What is the main structural difference between enveloped and nonenveloped viruses group of answer choices?

Open access peer-reviewed chapter

Submitted: December 6th, 2021 Reviewed: January 17th, 2022 Published: March 22nd, 2022

DOI: 10.5772/intechopen.102727

Abstract

Viruses exhibit a marked variation in their susceptibilities to chemical and physical inactivation. Identifying a trend within these variations, if possible, could be valuable in the establishment of an effective and efficient infection control or risk mitigation strategy. It has been observed that non-enveloped viruses are generally less susceptible than enveloped viruses and that smaller sized viruses seem less susceptible than larger viruses. A theory of a “hierarchy” of pathogen susceptibility has been proposed and widely referenced. This concept provides a useful general guide for predicting the susceptibility of a newly emerged pathogen. It also serves as a theoretical basis for implementing a limited scale viral inactivation study that is to be extrapolated onto many other viruses. The hierarchy concept should be interpreted with caution since the actual viral inactivation efficacy may, in some cases, be different from the general prediction. The actual efficacy is dependent on the type of chemistry and application conditions. The order of susceptibility is not always fixed; and viruses within the same family or even the same genus may exhibit drastic differences. This chapter reviews viral inactivation data for several commonly used chemistries against non-enveloped viruses, highlighting the cases wherein the order of susceptibility varied or even flipped. Possible underlying mechanisms are also discussed.

Keywords

  • enveloped viruses
  • non-enveloped viruses
  • hierarchy of susceptibility
  • disinfection
  • viral inactivation
  • virucidal efficacy

  • Sifang Steve Zhou*

    • Microbac Laboratories, Inc., Sterling, Virginia, USA

*Address all correspondence to:

1. Introduction

Bacteria, fungi [yeasts and molds], mycobacteria, prions, protozoa, and viruses are common pathogens infecting humans and animals. They typically exist within the host or in the environment. It has been observed that these microorganisms exhibit a notable difference in the natural survivability in the environment, as well as susceptibility to chemical and physical inactivation. For example, under ambient and dried conditions, human coronaviruses seem to lose their infectivity in a matter of several hours to several days [1], whereas endospores and prions may remain infectious for years to decades or even indefinitely [2, 3].

As more and more data have become available regarding the survivability and susceptibility of pathogens to microbicides, it has been observed that the pathogens seem to demonstrate an order of susceptibility to chemical and physical inactivation. E. H. Spaulding first proposed a classification system for the sterilization and disinfection of medical instruments based on the infection risk in 1939 [4]. On the basis of this classification, the concept of a hierarchy of pathogen susceptibility was proposed, in which microorganisms are placed into several groups and ranked from least susceptible to most susceptible. In this hierarchy concept, bacterial spores were ranked the least susceptible, followed by mycobacteria, non-enveloped viruses, fungi, vegetative bacteria, and enveloped viruses. The susceptibility hierarchy was also believed to be related to the biochemical and biophysical characteristics of a pathogen [5, 6].

This hierarchy concept has been slightly modified and expanded over the years. For example, prions were added and considered less susceptible to inactivation by microbicides than bacterial spores; small non-enveloped viruses were considered less susceptible than large non-enveloped viruses; and the order between mycobacteria and small non-enveloped viruses was sometimes reversed [Figure 1] [7, 8, 9, 10]. Additionally, it has been suggested that the hierarchy concept may be applied either “vertically” [i.e., ranking of susceptibility between classes of pathogens] and/or “horizontally” [i.e., ranking of susceptibility within a class of pathogens] [11].

Figure 1.

Proposed hierarchy of susceptibility of pathogens to microbicides. Note: slightly different versions of the hierarchy concept have been proposed in the literature. Mycobacteria have been placed above small non-enveloped viruses, and molds have been placed above large non-enveloped viruses in certain versions. In some versions, the small and large non-enveloped viruses are combined; and yeasts and molds may be combined.

The hierarchy concept has been quite useful for enabling scientists to better understand the innate difference among various types of pathogens. In the case of newly emerged pathogens, especially, the hierarchy concept has helped stakeholders design and implement a disinfection strategy swiftly with a reasonable level of confidence. The concept also helps the contaminant control for food, pharmaceutical, and biopharmaceutical products, as it is impractical to test every possible contaminating pathogen, and a robust infectivity assay system may be lacking for certain pathogens [e.g., hepatitis E virus].

Despite its usefulness, the hierarchy concept should be interpreted with caution, as it may oversimply the differences and trending of pathogen susceptibilities. Further examination and refinement of the concept may be necessary; and several important questions should be answered. For example, how often do exceptions to the hierarchy occur and what are the underlying reasons? Could a trending be specific to a given type of chemistry? Is the hierarchy the same between susceptibility to both chemical and physical inactivation? Why do pathogens in the same group, or even the same family or genus, sometimes exhibit striking differences in susceptibility? Is there a way to identify and separate reliable/consistent trending versus blurred/variable trending? A deeper look at the efficacy data for various types of microbicidal actives, especially for non-enveloped viruses, may help stakeholders understand the scope, reliability, and limitation of the hierarchy concept so that it can be best utilized.

This chapter reviews the inactivation efficacy data from the literature against non-enveloped viruses for several commonly used types of chemistries, either in formulated or unformulated form, in an effort to generate a separate relative order of susceptibility among these non-enveloped viruses for each type of chemistry and to differentiate consistent versus variable trending. Physical inactivation approaches are not covered in this chapter, although a significant degree of variation also exists for physical treatments. It is not clear that the physical inactivation approaches, in general, are governed by the same hierarchy to susceptibility as is observed for chemical inactivation approaches [12].

Advertisement

2. Common families of mammalian non-enveloped viruses

Currently, there are a total of 21 families of viruses [including enveloped and non-enveloped] identified for humans [13], which represent only a small part of the entire paradigm of viruses in nature, whose host ranges extend from vertebrates to plants to bacteria. The most common families of non-enveloped viruses for humans and animals include Adenoviridae, Astroviridae, Caliciviridae, Circoviridae, Hepeviridae, Papillomaviridae, Parvoviridae, Picornaviridae, Polyomaviridae, and Reoviridae. The genome structure, size of viral particle, and some representative viruses for each viral family are presented in Table 1.

FamilyExample virusAbbreviationGenusGenomeSize [nm]
Adenoviridae Adenovirus type 2 AdV-2 Mastadenovirus ds DNA 70–90
Adenovirus type 5 AdV-5 Mastadenovirus ds DNA 70–90
Adenovirus type 8 AdV-8 Mastadenovirus ds DNA 70–90
Astroviridae Human astrovirus HAstV Mamastrovirus ss RNA 28–35
Caliciviridae Feline calicivirus FCV Vesivirus ss RNA 28–40
Human norovirus HuNoV Norovirus ss RNA 28–40
Murine norovirus MNV Norovirus ss RNA 28–40
Tulane virus TuV Recovirus ss RNA 28–40
Circoviridae Porcine circovirus PCV Circovirus ss DNA ∼17
Hepeviridae Hepatitis E virus HEV Orthohepevirus ss DNA 32–34
Papillomaviridae Human papillomavirus HPV Papillomavirus ds DNA 50–60
Parvoviridae Bovine parvovirus BPV Bocaparvovirus ss DNA 20–28
Canine parvovirus CPV Protoparvovirus ss DNA 20–25
Human parvovirus B19 B19V Erythroparvovirus ss DNA 23–26
Minute virus of mice MVM [MMV] Protoparvovirus ss DNA 20–25
Porcine parvovirus PPV Protoparvovirus ss DNA 20–25
Picornaviridae Bovine enterovirus BEV Enterovirus ss RNA 30–32
Coxsackievirus Cox Enterovirus ss RNA 30–32
Echovirus 11 Echo11 Enterovirus ss RNA 30–32
Encephalomyocarditis virus EMCV Cardiovirus ss RNA 30–32
Enterovirus 71 EV-71 Enterovirus ss RNA 30–32
Enterovirus D68 EV-D68 Enterovirus ss RNA 30–32
Foot and mouth disease virus FMDV Aphthovirus ss RNA 30–32
Hepatitis A virus HAV Hepatovirus ss RNA 30–32
Poliovirus type 1 PV1 Enterovirus ss RNA 30–32
Rhinovirus RV Enterovirus ss RNA 30–32
Seneca Valley virus SVV Senecavirus ss RNA 30–32
Polyomaviridae Bovine polyomavirus BPyV Polyomavirus ds DNA 40–50
Simian virus 40 SV40 Betapolyomavirus ds DNA 40–50
Reoviridae Bluetongue virus BTV Orbivirus ds RNA 60–80
Reovirus type 3 REO-3 Orthoreovirus ds RNA 60–80
Rotavirus Rota Rotavirus ds RNA 60–80

Table 1.

Common families of human and animal non-enveloped viruses.

ss single-stranded;

ds double-stranded.

Among these, the Adenoviridae and Reoviridae families of viruses are generally considered large, non-enveloped viruses. Other non-enveloped viruses are generally considered small, non-enveloped viruses, although it should be noted that the particle sizes of Papillomaviruses and Polyomaviruses are notably larger than those for the rest of the small non-enveloped virus group [Table 1].

It is worth noting that viruses are typically classified taxonomically on the basis of virion properties [size, shape, envelope, physical, and chemical properties, etc.], genome organization, replication mechanism, antigenic properties, and biological properties [13, 14, 15]. The final classification is a combined consideration of these properties. However, the stability and susceptibility to inactivation of a virus may not relate to all of these properties and, as such, may not always align with the taxonomic classification system. For example, the susceptibility of a virus to surfactants may primarily be related to the envelope of the virion and not related to the genome structure or mode of replication.

The susceptibilities of non-enveloped viruses to chemicals have been found to be highly variable and somewhat hard to predict, since they do not always agree with the hierarchy concept. For example, according to the hierarchy concept as modified by Sattar [8], small non-enveloped viruses should be less susceptible than large non-enveloped viruses. Additionally, if there is a fixed hierarchy, all small non-enveloped viruses should either display similar levels of susceptibility or should demonstrate a definitive trend of relative susceptibility, regardless of the type of microbicide. Based on the literature, neither of these predictions appear to hold in every case. The relative order of susceptibility seems chemistry-dependent; and sometimes viruses within the same family or even genus have been found to exhibit unequivocal differences in their susceptibilities [reviewed in [16]]. Any trending or hierarchy, therefore, must be reviewed in the context of the type of chemistry, and it should not be assumed that non-enveloped viruses within the same family or genus will always display similar susceptibilities to a given microbicide.

Advertisement

3. Overview of chemical viral inactivation approaches

Viral inactivation may be achieved by chemical and/or physical methods. The subset of chemicals commonly used for inactivation of non-enveloped viruses includes alcohols, oxidizers, halogen compounds, quaternary ammonium compounds, phenolics, aldehydes, acids, and alkalines [17, 18, 19]. These differ with respect to efficacy, stability, toxicity, material or surface compatibility, cost, and sensitivity to organic soil load. Soil load is a term used to signify an organic matrix used to challenge the inactivating efficacy of a microbicide. It is intended to mimic secretions or excretions in which the virus would be released from an infected person or animal. Some chemistries [e.g., sodium hypochlorite, phenolics, and aldehydes] are mostly used for environmental or medical device disinfection. Other chemistries [e.g., ethanol] are more commonly used for hand hygiene, while some others [e.g., quaternary ammonium compounds] may be used for both environmental disinfection and skin antisepsis [Table 2].

ClassChemicalTypical conc.UsageMechanism of viral inactivationSensitivity to soil load
Alcohols Ethanol 50–95% Disinfection; Antisepsis Protein denaturation +
Isopropanol 70–90% Disinfection Protein denaturation +
Oxidizers Sodium hypochlorite 0.01–0.5% Disinfection Protein/genome damage ++
Chlorine dioxide 0.1–1 mg/L Disinfection; Water treatment Protein/genome damage
Hydrogen peroxide 0.1–10% Disinfection; Antisepsis Lipid/protein/genome damage +
Hypochlorous acid 0.002–0.1% Disinfection; Water treatment Protein/genome damage ++
Peracetic acid 0.01–1% Disinfection; Sterilization Protein denaturation
Povidone-iodine 0.02–8% Disinfection; Antisepsis Protein/genome damage ++
Chlorohexidine 0.02–0.2% Antisepsis Protein denaturation +
QAC BKC, DDAC, etc. 0.01–0.2% Disinfection Lipid/protein damage +
Low pH Acids ≤ pH 4 Sanitization; Biomanufacturing Capsid/protein damage
High pH NaOH, etc. ≥ pH 10 Disinfection; Tissue processing Capsid/genome damage
Aldehydes Glutaraldehyde 0.02–2% HLD; Sterilization Crosslinking/protein & genome damage
Formaldehyde 0.1–5% Disinfection/Preservation Alkylating/protein & genome damage
OPA 0.02–2% HLD; Sterilization Crosslinking/protein damage
Phenolics Phenylphenol, etc. 0.05–5% Disinfection Protein damage

Table 2.

Common types of chemistries used for non-enveloped viral inactivation.

Abbreviations used: BKC, benzalkonium chloride; Conc, concentration; DDAC, didecyldimethylammonium chloride; HLD, high-level disinfection; NaOH, sodium hydroxide; OPA, ortho-phthaldehyde; QAC, quaternary ammonium compounds.

The virucidal efficacy of a product is not only determined by the type and concentration of the chemical, but is also heavily influenced by the formulation, pH, exposure [contact or dwell] time, organic soil load, temperature, and surface characteristics [as applicable], etc. [10, 20, 21, 22]. Given the differences between various testing methods, as well as the intrinsic variability of viral infectivity [titration] assays, a general conclusion on the efficacy of a particular type of active ingredient will be enhanced if the efficacy is derived from multiple sets of data and under various application conditions [such as the concentration of the microbicidal active[s], contact time, formulation matrix [as applicable], and organic soil load, etc.] Additionally, in order best to explore the relative ranking of susceptibility between viruses, or the lack thereof, efficacy data from side-by-side studies wherein the same test methodologies and conditions were used would be preferable. Care should be taken when comparing data from different studies, especially if the formulations, test methods, and test conditions were different.

Advertisement

4. Inactivation of non-enveloped viruses by alcohols

Alcohols, primarily ethanol and isopropanol, are widely used for hand hygiene and environmental disinfection, and their efficacies against bacteria and viruses have been extensively studied [23, 24, 25]. Ethanol at a concentration of 70–90% and isopropanol at 70% have been broadly shown to be effective against enveloped viruses; however, their efficacies against non-enveloped viruses are much more variable.

The trending of the degree of susceptibility of non-enveloped viruses to ethanol and isopropanol is generally clearer and more consistent than it is for many other types of chemistries, thanks to the large amount of data in the literature. The relative ranking of susceptibility of non-enveloped viruses seems to differ between ethanol and isopropanol; and the ranking does not appear to align well with the classical virological taxonomy.

For ethanol, parvoviruses and the polyomavirus simian virus 40 have low susceptibility, while rotavirus [a reovirus] is susceptible [Table 3]. Viruses in the Picornaviridae family display clear differences in their susceptibilities to ethanol; and even viruses within the same genus display marked differences. For example, hepatitis A virus and human enterovirus 71 are much less susceptible than rhinovirus; and poliovirus, foot-and-mouth disease virus, and coxsackie virus seem to exhibit intermediate levels of susceptibility compared with the aforementioned viruses. The viral family Caliciviridae also has shown drastic differences among family members in the susceptibility to ethanol. Murine norovirus is quite susceptible to ethanol, whereas feline calicivirus, human norovirus, and Tulane virus are significantly more difficult to inactivate with ethanol. The Adenoviridae is another non-enveloped virus family that has shown intrafamily differences, wherein adenovirus 5 is rather susceptible but adenovirus 2 and adenovirus 8 are much less susceptible. The relative order of susceptibility between murine norovirus [a small, non-enveloped virus] and adenovirus types 2 and 8 [two large, non-enveloped viruses] clearly conflicts with the simplified hierarchy concept [Figure 1].

VirusaMethodSoil/MatrixbLog10 Reduction afterReferences30 s1 min5 min 10 min
70% Ethanol
PPV Stainless steel Erythrocytes + BSA 0.3 0.6 [26]
MVM Stainless steel Erythrocytes + BSA 0.3 0.7 [26]
HEV71 Suspension test Medium < 1 [27]
HAV Suspension test Medium 0.4 [28]
HAV Suspension test 20% fecal 0.4 [28]
HuNoV Suspension test 20% stool 3.6 [32]
MNV Suspension test Medium 5 [30]
Rotavirus Suspension test Medium > 3.1 [28]
75% Ethanol
RV86 Filter Medium >5 [35]
80% Ethanol
CPV Stainless steel Medium 0.1 [36]
SV40 Suspension test Medium 3 [46]
Sodium hypochlorite, 0.5%
MNV Stainless steel 10% stool < 1 ∼3.2 [44]
MVM Stainless steel Medium 1.2 2.2 [47]
MVM Suspension test Medium 2.5 > 4 [47]
FCV Stainless steel 10% stool 3.2 > 5 [44]
Hydrogen peroxide, ∼0.05%
HAV Stainless steel Medium ∼3.8 [47]
MVM Stainless steel Medium >4.6 [47]
Hydrogen peroxide, ∼0.1%
PV1 Glass Medium 0.4 0.9 [16]
RV14 Glass Medium >4.9 [16]
FCV Suspension test Medium >3 [48]
Hydrogen peroxide, 1%
Rotavirus Stainless steel Non-purified virus 1 [49]
Rotavirus Stainless steel Purified virus >3 [49]
MNV Stainless steel Medium 1.1 2.0 [50]
Hydrogen peroxide, 3%
PV1 Suspension test Medium 3 [76]
FCV Suspension test Medium 5 [48]
AdV-5 Stainless steel BSA 4.9–6.3 [34]
Rotavirus Suspension test Medium >5 [56]
Glutaraldehyde, 2%
PPV Stainless steel Erythrocytes + BSA 3.6 [26]
MVM Stainless steel Erythrocytes + BSA >4.4 [26]
PV1 Glass Medium >4 [31]
Formaldehyde, 2%
AdV-5 Suspension test Medium >5.0 [77]
Ortho-phthaldehyde, 0.55%
PPV Stainless steel Erythrocytes + BSA 3.6 [26]
MVM Stainless steel Erythrocytes + BSA >4. [26]

Table 8.

Efficacy of aldehydes against non-enveloped viruses.

a

See Table 1 for abbreviations used for viruses.

b

BSA, bovine serum albumin; medium, culture medium; RT, room temperature.


Entries in purple font indicate results from original or diluted formulations with microbicidal active ingredients.

Advertisement

9. General order of susceptibility of non-enveloped viruses to chemical inactivation

In the simplified hierarchy of susceptibility of pathogens to microbicides concept, small non-enveloped viruses are considered less susceptible than large non-enveloped viruses, and both groups of non-enveloped viruses are believed to be less susceptible than enveloped viruses. The hierarchy concept also assumes that the ranking applies to all types of microbicidal actives. Additionally, the hierarchy concept can generally lead to common notions that viruses that share similar virological properties [e.g., same family or genus of virus] may be expected to display similar degrees of susceptibility and that the smaller a virus is, the less susceptible it will be to microbicides in general.

These generalizations are correct, to a degree. For example, most enveloped viruses are indeed more susceptible than non-enveloped viruses to chemical inactivation. It should be noted though that exceptions to the hierarchy concept do exist, e.g., especially in the case of viral susceptibility to acids and alkalines [22], and exceptions are not uncommon for certain other chemistries. The hierarchy concept was never applied specifically to physical inactivation approaches, nor should it be. The evidence for heat inactivation, UV inactivation, and gamma irradiation indicates differing rankings of susceptibility to these modalities. Envelope status and particle size do not, in each case, relate to susceptibility for inactivation by these physical approaches [22, 78, 79, 80].

The validity of the hierarchy concept among non-enveloped viruses is much more blurred. Firstly, the order of susceptibility among non-enveloped viruses, if any generalization may be made, is dependent upon the type of chemistry, and there is no universal order that holds true for all types of chemistries. Secondly, large non-enveloped viruses [adenoviruses, reovirus, rotavirus, etc.] are not always more susceptible than small non-enveloped viruses [parvoviruses, picornaviruses, caliciviruses, etc.]. Thirdly, viruses within the same group [e.g., same family or genus] can exhibit profound and unequivocal differences in susceptibility. Finally, the rankings between viruses can be flipped [reversed], or nonexistent, depending on the type of microbicide. This implies that caution should be taken when interpreting the hierarchy concept for making predictions of efficacy for the non-enveloped viruses.

The accuracy and usefulness of a hierarchy concept can be improved if the model is broken into separate chemistries for non-enveloped viruses, since many viruses do exhibit a reliable and consistent trend of susceptibility for a specific type of chemical. Table 9 and Figure 2 provide a summary of the relative order of susceptibility for selected non-enveloped viruses under specific types of chemistry.

ChemicalLower susceptibilityMedium susceptibilityHigher susceptibility
Ethanol Animal parvovirus Poliovirus Murine norovirus
Simian virus 40 Foot and mouth disease virus Rhinovirus
Hepatitis A virus Human norovirus Adenovirus 5
Enterovirus 71 Feline calicivirus Rotavirus
Adenovirus 2, 8
Isopropanol Animal parvovirus Adenovirus 5, 8 Simian virus 40
Hepatitis A virus Murine norovirus Rotavirus
Enterovirus 71
Poliovirus
Feline calicivirus
NaOCl Porcine parvovirus Minute virus of mice Feline calicivirus
Hepatitis A virus Hepatitis A virus Adenovirus
Poliovirus Rotavirus
Enterovirus 71
Murine norovirus
H2O2 Animal parvovirus Poliovirus Rhinovirus
Hepatitis A virus Murine norovirus Feline calicivirus
Adenovirus Rotavirus
PAA Animal parvovirus Poliovirus Feline calicivirus
Hepatitis A virus Murine norovirus
Adenovirus
QAC Animal parvovirus Feline calicivirus Rotavirus
Poliovirus Murine norovirus Rhinovirus
Adenovirus 8, 25 Adenovirus 5 Coxsackievirus A11
Low pH Minute virus of mice Human parvovirus 4 Feline calicivirus
Hepatitis A virus Rhinovirus
Poliovirus Foot and mouth disease virus
Enterovirus 71 Enterovirus EV-D68
Coxsackievirus A9 Human parvovirus B19
Murine norovirus
Rotavirus
Reovirus
High pH Bovine viral diarrhea virus Reovirus
[enveloped virus]
Murine minute virus
Simian virus 40 Feline calicivirus
Hepatitis A virus Adenovirus
Canine parvovirus Rotavirus
Poliovirus Foot and mouth disease virus
Murine norovirus
Tulane virus
Aldehydes Porcine parvovirus Minute virus of mice Poliovirus
Hepatitis A virus
Feline calicivirus
Adenovirus
Reovirus
Rotavirus

Table 9.

Relative order of susceptibility of non-enveloped viruses to chemical inactivation.

Abbreviations used: H2O2, hydrogen peroxide; NaOCl, sodium hypochlorite; PAA, peracetic acid; QAC, quaternary ammonium compound.

Figure 2.

Relative order of susceptibility of non-enveloped viruses per microbicidal chemistry. Note: various types of adenoviruses exhibit different degrees of susceptibility to ethanol and quaternary ammonium compounds.

Advertisement

10. Discussion

The Spaulding concept of the hierarchy of susceptibility of pathogens to microbicidal inactivation, along with its modifications, has been widely influential. Multiple industries as well as regulatory agencies have adopted or referenced this concept to various degrees [9, 10, 81, 82]. The concept does provide a good tool for understanding the innate differences and trending of susceptibility among various types of pathogens. For the most part, the hierarchy is insightful and valuable. It is particularly helpful when a pathogen is newly emerged, and limited or no knowledge is yet available regarding its level of susceptibility to microbicides [83, 84]. In fact, the United States Environmental Protection Agency [U.S. EPA] and Centers for Disease Control and Prevention [U.S. CDC] use the hierarchy concept as the basis of the Emerging Viral Pathogen Guidance for Antimicrobial Pesticides and public hygiene [10, 82, 85, 86] specifically to deal with just such a possibility.

It should be cautioned, however, that the hierarchy concept is largely oversimplified and by no means perfect [87]. For viruses, although enveloped viruses are usually more susceptible than non-enveloped viruses, certain enveloped viruses such as bovine viral diarrhea virus can be less susceptible than some non-enveloped viruses [e.g., feline calicivirus] under certain chemistries [e.g., low pH and high pH].

The accuracy and applicability of the hierarchy concept are more complex and limited among non-enveloped viruses. The trending is highly dependent on the type of chemistry; and the size of the virion is not always a primary determinant of viral susceptibility among non-enveloped viruses. If a clearer and more consistent trending can be identified among non-enveloped viruses, albeit only specific to a given type of chemistry, the knowledge should be useful.

To generalize an order of susceptibility, for a specific chemistry, data from side-by-side studies wherein viruses are evaluated concurrently by the same test method and under the same conditions should, ideally, be used. When results from different studies are used, caution should be taken to exclude conditional or case-specific differences that result from the test methodology and/or condition. For instance, a surface [carrier] test may give different log10 reduction results than a suspension test of the same microbicide or formulation under certain situations [88]. For example, the data of Kindermann et al. [47] and Tyler et al. [31] indicate that sodium hypochlorite causes a higher log10 reduction value [LRV] when tested in a suspension test than in a surface test. On the other hand, glutaraldehyde has been found to cause similar log reduction in either methodology, while hydrogen peroxide causes higher LRV in the surface test, which is thought to be likely related to the consumption of hydrogen peroxide by the protein in the virus-suspending solution [31].

The organic soil load in which the challenge virus is suspended prior to inoculation can also impact the viral inactivation outcome, especially for oxidizers, alcohols, and QAC. It would be inaccurate or even misleading if a result from a light organic load [e.g., 5% animal serum or phosphate-buffered saline] were to be directly compared with a test that used a heavier organic load [e.g., 90% blood or 20% fecal suspension]. Tung et al. [29] reported that 500 ppm sodium hypochlorite inactivated MNV and FCV by ∼3-log10 in the absence of fecal suspension but only 0–0.5 log10 for these viruses in the presence of 20% fecal suspension.

Other testing conditions may also affect the reduction results. For instance, a higher contact temperature may work in the favor of the virucide under investigation, which may result in a higher log reduction. Nemoto et al. [56] reported that a 0.125% glutaraldehyde solution completely inactivated rotavirus after 10 min under ambient temperature, but not when evaluated on ice. The pH and other components in the product formulation could also affect the viral reduction outcome, presumably by activating the chemical and/or by a synergistic or additive effect between the pH and the active chemical [22, 39, 89]. The efficacy of formulated versus non-formulated microbicides may differ even within the same type and concentration of active[s]. For example, formulated QAC and ethanol products have been reported to exhibit strong activities against certain non-enveloped viruses albeit the efficacy may be weaker for non-formulated solutions [45, 54, 90, 91]. Therefore, the formulation of the microbicidal active must be considered. The viral stock [i.e., inoculum] preparation method and the challenge viral titer may also affect the reported viral reduction efficacy. For example, purified virus may be more susceptible than crude virus preparations [49]; viral clumps can make the virus less susceptible [92]; and a higher viral challenge titer could make the chemical harder to achieve an expected log10 reduction. Sometimes, viruses propagated in different host cell types may behave differently. It would therefore be ideal if all studies could use a standardized viral preparation and infectivity assay protocol. This is, of course, practically challenging. Last, but not least, the method for preparing the microbicide and the verification of the active concentration might also differ from lab to lab, thus potentially influencing the efficacy results obtained.

Despite these practically hard-to-avoid differences in test methodology and conditions, some generalizations on the pattern of susceptibility among non-enveloped viruses can still be made with confidence. For instance, it is quite apparent that the Picornaviridae family of viruses do not always exhibit a similar level of susceptibility to each other [16, 93]; and even the genus is not a good predictor for susceptibility to microbicides within this family. This reflects the ability of certain members of this family to infect the gastrointestinal tract [i.e., enteroviruses], while others infect primarily the respiratory system. The variation of susceptibility within this viral family is particularly striking for ethanol, hydrogen peroxide, QAC, and low pH.

The family Caliciviridae is another example of the existence of unequivocal intrafamily differences in susceptibility to microbicides [16]. For feline calicivirus and murine norovirus [the two most commonly used surrogate viruses for human norovirus], not only can their levels of susceptibility be very different, but the relative order of susceptibility between these two family members can be entirely reversed. For instance, murine norovirus is susceptible to ethanol but not very susceptible to low pH, whereas feline calicivirus is not very susceptible to ethanol but quite susceptible to low pH. For some other types of chemicals, such as peracetic acid and QAC, notable differences in susceptibility to these two viruses are not observed. Given the importance of human norovirus to public health and the lack of a convenient and robust tissue culture model for the virus, a more detailed research and discussion are needed with respect to the choice of feline calicivirus and murine norovirus as the best surrogate for evaluating inactivation products against human norovirus. This topic has been discussed extensively [94, 95, 96].

Different types of adenoviruses seem to exhibit varying degrees of susceptibility to ethanol and QAC. For example, adenovirus type 5 appears to be notably more susceptible to ethanol than are adenovirus types 2 and 8. In general, however, adenoviruses are more susceptible than many other non-enveloped viruses. Considering that adenovirus type 5 is listed as one of the allowable challenge viruses for a generic or “broad-spectrum” virucidal efficacy claim [i.e., a product that is effective for adenovirus type 5 may be considered effective against all viruses] [97, 98], this practice may not represent a challenge and lead to an insufficient safety margin, which is not supported by the published data.

Parvoviruses are among the smallest of non-enveloped viruses. The animal parvoviruses [e.g., minute virus of mice, porcine parvovirus, bovine parvovirus, canine parvovirus, etc.] are considered to exhibit very low susceptibility to chemical inactivation [99] and are commonly used as a worst-case model for viral inactivation studies. This literature review generally supports this notion, although it should be noted that the animal parvoviruses do not appear to represent a worst-case challenge for high-pH inactivation, and porcine parvovirus seems less susceptible than minute virus of mice at times. Additionally, human parvovirus B19 seems especially susceptible to acid treatment [100].

It has been observed that the particle size of a virus is not an exclusive or even a primary determinant of susceptibility to microbicides for non-enveloped viruses, albeit this characteristic may play a role. There are numerous reports demonstrating that larger non-enveloped viruses, such as adenoviruses and reoviruses, are less susceptible than some of the smaller non-enveloped viruses for certain chemistries. Interestingly though, rotavirus, a large non-enveloped virus, indeed seems to be the most susceptible among non-enveloped viruses, except to low pH.

The mechanisms underlying the large variation in susceptibility among non-enveloped viruses and the chemistry dependency are not always clear, but they could presumably be related to the physicochemical properties of the virus as well as the mechanisms of action of the chemical inactivants. For alcohols, for instance, it has been proposed that the hydrophobicity or hydrophilicity of the viral particles is an important determinant of susceptibility [101]. Poliovirus, which is hydrophilic, is more susceptible to ethanol than it is to isopropyl alcohol. This is attributed to the fact that ethanol is more hydrophilic than isopropanol. In comparison, the hydrophobic simian virus 40 is susceptible to isopropanol but not to ethanol [101]. Enterovirus 71 [EV71] and enterovirus EV-D68 [EV-D68] are both enteroviruses in the family Picornaviridae. Despite both infecting the gastrointestinal tract, EV71 displays low susceptibility to low pH, while EV-D68 is acid-labile. This can be explained by the observed acid-induced uncoating for EV-D68 but not for EV71 [67].

A review of the relative order of susceptibility for non-enveloped viruses under each chemistry reveals that the order for some chemicals [e.g. aldehydes] seems to fit the traditional hierarchy concept well [e.g., parvoviruses are less susceptible than larger viruses]; but the order for some other chemistries [e.g., low pH] does not seem to agree with the concept as well.

The variability in viral susceptibility to physical treatments is not covered in this chapter; however, a marked degree of variation also exists for physical treatments, both within non-enveloped viruses and between enveloped and non-enveloped viruses [12, 16, 21, 49]. A comparison of the order of susceptibility of viruses to chemical versus physical treatments and an exploration of the underlying mechanisms would be interesting and revealing.

11. Conclusions

This chapter reviewed the literature on chemical inactivation of non-enveloped viruses, with an emphasis on the relative difference and trending of susceptibility among some relevant [from a public health perspective] non-enveloped viruses under each type of chemistry. The traditional concept of a hierarchy of susceptibility to microbicides provides a useful tool in understanding and predicting the susceptibility of a pathogen; however, the concept tends to be oversimplified. The order of susceptibility among non-enveloped viruses depends on the type of chemistry, and there is no universal order that holds true for all types of chemistries. Picornaviruses and caliciviruses exhibit a particularly high degree of intrafamily variation, and the order may even be reversed between viruses, depending on the chemistry. Additionally, larger non-enveloped viruses are not always more susceptible than some of the smaller non-enveloped viruses. It may be inappropriate to consider adenovirus type 5 as a worst-case non-enveloped virus; and even the animal parvoviruses, universally considered among the least susceptible to chemical inactivation, do not actually represent the least susceptible virus type for certain chemistries.

Acknowledgments

The author thanks Drs. Raymond Nims and M. Khalid Ijaz for the critical review of the manuscript and discussion.

Conflict of interest

The author declares no conflict of interest.

References

  1. 1. Kampf G, Todt D, Pfaender S, Steinmann E. Persistence of coronaviruses on inanimate surfaces and their inactivation with biocidal agents. Journal of Hospital Infection. 2020;104[3]:246-251
  2. 2. Wiggins RC. Prion stability and infectivity in the environment. Neurochemical Results. 2009;34[1]:158-168
  3. 3. Doetsch RN, Cook TM. Introduction to Bacteria and Their Ecobiology. Berlin: Springer Science & Business Media; 1973. ISBN 978-94-015-1137-7
  4. 4. Spaulding EH. Chemical sterilization of surgical instruments. Surgical and Gynecological Observations. 1939;69:738-744
  5. 5. Spaulding EH. Chemical disinfection of medical and surgical materials. In: Lawrence CA, Block SS, editors. Disinfection, Sterilization, and Preservation. Philadelphia: Lea & Febiger; 1968. pp. 517-531
  6. 6. Spaulding EH. Chemical disinfection and antisepsis in the hospital. Journal of Hospital Research. 1972;9:5-31
  7. 7. Russell AD. Bacterial resistance to disinfectants: Present knowledge and future problems. Journal of Hospital Infection. 1998;43:S57-S68
  8. 8. Sattar SA. Hierarchy of susceptibility of viruses to environmental surface disinfectants: A predictor of activity against new and emerging viral pathogens. Journal of the AOAC International. 2007;90[6]:1655-1658
  9. 9. U.S. EPA. Draft White Paper—Consideration of Disinfection Hierarchy Concepts in the Registration of Antimicrobial Products. Washington, USA: US Environmental Protection Agency; 2015
  10. 10. U.S. CDC. Chemical disinfectants—guideline for disinfection and sterilization in healthcare facilities. Atlanta, USA:; U.S. Centers for Disease Control and Prevention; 2008
  11. 11. Rutala WA, Weber DA, HICPAC. Guideline for Disinfection and Sterilization in Healthcare Facilities, 2008. [//www.cdc.gov/hicpac/Disinfection_Sterilization/4_0efficacyDS.html#a2]
  12. 12. Nims R, Plavsic M. Identification of worst-case model viruses for selected viral clearance steps. BioProcessing Journal. 2014;13:6-13
  13. 13. Gelderblom HR. Structure and Classification of Viruses. in Medical Microbiology. 4th ed. Baron S, editor. Galveston: University of Texas Medical Branch at Galveston; 1996
  14. 14. Fauquet CM. Taxonomy, classification and nomenclature of viruses. In: Granoff A, Webster RG, editors. Encyclopedia of Virology. Amsterdam, Netherlands: Elsevier; 1999.1730–1756
  15. 15. ICTV reports on virus taxonomy. //talk.ictvonline.org/ictv-reports/
  16. 16. Nims RW, Zhou SS. Intra-family differences in efficacy of inactivation of small non-enveloped viruses. Biologicals. 2016;44[5]:456-462
  17. 17. Alvarez ME, Brien RT. Mechanisms of inactivation of poliovirus by chlorine dioxide and iodine. Applied and Environmental Microbiology. 1982;44:1064-1071
  18. 18. Bieker JM. Chemical Inactivation of Viruses. Manhattan, Kansas: Kansas State University; 2006. //hdl.handle.net/2097/226
  19. 19. Biering H, Denzin S, von Rheinbaben F, Meyer B. Virucidal Composition. Organization WIP, WO/2008/049454, editor. 2006
  20. 20. Lin Q, Lim JYC, Xue K, Yew PYM, Owh C, Chee PL, et al. Sanitizing agents for virus inactivation and disinfection. Viewpoints. 2020;24:e16
  21. 21. Li JW, Xin ZT, Wang XW, Zheng JL, Chao FH. Mechanisms of inactivation of hepatitis a virus by chlorine. Applied and Environmental Microbiology. 2002;68[10]:4951-4955
  22. 22. Nims R, Zhou SS, Plavsic M. Identification of worst-case model viruses for low and high pH inactivation. Bioprocessing Journal. 2017;16[1]:7-14
  23. 23. Verbund für Angewandte Hygiene [VAH], EV, et al. As a Biocidal Active Substance, Ethanol is Indispensable for Hygienic Hand Disinfection. [Authorized translation]. 29 October 2020, online available from. //vah-online.de/en/. German original to be published in HygMed. 2020;45[11]
  24. 24. Kampf G. Efficacy of ethanol against viruses in hand disinfection. Journal of Hospital Infection. 2018;98[4]:331-338
  25. 25. Edmonds S, McCormack R, Zhou SS, Macinga D, Fricker C. Hand hygiene regimens for the reduction of risk in foodservice environments. Journal of Food Protection. 2012;75[7]:1303-1309
  26. 26. Eterpi M, McDonnell G, Thomas V. Disinfection efficacy against parvoviruses compared with reference viruses. Journal of Hospital Infection. 2009;73[1]:64-70
  27. 27. Chang SC, Li WC, Huang KY, Huang YC, Chiu CH, Chen CJ, et al. Efficacy of alcohols and alcohol-based hand disinfectants against human enterovirus 71. Journal of Hospital Infection. 2013;83[4]:288-293
  28. 28. Abad FX, Pintó RM, Bosch A. Disinfection of human enteric viruses on fomites. FEMS Microbiology Letters. 1997;156:107-111
  29. 29. Tung G, Macinga D, Arbogast J, Jaykus LA. Efficacy of commonly used disinfectants for inactivation of human noroviruses and their surrogates. Journal of Food Protection. 2013;76[7]:1210-1217
  30. 30. Cromeans T, Park GW, Costantini V, Lee D, Wang Q, Farkas T, et al. Comprehensive comparison of cultivable norovirus surrogates in response to different inactivation and disinfection treatments. Applied and Environmental Microbiology. 2014;80[18]:5743-5751
  31. 31. Tyler R, Ayliffe GAJ, Bradley C. Virucidal activity of disinfectants: Studies with the poliovirus. Journal of Hospital Infection. 1990;15:339-345
  32. 32. Park GW, Barclay L, Macinga D, Charbonneau D, Pettigrew CA, Vinjé J. Comparative efficacy of seven hand sanitizers against murine norovirus, feline calicivirus, and GII.4 norovirus. Journal of Food Protection. 2010;73[12]:2232-2238
  33. 33. Uzuner H, Karadenizli A, Er DK, Osmani A. Investigation of the efficacy of alcohol-based solutions on adenovirus serotypes 8, 19 and 37, common causes of epidemic keratoconjunctivitis, after an adenovirus outbreak in hospital. Journal of Hospital Infection. 2018;100[3]:30-36
  34. 34. Rabenau HF, Steinmann J, Rapp I, Schwebke I, Eggers M. Evaluation of a virucidal quantitative carrier test for surface disinfectants. PLoS One. 2014;9[1]:1-10
  35. 35. Wang Y-H, Wang X-L, Song J, Song Q-Q, Luo X-N, Xia D, et al. Inactivation of human rhinovirus due to heat, UV irradiation and chemical disinfectants. Journal of Antivirals and Antiretrovirals. 2017;9[4]:96-101
  36. 36. van Engelenburg FA, Terpstra FG, Schuitemaker H, Moorer WR. The virucidal spectrum of a high concentration alcohol mixture. Journal of Hospital Infection. 2002;51:121-125
  37. 37. von Rheinbaben F, Wolff MH. Handbuch der viruswirksamen Desinfektion. Berlin: Springer Verlag; 2002
  38. 38. Kampf G, Grotheerc D, Steinmann J. Efficacy of three ethanol-based hand rubs against feline calicivirus, a surrogate virus for norovirus. Journal of Hospital Infection. 2005;60[2]:144-149
  39. 39. Harada Y, Lekcharoensuk P, Furuta T, Taniguchi T. Inactivation of foot-and-mouth disease virus by commercially available disinfectants and cleaners. Biocontrol Science. 2015;20[3]:205-208
  40. 40. Kramer A, Galabov AS, Sattar SA, Döhner L, Pivert A, Payan C, et al. Virucidal activity of a new hand disinfectant with reduced ethanol content: Comparison with other alcohol-based formulations. Journal of Hospital Infection. 2006;62[1]:98-106
  41. 41. Steinmann J, Becker B, Bischoff B, Magulski T, Steinmann J, Steinmann E. Virucidal activity of formulation I of the World Health Organization's alcohol-based handrubs: Impact of changes in key ingredient levels and test parameters. Antimicrobial Resistance and Infection Control. 2013;2:34. //www.aricjournal.com/content/2/1/34
  42. 42. Kurtz JB, Lee TW, Parsons AJ. The action of alcohols on rotavirus, astrovirus and enterovirus. Journal of Hospital Infection. 1980;1[4]:321-325
  43. 43. Terpstra FG, van den Blink AE, Bos LM, Boots AGC, Brinkhuis FHM, Gijsen E, et al. Resistance of surface-dried virus to common disinfection procedures. Journal of Hospital Infection. 2007;66 :332-338
  44. 44. Park GW, Sobsey MD. Simultaneous comparison of murine norovirus, feline calicivirus, coliphage MS2, and GII.4 norovirus to evaluate the efficacy of sodium hypochlorite against human norovirus on a fecally soiled stainless steel surface. Foodborne Pathogens and Disease. 2011;8[9]:1005-1010
  45. 45. Sattar SA, Jacobsen H, Springthorpe VS, Cusack TM, Rubino JR. Chemical disinfection to interrupt transfer of rhinovirus type 14 from environmental surfaces to hands. Applied and Environmental Microbiology. 1993;59:1579-1585
  46. 46. Kadurugamuwa JL, Shaheen E. Inactivation of human enterovirus 71 and coxsackie virus A16 and hand, foot, and mouth disease. American Journal of Infection Control. 2011;39[9]:788-789
  47. 47. Kindermann J, Karbiener M, Leydold SM, Knotzer S, Modrof J, Kreil TR. Virus disinfection for biotechnology applications: Different effectiveness on surface versus in suspension. Biologicals. 2020;64:1-9
  48. 48. Poschetto LF, Ike A, Papp T, Mohn U, Böhm R, Marschang RE. Comparison of the sensitivities of noroviruses and feline calicivirus to chemical disinfection under field-like conditions. Applied and Environmental Microbiology. 2007;73[17]:5494-5500
  49. 49. Kiryanova EV, Panteleeva LG, Shirman GA. Inactivation of simian rotavirus SA 11 by hydrogen peroxide. Zentralblatt-fuer-Hygiene-und-Umweltmedizin. 1993;194[3]:301-312
  50. 50. Li D, Baert L, Jonghe MD, Van Coillie E, Ryckeboer J, Devlieghere F, et al. Inactivation of murine norovirus 1, coliphage φX174, and Bacillus fragilis phage B40-8 on surfaces and fresh-cut iceberg lettuce by hydrogen peroxide and UV light. Applied and Environmental Microbiology. 2011;77[4]:1399-1404
  51. 51. Fraisse A, Temmam S, Deboosere N, Guillier L, Delobel A, Maris P, et al. Comparison of chlorine and peroxyacetic-based disinfectant to inactivate feline calicivirus, murine norovirus and hepatitis a virus on lettuce. International Journal of Food Microbiology. 2011;151[1]:98-104
  52. 52. Girard M, Mattison K, Fliss I, Jean J. Efficacy of oxidizing disinfectants at inactivating murine norovirus on ready-to-eat foods. International Journal of Food Microbiology. 2016;219:7-11
  53. 53. Sansebastiano G, Zoni R, Bigliardi L, Ghirardi E, Losio N. Comparative study on HAV and poliovirus 2 inactivation cinetics with peracetic acid. Igiene e Sanita Pubblica. 2003;59[5]:319-329
  54. 54. Gerba CP. Quaternary ammonium biocides: Efficacy in application. Applied and Environmental Microbiology. 2015;81[2]:464-469
  55. 55. Maillard J-V et al. Does microbicide use in consumer products promote antimicrobial resistance? A critical review and recommendations for a cohesive approach to risk assessment. Microbial Drug Resistance. 2013;19[5]:344-354
  56. 56. Nemoto M, Bannai H, Tsujimura K, Yamanaka T, Kondo T. Virucidal effect of commercially available disinfectants on equine group a rotavirus. Journal of Veterinary Medical Science. 2014;76[7]:1061-1063
  57. 57. Romanowski EG, Yates KA, Shanks RM, Kowalski RP. Benzalkonium chloride demonstrates concentration-dependent antiviral activity against adenovirus in vitro. Journal of Ocular Pharmacology and Therapeutics. 2019;35:311-314
  58. 58. Bauman PA, Lawrence LA, Biesert L, Dichtelmüller H, Fabbrizzi F, Gajardo R, et al. Critical factors influencing prion inactivation by sodium hydroxide. Vox Sanguinis. 2006;91[1]:34-40
  59. 59. Sofer G, Lister DC, Boose JA. Inactivation methods grouped by virus. BioPharm International. 2003;6:S37–S42
  60. 60. Yang B, Wang H, Kaleas K, Butler M, Franklin J, Bill A, et al. Clearance of porcine circovirus and porcine parvovirus from porcine-derived pepsin by low pH inactivation and cation exchange chromatography. Biotechnology Progress. 2020;36[4]:e2968
  61. 61. Baylis SA, Tuke PW, Miyagawa E, Blümel J. Studies on the inactivation of human parvovirus 4. Transfusion. 2013;53[10 Pt 2]:2585-2592
  62. 62. Duizer E, Bijkerk P, Rockx B, De Groot A, Twisk F, Koopmans M. Inactivation of caliciviruses. Applied and Environmental Microbiology. 2004;70[8]:4538-4543
  63. 63. Roberts PL, Lloyd D. Virus inactivation by protein denaturants used in affinity chromatography. Biologicals. 2007;35:343-347
  64. 64. Zhou S. unpublished data
  65. 65. Newman JF, Rowlands DJ, Brown F. A physico-chemical sub-grouping of the mammalian picornaviruses. Journal of General Virology. 1973;18[2]:171-180
  66. 66. Boschetti N, Wyss K, Mischler A, Hostettler T, Kempf C. Stability of minute virus of mice against temperature and sodium hydroxide. Biologicals. 2003;31[3]:181-185
  67. 67. Liu Y, Sheng J, van Vliet ALW, Buda G, van Kuppeveld FJM, Rossmann MG. Molecular basis for the acid-initiated uncoating of human enterovirus D68. Proceedings of the National Academy of Sciences [USA]. 2018;115[52]:E12209-E12217
  68. 68. Drulak MW, Wallbank AM, Lebtag I. The effectiveness of six disinfectants in inactivation of reovirus 3. Microbios. 1984;163:31-38
  69. 69. Drulak M, Wallbank AM, Lebtag I, Werboski L, Poffenroth L. The relative effectiveness of commonly used disinfectants in inactivation of coxsackievirus B5. Journal of Hygiene, Cambridge. 1978;81:389-397
  70. 70. Application note: Use of sodium hydroxide for cleaning and sanitizing chromatography media and systems. Amersham Biosciences. 2001;18-1124-57 AD
  71. 71. Borovec S, Broumis C, Adcock W, Fang R, Uren E. Inactivation kinetics of model and relevant blood-borne viruses by treatment with sodium hydroxide and heat. Biologicals. 1998;26[3]:237-244
  72. 72. Jannat R, Hsu D, Maheshwari G. Inactivation of adenovirus type 5 by caustics. Biotechnology Progress. 2005;21[2]:446-450
  73. 73. Maris P, Fresnel R. Activité de divers désinfectants sur sept virus non enveloppés. Annales de Recherches Vétérinaires. 1986;17:433-439
  74. 74. Lukula L, Chiossone C, Fanuel S, Suchmann D, Nims R, Zhou SS. Inactivation and disinfection of porcine parvovirus on a nonporous surface. Journal of Microbial & Biochemical Technology. 2017;9[5]:232-236
  75. 75. Passagot J, Crance JM, Biziagos E, Laveran H, Agbalika F, Deloince R. Effect of glutaraldehyde on the antigenicity and infectivity of hepatitis a virus. Journal of Virological Methods. 1987;16[1–2]:21-28
  76. 76. Bailly JL, Chambon M, Peigue-Lafeuille H, Laveran H, De Champs C, Beytout D. Activity of glutaraldehyde at low concentrations [less than 2%] against poliovirus and its relevance to gastrointestinal endoscope disinfection procedures. Applied and Environmental Microbiology. 1991;57[4]:1156-1160
  77. 77. Möller L, Schünadel L, Nitsche A, Schwebke I, Hanisch M, Laue M. Evaluation of virus inactivation by formaldehyde to enhance biosafety of diagnostic electron microscopy. Viruses. 2015;7[2]:666-679
  78. 78. Nims RW, Plavsic M. Intra-family and inter-family comparisons for viral susceptibility to heat inactivation. Journal of Microbial and Biochemical Technology. 2013;5:136-141
  79. 79. Zhou SS, Wilde C, Chen Z, Kapes T, Purgill J, Nims R, et al. Thermal inactivation of feline calicivirus and herpes simplex virus type 1: Side-By-Side Suspension and Carrier Studies. Integrative Journal of Veterinary Science. 2020;4[1]:1–6. DOI: 10.31038/IJVB.2020411
  80. 80. Zhou SS, Wilde C, Chen Z, Kapes T, Purgill J, Nims R, et al. Carrier and liquid heat inactivation of poliovirus and adenovirus. In: Disinfection. London: IntechOpen; 2018. ISBN 978-953-51-6084-7
  81. 81. Lin CS, Fuller J, Mayhall ES. Federal regulation of liquid chemical germicides by the U.S. Food and Drug Administration. In: Block S, editor. Disinfection, Sterilization, and Preservation. 5th ed. Philadelphia: Lippencott, Williams and Wilkens. 2001. pp. 881–917
  82. 82. U.S. Environmental Protection Agency. Guidance to Registrants: Process for Making Claims against Emerging Viral Pathogens not on EPA-registered Disinfectant Labels. 2016. //www.epa.gov/sites/default/files/2016-09/documents/emerging_viral_pathogen_program_guidance_final_8_19_16_001_0.pdf
  83. 83. Ijaz MK, Nims RW, Cutts TA, McKinney J, Gerba CP. Predicted and measured virucidal efficacy of microbicides for emerging/and re-emerging viruses associated with WHO priority diseases. In: Disinfection of Viruses. London: InTech Open; in press
  84. 84. Ijaz MK, Sattar SA, Rubino JR, Nims RW, Gerba CP. Combating SARS-CoV-2: Leveraging microbicidal experiences with other emerging/re-emerging viruses. PeerJ. 2020;8:e9914. DOI: 10.7717/peerj.9914
  85. 85. U.S. Environmental Protection Agency. Emerging Viral Pathogen Guidance for Antimicrobial Pesticides. //www.epa.gov/pesticide-registration/emerging-viral-pathogen-guidance-antimicrobial-pesticides. 2021
  86. 86. U.S. EPA, Final Summary of the Disinfection Hierarchy Workshop. US Environmental Protection Agency. USA: Washington; 2016
  87. 87. Disinfection: Is it time to reconsider Spaulding? Journal of Hospital Infection. 2011;78:163-170
  88. 88. Ijaz MK, Rubino JR. Should test methods for disinfectants use vertebrate virus dried on carriers to advance virucidal claims? Infection Control and Hospital Epidemiology. 2008;29[2]:192-194
  89. 89. Vaughn JM, Chen YS, et al. Inactivation of human and simian rotaviruses by chlorine. Applied and Environmental Microbiology. 1986;51[2]:391-394
  90. 90. Sattar SA, Jacobsen H, Rahman H, Cusack TM, Rubino JR. Interruption of rotavirus spread through chemical disinfection. Infection Control and Hospital Epidemiology. 1994;15[12]:751-756
  91. 91. Macinga DR, Sattar SA, Jaykus L-A, Arbogast JW. Improved inactivation of nonenveloped enteric viruses and their surrogates by a novel alcohol-based hand sanitizer. Applied and Environmental Microbiology. 2008;74[16]:5047-5052
  92. 92. Gerba CP, Betancourt WQ. Viral aggregation: Impact on virus behavior in the environment. Environmental Science & Technology. 2017;51[13]:7318-7325
  93. 93. Su Y, Han J, Li J, Ren Z, Huang L, Xu B, et al. Resistance of poliovirus 1 and enterovirus A71 against alcohol and other disinfectants. Journal of Virological Methods. 2021;298:114292. DOI: 10.1016/j.jviromet.2021.114292
  94. 94. Nims R, Plavsic M. Inactivation of caliciviruses. Pharmaceuticals. 2013;6:358-392
  95. 95. Cannon JL, Papafragkou E, Park GW, Osborne J, Jaykus LA, Vinjé J. Surrogates for the study of norovirus stability and inactivation in the environment: A comparison of murine norovirus and feline calicivirus. Journal of Food Protection. 2006;69[11]:2761-2765
  96. 96. Hoelzer K, Fanaselle W, Pouillot R, Van Doren JM, Dennis S. Virus inactivation on hard surfaces or in suspension by chemical disinfectants: Systematic review and meta-analysis of norovirus surrogates. Journal of Food Protection. 2013;76[6]:1006-1016
  97. 97. Health Canada. Guidance document—Safety and Efficacy Requirements for Hard Surface Disinfectant Drugs. 2014. //www.canada.ca/en/health-canada/services/drugs-health-products/drug-products/applications-submissions/guidance-documents/disinfectants/safety-efficacy-requirements-hard-surface-disinfectant-drugs.html
  98. 98. EN 14476:2013+A2:2019[E]. Chemical disinfectants and antiseptics—Quantitative suspension test for the evaluation of virucidal activity in the medical area—Test method and requirements [Phase 2/Step 1]. European Standard, July 2019
  99. 99. United States Pharmacopeia . Design, evaluation, and characterization of viral clearance procedures
  100. 100. Boschetti N, Niederhauser I, Kempf C, Stühler A, Löwer J, Blümel J. Different susceptibility of B19 virus and mice minute virus to low pH treatment. Transfusion. 2004;44[7]:1079-1086
  101. 101. Ionidis G, Hübscher J, Jack T, Becker B, Bischoff B, Todt D, et al. Development and virucidal activity of a novel alcohol-based hand disinfectant supplemented with urea and citric acid. BMC Infectious Diseases. 2016;16 :77. DOI: 10.1186/s12879-016-1410-9

Written By

Sifang Steve Zhou

Submitted: December 6th, 2021 Reviewed: January 17th, 2022 Published: March 22nd, 2022

© 2022 The Author[s]. Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution 3.0 License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

What is the main structural difference between enveloped and Nonenveloped?

One of the major and best-known virus classifications is the separation of enveloped from non-enveloped viruses. In general, what distinguishes them is the presence [for enveloped viruses] or absence [for non-enveloped viruses] of a lipid bilayer membrane on the outer part of the virus.

What are the main structural components of an enveloped virus?

In enveloped viruses, the nucleocapsid is surrounded by a lipid bilayer derived from the modified host cell membrane and studded with an outer layer of virus envelope glycoproteins.

What is the general structure of both enveloped and non

Non-enveloped viruses are composed of capsid protein and nucleic acid [DNA or RNA], viz. nucleocapsid., which constitute an infectious unit, the virion, whereas enveloped viruses are composed of an envelope and nucleocapsid.

What is different about enveloped viruses?

Viruses are either enveloped or non-enveloped. Enveloped viruses contain the viral genome and core proteins wrapped within one or more membranes. These membranes are acquired from the host cell during virus assembly and budding [166].

Bài Viết Liên Quan

Chủ Đề