and vomiting. Most infected people do not able to survive on inert surfaces long enough to suggest consult a medical practitioner. Therefore, the majority that contaminated surfaces may have a relevant role in the of cases is not reported and subsequently investigated. secondary transmission of these viruses (Abad et al. 2001). 2. Capable of multiplying elsewhere in the body. These Information about the survival of HEV in environment is viruses include enteroviruses (e.g. poliovirus or still lacking. 123 26 Food Environ Virol (2010) 2:24–34 Respiratory Infections particles could be transferred from hands and fingers to surfaces and back again (Brady et al. 1990; Gwaltney and Respiratory viral infections are a major health burden Hendley 1982; Hendley et al. 1973; Winther et al. 2007). (Winther et al. 2006). Although these diseases are often regarded as trivial, hospital admission and mortality rates in infant or elderly are considerable. For instance, respi- Factors Affecting Virus Survival on Surfaces ratory viruses cause more than 400,000 hospitalizations per year in children less than 18 years of age in the United The potential of viral spreading via contaminated surfaces States (Henrickson et al. 2004). Viral agents that primarily depends particularly on the ability of the viruses to maintain infect the upper or lower respiratory tract include influenza infectivity whilst they are in the environment (Boone and and parainfluenza viruses, adenoviruses, respiratory syn- Gerba 2007). Their survival in the environment is affected by cytial virus (RSV), coronaviruses, human metapneumovi- a combination of biological, physical and chemical factors rus, rhinoviruses and enteroviruses (Kesson 2007). (Fig. 1). To date, complete information regarding the influ- It is generally accepted that respiratory viruses are ence of the environment on all viruses and their stability in spread from person to person by aerosol transmission due external conditions does not exist. Most studies have used to sneezing or coughing (Goldmann 2000). Additionally, only few target viruses or their surrogates. Since experi- there is evidence to suggest that a significant proportion of mental condition and methods vary, it is difficult to draw flu viruses and other respiratory viruses are spread via conclusions from these studies (Carter 2005). contaminated hands and fomites (Hall et al. 1980; Tiwari Once the surface is contaminated, it can be source of et al. 2006; Winther et al. 2007). contamination for other animate or inanimate objects, e.g. RSV was recovered from counters for up to 6 h, from contaminated door handles and hands were found to be an rubber gloves for up to 1.5 h, from clothing gowns and efficient vector of viruses. At least 14 persons could be paper tissue for 30–45 min, and from skin for up to 20 min. contaminated or infected by touching a polluted door Additional experiments demonstrated that infectious RSV handle. Successive transmission of virus from one person could be transferred to hands by touching these contami- to another could be followed up to the sixth contact person nated surfaces and could be further recovered from these (von Rheinbaben et al. 2000). It was also found that con- hands for up to 25 min (Hall et al. 1980). A study done by taminated fingers could subsequently transfer a virus from Winther et al. (2007) was designed to assess rhinovirus up to seven clean surfaces (Barker et al. 2004). contamination of surfaces and rhinovirus transfer from these surfaces to fingertips during normal daily activities of Virus Characterisation and Classification adults. Common virus-positive sites were door handles, pens, light switches, TV remote controls, faucets and The most important aspects affecting virus survival are telephones. Rhinovirus was transferred from surfaces to biological factors like the presence of the envelope and fingertips in 60% trials 1 h after contamination and in 33% virus type. These basic characteristics influence and help to after 18 h after contamination. predict virus survival in the environment and behaviour in Influenza viruses, and parainfluenza viruses are also able a host organism. to survive on hands long enough to permit self-inoculation. Persistence of a virus in the environment is primarily It has been demonstrated that these infectious viral affected by the presence of a viral envelope. The non- Fig. 1 Factors affecting virus survival on surfaces 123 Food Environ Virol (2010) 2:24–34 27 enveloped viruses have higher resistance to drying or des- was kept either low or high than when RH has medium iccation methods and therefore are spread more easily than range. Sattar et al. (1986) reported that human rotavirus enveloped viruses (which are less stable in the environment). survived for a shorter period of time at high RH. Abad et al. The non-enveloped enteric viruses like HAV, rotavirus or (1994) also observed that human rotavirus and poliovirus astrovirus are able to remain infective on surfaces for at least exhibited greater persistence at high RH on non-porous 2 months. In contrast, enveloped respiratory viruses usually material. The survival of adenovirus was not affected by remain infectious for several hours to several days (Duizer RH. At 5C RH had a little effect on survival time of et al. 2004). Reovirus, non-enveloped virus, when dried in an norovirus, but its survival was longest at 20C and low RH. organic matrix can survive for a period of 30 days, whereas Sattar et al. (1987) investigated rhinovirus on surfaces. the enveloped Sindibis virus dies rapidly (Howie et al. 2008). Humidity was used as a variable factor. The study found Variation in virus survival occurs within a viral family that rhinovirus exhibits optimum survival at 50% RH. or even genus. Feline calicivirus (FCV) and norovirus belong to the same family. Their physicochemical prop- Temperature erties and genome organisation are similar. Therefore, FCV is used as a surrogate model, e.g. to determine the efficacy However the degree of virus survival on surfaces is affected of disinfectants against norovirus on fresh produce or by temperature, it depends also on the virus type and RH. surfaces (Gulati et al. 2001). Duizer et al. (2004) reported Viral particles are able to persist from days to months over a that norovirus is profoundly more resistant to low and high range of temperatures in the environment, and being pre- pH than FCV and canine calicivirus, which are members of served by refrigeration or freezing (Cliver 2009). the same family. Hewitt and Greening (2004) mentioned Temperature is one of the most important of determining that in comparison to norovirus, FCV is more sensitive to norovirus survival in the environment. Recent studies indi- environmental factors in general. Examples of survival cate that noroviruses can survive for a prolonged period of variation within the genus are coronaviruses OC43 and time at a low temperature and can be transmitted to a sus- 229E. After drying, coronavirus 229E infectivity was ceptible population via different environmental media detectable after 3 h on various surfaces (aluminium, sterile including surfaces (Mattison et al. 2007). Doultree et al. latex surgical gloves and sterile sponges), whilst corona- (1999) found that FCV dried onto glass and stored at 4C virus OC43 survived 1 h or less (Sizun et al. 2000). displays a 4.75 log reduction over 56 days. FCV survival was lower at room temperature, but still prolonged. The number Relative Humidity of infectious FCV declined to undetectable levels by 21– 28 days. FCV was not detected at 37C after 1 day. Com- Effect of relative humidity (RH) varies within virus type. It parative analyses indicated that FCV survival was greater at is believed that the survival of enveloped viruses on 4C than at room temperature. Therefore, outbreaks caused inanimate surfaces is better when RH levels are below by noroviruses are much more prevalent in the winter than in 50%. On the other hand, RH levels higher than 80% are the summertime (Doultree et al. 1999; Mattison et al. 2007). considered to be more beneficial to the survival of non- Rotavirus particles are able to survive storage in ambient enveloped viruses. In general, viruses with higher lipid tropical temperatures for more than 2 months (Fischer et al. content tend to be more persistent at a lower RH, whilst 2002). Moe and Shirley (1982) reported that rotavirus viruses with lesser or no lipid content are more stable at a infectivity decreases more rapidly under all RH at 37C higher RH (Assar and Block 2000; Moce-Llivina et al. than at 4 or 20C. According to a study done by Sattar et al. 2006). However, there are exceptions. (1986), rotaviruses can persist longer at a lower tempera- Studies have shown that HAV is able to survive better at ture (4C) and RH (25–50%), with approximately 10% low levels of RH, which is in contrast to the behaviour of infectious virus remaining after 10 days, in comparison to other enteroviruses (Mbithi et al. 1991; Stine et al. 2005). less than 1% after 2 days at 22C and 85% RH. Abad et al. When its persistence in high and medium RH (85.7–90.3% (2001) investigated the survival of an astrovirus at 4 and and 45.1–48.4%) was compared, HAV survived longer on 20C with a high RH (90 ± 5%). At 4C, the virus was lettuce in dry conditions. Based on the calculated inacti- able to persist for 60 days desiccated on non-porous vation rates, a 99.9% reduction in HAV could take material and for 90 days on porous material. Faster decay 822 days in pre-harvest conditions of contaminated vege- was observed at 20C. Short-term survival of astrovirus tables (Stine et al. 2005). In contrast, Abad et al. (1994) was compared to that observed for other enteric viruses found that survival of HAV was enhanced at high RH. significant for health, such as rotavirus, adenovirus, Data regarding rotavirus survival was determined to be poliovirus and HAV. Overall, astrovirus persisted better contradictory. Moe and Shirley (1982) showed that a field than poliovirus and adenovirus, although they exhibited a strain of human rotavirus could survive longer when RH shorter survival than the rotavirus and HAV. 123 28 Food Environ Virol (2010) 2:24–34 Amongst other factors, the effect of freezing on enteric depends especially on fragment size of viral nucleic acid. viruses in berries and herbs was tested by Butot et al. Nevertheless, it also shows that the viral capsid structure (2008). This study revealed that freezing does not signifi- has an important protective role against UV radiation cantly reduce the viability of norovirus, HAV and rotavi- (Simonet and Gantzer 2006). rus. Only infectivity of FCV on strawberries can be decreased. Freezing for 3 months had a limited effect on Type of Surface HAV and rotavirus in all tested food products. A higher decay rate was observed in frozen raspberries and straw- Several studies have compared the survival of different berries contaminated with FCV due to the acidic pH (Butot types of viruses on porous and non-porous surfaces. The et al. 2008). No reduction of MNV-1 PFUs was observed majority of viruses remain viable for a longer period of on frozen onions or spinach during storage for 6 months time on non-porous materials, although there are excep- (Baert et al. 2008). Kurdziel et al. (2001) reported a tions (Abad et al. 1994; Boone and Gerba 2007; Lam- reduction of \2 log units of poliovirus on frozen straw- houjeb et al. 2009; Tiwari et al. 2006); e.g. higher berries after 15 days of storage. So far, no data about persistence of poliovirus and adenovirus was observed on survival of other viruses during freezing are available. porous materials (paper and cotton cloth) compared to non- porous materials: aluminium, china, glazed tile, latex, and Sunlight and UV polystyrene (Abad et al. 1994). The enteric viruses reveal exhibited inactivation rates (at least 2 logs lower) than Ultraviolet radiation is the crucial virucidal agent, which respiratory viruses, with the exception of adenovirus and primary targets viral nucleic acid but also modifies capsid influenza virus (Boone and Gerba 2007). Tiwari et al. proteins. Virus resistance to UV exposure also appears to (2006) studied survival of avian metapneumovirus and vary according to virus type. Viruses with single-stranded avian influenza virus on 12 different porous and non-por- nucleic acid (ssDNA and ssRNA) are more susceptible to ous materials. Both viruses persisted longer (up to 6 days) UV inactivation than viruses with double-stranded nucleic on non-porous surfaces than on porous ones. acid: dsDNA and dsRNA (Gerba et al. 2002; Hijnen et al. Survival times for enteric viruses have been determined 2006; Tseng and Li 2007). on a range of different fruit and vegetable commodities According to Hijnen et al. (2006), adenoviruses are (Seymour and Appleton 2001). Mattison et al. (2007) sug- classified as the most resistant virus type to UV. The gested that smooth surfaces, such a lettuce leaf, might pro- obtained k-values, which characterise UV-sensitivity of the vide less protection to the virus than coarse surfaces like ham microorganism, are similar for FCV, rotavirus, poliovirus has. Results of other studies indicated that on plant surfaces, and Coxsackievirus. HAV is more sensitive then the above- viruses are exposed to potentially toxic compounds, such as mentioned viruses. The correlation between low and high phenols, ethanol, and acetaldehyde, which could accelerate solar virucidal radiation and high and low influenza prev- the inactivation process (Lamhoujeb et al. 2009). alence suggest that inactivation of viruses in the environ- Some specific chemical surfaces (e.g. heavy metals) are ment by solar UV radiation has a stronger effect than virucidal. Influenza virus particles (2 9 10 ) were inocu- expected and can play a role in seasonal occurrence, e.g. lated onto cooper and stainless steel surfaces in a study by influenza pandemics (Sagripanti and Lytle 2007). Noyce et al. (2007). After incubation for 24 h on stainless Duizer et al. (2004) exposed surrogate caliciviruses steel, 500,000 virus particles were still infectious in com- (enteric canine calicivirus and respiratory FCV) to UV-B parison with cooper, where only 500 viral particles were radiation as a factor affecting environmental survival. active after incubation for 6 h. Other recent studies also Results were comparable to enteroviruses (Gerba et al. suggest the antimicrobial properties of cooper-based sur- 2002), less effective than for vegetative bacteria, but more faces (Barker et al. 2004; Faundez et al. 2004; Iriarte et al. effective than for phage MS2 (Husman et al. 2004), ade- 2007; Noyce et al. 2006, 2007). It has been reported that noviruses (Gerba et al. 2002; Nwachuku et al. 2005), and aluminium also has virucidal activity. Adenovirus, polio- Baccilus subtilis spores (Chang et al. 1985). Parallel virus and the B40-8 phage persist for a shorter time on analysis of four RNA virus models (poliovirus 1, phage aluminium than on other non-porous material (Abad et al. MS2, phage GA and phage Qb) showed that the least 1994; Thurman and Gerba 1988). resistant virus to UV radiation was poliovirus 1. Qb phage had intermediate sensitivity, whilst MS2 and GA phages Adsorption State and Organic Matter were the most resistant. The rate of RNA degradation increased linearly with increasing fragment size, except The extent and state of virus adsorption on surfaces has an viruses with a similar size of genome (poliovirus 1 and important influence on virus survival. Studies have shown MS2). Based on these results, viral resistance to UV that the survival of viruses is increased with increased 123 Food Environ Virol (2010) 2:24–34 29 adsorption to the surfaces and that immobilized (adsorbed) The viral adsorption to the surfaces can be influenced by viral particles most often keep their infectious potential ionic strengths; therefore, salts are commonly used to after desorption. Interactions that take place between favour the attachment of viruses to different types of sur- viruses and surfaces are determined by their characteristics faces. Theoretically, adsorption of viral particles is better in and involve electrostatic, hydrophobic interactions, and/or high ionic strength. Enteric viruses are destabilized and 2? ionic strength (Hurst et al. 1980; Lacroix-Gueu et al. 2005). inactivated by water lacking salt ions, e.g. Mg . On the Vega et al. (2008) compared the relative contributions of contrary, increased concentrations of salts (e.g. NaCl) are these interactions with the nonspecific attachment of antiviral for many viruses. echovirus 11, FCV, MS2, and uX174 to butterhead lettuce. The results imply that electrostatic forces play a major role in controlling virus adsorption to lettuce. Interaction of Pathogenic Viruses with Other Many viruses can be stabilized and protected by dis- Microorganisms During their Presence on Surfaces solved, colloidal and solid organic matter; including faecal and humic material. Organic matter has a low isoelectric Data about the influence of other microorganisms on virus point, and thus carries a negative surface charge at most survival are contradictory. Virus survival may increase or naturally occurring pH levels (Boone and Gerba 2007). decrease with the number of microbes present on the sur- Kiseleva (1971) reported that strains of poliomyelitis virus, face. Bacteria or microscopic fungi are able to attack and echovirus and coxsackievirus remained infectious from two inactivate infectious viral particles. Some bacteria can to more than 12 days on the surface of substances used in produce low molecular weight substances that apparently various household objects. The greater survival was inactivate viruses. Others appear to use viral capsid proteins observed, if the inoculum also contained coliform bacteria, as substrates (Deng and Cliver 1995a, b; Cliver 2009; proteins, fats and dust particles, but no precise results or Herrmann et al. 1974). By contrast increasing amount of experimental details were given (Kiseleva 1971 as quoted by microbes can protect viruses from desiccation and disin- Rzezutka and Cook 2004). Lee et al. (2008) found that fection. Interactions of pathogenic viruses with bacterial murine norovirus is more stable in a stool suspension than on biofilms have been reported (Lacroix-Gueu et al. 2005; different types of surfaces. After 30 days of incubation at Skraber et al. 2005). As biofilms can form on a wide spectra 18C, there was a 2.7-log reduction in the stool suspension, of surfaces (Davey and O’toole 2000), their influence on compared to the maximum reduction of 5.3-log on a gauze virus survival is also discussed in this review. or diaper surface. A study by Abad et al. (1994) showed that on non-porous surfaces, poliovirus and adenovirus persist Negative Influence of Other Microorganisms better in the presence of faeces. However, on porous fomites on Virus Survival the presence of faecal material has a negative influence on the survival of these viruses. HAV and human rotavirus One proposed mechanism of viral loss in the environment is persistence is not affected by the presence of faeces. inactivation by the direct or indirect action of microorgan- isms. Environmental isolates of bacteria with antiviral pH and Presence of Salts ability have been found on several occasions. These microbes are able to produce metabolites, which adversely In general, pH has a minimal effect on virus survival in an affect viral particles, or can use the viral capsid as a nutrient indoor environment. Hurst et al. (1980) measured the source (Deng and Cliver 1995a, b; Ward 1982). The inac- effects of several environmental conditions on virus per- tivation of viruses by bacterial cultures is temperature sistence in soil. They found that the temperature and virus dependent. The lower the temperature of the mixed waste, adsorption to soil is more important for virus survival than the longer the virus is able to persist. Moreover temperature the effect of pH. Enteric viruses are able to survive severe could strongly influence microbial activity, and thus influ- conditions in the gastrointestinal tract, such as low pH in ence viral persistence (Deng and Cliver 1992). stomach or high bile concentration. They are generally most Ward (1982) investigated the influence of mixed-liquor stable near pH 7, but prefer low pH’s (3–5) rather than suspended solids (MLSS) of inactivated sludge on a alkaline pH’s (9–12). It was shown that noroviruses are able poliovirus 1 survival. The first experiment was conducted to persist at pH 2.7 and room temperature more than 3 h in order to determine the effect of MLSS on the recovery of (Duizer et al. 2004). As the surface charge of viral particles poliovirus after a different period of time. The second varies depending on the pH, disruption of electrostatic experiment was designed to find out the role of different interactions between viral particles and environmental MLSS components in virus loss. Results of these studies surfaces commonly consists of changing the pH, and thus indicate that MLSS contain a component(s) which can affect viral persistence in the environment (Gerba 1984). inactivate poliovirus 1. These components were pelleted 123 30 Food Environ Virol (2010) 2:24–34 during centrifugation, destroyed by autoclaving, and during biofilms erosion or sloughing, protected immobilised removed by filtration. Consecutively, residual activity of an viral particles may be released in the environment, and then MLSS supernatant fraction was also studied to confirm the contact their target host commencing the viral infectious absence of antiviral activity in non-living heat-sensitive cycle (Briandet et al. 2008; Helmi et al. 2008; Lacroix-Gueu material in the MLSS. Subsequent increasing activity of et al. 2005; Lehtola et al. 2007; Quignon et al. 1997). Viral this supernatant, coupled with the previous results, strongly attachment rates to biofilms vary greatly and may depend on indicates the antiviral activity of some microbial species. many factors such as the biofilm or viral characteristics Deng and Cliver (1992) demonstrated the antiviral effect of (size, shape, isoelectric point), and concentration of viral several bacterial cultures from swine manure slurry and particles (Helmi et al. 2008). mixed septic tank effluent. These cultures were identified Helmi et al. (2008) reported that poliovirus 1 adsorption as Micrococcus luteus, Staphylococcus epidermidis, was higher in wastewater biofilm than in drinking water Bacillus sp. and Streptococcus sanguis group. A compari- biofilm. Infectious viral particles were detected in the son of poliovirus 1 inactivation in raw mixed waste, drinking water biofilm for up to 6 days after inoculation, autoclaved mixed waste, and bacterium-free filtrate of raw whilst the viral genome was still detectable at day 34. Hock mixed waste demonstrated that virus inactivation is related, and Botzenhart (2002, 2003) injected phages MS2, uX174 at least in part, to microbial activity in similar environ- and poliovirus 1 at comparable concentrations into a lab- mental conditions. Inhibition of poliovirus 1 inactivation oratory reactor containing approximately 100 ml of by protease inhibitors suggested that antiviral activity of drinking water. After the contact time of 1 h, concentra- mixed waste was partially due to proteolytic enzymes tions of 0.04, 0.13 and 0.27% were recovered from the produced by bacteria in wastes. biofilm. MS2 showed less adsorption to the biofilm than Bacteria may also produce substances that inactivate uX174 and poliovirus 1 (Hock and Botzenhart 2002; Hock viruses by processes other than enzymatic ones, e.g. and Botzenhart 2003 as quoted by Skraber et al. 2005). Pseudomonas aeruginosa can produce substances with These results can be explained by the fact that MS2 is more molecular weights below 500 Da which appear to inacti- negatively charged than other tested viruses. In contrast, vate viral particles. Substances with such low molecular Storey and Ashbolt (2003a, b) estimated that the attach- weights cannot act enzymatically and they are referred to ment rates of MS2 and uX174 were similar: 1% of the as virolytic substances (Cliver and Hermann 1972; Deng initial input. The efficiency of viral recovery was prede- and Cliver 1992). Deng and Cliver (1995a) studied the role termined for MS2, but not for uX174 or poliovirus in the of the microbial activity of animal wastes in inactivation of mentioned studies. Due to this fact, differences or simi- HAV. Ten out of 31 bacterial isolates were able to effi- larities between apparent attachments can be explained by ciently inactivate HAV. The inactivation capacity of four variation between efficiencies of viral recovery. of the nine culture filtrates was significantly reduced by Results published by Quignon et al. (1997) showed that incubation with selected protease inhibitors before the water biofilm can protect viruses form inactivation. This virus was added. These inhibitors did not affect the activ- hypothesis is supported by the study of Storey and Ashbolt ities of the other five culture filtrates. Fractions prepared by (2001). Phages MS2 and B40-8 were recovered from biofilm ultrafiltration (nominal molecular weights \1,000 Da) in the presence of the average concentration of 0.2 mg free from two of these cultures inactivated HAV suggested that chlorine/l during a 30-day period. In comparison, Duran et al. their mode of action was not enzymatic. (2003) reported that phages MS2 and B40-8 showed 3.2 and 1.7 log -units reduction after only ten min in groundwater Viruses Within Biofilms containing 0.5 mg free chlorine/l. Storey and Ashbolt (2003b) compared the inactivation of two phages (B40-8 and From a public health point of view, biofilms have been MS2) within biofilms. Results indicated that the subpopu- already regarded as a common cause of bacterial infections. lation of approximately 0.01% of phages had the potential to It has also been hypothesised that produced exopolymeric persist over 100 days for B40-8 and almost 10 times longer substances (EPS) may protect biofilms from viruses, espe- for MS2 in the presence of free chlorine. The level of viral cially phage penetration (Sutherland et al. 2004). Recent protection may depend on parameters such as the composi- studies have revealed that, even in the absence of specific tion, thickness, or structure of biofilms. enzymatic reactions, viral particles are able to penetrate Various studies have suggested that biofilms may trap inside the EPS structure of mucoid biofilms. After pene- and accumulate virus-sized particles and produce a poten- tration inside the polymeric matrix, the viruses may take tial reservoir of human or bacterial pathogens. In natural advantage from the specific ‘biofilm lifestyle’, and benefit environments, biofilms are mixed microbial cultures nor- from protection against environmental stress, such as des- mally consisting of predominantly prokaryotes with some iccation or other actions of antimicrobial agents. Moreover eukaryotes (Sutherland et al. 2004). Although virus 123 Food Environ Virol (2010) 2:24–34 31 attachments to biofilms have been observed experimentally It is obvious that physical properties of the surface could and contamination of natural biofilms with pathogenic further reduce recovery of viral particles form surfaces. viruses can be very low, biofilms should be considered as a Viruses can be trapped within the matrix, especially if the protective reservoir for pathogenic viruses, and could be surface is porous (Scherer et al. 2009). Therefore, sampling responsible for numerous persistent viral infections (Lac- and detection methods must be sensitive enough to detect roix-Gueu et al. 2005). low levels of viral particles. Cell culture methods are sensitive and can determine infectivity of isolated viral particles, but these methods are time consuming. More- Specific Antiviral Chemicals over, there is a problem of interference amongst viruses, which are able to grow on the same cell line (e.g. reovirus Due to the importance in preventing the spread of viruses and enterovirus) or can allow chronic infections without a in healthcare settings and food establishments, the effect of visible cytopathic effect (e.g. HAV or reovirus). Even if chemical disinfectants on contaminated surfaces has been this cytopathic effect is evident, the identification of iso- extensively studied. Some studies demonstrated that sus- lated agents requires additional techniques for confirmation pension tests performed with the same disinfectants of virus strain or type. Finally, cultivation methods cannot showed different virus inactivation rates, thus failing to be used for non-cell culture viruses (e.g. HEV). For enu- provide a reliable indication of the extent of virus disin- meration of infectious viruses it is necessary to use cell fection on surfaces. The activity of disinfectants is strongly culture in a quantitative format, e.g. plaque assay. The related to RH and temperature (Casella and Schmidt-Lor- number of infectious viruses remaining in the sample is enz 1989; Theilen et al. 1987). compared with the number which was introduced, and a Viruses without envelope are more resistant to desic- statistical procedure can be performed to calculate any cation. Biocides that have activity against both enveloped degree of decline. and non-enveloped viruses include chlorine- and iodine- Molecular methods are an alternative which can be used releasing agents, peracids and ozone. Their effectiveness for virus detection. PCR and NASBA techniques represent depends on the nature of the virus, the surface carrier, the high sensitive and specific methods. They can be used for presence of interfering substances such as organic soil or all types of viruses, require a short time for execution, can hard water salts, and contact time. However, some cleaning determine different agents in the same sample, and allow products or disinfectants are ineffective against viruses, identification of non-cultivable virus. Nevertheless, analy- and can result in viral spread or cross-contamination of ses may be hindered by inhibitory substances present in the surfaces (Boone and Gerba 2007). environment, so there is a risk of occurrence of false negative results. Due to this fact it is necessary to imple- Chemical disinfection on food contact surfaces and rising food items with sanitizers is generally relied on ment internal amplification controls. Moreover viruses prevention and control food-borne outbreaks. Numerous detected by these techniques are not necessary infectious. authors have reported on the efficacy of disinfectants for Molecular methods can reveal nucleic acid originating the inactivation of cultivable viruses using standard sus- from partially denatured viral particles. Thus, viral capsid pension tests, but data for gastroenteritis viruses and HAV is still capable of protecting nucleic acid, but the viral are lacking (Seymour and Appleton 2001). This is partially particle is not infectious. Therefore, the combination of due to the lack of methods for propagation of these viruses molecular techniques and cell culture methods should be in vitro (Gulati et al. 2001). used for the detection of viruses (Cliver 2009; Cook 2003). Detection of Viruses on Surfaces Conclusion Sufficient detection of infectious viral particles in the In conclusion, there is strong evidence to suggest that transmission of viruses via contaminated surfaces is a environment is affected by several obstacles such as: virus size, the large variability amongst and within viral genera, significant factor contributing to the spread of disease. the low concentration, the presence of substances which Virological monitoring of surfaces can be very useful in can interfere with analysis procedures, the limits of risk analysis to identify ways of viruses spreading, to detection of proposed techniques, and absence of reliable monitor environmental pollution, and thus assess the risk of controls. Therefore, appropriate sampling and sensitive infection. Moreover detection of viral contamination of the detection methods are necessary to help better under- environment allows molecular epidemiologic and phylo- standing of viral transmission routes. genetic data for virus surveillance and circulation. 123 32 Food Environ Virol (2010) 2:24–34 Acknowledgments This study was supported by Grants No. effectiveness of gaseous formaldehyde and level of residues in MZE0002716202 (Ministry of Agriculture of the Czech Republic), dependence on concentration, temperature and relative humidity. OC08045 (support of the Cost Action 929) and AdmireVet (Ministry International Journal of Hygiene and Environmental Medicine, of Education, Youth and Sports of the Czech Republic), Cost Action 188(6), 533–549. 929 ENVIRONET of Brussels, EC and the Italian National Institute Chang, J. C. H., Ossoff, S. F., Lobe, D. C., Dorfman, M. H., Dumais, of Occupational Safety and Prevention. The authors wish to thank C. M., Qualls, R. G., et al. (1985). 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