DOI: 10.1099/0022-1317-83-2-333. Genetic clustering of all 102 human rhinovirus prototype strains: serotype 87 is close to human enterovirus 70

Genetic clustering of all 102 human rhinovirus prototype strains: serotype 87 is close to human enterovirus 70

10.1099/0022-1317-83-2-333

Crossref journal-article

Microbiology Society

Journal of General Virology (345)

Abstract

Human rhinoviruses (HRV), common agents of respiratory infections, comprise 102 designated serotypes. The genetic relationships of HRV prototype strains and the possibility of using genetic identification of a given HRV field strain were studied. Genomic sequences in the VP4/VP2 region were obtained from all 102 prototype strains. Phylogenetic analysis included 61 recently isolated Finnish field strains. Seventy-six out of the 102 prototype strains clustered in the HRV genetic group A and 25 in group B. Serotype 87 clustered separately and together with human enterovirus 70. The ‘percentage’ interserotypic differences were generally similar to those between different enterovirus serotypes, but for six pairs of HRV serotypes they were less than 10%. The maximum variation in genetic group A was 41% at the nucleotide level and 28% at the amino acid level, and in genetic group B 34% and 20%, respectively. Judging from the observed interserotypic differences, the 61 Finnish field isolates might represent as many as 19 different serotypes. One cluster of the field strains did not directly associate with any of the prototype strains and might represent a new serotype. However, larger numbers of field isolates of known serotype need to be characterized, possibly also in the VP1 region, to evaluate the feasibility of genetic typing of HRV strains.

Bibliography

Savolainen, C., Blomqvist, S., Mulders, M. N., & Hovi, T. (2002). Genetic clustering of all 102 human rhinovirus prototype strains: serotype 87 is close to human enterovirus 70. Journal of General Virology, 83(2), 333â340.

Authors 4

Carita Savolainen (first)
Soile Blomqvist (additional)
Mick N. Mulders (additional)
Tapani Hovi (additional)

References 31 Referenced 188

10.1128/JVI.51.2.340-345.1984 / Journal of Virology / Many rhinovirus serotypes share the same cellular receptor by Abraham (1984)
10.1097/00006454-199012000-00005 / Pediatric Infectious Disease Journal / Viral pneumonia in the first month of life by Abzug (1990)
10.1128/JCM.37.3.524-530.1999 / Journal of Clinical Microbiology / Improved detection of rhinoviruses in clinical samples by using a newly developed nested reverse transcription–PCR assay by Andeweg (1999)
10.1128/JVI.64.3.1117-1123.1990 / Journal of Virology / Two groups of rhinoviruses revealed by a panel of antiviral compounds present sequence divergence and differential pathogenicity . by Andries (1990)
10.1016/S0022-3476(88)80380-9 / Journal of Pediatrics / Rhinoviruses in acute otitis media by Arola (1988)
10.1006/mcpr.1993.1055 / Molecular and Cellular Probes / Detection of human rhinovirus RNA in nasal washings by PCR by Arruda (1993)
10.1128/JCM.37.9.2813-2816.1999 / Journal of Clinical Microbiology / Rapid detection of human rhinoviruses in nasopharyngeal aspirates by a microwell reverse transcription–PCR-hybridization assay by Blomqvist (1999)
10.1128/IAI.37.2.642-647.1982 / Infection and Immunology / Antigenic groupings of 90 rhinovirus serotypes by Cooney (1982)
{'key': 'R9', 'first-page': '709', 'article-title': 'Rhinoviruses', 'volume-title': 'In Laboratory Diagnosis of Viral Infections', 'author': 'Couch', 'year': '1992'} / In Laboratory Diagnosis of Viral Infections / Rhinoviruses by Couch (1992)
10.1073/pnas.84.9.2605 / Proceedings of the National Academy of Sciences, USA / Evolutionary relationships within the human rhinovirus genus: comparison of serotypes 89, 2 and 14 by Duechler (1987)
{'key': 'R11', 'volume-title': 'PHYLIP (Phylogeny Inference package) version 3.5c. Distributed by the author, Department of Genetics', 'author': 'Felsenstein', 'year': '1993'} / PHYLIP (Phylogeny Inference package) version 3.5c. Distributed by the author, Department of Genetics by Felsenstein (1993)
10.1002/jmv.1890280204 / Journal of Medical Virology / Amplification of rhinovirus specific nucleic acids from clinical samples using the polymerase chain reaction by Gama (1989)
10.1128/JCM.33.3.648-653.1995 / Journal of Clinical Microbiology / Detection of enteroviruses and rhinoviruses in clinical specimens by PCR and liquid-phase hybridization by Halonen (1995)
10.1093/emboj/19.23.6317 / EMBO Journal / The cellular receptor to human rhinovirus 2 binds around the 5-fold axis and not in the canyon: a structural view by Hewat (2000)
10.1099/0022-1317-76-10-2549 / Journal of General Virology / Molecular relationships between 21 human rhinovirus serotypes by Horsnell (1995)
10.1099/0022-1317-69-1-49 / Journal of General Virology / The nucleotide sequence of human rhinovirus 1B: molecular relationships within the rhinovirus genus by Hughes (1988)
10.1099/0022-1317-70-12-3261 / Journal of General Virology / Polymerase chain reaction for human picornaviruses by Hyypiä (1989)
10.1002/jmv.1890400204 / Journal of Medical Virology / Improved detection of rhinoviruses in nasal and throat swabs by seminested RT–PCR by Ireland (1993)
10.1128/JCM.31.1.111-117.1993 / Journal of Clinical Microbiology / Use of polymerase chain reaction for diagnosis of picornavirus infection in subjects with and without respiratory symptoms by Johnston (1993)
10.1136/bmj.310.6989.1225 / British Medical Journal / Community study of role of virus infections in exacerbations of asthma in 9–11 year old children by Johnston (1995)
10.1016/S1044-5773(05)80017-4 / Seminars in Virology / Molecular epidemiology of enteroviruses by Kew (1995)
10.1128/JCM.36.2.539-542.1998 / Journal of Clinical Microbiology / Viruses and bacteria in the etiology of the common cold by Mäkelä (1998)
10.1099/0022-1317-81-3-803 / Journal of General Virology / Molecular epidemiology of coxsackievirus B4 and disclosure of the correct VP1/2Apro cleavage site: evidence for high genomic diversity and long-term endemicity of distinct genotypes by Mulders (2000)
10.1128/JVI.73.3.1941-1948.1999 / Journal of Virology / Molecular evolution of the human enteroviruses: correlation of serotype with VP1 sequence and application to picornavirus classification by Oberste (1999a)
10.1128/JCM.37.5.1288-1293.1999 / Journal of Clinical Microbiology / Typing of human enteroviruses by partial sequencing of VP1 by Oberste (1999b)
{'key': 'R26', 'first-page': '609', 'article-title': 'Picornaviridae : the viruses and their replication', 'volume-title': 'In Fields Virology', 'author': 'Rueckert', 'year': '1996'} / In Fields Virology / Picornaviridae : the viruses and their replication by Rueckert (1996)
10.1016/S0166-0934(98)00006-8 / Journal of Virological Methods / Development and application of a new method for amplification and detection of human rhinovirus RNA by Samuelson (1998)
{'key': 'R28', 'article-title': 'Phylogenetic analysis of rhinovirus isolates collected during successive epidemic seasons', 'author': 'Savolainen', 'year': '2001', 'journal-title': 'Virus Research'} / Virus Research / Phylogenetic analysis of rhinovirus isolates collected during successive epidemic seasons by Savolainen (2001)
10.1016/0042-6822(91)90098-V / Virology / The major and minor group receptor families contain all but one human rhinovirus serotype by Uncapher (1991)
10.1099/0022-1317-63-1-141 / Journal of General Virology / Neuraminidase-sensitive erythrocyte receptor for enterovirus type 70 by Utagawa (1982)
10.1097/00006454-200106000-00006 / Pediatric Infectious Disease Journal / Epidemiology of documented viral respiratory infections and acute otitis media in a cohort of children followed from two to twenty-four months of age by Vesa (2001)

Dates

Type	When
Created	10 years ago (Aug. 26, 2015, 12:17 p.m.)
Deposited	4 years, 8 months ago (Dec. 23, 2020, 1:44 a.m.)
Indexed	2 months, 3 weeks ago (June 14, 2025, 8:26 p.m.)
Issued	23 years, 7 months ago (Feb. 1, 2002)
Published	23 years, 7 months ago (Feb. 1, 2002)
Published Print	23 years, 7 months ago (Feb. 1, 2002)

Funders 0

None

BibTeX

@article{Savolainen_2002, title={Genetic clustering of all 102 human rhinovirus prototype strains: serotype 87 is close to human enterovirus 70}, volume={83}, ISSN={1465-2099}, url={http://dx.doi.org/10.1099/0022-1317-83-2-333}, DOI={10.1099/0022-1317-83-2-333}, number={2}, journal={Journal of General Virology}, publisher={Microbiology Society}, author={Savolainen, Carita and Blomqvist, Soile and Mulders, Mick N. and Hovi, Tapani}, year={2002}, month=feb, pages={333–340} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        6,
        15
      ]
    ],
    "date-time": "2025-06-15T00:26:02Z",
    "timestamp": 1749947162729
  },
  "reference-count": 31,
  "publisher": "Microbiology Society",
  "issue": "2",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        2002,
        2,
        1
      ]
    ]
  },
  "abstract": "<jats:p>Human rhinoviruses (HRV), common agents of respiratory infections, comprise 102 designated serotypes. The genetic relationships of HRV prototype strains and the possibility of using genetic identification of a given HRV field strain were studied. Genomic sequences in the VP4/VP2 region were obtained from all 102 prototype strains. Phylogenetic analysis included 61 recently isolated Finnish field strains. Seventy-six out of the 102 prototype strains clustered in the HRV genetic group A and 25 in group B. Serotype 87 clustered separately and together with human enterovirus 70. The \u2018percentage\u2019 interserotypic differences were generally similar to those between different enterovirus serotypes, but for six pairs of HRV serotypes they were less than 10%. The maximum variation in genetic group A was 41% at the nucleotide level and 28% at the amino acid level, and in genetic group B 34% and 20%, respectively. Judging from the observed interserotypic differences, the 61 Finnish field isolates might represent as many as 19 different serotypes. One cluster of the field strains did not directly associate with any of the prototype strains and might represent a new serotype. However, larger numbers of field isolates of known serotype need to be characterized, possibly also in the VP1 region, to evaluate the feasibility of genetic typing of HRV strains.</jats:p>",
  "DOI": "10.1099/0022-1317-83-2-333",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2015,
        8,
        26
      ]
    ],
    "date-time": "2015-08-26T16:17:57Z",
    "timestamp": 1440605877000
  },
  "page": "333-340",
  "source": "Crossref",
  "is-referenced-by-count": 188,
  "title": "Genetic clustering of all 102 human rhinovirus prototype strains: serotype 87 is close to human enterovirus 70",
  "prefix": "10.1099",
  "volume": "83",
  "author": [
    {
      "given": "Carita",
      "family": "Savolainen",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Enterovirus Laboratory, Department of Microbiology, National Public Health Institute (KTL), Mannerheimintie 166, FIN-00300 Helsinki, Finland1"
        }
      ]
    },
    {
      "given": "Soile",
      "family": "Blomqvist",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Enterovirus Laboratory, Department of Microbiology, National Public Health Institute (KTL), Mannerheimintie 166, FIN-00300 Helsinki, Finland1"
        }
      ]
    },
    {
      "given": "Mick N.",
      "family": "Mulders",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Enterovirus Laboratory, Department of Microbiology, National Public Health Institute (KTL), Mannerheimintie 166, FIN-00300 Helsinki, Finland1"
        }
      ]
    },
    {
      "given": "Tapani",
      "family": "Hovi",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Enterovirus Laboratory, Department of Microbiology, National Public Health Institute (KTL), Mannerheimintie 166, FIN-00300 Helsinki, Finland1"
        }
      ]
    }
  ],
  "member": "345",
  "reference": [
    {
      "key": "R1",
      "doi-asserted-by": "crossref",
      "first-page": "340",
      "DOI": "10.1128/JVI.51.2.340-345.1984",
      "article-title": "Many rhinovirus serotypes share the same cellular receptor",
      "volume": "51",
      "author": "Abraham",
      "year": "1984",
      "journal-title": "Journal of Virology"
    },
    {
      "key": "R2",
      "doi-asserted-by": "crossref",
      "first-page": "881",
      "DOI": "10.1097/00006454-199012000-00005",
      "article-title": "Viral pneumonia in the first month of life",
      "volume": "9",
      "author": "Abzug",
      "year": "1990",
      "journal-title": "Pediatric Infectious Disease Journal"
    },
    {
      "key": "R3",
      "doi-asserted-by": "crossref",
      "first-page": "524",
      "DOI": "10.1128/JCM.37.3.524-530.1999",
      "article-title": "Improved detection of rhinoviruses in clinical samples by using a newly developed nested reverse transcription\u2013PCR assay",
      "volume": "37",
      "author": "Andeweg",
      "year": "1999",
      "journal-title": "Journal of Clinical Microbiology"
    },
    {
      "key": "R4",
      "doi-asserted-by": "crossref",
      "first-page": "1117",
      "DOI": "10.1128/JVI.64.3.1117-1123.1990",
      "article-title": "Two groups of rhinoviruses revealed by a panel of antiviral compounds present sequence divergence and differential pathogenicity .",
      "volume": "64",
      "author": "Andries",
      "year": "1990",
      "journal-title": "Journal of Virology"
    },
    {
      "key": "R5",
      "doi-asserted-by": "crossref",
      "first-page": "693",
      "DOI": "10.1016/S0022-3476(88)80380-9",
      "article-title": "Rhinoviruses in acute otitis media",
      "volume": "113",
      "author": "Arola",
      "year": "1988",
      "journal-title": "Journal of Pediatrics"
    },
    {
      "key": "R6",
      "doi-asserted-by": "crossref",
      "first-page": "373",
      "DOI": "10.1006/mcpr.1993.1055",
      "article-title": "Detection of human rhinovirus RNA in nasal washings by PCR",
      "volume": "7",
      "author": "Arruda",
      "year": "1993",
      "journal-title": "Molecular and Cellular Probes"
    },
    {
      "key": "R7",
      "doi-asserted-by": "crossref",
      "first-page": "2813",
      "DOI": "10.1128/JCM.37.9.2813-2816.1999",
      "article-title": "Rapid detection of human rhinoviruses in nasopharyngeal aspirates by a microwell reverse transcription\u2013PCR-hybridization assay",
      "volume": "37",
      "author": "Blomqvist",
      "year": "1999",
      "journal-title": "Journal of Clinical Microbiology"
    },
    {
      "key": "R8",
      "doi-asserted-by": "crossref",
      "first-page": "642",
      "DOI": "10.1128/IAI.37.2.642-647.1982",
      "article-title": "Antigenic groupings of 90 rhinovirus serotypes",
      "volume": "37",
      "author": "Cooney",
      "year": "1982",
      "journal-title": "Infection and Immunology"
    },
    {
      "key": "R9",
      "first-page": "709",
      "article-title": "Rhinoviruses",
      "volume-title": "In Laboratory Diagnosis of Viral Infections",
      "author": "Couch",
      "year": "1992"
    },
    {
      "key": "R10",
      "doi-asserted-by": "crossref",
      "first-page": "2605",
      "DOI": "10.1073/pnas.84.9.2605",
      "article-title": "Evolutionary relationships within the human rhinovirus genus: comparison of serotypes 89, 2 and 14",
      "volume": "84",
      "author": "Duechler",
      "year": "1987",
      "journal-title": "Proceedings of the National Academy of Sciences, USA"
    },
    {
      "key": "R11",
      "volume-title": "PHYLIP (Phylogeny Inference package) version 3.5c. Distributed by the author, Department of Genetics",
      "author": "Felsenstein",
      "year": "1993"
    },
    {
      "key": "R12",
      "doi-asserted-by": "crossref",
      "first-page": "73",
      "DOI": "10.1002/jmv.1890280204",
      "article-title": "Amplification of rhinovirus specific nucleic acids from clinical samples using the polymerase chain reaction",
      "volume": "28",
      "author": "Gama",
      "year": "1989",
      "journal-title": "Journal of Medical Virology"
    },
    {
      "key": "R13",
      "doi-asserted-by": "crossref",
      "first-page": "648",
      "DOI": "10.1128/JCM.33.3.648-653.1995",
      "article-title": "Detection of enteroviruses and rhinoviruses in clinical specimens by PCR and liquid-phase hybridization",
      "volume": "33",
      "author": "Halonen",
      "year": "1995",
      "journal-title": "Journal of Clinical Microbiology"
    },
    {
      "key": "R14",
      "doi-asserted-by": "crossref",
      "first-page": "6317",
      "DOI": "10.1093/emboj/19.23.6317",
      "article-title": "The cellular receptor to human rhinovirus 2 binds around the 5-fold axis and not in the canyon: a structural view",
      "volume": "19",
      "author": "Hewat",
      "year": "2000",
      "journal-title": "EMBO Journal"
    },
    {
      "key": "R15",
      "doi-asserted-by": "crossref",
      "first-page": "2549",
      "DOI": "10.1099/0022-1317-76-10-2549",
      "article-title": "Molecular relationships between 21 human rhinovirus serotypes",
      "volume": "76",
      "author": "Horsnell",
      "year": "1995",
      "journal-title": "Journal of General Virology"
    },
    {
      "key": "R16",
      "doi-asserted-by": "crossref",
      "first-page": "49",
      "DOI": "10.1099/0022-1317-69-1-49",
      "article-title": "The nucleotide sequence of human rhinovirus 1B: molecular relationships within the rhinovirus genus",
      "volume": "69",
      "author": "Hughes",
      "year": "1988",
      "journal-title": "Journal of General Virology"
    },
    {
      "key": "R17",
      "doi-asserted-by": "crossref",
      "first-page": "3261",
      "DOI": "10.1099/0022-1317-70-12-3261",
      "article-title": "Polymerase chain reaction for human picornaviruses",
      "volume": "70",
      "author": "Hyypi\u00e4",
      "year": "1989",
      "journal-title": "Journal of General Virology"
    },
    {
      "key": "R18",
      "doi-asserted-by": "crossref",
      "first-page": "96",
      "DOI": "10.1002/jmv.1890400204",
      "article-title": "Improved detection of rhinoviruses in nasal and throat swabs by seminested RT\u2013PCR",
      "volume": "40",
      "author": "Ireland",
      "year": "1993",
      "journal-title": "Journal of Medical Virology"
    },
    {
      "key": "R19",
      "doi-asserted-by": "crossref",
      "first-page": "111",
      "DOI": "10.1128/JCM.31.1.111-117.1993",
      "article-title": "Use of polymerase chain reaction for diagnosis of picornavirus infection in subjects with and without respiratory symptoms",
      "volume": "31",
      "author": "Johnston",
      "year": "1993",
      "journal-title": "Journal of Clinical Microbiology"
    },
    {
      "key": "R20",
      "doi-asserted-by": "crossref",
      "first-page": "1225",
      "DOI": "10.1136/bmj.310.6989.1225",
      "article-title": "Community study of role of virus infections in exacerbations of asthma in 9\u201311 year old children",
      "volume": "310",
      "author": "Johnston",
      "year": "1995",
      "journal-title": "British Medical Journal"
    },
    {
      "key": "R21",
      "doi-asserted-by": "crossref",
      "first-page": "401",
      "DOI": "10.1016/S1044-5773(05)80017-4",
      "article-title": "Molecular epidemiology of enteroviruses",
      "volume": "6",
      "author": "Kew",
      "year": "1995",
      "journal-title": "Seminars in Virology"
    },
    {
      "key": "R22",
      "doi-asserted-by": "crossref",
      "first-page": "539",
      "DOI": "10.1128/JCM.36.2.539-542.1998",
      "article-title": "Viruses and bacteria in the etiology of the common cold",
      "volume": "36",
      "author": "M\u00e4kel\u00e4",
      "year": "1998",
      "journal-title": "Journal of Clinical Microbiology"
    },
    {
      "key": "R23",
      "doi-asserted-by": "crossref",
      "first-page": "803",
      "DOI": "10.1099/0022-1317-81-3-803",
      "article-title": "Molecular epidemiology of coxsackievirus B4 and disclosure of the correct VP1/2Apro cleavage site: evidence for high genomic diversity and long-term endemicity of distinct genotypes",
      "volume": "81",
      "author": "Mulders",
      "year": "2000",
      "journal-title": "Journal of General Virology"
    },
    {
      "key": "R24",
      "doi-asserted-by": "crossref",
      "first-page": "1941",
      "DOI": "10.1128/JVI.73.3.1941-1948.1999",
      "article-title": "Molecular evolution of the human enteroviruses: correlation of serotype with VP1 sequence and application to picornavirus classification",
      "volume": "73",
      "author": "Oberste",
      "year": "1999a",
      "journal-title": "Journal of Virology"
    },
    {
      "key": "R25",
      "doi-asserted-by": "crossref",
      "first-page": "1288",
      "DOI": "10.1128/JCM.37.5.1288-1293.1999",
      "article-title": "Typing of human enteroviruses by partial sequencing of VP1",
      "volume": "37",
      "author": "Oberste",
      "year": "1999b",
      "journal-title": "Journal of Clinical Microbiology"
    },
    {
      "key": "R26",
      "first-page": "609",
      "article-title": "Picornaviridae : the viruses and their replication",
      "volume-title": "In Fields Virology",
      "author": "Rueckert",
      "year": "1996"
    },
    {
      "key": "R27",
      "doi-asserted-by": "crossref",
      "first-page": "197",
      "DOI": "10.1016/S0166-0934(98)00006-8",
      "article-title": "Development and application of a new method for amplification and detection of human rhinovirus RNA",
      "volume": "71",
      "author": "Samuelson",
      "year": "1998",
      "journal-title": "Journal of Virological Methods"
    },
    {
      "key": "R28",
      "article-title": "Phylogenetic analysis of rhinovirus isolates collected during successive epidemic seasons",
      "author": "Savolainen",
      "year": "2001",
      "journal-title": "Virus Research"
    },
    {
      "key": "R29",
      "doi-asserted-by": "crossref",
      "first-page": "814",
      "DOI": "10.1016/0042-6822(91)90098-V",
      "article-title": "The major and minor group receptor families contain all but one human rhinovirus serotype",
      "volume": "180",
      "author": "Uncapher",
      "year": "1991",
      "journal-title": "Virology"
    },
    {
      "key": "R30",
      "doi-asserted-by": "crossref",
      "first-page": "141",
      "DOI": "10.1099/0022-1317-63-1-141",
      "article-title": "Neuraminidase-sensitive erythrocyte receptor for enterovirus type 70",
      "volume": "63",
      "author": "Utagawa",
      "year": "1982",
      "journal-title": "Journal of General Virology"
    },
    {
      "key": "R31",
      "doi-asserted-by": "crossref",
      "first-page": "574",
      "DOI": "10.1097/00006454-200106000-00006",
      "article-title": "Epidemiology of documented viral respiratory infections and acute otitis media in a cohort of children followed from two to twenty-four months of age",
      "volume": "20",
      "author": "Vesa",
      "year": "2001",
      "journal-title": "Pediatric Infectious Disease Journal"
    }
  ],
  "container-title": "Journal of General Virology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://www.microbiologyresearch.org/content/journal/jgv/10.1099/0022-1317-83-2-333?crawler=true",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2020,
        12,
        23
      ]
    ],
    "date-time": "2020-12-23T06:44:14Z",
    "timestamp": 1608705854000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://www.microbiologyresearch.org/content/journal/jgv/10.1099/0022-1317-83-2-333"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2002,
        2,
        1
      ]
    ]
  },
  "references-count": 31,
  "journal-issue": {
    "issue": "2",
    "published-print": {
      "date-parts": [
        [
          2002,
          2,
          1
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1099/0022-1317-83-2-333",
  "relation": {},
  "ISSN": [
    "0022-1317",
    "1465-2099"
  ],
  "subject": [],
  "published": {
    "date-parts": [
      [
        2002,
        2,
        1
      ]
    ]
  }
}