Common families of human and animal non-enveloped viruses.
\\n\\n
Released this past November, the list is based on data collected from the Web of Science and highlights some of the world’s most influential scientific minds by naming the researchers whose publications over the previous decade have included a high number of Highly Cited Papers placing them among the top 1% most-cited.
\\n\\nWe wish to congratulate all of the researchers named and especially our authors on this amazing accomplishment! We are happy and proud to share in their success!
Note: Edited in March 2021
\\n"}]',published:!0,mainMedia:{caption:"Highly Cited",originalUrl:"/media/original/117"}},components:[{type:"htmlEditorComponent",content:'IntechOpen is proud to announce that 191 of our authors have made the Clarivate™ Highly Cited Researchers List for 2020, ranking them among the top 1% most-cited.
\n\nThroughout the years, the list has named a total of 261 IntechOpen authors as Highly Cited. Of those researchers, 69 have been featured on the list multiple times.
\n\n\n\nReleased this past November, the list is based on data collected from the Web of Science and highlights some of the world’s most influential scientific minds by naming the researchers whose publications over the previous decade have included a high number of Highly Cited Papers placing them among the top 1% most-cited.
\n\nWe wish to congratulate all of the researchers named and especially our authors on this amazing accomplishment! We are happy and proud to share in their success!
Note: Edited in March 2021
\n'}],latestNews:[{slug:"webinar-introduction-to-open-science-wednesday-18-may-1-pm-cest-20220518",title:"Webinar: Introduction to Open Science | Wednesday 18 May, 1 PM CEST"},{slug:"step-in-the-right-direction-intechopen-launches-a-portfolio-of-open-science-journals-20220414",title:"Step in the Right Direction: IntechOpen Launches a Portfolio of Open Science Journals"},{slug:"let-s-meet-at-london-book-fair-5-7-april-2022-olympia-london-20220321",title:"Let’s meet at London Book Fair, 5-7 April 2022, Olympia London"},{slug:"50-books-published-as-part-of-intechopen-and-knowledge-unlatched-ku-collaboration-20220316",title:"50 Books published as part of IntechOpen and Knowledge Unlatched (KU) Collaboration"},{slug:"intechopen-joins-the-united-nations-sustainable-development-goals-publishers-compact-20221702",title:"IntechOpen joins the United Nations Sustainable Development Goals Publishers Compact"},{slug:"intechopen-signs-exclusive-representation-agreement-with-lsr-libros-servicios-y-representaciones-s-a-de-c-v-20211123",title:"IntechOpen Signs Exclusive Representation Agreement with LSR Libros Servicios y Representaciones S.A. de C.V"},{slug:"intechopen-expands-partnership-with-research4life-20211110",title:"IntechOpen Expands Partnership with Research4Life"},{slug:"introducing-intechopen-book-series-a-new-publishing-format-for-oa-books-20210915",title:"Introducing IntechOpen Book Series - A New Publishing Format for OA Books"}]},book:{item:{type:"book",id:"7003",leadTitle:null,fullTitle:"Herbs and Spices",title:"Herbs and Spices",subtitle:null,reviewType:"peer-reviewed",abstract:"This edited volume, “Herbs and Spices”, is a collection of reviewed and relevant research chapters, offering a comprehensive overview of recent developments in the field of agricultural and biological sciences. The book comprises single chapters authored by various researchers and edited by an expert active in the medical research area. All chapters are complete in itself but united under a common research study topic. This publication aims at providing a thorough overview of the latest research efforts by international authors on herbs and spices, and opening new possible research paths for further novel developments.",isbn:"978-1-83962-936-5",printIsbn:"978-1-83962-935-8",pdfIsbn:"978-1-83962-937-2",doi:"10.5772/intechopen.73759",price:119,priceEur:129,priceUsd:155,slug:"herbs-and-spices",numberOfPages:112,isOpenForSubmission:!1,isInWos:null,isInBkci:!1,hash:"1f33df17010fa5e54988c44e32db2b40",bookSignature:"Muhammad Akram and Rabia Shabir Ahmad",publishedDate:"October 7th 2020",coverURL:"https://cdn.intechopen.com/books/images_new/7003.jpg",numberOfDownloads:4506,numberOfWosCitations:6,numberOfCrossrefCitations:2,numberOfCrossrefCitationsByBook:0,numberOfDimensionsCitations:10,numberOfDimensionsCitationsByBook:0,hasAltmetrics:1,numberOfTotalCitations:18,isAvailableForWebshopOrdering:!0,dateEndFirstStepPublish:"October 29th 2019",dateEndSecondStepPublish:"March 13th 2020",dateEndThirdStepPublish:"May 12th 2020",dateEndFourthStepPublish:"July 31st 2020",dateEndFifthStepPublish:"September 29th 2020",currentStepOfPublishingProcess:5,indexedIn:"1,2,3,4,5,6",editedByType:"Edited by",kuFlag:!1,featuredMarkup:null,editors:[{id:"275728",title:"Dr.",name:"Muhammad",middleName:null,surname:"Akram",slug:"muhammad-akram",fullName:"Muhammad Akram",profilePictureURL:"https://mts.intechopen.com/storage/users/275728/images/system/275728.jpg",biography:"Muhammad Akram is currently working as the Chairperson and Associate Professor at the Government College University Faisalabad, Pakistan. He obtained his PhD degree in Eastern Medicine from Humdard University, Pakistan. He is serving as an Mphil and PhD supervisor. He has published 151 journal papers, 11 books, and 10 book chapters. He has attended national and international conferences as speaker. He is currently serving as a reviewer and editorial board member of multiple reputed high impact factor journals. His research interests include: phytochemistry, bioactivity, and phytopharmaceutical evaluation of herbs, medicinal plants, biochemistry and bioinformatics. Currently, he is serving as a potential member of national and international scientific committees.",institutionString:"Government College University Faisalabad",position:null,outsideEditionCount:0,totalCites:0,totalAuthoredChapters:"3",totalChapterViews:"0",totalEditedBooks:"1",institution:{name:"Government College University, Faisalabad",institutionURL:null,country:{name:"Pakistan"}}}],equalEditorOne:null,equalEditorTwo:null,equalEditorThree:null,coeditorOne:{id:"239057",title:"Dr.",name:"Rabia Shabir",middleName:null,surname:"Ahmad",slug:"rabia-shabir-ahmad",fullName:"Rabia Shabir Ahmad",profilePictureURL:"https://mts.intechopen.com/storage/users/239057/images/system/239057.jpg",biography:"Dr. Rabia Shabir Ahmad has a strong background in academics, teaching, and research. She successfully completed doctoral research funded by the Indigenous Fellowship Program, Higher Education Commission (HEC), Pakistan. During her academic career, Dr. Ahmad was awarded and successfully completed a Start-Up Research Grant Program (SRGP) and National Research Program for Universities (NRPU) project from the HEC as Principal Investigator in the area of functional foods. Along with her teaching and research supervising responsibilities, Dr. Ahmad is also a journal reviewer. She has published numerous research papers in international and national journals and edited several books.",institutionString:"Government College University, Faisalabad",position:null,outsideEditionCount:0,totalCites:0,totalAuthoredChapters:"5",totalChapterViews:"0",totalEditedBooks:"1",institution:{name:"Government College University, Faisalabad",institutionURL:null,country:{name:"Pakistan"}}},coeditorTwo:null,coeditorThree:null,coeditorFour:null,coeditorFive:null,topics:[{id:"369",title:"Pharmacology",slug:"agricultural-and-biological-sciences-plant-biology-pharmacology"}],chapters:[{id:"73211",title:"Introductory Chapter: Mentha piperita (a Valuable Herb): Brief Overview",doi:"10.5772/intechopen.93627",slug:"introductory-chapter-em-mentha-piperita-em-a-valuable-herb-brief-overview",totalDownloads:529,totalCrossrefCites:0,totalDimensionsCites:0,hasAltmetrics:0,abstract:null,signatures:"Rabia Shabir Ahmad, Ali Imran, Muhammad Sajid Arshad, Muhammad Bilal Hussain, Marwa Waheed, Saira Safdar and Zarina Yasmin",downloadPdfUrl:"/chapter/pdf-download/73211",previewPdfUrl:"/chapter/pdf-preview/73211",authors:[{id:"239057",title:"Dr.",name:"Rabia Shabir",surname:"Ahmad",slug:"rabia-shabir-ahmad",fullName:"Rabia Shabir Ahmad"},{id:"192998",title:"Dr.",name:"Muhammad Sajid",surname:"Arshad",slug:"muhammad-sajid-arshad",fullName:"Muhammad Sajid Arshad"},{id:"243634",title:"Mr.",name:"Muhammad Bilal",surname:"Hussain",slug:"muhammad-bilal-hussain",fullName:"Muhammad Bilal Hussain"},{id:"248687",title:"Ms.",name:"Marwa",surname:"Waheed",slug:"marwa-waheed",fullName:"Marwa Waheed"},{id:"329114",title:"Dr.",name:"Ali",surname:"Imran",slug:"ali-imran",fullName:"Ali Imran"},{id:"329115",title:"Dr.",name:"Saira",surname:"Safdar",slug:"saira-safdar",fullName:"Saira Safdar"},{id:"329116",title:"Dr.",name:"Zarina",surname:"Yasmin",slug:"zarina-yasmin",fullName:"Zarina Yasmin"}],corrections:null},{id:"71092",title:"Role of Herbs and Medicinal Spices as Modulators of Gut Microbiota",doi:"10.5772/intechopen.91208",slug:"role-of-herbs-and-medicinal-spices-as-modulators-of-gut-microbiota",totalDownloads:902,totalCrossrefCites:2,totalDimensionsCites:3,hasAltmetrics:1,abstract:"Currently, herbs, medicinal spices, green medicine, or traditional Chinese medicine has gained many followers in the world, especially as a way of life and as an alternative to the indiscriminate use of synthetic medicines such as antibiotics. These natural products are rich in secondary metabolites or phytochemicals, which are chemical compounds of relatively complex structures and restricted distribution; these compounds have defensive functions against insects, bacteria, fungi, parasites, and viruses. Likewise, several studies have shown their effectiveness in the prevention and treatment of several diseases such as cancer, autoimmune diseases, gastrointestinal diseases, diabetes, neurodegenerative diseases, Crohn’s disease, and human immunodeficiency virus (HIV), among others. In addition, this review addresses the mechanisms of action of the herbs and medicinal spices on intestinal microbiota, increasing competitive exclusion in the intestinal membrane and inhibiting bacterial translocation and damage to the intestinal barrier.",signatures:"Yordan Martínez and Dairon Más",downloadPdfUrl:"/chapter/pdf-download/71092",previewPdfUrl:"/chapter/pdf-preview/71092",authors:[{id:"262165",title:"Ph.D.",name:"Yordan",surname:"Martínez",slug:"yordan-martinez",fullName:"Yordan Martínez"},{id:"316635",title:"MSc.",name:"Dairon",surname:"Más",slug:"dairon-mas",fullName:"Dairon Más"}],corrections:null},{id:"72879",title:"Study Biochemistry of Mentha longifolia (L.) Huds.: A Review",doi:"10.5772/intechopen.92732",slug:"study-biochemistry-of-em-mentha-longifolia-em-l-huds-a-review",totalDownloads:439,totalCrossrefCites:0,totalDimensionsCites:0,hasAltmetrics:0,abstract:"The Mentha longifolia were found to be a rich source of phytochemical compounds like piperitone, piperitone oxide, piperitenone, pulegone, d-limonene, menthone, carvone, menthol, β-caryophyllene, 1,8-cineole, 5,7,4-trihydroxy-6,2,3-trimethoxyflavone, carvone, limonene, tripal, and oxathiane. Mentha longifolia possess antioxidant effect that could be attributed to the presence of phytosterosls, unsaturated fatty acids, phenolic compounds, and specific volatile constituents and antimicrobial and interfere in the treatment of many diseases.",signatures:"Sadeq Sabeeh Kareem Al-Taie and Noor Falah Mahde Al-Kenane",downloadPdfUrl:"/chapter/pdf-download/72879",previewPdfUrl:"/chapter/pdf-preview/72879",authors:[{id:"313796",title:"M.Sc.",name:"Sadeq",surname:"Altaie",slug:"sadeq-altaie",fullName:"Sadeq Altaie"},{id:"320357",title:"Dr.",name:"Noor Falah Mahde",surname:"AL-Kenane",slug:"noor-falah-mahde-al-kenane",fullName:"Noor Falah Mahde AL-Kenane"}],corrections:null},{id:"72252",title:"Rhus coriaria (Sumac): A Magical Spice",doi:"10.5772/intechopen.92676",slug:"-em-rhus-coriaria-em-sumac-a-magical-spice",totalDownloads:682,totalCrossrefCites:0,totalDimensionsCites:2,hasAltmetrics:1,abstract:"Rhus coriaria L. (Sumac) has been used as folk medicine since ancient times. Rhus genus has over 91 of accepted species names in the Anacardiaceae family, Rhus coriaria L. is the only species in Iraq that growth wildly and/or cultivated near the villages in the north of Iraq. It has a characteristic taste and morphological features, making it to be considered as one of the popular flavoring spice, drink, appetizer, and as acidulant in food recipes, in addition to its role as plant medicine. A scrutiny of literature revealed some notable pharmacological activities of the plant such as antioxidant, anti-ischemic, antimicrobial as well as hypoglycemic and hypolipidimic effects. This chapter attempts to comprise the published obtainable literatures on Rhus coriaria with respect to its pharmacognostic characters, ethanobotanical/traditional uses, chemical constituents and summary of its various pharmacological activities, clinical effects, functional food industries and dentistry.",signatures:"Thukaa Zuhair Abdul-Jalil",downloadPdfUrl:"/chapter/pdf-download/72252",previewPdfUrl:"/chapter/pdf-preview/72252",authors:[{id:"315105",title:"Ph.D.",name:"Thukaa",surname:"Abdul-Jalil",slug:"thukaa-abdul-jalil",fullName:"Thukaa Abdul-Jalil"}],corrections:null},{id:"72203",title:"An Overview of Genus Zanthoxylum with Special Reference to Its Herbal Significance and Application",doi:"10.5772/intechopen.92459",slug:"an-overview-of-genus-em-zanthoxylum-em-with-special-reference-to-its-herbal-significance-and-applica",totalDownloads:444,totalCrossrefCites:0,totalDimensionsCites:3,hasAltmetrics:0,abstract:"The plants of genus Zanthoxylum are effectually utilized in conventional and present-day medicine system to fight many diseases and disorders like pain, seizures, inflammation, cancer, liver and heart malady. Many of its plants—trees and shrubs, are citrus in nature, with curative antimicrobial, antihelminthic, antipyretic, and antiviral activities. More than 100 of its plant species have been identified and recorded for their potential as an herb in modern pharmacopeia. The species of this genus also have potent ethno-pharmacological significance. Many medicinal secondary metabolites like terpenoids, flavonoids, and alkaloids have also been profiled in many Zanthoxylum species. Additionally, fruit of many of the species is also significantly utilized as a major spice under the name “Sichuan pepper” in many countries like China and India. Thus, this unique blend of herb and spice characteristic of the genus needs a detailed description. This chapter highlights the major significant discoveries in the recent decade in this genus, which can add a step in the way of development of herbal medicines. Documentation of such medicinal plants may aid in derivation of plant-based medicines, which is the demand of the hour.",signatures:"Gyanmani Ekka, Shailesh Kumar Jadhav and Afaque Quraishi",downloadPdfUrl:"/chapter/pdf-download/72203",previewPdfUrl:"/chapter/pdf-preview/72203",authors:[{id:"315637",title:"Dr.",name:"Afaque",surname:"Quraishi",slug:"afaque-quraishi",fullName:"Afaque Quraishi"},{id:"318422",title:"Ms.",name:"Gyanmani",surname:"Ekka",slug:"gyanmani-ekka",fullName:"Gyanmani Ekka"},{id:"318423",title:"Prof.",name:"S.K.",surname:"Jadhav",slug:"s.k.-jadhav",fullName:"S.K. Jadhav"}],corrections:null},{id:"72150",title:"Metabolomics",doi:"10.5772/intechopen.92423",slug:"metabolomics",totalDownloads:474,totalCrossrefCites:0,totalDimensionsCites:1,hasAltmetrics:0,abstract:"The aim of this chapter is to make a brief understanding on Metabolomics identification, extraction, and analysis techniques. As the name suggests, Metabolomics is the study of metabolites present in the body fluid (blood, plasma, urine, and saliva) or body parts (muscles, bone, tissue, and cells). These might be known metabolites or unknown metabolites. The metabolites can be endogenous (present in the body) or exogenous (formed by consuming external medicinal product). The molecular mass of these metabolites is usually lower (50–1500 Dalton) than the proteins and macromolecules. These metabolites can be extracted using various techniques such as solid phase extraction, liquid-liquid extraction, or simple protein precipitation. Extracted sample of metabolite then can be analyzed qualitatively or quantitatively using numerous analytical techniques such as high performance liquid chromatography (HPLC), liquid chromatography mass spectrometry (LC–MS/MS), dry blood spot (DBS), infrared (IR) spectroscopy, ultraviolet visible (UV) spectroscopy, nuclear magnetic resonance (NMR), ELISA, and chemiluminescence. Sensitivity of detection is the key factor, among many others, to decide which technique would be suitable for analysis. Liquid chromatography mass spectrometry (LC–MS/MS) is the latest and most sensitive technique among all the available methodology till date that has been extensively and exclusively used in current scenario.",signatures:"Naveen Kumar Dubey",downloadPdfUrl:"/chapter/pdf-download/72150",previewPdfUrl:"/chapter/pdf-preview/72150",authors:[{id:"291419",title:"Dr.",name:"Naveen",surname:"Kumar Dubey",slug:"naveen-kumar-dubey",fullName:"Naveen Kumar Dubey"}],corrections:null},{id:"72371",title:"The Antibacterial Activity of Mentha",doi:"10.5772/intechopen.92425",slug:"the-antibacterial-activity-of-em-mentha-em-",totalDownloads:670,totalCrossrefCites:0,totalDimensionsCites:1,hasAltmetrics:0,abstract:"The topic of this chapter is the antibacterial activity of Mentha against several pathogenic bacteria. Some aromatic plants are recently being studied for their antibacterial properties, such as citrus essential oils, Armoracia rusticana, etc., showing inhibition against bacteria, fungi and yeasts. This chapter highlights the antibacterial characteristics of Mentha piperita (peppermint) and other Mentha sp. that are used daily as folk remedies and in food industry too. Mentha acts as counterirritant and analgesic with the ability to reduce pain and improve blood flow to the affected area. For these reasons, mint essential oils are well studied due to their antibacterial activities against both Gram-negative and Gram-positive ones and can be useful as a substitute to some antibiotics and combat the antimicrobial bacterial resistance.",signatures:"Monique Mancuso",downloadPdfUrl:"/chapter/pdf-download/72371",previewPdfUrl:"/chapter/pdf-preview/72371",authors:[{id:"318562",title:"Dr.",name:"Monique",surname:"Mancuso",slug:"monique-mancuso",fullName:"Monique Mancuso"}],corrections:null},{id:"72037",title:"Determination of In Vitro Antiprotease, Antimicrobial, and Antibiofilm Activities of Beta vulgaris var. cicla against Multidrug-Resistant Strains of Pseudomonas aeruginosa",doi:"10.5772/intechopen.92370",slug:"determination-of-in-vitro-antiprotease-antimicrobial-and-antibiofilm-activities-of-em-beta-vulgaris-",totalDownloads:369,totalCrossrefCites:0,totalDimensionsCites:0,hasAltmetrics:0,abstract:"Antibiotic resistance of Pseudomonas aeruginosa causes many infectious diseases and it is agreat. So, the aim of the present work was to assess the antibacterial, antibiofilm activity of Beta vulgaris extracts against resistance bacteria P. aeruginosa that were clinically isolated and tested for their antiprotease potential. Result showed that methanol extract exhibited important antiprotease activity against Trypsin, Savinase, and digestive proteases of blue crab with percentage of inhibition of 94.66, 91.39, and 86.41%, respectively. It showed also important antibiofilm activities against multidrug-resistant P. aeruginosa with inhibition values upper than 80% with a concentration of 4MIC. Our investigation delivered that Beta vulgaris might be possible source of natural antienzymatic, antimicrobial, and antibiofilm agents.",signatures:"Hayet Edziri, Rim Nasri, Marwa Hamdi and Maha Mastouri",downloadPdfUrl:"/chapter/pdf-download/72037",previewPdfUrl:"/chapter/pdf-preview/72037",authors:[{id:"316024",title:"Dr.",name:"Edziri",surname:"Hayet",slug:"edziri-hayet",fullName:"Edziri Hayet"},{id:"320785",title:"Dr.",name:"Rim",surname:"Nasri",slug:"rim-nasri",fullName:"Rim Nasri"},{id:"320786",title:"Dr.",name:"Marwa",surname:"Hamdi",slug:"marwa-hamdi",fullName:"Marwa Hamdi"},{id:"320787",title:"Dr.",name:"Maha",surname:"Mastouri",slug:"maha-mastouri",fullName:"Maha Mastouri"}],corrections:null}],productType:{id:"1",title:"Edited Volume",chapterContentType:"chapter",authoredCaption:"Edited by"},subseries:null,tags:null},relatedBooks:[{type:"book",id:"5680",title:"Licorice Ingredients",subtitle:"Biological Activities and Action Mechanisms of",isOpenForSubmission:!1,hash:"c46b16db49ffe04f604e0ba00134cd24",slug:"biological-activities-and-action-mechanisms-of-licorice-ingredients",bookSignature:"Hiroshi Sakagami",coverURL:"https://cdn.intechopen.com/books/images_new/5680.jpg",editedByType:"Edited by",editors:[{id:"82603",title:"Prof.",name:"Hiroshi",surname:"Sakagami",slug:"hiroshi-sakagami",fullName:"Hiroshi Sakagami"}],equalEditorOne:null,equalEditorTwo:null,equalEditorThree:null,productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"1591",title:"Infrared Spectroscopy",subtitle:"Materials Science, Engineering and Technology",isOpenForSubmission:!1,hash:"99b4b7b71a8caeb693ed762b40b017f4",slug:"infrared-spectroscopy-materials-science-engineering-and-technology",bookSignature:"Theophile Theophanides",coverURL:"https://cdn.intechopen.com/books/images_new/1591.jpg",editedByType:"Edited by",editors:[{id:"37194",title:"Dr.",name:"Theophile",surname:"Theophanides",slug:"theophile-theophanides",fullName:"Theophile Theophanides"}],equalEditorOne:null,equalEditorTwo:null,equalEditorThree:null,productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"3161",title:"Frontiers in Guided Wave Optics and Optoelectronics",subtitle:null,isOpenForSubmission:!1,hash:"deb44e9c99f82bbce1083abea743146c",slug:"frontiers-in-guided-wave-optics-and-optoelectronics",bookSignature:"Bishnu Pal",coverURL:"https://cdn.intechopen.com/books/images_new/3161.jpg",editedByType:"Edited by",editors:[{id:"4782",title:"Prof.",name:"Bishnu",surname:"Pal",slug:"bishnu-pal",fullName:"Bishnu Pal"}],equalEditorOne:null,equalEditorTwo:null,equalEditorThree:null,productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"3092",title:"Anopheles mosquitoes",subtitle:"New insights into malaria vectors",isOpenForSubmission:!1,hash:"c9e622485316d5e296288bf24d2b0d64",slug:"anopheles-mosquitoes-new-insights-into-malaria-vectors",bookSignature:"Sylvie Manguin",coverURL:"https://cdn.intechopen.com/books/images_new/3092.jpg",editedByType:"Edited by",editors:[{id:"50017",title:"Prof.",name:"Sylvie",surname:"Manguin",slug:"sylvie-manguin",fullName:"Sylvie Manguin"}],equalEditorOne:null,equalEditorTwo:null,equalEditorThree:null,productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"371",title:"Abiotic Stress in Plants",subtitle:"Mechanisms and Adaptations",isOpenForSubmission:!1,hash:"588466f487e307619849d72389178a74",slug:"abiotic-stress-in-plants-mechanisms-and-adaptations",bookSignature:"Arun Shanker and B. 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Bushe and John Pendlebury",reviewType:"peer-reviewed",authors:[{id:"52184",title:"Dr.",name:null,middleName:null,surname:"Bushe",fullName:"Bushe",slug:"bushe"},{id:"53918",title:"Mr.",name:"John",middleName:null,surname:"Pendlebury",fullName:"John Pendlebury",slug:"john-pendlebury"}]},{id:"25001",type:"chapter",title:"Tolerance to Tick-Borne Diseases in Sheep: Highlights of a Twenty-Year Experience in a Mediterranean Environment",slug:"tolerance-to-tick-borne-diseases-in-sheep-highlights-of-a-twenty-year-experience-in-a-mediterranean-",totalDownloads:1871,totalCrossrefCites:2,signatures:"Elisa Pieragostini, Elena Ciani, Giuseppe Rubino and Ferruccio Petazzi",reviewType:"peer-reviewed",authors:[{id:"51521",title:"Prof.",name:"Elisa",middleName:null,surname:"Pieragostini",fullName:"Elisa Pieragostini",slug:"elisa-pieragostini"},{id:"55877",title:"Dr.",name:"Elena",middleName:null,surname:"Ciani",fullName:"Elena Ciani",slug:"elena-ciani"},{id:"55878",title:"Dr.",name:"Giuseppe",middleName:null,surname:"Rubino",fullName:"Giuseppe Rubino",slug:"giuseppe-rubino"},{id:"55879",title:"Prof.",name:"Ferruccio",middleName:null,surname:"Petazzi",fullName:"Ferruccio Petazzi",slug:"ferruccio-petazzi"}]},{id:"25002",type:"chapter",title:"The Foragining Ecology of the Green Turtle in the Baja California Peninsula: Health Issues",slug:"the-foragining-ecology-of-the-green-turtle-in-the-baja-california-peninsula-health-issues",totalDownloads:2411,totalCrossrefCites:0,signatures:"Rafael Riosmena-Rodriguez, Ana Luisa Talavera-Saenz, Gustavo Hinojosa-Arango, Mónica Lara-Uc and Susan Gardner",reviewType:"peer-reviewed",authors:[{id:"36024",title:"Dr.",name:"Rafael",middleName:null,surname:"Riosmena-Rodriguez",fullName:"Rafael Riosmena-Rodriguez",slug:"rafael-riosmena-rodriguez"},{id:"56096",title:"Dr.",name:"Susan",middleName:null,surname:"Gardner",fullName:"Susan Gardner",slug:"susan-gardner"},{id:"56104",title:"Dr.",name:"Gustavo",middleName:null,surname:"Hinojosa-Arango",fullName:"Gustavo Hinojosa-Arango",slug:"gustavo-hinojosa-arango"},{id:"56105",title:"Dr.",name:"Ana Luisa",middleName:null,surname:"Talavera-Saenz",fullName:"Ana Luisa Talavera-Saenz",slug:"ana-luisa-talavera-saenz"},{id:"56106",title:"Dr.",name:"Monica",middleName:null,surname:"Lara-Uc",fullName:"Monica Lara-Uc",slug:"monica-lara-uc"}]}]},relatedBooks:[{type:"book",id:"5115",title:"Health Management",subtitle:null,isOpenForSubmission:!1,hash:"6af1c688ae4cf514c5c3ed6e801f6725",slug:"health-management",bookSignature:"Krzysztof Smigorski",coverURL:"https://cdn.intechopen.com/books/images_new/5115.jpg",editedByType:"Edited by",editors:[{id:"12528",title:"Dr.",name:"Krzysztof",surname:"Smigorski",slug:"krzysztof-smigorski",fullName:"Krzysztof Smigorski"}],equalEditorOne:null,equalEditorTwo:null,equalEditorThree:null,productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"},chapters:[{id:"11519",title:"The PRISMA France Study: Is There a Way to Measure Implementation of Integration in Different Countries?",slug:"the-prisma-france-study-is-there-a-way-to-measure-implementation-of-integration-in-different-countri",signatures:"Trouve H., Veil A., Hebert R. and Somme D.",authors:[null]},{id:"11527",title:"A Proposed Care Model for Complex Chronic Condition: Multiple Chemical Sensitivity",slug:"a-proposed-model-of-care-management-for-complex-chronic-conditions-based-on-the-multidisciplinary-ca",signatures:"Roy Fox, Tara Sampalli and Jonathan Fox",authors:[null]},{id:"11528",title:"Pain Experience and Expression in Patients with Dementia",slug:"the-experience-and-expression-of-pain-in-patients-with-dementia",signatures:"Krzysztof Smigorski and Jerzy Leszek",authors:[null]},{id:"11529",title:"Treatment of Childhood Pneumonia in Developing Countries",slug:"treatment-of-childhood-pneumonia-in-developing-countries",signatures:"Hasan Ashraf, Mohammud Jobayer Chisti and Nur Haque Alam",authors:[null]},{id:"11530",title:"Chronic Kidney Disease",slug:"management-of-chronic-kidney-disease",signatures:"Mai Ots Rosenberg",authors:[null]},{id:"11531",title:"Integrated Vehicle Health Management in the Automotive Industry",slug:"integrated-vehicle-health-management-in-the-automotive-industry",signatures:"Steven Holland",authors:[null]}]}],publishedBooks:[{type:"book",id:"6142",title:"Family Planning",subtitle:null,isOpenForSubmission:!1,hash:"4993c79cffba3126a9ca1ef7c9902c7e",slug:"family-planning",bookSignature:"Zouhair O. 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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
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].
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
Family | Example virus | Abbreviation | Genus | Genome | Size (nm) |
---|---|---|---|---|---|
Adenovirus type 2 | AdV-2 | ds DNA | 70–90 | ||
Adenovirus type 5 | AdV-5 | ds DNA | 70–90 | ||
Adenovirus type 8 | AdV-8 | ds DNA | 70–90 | ||
Human astrovirus | HAstV | ss RNA | 28–35 | ||
Feline calicivirus | FCV | ss RNA | 28–40 | ||
Human norovirus | HuNoV | ss RNA | 28–40 | ||
Murine norovirus | MNV | ss RNA | 28–40 | ||
Tulane virus | TuV | ss RNA | 28–40 | ||
Porcine circovirus | PCV | ss DNA | ∼17 | ||
Hepatitis E virus | HEV | ss DNA | 32–34 | ||
Human papillomavirus | HPV | ds DNA | 50–60 | ||
Bovine parvovirus | BPV | ss DNA | 20–28 | ||
Canine parvovirus | CPV | ss DNA | 20–25 | ||
Human parvovirus B19 | B19V | ss DNA | 23–26 | ||
Minute virus of mice | MVM (MMV) | ss DNA | 20–25 | ||
Porcine parvovirus | PPV | ss DNA | 20–25 | ||
Bovine enterovirus | BEV | ss RNA | 30–32 | ||
Coxsackievirus | Cox | ss RNA | 30–32 | ||
Echovirus 11 | Echo11 | ss RNA | 30–32 | ||
Encephalomyocarditis virus | EMCV | ss RNA | 30–32 | ||
Enterovirus 71 | EV-71 | ss RNA | 30–32 | ||
Enterovirus D68 | EV-D68 | ss RNA | 30–32 | ||
Foot and mouth disease virus | FMDV | ss RNA | 30–32 | ||
Hepatitis A virus | HAV | ss RNA | 30–32 | ||
Poliovirus type 1 | PV1 | ss RNA | 30–32 | ||
Rhinovirus | RV | ss RNA | 30–32 | ||
Seneca Valley virus | SVV | ss RNA | 30–32 | ||
Bovine polyomavirus | BPyV | ds DNA | 40–50 | ||
Simian virus 40 | SV40 | ds DNA | 40–50 | ||
Bluetongue virus | BTV | ds RNA | 60–80 | ||
Reovirus type 3 | REO-3 | ds RNA | 60–80 | ||
Rotavirus | Rota | ds RNA | 60–80 |
Common families of human and animal non-enveloped viruses.
Among these, the
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.
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).
Class | Chemical | Typical conc. | Usage | Mechanism of viral inactivation | Sensitivity 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 | — |
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.
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
Virusa | Method | Soil/Matrixb | Log10 Reduction after | References | |||
---|---|---|---|---|---|---|---|
30 s | 1 min | 5 min | 10 min | ||||
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 | <0.5 | [29] | |||
TuV | Suspension test | Medium | <0.5 | [30] | |||
PV1 | Suspension test | 20% fecal | 0.3 | [28] | |||
PV1 | Suspension test | Medium | 0.4 | [31] | |||
PV1 | Glass | Medium | 2.3 | 1.0 | 5.0 | [31] | |
PV1 | Stainless steel | Erythrocytes + BSA | 2.1 | 1.8 | [26] | ||
PV1 | Suspension test | Medium | 4 | [28] | |||
FCV | Suspension test | Medium | 1.7 | 2.2 | [30] | ||
AdV-8 | Suspension test | Medium | 1.9 | [33] | |||
AdV-5 | Stainless steel | Erythrocytes + BSA | 2.4 | >4.1 | [26] | ||
AdV-5 | Stainless steel | Medium | ∼5 | [34] | |||
MNV | Suspension test | Medium | 5 | [30] | |||
Rotavirus | Suspension test | Medium | > 3.1 | [28] | |||
CPV | Stainless steel | Medium | 0.1 | [36] | |||
SV40 | Suspension test | Medium | <1 | [37] | |||
PV1 | Glass | Medium | 2.9 | 2.9 | 5.4 | [31] | |
TuV | Suspension test | Medium | <0.5 | [30] | |||
FCV | Suspension test | Medium | <0.5 | [30] | |||
HEV71 | Suspension test | Medium | <1 | [27] | |||
PV1 | Suspension test | medium | <1 | [37] | |||
PV1 | Glass | Medium | 1.2 | 1.3 | 1.0 | [31] | |
AdV-5 | Stainless steel | Medium | ∼1 | [34] | |||
AdV-8 | Suspension test | Medium | 2.0 | [33] | |||
MNV | Suspension test | Medium | 1.8 | 3.1 | [30] | ||
SV40 | Suspension test | Medium | >4 | [37] | |||
Rotavirus | Suspension test | Medium | > 4 | [42] |
Efficacy of alcohols against non-enveloped viruses.
See Table 1 for abbreviations used for viruses.
BSA, bovine serum albumin; medium, culture medium; RT, room temperature.
Entries in purple font indicate results from undiluted or diluted formulations with the indicated microbicidal active ingredients.
Interestingly, the above order of susceptibility does not appear to hold the same for isopropanol (Table 3). For example, the polyomavirus simian virus 40 is much more susceptible to isopropanol than many other non-enveloped viruses; and poliovirus appears to display a lower susceptibility, similar to that of hepatitis A virus and human enterovirus 71. Murine norovirus is still more susceptible than feline calicivirus to isopropanol, but not as susceptible as simian virus 40 or rotavirus. The apparent difference between adenovirus 5 and adenovirus 8 that has been observed for ethanol has not been observed for isopropanol.
An oxidizer or oxidizing agent is a chemical that has the ability to oxidize other molecules, i.e., to accept their electrons. Common oxidizing agents used for disinfection, sterilization, or antisepsis include hydrogen peroxide, peracetic acid, ozone, and halogen-containing compounds such as sodium hypochlorite (bleach), hypochlorous acid, povidone-iodine, chlorohexidine, and chlorine dioxide, etc. These compounds can react with and alter the proteins and nucleic acids of non-enveloped viruses and render them noninfectious. Oxidizers comprise a large group of chemicals, and the relative order of susceptibility of non-enveloped viruses to oxidizers seems to vary by specific type of active ingredient (Table 4).
Virusa | Method | Soil/Matrixb | Log10 Reduction after | References | |||
---|---|---|---|---|---|---|---|
≤ 1 min | 2 min | 5 min | 10 min | ||||
FCV | Suspension test | Medium | 3 | [29] | |||
FCV | Suspension test | 20% stool | 0.5 | [29] | |||
MNV | Suspension test | Medium | 3 | [29] | |||
MNV | Suspension test | 20% stool | 0.0 | [29] | |||
CPV | Stainless steel | 90% plasma | < 1 | [43] | |||
CPV | Stainless steel | 5% serum | 5 | [43] | |||
HAV | Stainless steel | 5% serum | 5 | [43] | |||
HAV | Stainless steel | 90% plasma | <1 | 5 | [43] | ||
HAV | Suspension test | PBS/20% fecal | 4 | [28] | |||
PV1 | Suspension test | PBS/20% fecal | 4 | [28] | |||
PPV | Stainless steel | Erythrocytes + BSA | 0.6 | 1.0 | [26] | ||
MVM | Stainless steel | Erythrocytes + BSA | 3.0 | 4.4 | [26] | ||
PV1 | Stainless steel | Erythrocytes + BSA | 2.8 | 4.5 | [26] | ||
AdV-5 | Stainless steel | Erythrocytes + BSA | 4 | [26] | |||
PV1 | Glass | Medium | 0.4 | 0.9 | [16] | ||
RV14 | Glass | Medium | >4.9 | [16] | |||
PPV | Stainless steel | Erythrocytes + BSA | 0.5 | [26] | |||
MVM | Stainless steel | Erythrocytes + BSA | 1.5 | [26] | |||
PV1 | Stainless steel | Erythrocytes + BSA | 3.9 | [26] | |||
AdV-5 | Stainless steel | Erythrocytes + BSA | 2.3 | [26] | |||
MNV | Suspension test | Medium | ∼3 | [52] | |||
HAV | Suspension test | Medium | ∼3 | [53] | |||
PV | Suspension test | Medium | >3 | [53] | |||
CPV | Stainless steel | BSA | 1.6 | [34] | |||
MVM | Stainless steel | BSA | 2.3-2.9 | [34] | |||
PPV | Stainless steel | BSA | 3.8-5.5 | [34] | |||
AdV-5 | Stainless steel | BSA | 4.9-5.8 | [34] |
Efficacy of oxidizers against non-enveloped viruses.
See Table 1 for abbreviations used for viruses.
BSA, bovine serum albumin; PBS, phosphate buffered saline; medium, culture medium; RT, room temperature.
Viral-inoculated lettuce was washed with PAA solution for a defined period of time.
Entries in purple font indicate results from undiluted original or diluted formulations with microbicidal active ingredients.
Parvoviruses are generally among the least susceptible viruses to various types of oxidizers, including sodium hypochlorite, hydrogen peroxide, and peracetic acid. However, for sodium hypochlorite, minute virus of mice appears to be more susceptible than porcine parvovirus and canine parvovirus. All picornaviruses appear to exhibit a similar degree of susceptibility to sodium hypochlorite; but within the family of
The trending for hydrogen peroxide seems more complex than that for sodium hypochlorite. For example, there seems a higher level of variability within the
For peracetic acid, hepatitis A virus also seems less susceptible than poliovirus. Both feline calicivirus and murine norovirus are susceptible to peracetic acid and so is adenovirus.
Quaternary ammonium compounds (QAC) are widely used as active ingredients for disinfectants. Among the advantages of QAC are good stability, dual function of disinfection and cleaning, surface activity, low toxicity, and lack of odor, etc. The potential limitation in the microbicidal efficacy and possible effect in promoting antimicrobial resistance of QAC have also been discussed in the literature [54, 55].
Quaternary ammonium compounds are generally efficacious on most vegetative bacteria and enveloped viruses. Their efficacies against non-enveloped viruses, however, are generally much weaker. Nevertheless, several non-enveloped viruses, such as rotavirus, rhinovirus, and coxsackievirus A11, have been shown to be susceptible to QAC. The susceptibility levels among the
Virusa | Method | Soil/matrixb | Log10 reduction after | References | |||
---|---|---|---|---|---|---|---|
30 s | 1 min | 10 min | 60 min | ||||
PPV | Stainless steel | Erythrocytes + BSA | 0.4 | [26] | |||
MVM | Stainless steel | Erythrocytes + BSA | 0.5 | [26] | |||
PV1 | Stainless steel | Erythrocytes + BSA | 0.5 | [26] | |||
AdV-5 | Stainless steel | Erythrocytes + BSA | 1.8 | [26] | |||
AdV-8 | Suspension test | Medium | 1.0-1.8 | [57] | |||
AdV-5 | Suspension test | Medium | 3.7-5.3 | [57] | |||
TuV | Suspension test | Medium | <0.5 | [30] | |||
PV1 | Suspension test | BSA/yeast extract | 0.0 | [58] | |||
AdV-25 | Suspension test | BSA/yeast extract | 0.3 | [58] | |||
Cox A11 | Suspension test | BSA/yeast extract | >5.1 | [58] | |||
FCV | Suspension test | Medium | <0.5 | [29] | |||
MNV | Suspension test | Medium | <0.5 | [29] | |||
Rhinovirus | Glass | Medium | >3.0 | >3.3 | [16] |
Efficacy of QAC against non-enveloped viruses.
See Table 1 for abbreviations used for viruses.
BSA, bovine serum albumin; medium, culture medium; QAC, quaternary ammonium compound.
Entries in purple font indicate results from original or diluted formulations with microbicidal active ingredients.
Acids and alkalines, either used alone or in combination with other active ingredients in formulated products, can be an effective means for viral inactivation. Acids may be used for disinfection, sanitization, textile or face mask pretreatment, or viral clearance during biopharmaceutical manufacturing. Alkalines may also be used for disinfection, sanitization, and viral clearance during biopharmaceutical manufacturing and can be effective against even the least susceptible of pathogens, the prions [58].
It has been widely reported that a low-pH treatment (typically at pH 4 and below) can effectively inactivate most enveloped viruses, although some enveloped viruses, such as bovine viral diarrhea virus, still exhibit a relatively low susceptibility to this treatment pH [22]. The range of susceptibilities of non-enveloped viruses to low pH seems quite scattered and often goes against the “conventional wisdom” that non-enveloped viruses are not susceptible to acidic pH (Table 6). For instance, in the family of
Virusa | Method | Soil/Matrixb | Log10 Reduction after | References | |||
---|---|---|---|---|---|---|---|
20 min | 30 min | 45 min | 1–2 hr | ||||
REO-3 | Suspension test | Medium | 1–3 | [59] | |||
PCV | Suspension test | Medium | >3 | [60] | |||
MVM | Suspension test | Medium | <1 | [61] | |||
MNV | Suspension test | Medium | <0.5 | [30] | |||
TuV | Suspension test | Medium | <0.5 | [30] | |||
PARV4 | Suspension test | Medium | 2–3 | [61] | |||
B19V | Suspension test | Medium | > 4 | [61] | |||
FCV | Suspension test | Medium | 6.3 | [30] | |||
FCV | Suspension test | Medium | >5 | [62] | |||
PV | Suspension test | Medium | <1 | [63] | |||
PV | Suspension test | Medium | <1 | [64] | |||
HAV | Suspension test | Medium | <1 | [64] | |||
MNV | Suspension test | Medium | <0.5 | [30] | |||
TuV | Suspension test | Medium | <0.5 | [30] | |||
Cox A9 | Suspension test | Medium | <1 | [65] | |||
FCV | Suspension test | Medium | ∼3 | [30] | |||
FCV | Suspension test | Medium | ∼4.7 | [62] | |||
RV | Suspension test | Medium | >3 | [65] | |||
FMDV | Suspension test | Medium | >3 | [65] | |||
MVM | Suspension test | Medium | <1 | [66] | |||
EV71 | Suspension test | Medium | <1 | [67] | |||
EV-D68 | Suspension test | Medium | ∼4–5 | <5 | [67] | ||
B19V | Suspension test | Medium | [66] |
Efficacy of low pH against non-enveloped viruses.
The
Feline calicivirus and murine norovirus in the family
Viruses, both enveloped and non-enveloped, are generally susceptible to high pH. At an environment of pH 12 or above, most if not all non-enveloped viruses would be inactivated, with extent depending both on temperature and contact time. Reovirus, simian virus 40, hepatitis A virus, canine parvovirus, poliovirus, murine norovirus, and Tulane virus seem to be less susceptible than minute virus of mice, feline calicivirus, adenovirus, rotavirus, and foot-and-mouth disease virus. It may be worth noting that the order of susceptibility to high pH seems to be in discord with the hierarchy concept by the greatest degree: in this case, an enveloped virus, bovine viral diarrhea virus, seems to be less susceptible than most, if not all, non-enveloped viruses [22]; parvoviruses are not necessarily less susceptible than many other non-enveloped viruses; and the size of the viral particle does not seem to matter much with regard to the degree of susceptibility (Table 7).
Virusa | Method | Soil/Matrixb | Log10 Reduction after | References | |||
---|---|---|---|---|---|---|---|
≤ 1 min | 10 min | 30 min | 1 hr | ||||
MNV | Suspension test | Medium | ∼2 | [30] | |||
TuV | Suspension test | Medium | ∼2.2 | [30] | |||
FCV | Suspension test | Medium | >5.5 | [30] | |||
REO-3 | Suspension test | Medium | 3 | [68] | |||
Cox B | Suspension test | Medium | 5 | [69] | |||
Echo 11 | Suspension test | Medium | 6 | [68] | |||
BVDV | Suspension test | Medium | 2.5 | [70] | |||
HAV | Suspension test | Medium | 2.7 | [59] | |||
SV40 | Suspension test | Medium | 3.9 | [70] | |||
HAV | Stainless steel | 5% serum | 3.0 | [43] | |||
HAV | Stainless steel | 90% plasma | 3.6 | [43] | |||
CPV | Stainless steel | 5% serum | 3.5 | [43] | |||
CPV | Stainless steel | 90% plasma | 5.2 | [43] | |||
MVM | Suspension test | Medium | >4.7 | [71] | |||
MVM | Suspension test | Medium | >4 | [66] | |||
CPV | Suspension test | Medium | 5.6 | [70] | |||
PV | Suspension test | Medium | 5.9 | [70] | |||
AdV-2 | Suspension test | Medium | >6.9 | [70] | |||
AdV-5 | Suspension test | Medium | >6 | [72] | |||
HAV | suspension test | Medium | 2.4 | [59] | |||
PV | suspension test | Medium | 4.1 | [63] | |||
Avian Reo | Suspension test | Medium | 4 | [73] | |||
PV | Suspension test | Medium | 5.1 | [73] | |||
Bovine Rota | Suspension test | Medium | >6 | [73] |
Efficacy of high pH against non-enveloped viruses.
Entries in purple font indicate results from undiluted or diluted formulations with microbicidal active ingredients.
Aldehydes, such as glutaraldehyde, formaldehyde, and
Virusa | Method | Soil/Matrixb | Log10 Reduction after | References | |||
---|---|---|---|---|---|---|---|
5 min | 10 min | 30 min | 60 min | ||||
HAV | Suspension test | Medium | 3.0 | [75] | |||
PPV | Stainless steel | BSA | 1.7–2.8 | [34] | |||
MVM | Stainless steel | BSA | 2.5–3.3 | [34] | |||
PV1 | Suspension test | Medium | >3 | [76] | |||
AdV-5 | Stainless steel | BSA | 4.9–6.3 | [34] | |||
PPV | Stainless steel | Erythrocytes + BSA | 3.6 | [26] | |||
MVM | Stainless steel | Erythrocytes + BSA | >4.4 | [26] | |||
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] |
Efficacy of aldehydes against non-enveloped viruses.
See Table 1 for abbreviations used for viruses.
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.
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
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.
Chemical | Lower susceptibility | Medium susceptibility | Higher 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 | 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 |
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.
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.
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
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
The family
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
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.
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.
The author thanks Drs. Raymond Nims and M. Khalid Ijaz for the critical review of the manuscript and discussion.
The author declares no conflict of interest.
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