DOI: 10.1128/iai.67.4.1871-1877.1999. Risk Factors in the Pathogenesis of Invasive Group A Streptococcal Infections: Role of Protective Humoral Immunity

Risk Factors in the Pathogenesis of Invasive Group A Streptococcal Infections: Role of Protective Humoral Immunity

10.1128/iai.67.4.1871-1877.1999

Crossref journal-article

American Society for Microbiology

Infection and Immunity (235)

Abstract

ABSTRACTAn impressive change in the epidemiology and severity of invasive group A streptococcal infections occurred in the 1980s, and the incidence of streptococcal toxic shock syndrome cases continues to rise. The reason for the resurgence of severe invasive cases remains a mystery—has there been a change in the pathogen or in host protective immunity? To address these questions, we have studied 33 patients with invasive infection caused by genotypically indistinguishable M1T1 strains ofStreptococcus pyogeneswho had different disease outcomes. Patients were classified as having severe (n= 21) and nonsevere (n= 12) invasive infections based on the presence or absence of shock and organ failure. Levels of anti-M1 bactericidal antibodies and of anti-streptococcal superantigen neutralizing antibodies in plasma were significantly lower in both groups than in age- and geographically matched healthy controls (P< 0.01). Importantly, the levels of these protective antibodies in plasma samples from severe and nonsevere invasive cases were not different. Together the data suggest that low levels of protective antibodies may contribute to host susceptibility to invasive streptococcal infection but do not modulate disease outcome. Other immunogenetic factors that regulate superantigen responses may influence the severity of systemic manifestations associated with invasive streptococcal infection.

Bibliography

Basma, H., Norrby-Teglund, A., Guedez, Y., McGeer, A., Low, D. E., El-Ahmedy, O., Schwartz, B., & Kotb, M. (1999). Risk Factors in the Pathogenesis of Invasive Group A Streptococcal Infections: Role of Protective Humoral Immunity. Infection and Immunity, 67(4), 1871â1877.

Authors 8

Hesham Basma (first)
Anna Norrby-Teglund (additional)
Yajaira Guedez (additional)
Allison McGeer (additional)
Donald E. Low (additional)
Omar El-Ahmedy (additional)
Benjamin Schwartz (additional)
Malak Kotb (additional)

References 53 Referenced 111

Alouf J. E. Knoll H. Kohler W. The family of mitogenic shock-inducing and superantigenic toxins from staphylococci and streptococci Sourcebook of bacterial protein toxins. Alouf J. E. Freer J. H. 1991 367 414 Academic Press London United Kingdom
10.1128/IAI.66.5.2279-2283.1998
Beachey E. H. Seyer J. M. Primary structure and immunochemistry of group A streptococcal M proteins.Semin. Infect. Dis.41982401410 / Semin. Infect. Dis. / Primary structure and immunochemistry of group A streptococcal M proteins by Beachey E. H. (1982)
10.1056/NEJM199601253340407
10.1016/S0022-3476(96)70072-0
Chatellier et al. Unpublished data.
10.1093/infdis/173.4.901
10.1016/S0140-6736(94)90629-7
10.1001/jama.1997.03540250046030
10.1056/NEJM198707163170305
10.1056/NEJM199608223350803
10.1007/BF00196680
Demers B. Low D. E. Simor A. E. Vellend H. Jamieson F. Walmsley S. Green K. Krishnan C. Severe group A streptococcal disease—southern Ontario. Ontario Streptococcal Study Group.Can. Dis. Weekly Rep.171991192194 / Can. Dis. Weekly Rep. / Severe group A streptococcal disease—southern Ontario. Ontario Streptococcal Study Group by Demers B. (1991)
10.1093/clind/16.6.792
10.1097/00006454-199110001-00005
10.1007/BF00918364
10.1038/scientificamerican0691-58
10.1017/S095026880006739X
10.1093/nar/16.10.4667
10.1001/jama.1993.03500030082037
10.3109/00365549009027073
10.1093/infdis/166.1.31
10.1128/iai.65.9.3828-3833.1997
10.1016/S0002-9343(97)00160-5
10.1086/516540
Kohler W. Epidemiology and pathogenesis of streptococcal infection.Immun. Infekt.2019929298 / Immun. Infekt. / Epidemiology and pathogenesis of streptococcal infection by Kohler W. (1992)
10.1128/CMR.8.3.411
10.1097/00001432-199206000-00010
10.1128/iai.61.4.1194-1201.1993
Kraus W. Dale J. B. Beachey E. H. Identification of an epitope of type 1 streptococcal M protein that is shared with a 43-kD protein of human myocardium and renal glomeruli.J. Immunol.145199040894093 (10.4049/jimmunol.145.12.4089) / J. Immunol. / Identification of an epitope of type 1 streptococcal M protein that is shared with a 43-kD protein of human myocardium and renal glomeruli by Kraus W. (1990)
10.1111/j.1442-200X.1996.tb03425.x
Low D. E. Schwartz B. McGeer A. The reemergence of severe group A streptococcal disease: an evolutionary perspective Emerging infections I. Scheld W. M. Armston D. Hughes J. M. 1997 93 123 American Society for Microbiology Washington D.C (10.1128/9781555816940.ch7)
10.3109/00365549009027073
10.1172/JCI116641
10.1007/978-1-4899-1825-3_50
10.1093/infdis/167.2.337
10.1093/infdis/166.5.1014
10.1086/514588
10.1128/iai.64.12.5395-5398.1996
Norrby-Teglund A. Kaul R. Low D. E. McGeer A. Andersson J. P. Andersson U. G. Kotb M. Plasma from patients with severe invasive group A streptococcal infections treated with normal polyspecific IgG inhibits streptococcal superantigen-induced T cell proliferation and cytokine production.J. Immunol.156199630573064 (10.4049/jimmunol.156.8.3057) / J. Immunol. / Plasma from patients with severe invasive group A streptococcal infections treated with normal polyspecific IgG inhibits streptococcal superantigen-induced T cell proliferation and cytokine production by Norrby-Teglund A. (1996)
10.1128/iai.65.12.5209-5215.1997
10.1128/iai.62.9.3731-3738.1994
10.1093/infdis/170.3.585
10.1097/00006454-199602000-00012
10.1093/infdis/167.5.997
10.1093/clinids/15.2.277
10.1128/iai.64.3.870-877.1996
10.1007/978-1-4899-1825-3_75
10.1093/clinids/14.1.2
10.1056/NEJM198907063210101
10.1097/00001432-199106000-00014
10.1093/infdis/171.1.74
10.1001/jama.1993.03500030088038

Dates

Type	When
Created	5 years, 5 months ago (March 9, 2020, 3:45 p.m.)
Deposited	1 year, 11 months ago (Sept. 28, 2023, 6:54 a.m.)
Indexed	2 weeks, 5 days ago (Aug. 19, 2025, 6:42 a.m.)
Issued	26 years, 5 months ago (April 1, 1999)
Published	26 years, 5 months ago (April 1, 1999)
Published Print	26 years, 5 months ago (April 1, 1999)

Funders 0

None

BibTeX

@article{Basma_1999, title={Risk Factors in the Pathogenesis of Invasive Group A Streptococcal Infections: Role of Protective Humoral Immunity}, volume={67}, ISSN={1098-5522}, url={http://dx.doi.org/10.1128/iai.67.4.1871-1877.1999}, DOI={10.1128/iai.67.4.1871-1877.1999}, number={4}, journal={Infection and Immunity}, publisher={American Society for Microbiology}, author={Basma, Hesham and Norrby-Teglund, Anna and Guedez, Yajaira and McGeer, Allison and Low, Donald E. and El-Ahmedy, Omar and Schwartz, Benjamin and Kotb, Malak}, editor={Barbieri, J. T.}, year={1999}, month=apr, pages={1871–1877} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        19
      ]
    ],
    "date-time": "2025-08-19T10:42:54Z",
    "timestamp": 1755600174797
  },
  "reference-count": 53,
  "publisher": "American Society for Microbiology",
  "issue": "4",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            1999,
            4,
            1
          ]
        ],
        "date-time": "1999-04-01T00:00:00Z",
        "timestamp": 922924800000
      },
      "content-version": "tdm",
      "delay-in-days": 0,
      "URL": "https://journals.asm.org/non-commercial-tdm-license"
    }
  ],
  "content-domain": {
    "domain": [
      "journals.asm.org"
    ],
    "crossmark-restriction": true
  },
  "published-print": {
    "date-parts": [
      [
        1999,
        4
      ]
    ]
  },
  "abstract": "<jats:title>ABSTRACT</jats:title><jats:p>An impressive change in the epidemiology and severity of invasive group A streptococcal infections occurred in the 1980s, and the incidence of streptococcal toxic shock syndrome cases continues to rise. The reason for the resurgence of severe invasive cases remains a mystery\u2014has there been a change in the pathogen or in host protective immunity? To address these questions, we have studied 33 patients with invasive infection caused by genotypically indistinguishable M1T1 strains of<jats:italic>Streptococcus pyogenes</jats:italic>who had different disease outcomes. Patients were classified as having severe (<jats:italic>n</jats:italic>= 21) and nonsevere (<jats:italic>n</jats:italic>= 12) invasive infections based on the presence or absence of shock and organ failure. Levels of anti-M1 bactericidal antibodies and of anti-streptococcal superantigen neutralizing antibodies in plasma were significantly lower in both groups than in age- and geographically matched healthy controls (<jats:italic>P</jats:italic>&lt; 0.01). Importantly, the levels of these protective antibodies in plasma samples from severe and nonsevere invasive cases were not different. Together the data suggest that low levels of protective antibodies may contribute to host susceptibility to invasive streptococcal infection but do not modulate disease outcome. Other immunogenetic factors that regulate superantigen responses may influence the severity of systemic manifestations associated with invasive streptococcal infection.</jats:p>",
  "DOI": "10.1128/iai.67.4.1871-1877.1999",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2020,
        3,
        9
      ]
    ],
    "date-time": "2020-03-09T19:45:06Z",
    "timestamp": 1583783106000
  },
  "page": "1871-1877",
  "update-policy": "http://dx.doi.org/10.1128/asmj-crossmark-policy-page",
  "source": "Crossref",
  "is-referenced-by-count": 111,
  "title": "Risk Factors in the Pathogenesis of Invasive Group A Streptococcal Infections: Role of Protective Humoral Immunity",
  "prefix": "10.1128",
  "volume": "67",
  "author": [
    {
      "given": "Hesham",
      "family": "Basma",
      "sequence": "first",
      "affiliation": [
        {
          "name": "<!--label omitted: 1-->Veterans Affairs Medical Center, Research Service, Memphis, Tennessee 381041;"
        },
        {
          "name": "<!--label omitted: 2-->Departments of Surgery and of Microbiology and Immunology, University of Tennessee, Memphis, Tennessee 381632;"
        }
      ]
    },
    {
      "given": "Anna",
      "family": "Norrby-Teglund",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "<!--label omitted: 1-->Veterans Affairs Medical Center, Research Service, Memphis, Tennessee 381041;"
        }
      ]
    },
    {
      "given": "Yajaira",
      "family": "Guedez",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "<!--label omitted: 2-->Departments of Surgery and of Microbiology and Immunology, University of Tennessee, Memphis, Tennessee 381632;"
        }
      ]
    },
    {
      "given": "Allison",
      "family": "McGeer",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "<!--label omitted: 3-->Department of Microbiology, Mount Sinai Hospital, and the University of Toronto, Toronto, Ontario, Canada M5G 1X53; and"
        }
      ]
    },
    {
      "given": "Donald E.",
      "family": "Low",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "<!--label omitted: 3-->Department of Microbiology, Mount Sinai Hospital, and the University of Toronto, Toronto, Ontario, Canada M5G 1X53; and"
        }
      ]
    },
    {
      "given": "Omar",
      "family": "El-Ahmedy",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "<!--label omitted: 1-->Veterans Affairs Medical Center, Research Service, Memphis, Tennessee 381041;"
        }
      ]
    },
    {
      "given": "Benjamin",
      "family": "Schwartz",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "<!--label omitted: 4-->Centers for Disease Control and Prevention, Atlanta, Georgia 303334"
        }
      ]
    },
    {
      "given": "Malak",
      "family": "Kotb",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "<!--label omitted: 1-->Veterans Affairs Medical Center, Research Service, Memphis, Tennessee 381041;"
        },
        {
          "name": "<!--label omitted: 2-->Departments of Surgery and of Microbiology and Immunology, University of Tennessee, Memphis, Tennessee 381632;"
        }
      ]
    }
  ],
  "member": "235",
  "reference": [
    {
      "key": "e_1_3_2_2_2",
      "unstructured": "Alouf J. E. Knoll H. Kohler W. The family of mitogenic shock-inducing and superantigenic toxins from staphylococci and streptococci Sourcebook of bacterial protein toxins. Alouf J. E. Freer J. H. 1991 367 414 Academic Press London United Kingdom"
    },
    {
      "key": "e_1_3_2_3_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/IAI.66.5.2279-2283.1998"
    },
    {
      "key": "e_1_3_2_4_2",
      "first-page": "401",
      "article-title": "Primary structure and immunochemistry of group A streptococcal M proteins",
      "volume": "4",
      "author": "Beachey E. H.",
      "year": "1982",
      "unstructured": "Beachey E. H. Seyer J. M. Primary structure and immunochemistry of group A streptococcal M proteins.Semin. Infect. Dis.41982401410",
      "journal-title": "Semin. Infect. Dis."
    },
    {
      "key": "e_1_3_2_5_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1056/NEJM199601253340407"
    },
    {
      "key": "e_1_3_2_6_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0022-3476(96)70072-0"
    },
    {
      "key": "e_1_3_2_7_2",
      "unstructured": "Chatellier et al. Unpublished data."
    },
    {
      "key": "e_1_3_2_8_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/infdis/173.4.901"
    },
    {
      "key": "e_1_3_2_9_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0140-6736(94)90629-7"
    },
    {
      "key": "e_1_3_2_10_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1001/jama.1997.03540250046030"
    },
    {
      "key": "e_1_3_2_11_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1056/NEJM198707163170305"
    },
    {
      "key": "e_1_3_2_12_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1056/NEJM199608223350803"
    },
    {
      "key": "e_1_3_2_13_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF00196680"
    },
    {
      "key": "e_1_3_2_14_2",
      "first-page": "192",
      "article-title": "Severe group A streptococcal disease\u2014southern Ontario. Ontario Streptococcal Study Group",
      "volume": "17",
      "author": "Demers B.",
      "year": "1991",
      "unstructured": "Demers B. Low D. E. Simor A. E. Vellend H. Jamieson F. Walmsley S. Green K. Krishnan C. Severe group A streptococcal disease\u2014southern Ontario. Ontario Streptococcal Study Group.Can. Dis. Weekly Rep.171991192194",
      "journal-title": "Can. Dis. Weekly Rep."
    },
    {
      "key": "e_1_3_2_15_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/clind/16.6.792"
    },
    {
      "key": "e_1_3_2_16_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1097/00006454-199110001-00005"
    },
    {
      "key": "e_1_3_2_17_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF00918364"
    },
    {
      "key": "e_1_3_2_18_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/scientificamerican0691-58"
    },
    {
      "key": "e_1_3_2_19_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1017/S095026880006739X"
    },
    {
      "key": "e_1_3_2_20_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/nar/16.10.4667"
    },
    {
      "key": "e_1_3_2_21_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1001/jama.1993.03500030082037"
    },
    {
      "key": "e_1_3_2_22_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.3109/00365549009027073"
    },
    {
      "key": "e_1_3_2_23_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/infdis/166.1.31"
    },
    {
      "key": "e_1_3_2_24_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.65.9.3828-3833.1997"
    },
    {
      "key": "e_1_3_2_25_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0002-9343(97)00160-5"
    },
    {
      "key": "e_1_3_2_26_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1086/516540"
    },
    {
      "key": "e_1_3_2_27_2",
      "first-page": "92",
      "article-title": "Epidemiology and pathogenesis of streptococcal infection",
      "volume": "20",
      "author": "Kohler W.",
      "year": "1992",
      "unstructured": "Kohler W. Epidemiology and pathogenesis of streptococcal infection.Immun. Infekt.2019929298",
      "journal-title": "Immun. Infekt."
    },
    {
      "key": "e_1_3_2_28_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/CMR.8.3.411"
    },
    {
      "key": "e_1_3_2_29_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1097/00001432-199206000-00010"
    },
    {
      "key": "e_1_3_2_30_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.61.4.1194-1201.1993"
    },
    {
      "key": "e_1_3_2_31_2",
      "doi-asserted-by": "crossref",
      "first-page": "4089",
      "DOI": "10.4049/jimmunol.145.12.4089",
      "article-title": "Identification of an epitope of type 1 streptococcal M protein that is shared with a 43-kD protein of human myocardium and renal glomeruli",
      "volume": "145",
      "author": "Kraus W.",
      "year": "1990",
      "unstructured": "Kraus W. Dale J. B. Beachey E. H. Identification of an epitope of type 1 streptococcal M protein that is shared with a 43-kD protein of human myocardium and renal glomeruli.J. Immunol.145199040894093",
      "journal-title": "J. Immunol."
    },
    {
      "key": "e_1_3_2_32_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1442-200X.1996.tb03425.x"
    },
    {
      "key": "e_1_3_2_33_2",
      "doi-asserted-by": "crossref",
      "unstructured": "Low D. E. Schwartz B. McGeer A. The reemergence of severe group A streptococcal disease: an evolutionary perspective Emerging infections I. Scheld W. M. Armston D. Hughes J. M. 1997 93 123 American Society for Microbiology Washington D.C",
      "DOI": "10.1128/9781555816940.ch7"
    },
    {
      "key": "e_1_3_2_34_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.3109/00365549009027073"
    },
    {
      "key": "e_1_3_2_35_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1172/JCI116641"
    },
    {
      "key": "e_1_3_2_36_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/978-1-4899-1825-3_50"
    },
    {
      "key": "e_1_3_2_37_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/infdis/167.2.337"
    },
    {
      "key": "e_1_3_2_38_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/infdis/166.5.1014"
    },
    {
      "key": "e_1_3_2_39_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1086/514588"
    },
    {
      "key": "e_1_3_2_40_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.64.12.5395-5398.1996"
    },
    {
      "key": "e_1_3_2_41_2",
      "doi-asserted-by": "crossref",
      "first-page": "3057",
      "DOI": "10.4049/jimmunol.156.8.3057",
      "article-title": "Plasma from patients with severe invasive group A streptococcal infections treated with normal polyspecific IgG inhibits streptococcal superantigen-induced T cell proliferation and cytokine production",
      "volume": "156",
      "author": "Norrby-Teglund A.",
      "year": "1996",
      "unstructured": "Norrby-Teglund A. Kaul R. Low D. E. McGeer A. Andersson J. P. Andersson U. G. Kotb M. Plasma from patients with severe invasive group A streptococcal infections treated with normal polyspecific IgG inhibits streptococcal superantigen-induced T cell proliferation and cytokine production.J. Immunol.156199630573064",
      "journal-title": "J. Immunol."
    },
    {
      "key": "e_1_3_2_42_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.65.12.5209-5215.1997"
    },
    {
      "key": "e_1_3_2_43_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.62.9.3731-3738.1994"
    },
    {
      "key": "e_1_3_2_44_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/infdis/170.3.585"
    },
    {
      "key": "e_1_3_2_45_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1097/00006454-199602000-00012"
    },
    {
      "key": "e_1_3_2_46_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/infdis/167.5.997"
    },
    {
      "key": "e_1_3_2_47_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/clinids/15.2.277"
    },
    {
      "key": "e_1_3_2_48_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.64.3.870-877.1996"
    },
    {
      "key": "e_1_3_2_49_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/978-1-4899-1825-3_75"
    },
    {
      "key": "e_1_3_2_50_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/clinids/14.1.2"
    },
    {
      "key": "e_1_3_2_51_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1056/NEJM198907063210101"
    },
    {
      "key": "e_1_3_2_52_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1097/00001432-199106000-00014"
    },
    {
      "key": "e_1_3_2_53_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/infdis/171.1.74"
    },
    {
      "key": "e_1_3_2_54_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1001/jama.1993.03500030088038"
    }
  ],
  "container-title": "Infection and Immunity",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://journals.asm.org/doi/pdf/10.1128/IAI.67.4.1871-1877.1999",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://journals.asm.org/doi/pdf/10.1128/IAI.67.4.1871-1877.1999",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        9,
        28
      ]
    ],
    "date-time": "2023-09-28T10:54:34Z",
    "timestamp": 1695898474000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://journals.asm.org/doi/10.1128/IAI.67.4.1871-1877.1999"
    }
  },
  "subtitle": [],
  "editor": [
    {
      "given": "J. T.",
      "family": "Barbieri",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1999,
        4
      ]
    ]
  },
  "references-count": 53,
  "aliases": [
    "10.1128/.67.4.1871-1877.1999"
  ],
  "journal-issue": {
    "issue": "4",
    "published-print": {
      "date-parts": [
        [
          1999,
          4
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1128/IAI.67.4.1871-1877.1999"
  ],
  "URL": "http://dx.doi.org/10.1128/IAI.67.4.1871-1877.1999",
  "relation": {},
  "ISSN": [
    "0019-9567",
    "1098-5522"
  ],
  "subject": [],
  "container-title-short": "Infect Immun",
  "published": {
    "date-parts": [
      [
        1999,
        4
      ]
    ]
  },
  "assertion": [
    {
      "value": "1998-10-01",
      "order": 0,
      "name": "received",
      "label": "Received",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    },
    {
      "value": "1999-01-10",
      "order": 1,
      "name": "accepted",
      "label": "Accepted",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    },
    {
      "value": "1999-04-01",
      "order": 2,
      "name": "published",
      "label": "Published",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    }
  ]
}