Association of Antibody Responses to Fusobacterium nucleatum and Streptococcus gallolyticus Proteins with Colorectal Adenoma and Colorectal Cancer
Background Streptococcus gallolyticus subspecies gallolyticus (SGG) and Fusobacterium (F.) nucleatum have been implicated in colorectal carcinogenesis. Here, the association of immune responses to bacterial exposure with advancing stages of colorectal neoplasia was assessed by multiplex serology. Me...
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| Veröffentlicht in: | Digestive diseases and sciences 2023-08, Vol.68 (8), p.3300-3311 |
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| creator | Genua, Flavia Butt, Julia Waterboer, Tim Hughes, David J. |
| description | Background
Streptococcus gallolyticus subspecies gallolyticus
(SGG) and
Fusobacterium (F.) nucleatum
have been implicated in colorectal carcinogenesis. Here, the association of immune responses to bacterial exposure with advancing stages of colorectal neoplasia was assessed by multiplex serology.
Methods
Immunoglobulin (Ig) A and G antibody responses to eleven proteins each of
F. nucleatum
and SGG were measured in plasma of controls (
n
= 100) and patients with colorectal cancer (CRC,
n
= 25), advanced adenoma (
n
= 82), or small polyps (
n
= 85). Multivariable logistic regression was used to evaluate the association of bacterial sero-positivity with colorectal neoplasia. In a cohort subset with matched data (
n
= 45),
F. nucleatum
sero-positivity was correlated with bacterial abundance in both neoplastic and matched normal tissue.
Results
IgG sero-positivity to Fn1426 of
F. nucleatum
was associated with an increased CRC risk (OR = 4.84; 95% CI 1.46–16.0), while IgA sero-positivity to any SGG protein or specifically Gallo0272 and Gallo1675 alone was associated with increased advanced adenoma occurrence (OR = 2.02, 95% CI 1.10–3.71; OR = 2.67, 95% CI 1.10–6.46; and OR = 6.17, 95% CI 1.61–23.5, respectively). Only
F. nucleatum
abundance in the normal mucosa positively correlated with the IgA response to the Fn1426 antigen (Correlation coefficient (r) = 0.38,
p
|
| doi_str_mv | 10.1007/s10620-023-08001-4 |
| format | Article |
| fullrecord | <record><control><sourceid>gale_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_10352388</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><galeid>A757583254</galeid><sourcerecordid>A757583254</sourcerecordid><originalsourceid>FETCH-LOGICAL-c542t-77ef2f6face1575c97e02eff91332e69ca7101fe6846c73a856ae576e11235e03</originalsourceid><addsrcrecordid>eNp9UstuFDEQHCEQ2QR-gAOyxIXLBD_W9swJrVYkIEUC8ThbXm9742jGvdge0P4GX4w3G_JACPngdndVWdWqpnnB6CmjVL_JjCpOW8pFSztKWTt_1MyY1KLlUnWPmxllqtaMqaPmOOcrSmmvmXraHAktRKeYnjW_FjmjC7YEjAQ9WcQSVrjekc-QtxgzZFKQnE0ZV9YVSGEaSZzcALbUysY1-VISbAs6dG7KZGOHAYddCfvHp4QFQszkZyiXZIkDJnDFDmSxhoijvebfay9tdJCeNU-8HTI8v7lPmm9n774u37cXH88_LBcXrZNzXlqtwXOvvHVQPUvXa6AcvO-ZEBxU76xmlHlQ3Vw5LWwnlQWpFTDGhQQqTpq3B93ttBph7SCWZAezTWG0aWfQBvNwEsOl2eAPw6iQXHRdVXh9o5Dw-wS5mDFkB8NgI-CUDe-47jmTal6hr_6CXuGUYvVXUaKbSyF0f4eqawQTosf6sduLmoWuJjvB5V7r9B-oetYwBocRfKj9BwR-ILiEOSfwtyYZNfsomUOUTI2SuY6S2ZNe3l_PLeVPdipAHAC5juIG0p2l_8j-BhZ71mU</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2838453379</pqid></control><display><type>article</type><title>Association of Antibody Responses to Fusobacterium nucleatum and Streptococcus gallolyticus Proteins with Colorectal Adenoma and Colorectal Cancer</title><source>SpringerLink Journals</source><creator>Genua, Flavia ; Butt, Julia ; Waterboer, Tim ; Hughes, David J.</creator><creatorcontrib>Genua, Flavia ; Butt, Julia ; Waterboer, Tim ; Hughes, David J.</creatorcontrib><description>Background
Streptococcus gallolyticus subspecies gallolyticus
(SGG) and
Fusobacterium (F.) nucleatum
have been implicated in colorectal carcinogenesis. Here, the association of immune responses to bacterial exposure with advancing stages of colorectal neoplasia was assessed by multiplex serology.
Methods
Immunoglobulin (Ig) A and G antibody responses to eleven proteins each of
F. nucleatum
and SGG were measured in plasma of controls (
n
= 100) and patients with colorectal cancer (CRC,
n
= 25), advanced adenoma (
n
= 82), or small polyps (
n
= 85). Multivariable logistic regression was used to evaluate the association of bacterial sero-positivity with colorectal neoplasia. In a cohort subset with matched data (
n
= 45),
F. nucleatum
sero-positivity was correlated with bacterial abundance in both neoplastic and matched normal tissue.
Results
IgG sero-positivity to Fn1426 of
F. nucleatum
was associated with an increased CRC risk (OR = 4.84; 95% CI 1.46–16.0), while IgA sero-positivity to any SGG protein or specifically Gallo0272 and Gallo1675 alone was associated with increased advanced adenoma occurrence (OR = 2.02, 95% CI 1.10–3.71; OR = 2.67, 95% CI 1.10–6.46; and OR = 6.17, 95% CI 1.61–23.5, respectively). Only
F. nucleatum
abundance in the normal mucosa positively correlated with the IgA response to the Fn1426 antigen (Correlation coefficient (r) = 0.38,
p
< 0.01).
Conclusion
Antibody responses to SGG and
F. nucleatum
were associated with occurrence of colorectal adenomas and CRC, respectively. Further studies are needed to clarify the role these microbes or the immune response to their antigens may have in colorectal carcinogenesis stages.
Graphical Abstract</description><identifier>ISSN: 0163-2116</identifier><identifier>EISSN: 1573-2568</identifier><identifier>DOI: 10.1007/s10620-023-08001-4</identifier><identifier>PMID: 37338617</identifier><language>eng</language><publisher>New York: Springer US</publisher><subject>Adenoma ; Antibodies ; Biochemistry ; Colorectal cancer ; Gastroenterology ; Gram-negative bacteria ; Hepatology ; Immune response ; Immunoglobulin A ; Medicine ; Medicine & Public Health ; Oncology ; Original ; Original Article ; Proteins ; Streptococcus infections ; Transplant Surgery ; Tumors</subject><ispartof>Digestive diseases and sciences, 2023-08, Vol.68 (8), p.3300-3311</ispartof><rights>The Author(s) 2023</rights><rights>2023. The Author(s).</rights><rights>COPYRIGHT 2023 Springer</rights><rights>The Author(s) 2023. This work is published under http://creativecommons.org/licenses/by-nc/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c542t-77ef2f6face1575c97e02eff91332e69ca7101fe6846c73a856ae576e11235e03</citedby><cites>FETCH-LOGICAL-c542t-77ef2f6face1575c97e02eff91332e69ca7101fe6846c73a856ae576e11235e03</cites><orcidid>0000-0003-3724-7122</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s10620-023-08001-4$$EPDF$$P50$$Gspringer$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s10620-023-08001-4$$EHTML$$P50$$Gspringer$$Hfree_for_read</linktohtml><link.rule.ids>230,314,778,782,883,27907,27908,41471,42540,51302</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37338617$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Genua, Flavia</creatorcontrib><creatorcontrib>Butt, Julia</creatorcontrib><creatorcontrib>Waterboer, Tim</creatorcontrib><creatorcontrib>Hughes, David J.</creatorcontrib><title>Association of Antibody Responses to Fusobacterium nucleatum and Streptococcus gallolyticus Proteins with Colorectal Adenoma and Colorectal Cancer</title><title>Digestive diseases and sciences</title><addtitle>Dig Dis Sci</addtitle><addtitle>Dig Dis Sci</addtitle><description>Background
Streptococcus gallolyticus subspecies gallolyticus
(SGG) and
Fusobacterium (F.) nucleatum
have been implicated in colorectal carcinogenesis. Here, the association of immune responses to bacterial exposure with advancing stages of colorectal neoplasia was assessed by multiplex serology.
Methods
Immunoglobulin (Ig) A and G antibody responses to eleven proteins each of
F. nucleatum
and SGG were measured in plasma of controls (
n
= 100) and patients with colorectal cancer (CRC,
n
= 25), advanced adenoma (
n
= 82), or small polyps (
n
= 85). Multivariable logistic regression was used to evaluate the association of bacterial sero-positivity with colorectal neoplasia. In a cohort subset with matched data (
n
= 45),
F. nucleatum
sero-positivity was correlated with bacterial abundance in both neoplastic and matched normal tissue.
Results
IgG sero-positivity to Fn1426 of
F. nucleatum
was associated with an increased CRC risk (OR = 4.84; 95% CI 1.46–16.0), while IgA sero-positivity to any SGG protein or specifically Gallo0272 and Gallo1675 alone was associated with increased advanced adenoma occurrence (OR = 2.02, 95% CI 1.10–3.71; OR = 2.67, 95% CI 1.10–6.46; and OR = 6.17, 95% CI 1.61–23.5, respectively). Only
F. nucleatum
abundance in the normal mucosa positively correlated with the IgA response to the Fn1426 antigen (Correlation coefficient (r) = 0.38,
p
< 0.01).
Conclusion
Antibody responses to SGG and
F. nucleatum
were associated with occurrence of colorectal adenomas and CRC, respectively. Further studies are needed to clarify the role these microbes or the immune response to their antigens may have in colorectal carcinogenesis stages.
Graphical Abstract</description><subject>Adenoma</subject><subject>Antibodies</subject><subject>Biochemistry</subject><subject>Colorectal cancer</subject><subject>Gastroenterology</subject><subject>Gram-negative bacteria</subject><subject>Hepatology</subject><subject>Immune response</subject><subject>Immunoglobulin A</subject><subject>Medicine</subject><subject>Medicine & Public Health</subject><subject>Oncology</subject><subject>Original</subject><subject>Original Article</subject><subject>Proteins</subject><subject>Streptococcus infections</subject><subject>Transplant Surgery</subject><subject>Tumors</subject><issn>0163-2116</issn><issn>1573-2568</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>C6C</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><recordid>eNp9UstuFDEQHCEQ2QR-gAOyxIXLBD_W9swJrVYkIEUC8ThbXm9742jGvdge0P4GX4w3G_JACPngdndVWdWqpnnB6CmjVL_JjCpOW8pFSztKWTt_1MyY1KLlUnWPmxllqtaMqaPmOOcrSmmvmXraHAktRKeYnjW_FjmjC7YEjAQ9WcQSVrjekc-QtxgzZFKQnE0ZV9YVSGEaSZzcALbUysY1-VISbAs6dG7KZGOHAYddCfvHp4QFQszkZyiXZIkDJnDFDmSxhoijvebfay9tdJCeNU-8HTI8v7lPmm9n774u37cXH88_LBcXrZNzXlqtwXOvvHVQPUvXa6AcvO-ZEBxU76xmlHlQ3Vw5LWwnlQWpFTDGhQQqTpq3B93ttBph7SCWZAezTWG0aWfQBvNwEsOl2eAPw6iQXHRdVXh9o5Dw-wS5mDFkB8NgI-CUDe-47jmTal6hr_6CXuGUYvVXUaKbSyF0f4eqawQTosf6sduLmoWuJjvB5V7r9B-oetYwBocRfKj9BwR-ILiEOSfwtyYZNfsomUOUTI2SuY6S2ZNe3l_PLeVPdipAHAC5juIG0p2l_8j-BhZ71mU</recordid><startdate>20230801</startdate><enddate>20230801</enddate><creator>Genua, Flavia</creator><creator>Butt, Julia</creator><creator>Waterboer, Tim</creator><creator>Hughes, David J.</creator><general>Springer US</general><general>Springer</general><general>Springer Nature B.V</general><scope>C6C</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7RV</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BENPR</scope><scope>CCPQU</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>K9-</scope><scope>K9.</scope><scope>KB0</scope><scope>M0R</scope><scope>M0S</scope><scope>M1P</scope><scope>NAPCQ</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-3724-7122</orcidid></search><sort><creationdate>20230801</creationdate><title>Association of Antibody Responses to Fusobacterium nucleatum and Streptococcus gallolyticus Proteins with Colorectal Adenoma and Colorectal Cancer</title><author>Genua, Flavia ; Butt, Julia ; Waterboer, Tim ; Hughes, David J.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c542t-77ef2f6face1575c97e02eff91332e69ca7101fe6846c73a856ae576e11235e03</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Adenoma</topic><topic>Antibodies</topic><topic>Biochemistry</topic><topic>Colorectal cancer</topic><topic>Gastroenterology</topic><topic>Gram-negative bacteria</topic><topic>Hepatology</topic><topic>Immune response</topic><topic>Immunoglobulin A</topic><topic>Medicine</topic><topic>Medicine & Public Health</topic><topic>Oncology</topic><topic>Original</topic><topic>Original Article</topic><topic>Proteins</topic><topic>Streptococcus infections</topic><topic>Transplant Surgery</topic><topic>Tumors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Genua, Flavia</creatorcontrib><creatorcontrib>Butt, Julia</creatorcontrib><creatorcontrib>Waterboer, Tim</creatorcontrib><creatorcontrib>Hughes, David J.</creatorcontrib><collection>Springer Nature OA Free Journals</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Nursing & Allied Health Database</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>ProQuest Central</collection><collection>ProQuest One Community College</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>Consumer Health Database (Alumni Edition)</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Consumer Health Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Nursing & Allied Health Premium</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Digestive diseases and sciences</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Genua, Flavia</au><au>Butt, Julia</au><au>Waterboer, Tim</au><au>Hughes, David J.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Association of Antibody Responses to Fusobacterium nucleatum and Streptococcus gallolyticus Proteins with Colorectal Adenoma and Colorectal Cancer</atitle><jtitle>Digestive diseases and sciences</jtitle><stitle>Dig Dis Sci</stitle><addtitle>Dig Dis Sci</addtitle><date>2023-08-01</date><risdate>2023</risdate><volume>68</volume><issue>8</issue><spage>3300</spage><epage>3311</epage><pages>3300-3311</pages><issn>0163-2116</issn><eissn>1573-2568</eissn><abstract>Background
Streptococcus gallolyticus subspecies gallolyticus
(SGG) and
Fusobacterium (F.) nucleatum
have been implicated in colorectal carcinogenesis. Here, the association of immune responses to bacterial exposure with advancing stages of colorectal neoplasia was assessed by multiplex serology.
Methods
Immunoglobulin (Ig) A and G antibody responses to eleven proteins each of
F. nucleatum
and SGG were measured in plasma of controls (
n
= 100) and patients with colorectal cancer (CRC,
n
= 25), advanced adenoma (
n
= 82), or small polyps (
n
= 85). Multivariable logistic regression was used to evaluate the association of bacterial sero-positivity with colorectal neoplasia. In a cohort subset with matched data (
n
= 45),
F. nucleatum
sero-positivity was correlated with bacterial abundance in both neoplastic and matched normal tissue.
Results
IgG sero-positivity to Fn1426 of
F. nucleatum
was associated with an increased CRC risk (OR = 4.84; 95% CI 1.46–16.0), while IgA sero-positivity to any SGG protein or specifically Gallo0272 and Gallo1675 alone was associated with increased advanced adenoma occurrence (OR = 2.02, 95% CI 1.10–3.71; OR = 2.67, 95% CI 1.10–6.46; and OR = 6.17, 95% CI 1.61–23.5, respectively). Only
F. nucleatum
abundance in the normal mucosa positively correlated with the IgA response to the Fn1426 antigen (Correlation coefficient (r) = 0.38,
p
< 0.01).
Conclusion
Antibody responses to SGG and
F. nucleatum
were associated with occurrence of colorectal adenomas and CRC, respectively. Further studies are needed to clarify the role these microbes or the immune response to their antigens may have in colorectal carcinogenesis stages.
Graphical Abstract</abstract><cop>New York</cop><pub>Springer US</pub><pmid>37338617</pmid><doi>10.1007/s10620-023-08001-4</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0003-3724-7122</orcidid><oa>free_for_read</oa></addata></record> |
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| identifier | ISSN: 0163-2116 |
| ispartof | Digestive diseases and sciences, 2023-08, Vol.68 (8), p.3300-3311 |
| issn | 0163-2116 1573-2568 |
| language | eng |
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| source | SpringerLink Journals |
| subjects | Adenoma Antibodies Biochemistry Colorectal cancer Gastroenterology Gram-negative bacteria Hepatology Immune response Immunoglobulin A Medicine Medicine & Public Health Oncology Original Original Article Proteins Streptococcus infections Transplant Surgery Tumors |
| title | Association of Antibody Responses to Fusobacterium nucleatum and Streptococcus gallolyticus Proteins with Colorectal Adenoma and Colorectal Cancer |
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