Distinct patterns of IgG and IgA against food and microbial antigens in serum and feces of patients with inflammatory bowel diseases
Lisa Frehn, Anke Jansen, Eveline Bennek, Ana D Mandic, Ilknur Temizel, Stefanie Tischendorf, Julien Verdier, Frank Tacke, Konrad Streetz, Christian Trautwein, Gernot Sellge, Lisa Frehn, Anke Jansen, Eveline Bennek, Ana D Mandic, Ilknur Temizel, Stefanie Tischendorf, Julien Verdier, Frank Tacke, Konrad Streetz, Christian Trautwein, Gernot Sellge
Abstract
Background: Inflammatory bowel disease (IBD) is associated with a defective intestinal barrier and enhanced adaptive immune responses against commensal microbiota. Immune responses against food antigens in IBD patients remain poorly defined.
Methods: IgG and IgA specific for food and microfloral antigens (wheat and milk extracts; purified ovalbumin; Escherichia coli and Bacteroides fragilis lysates; mannan from Saccharomyces cerevisiae) were analyzed by ELISA in the serum and feces of patients with Crohn's disease (CD; n = 52 for serum and n = 20 for feces), ulcerative colitis (UC; n = 29; n = 17), acute gastroenteritis/colitis (AGE; n = 12; n = 9) as well as non-inflammatory controls (n = 61; n = 39).
Results: Serum anti-Saccharomyces cerevisiae antibodies (ASCA) and anti-B. fragilis IgG and IgA levels were increased in CD patients whereas antibody (Ab) levels against E. coli and food antigens were not significantly different within the patient groups and controls. Subgroup analysis revealed that CD patients with severe diseases defined by stricturing and penetrating lesions have slightly higher anti-food and anti-microbial IgA levels whereas CD and UC patients with arthropathy have decreased anti-food IgG levels. Treatment with anti-TNF-α Abs in CD patients was associated with significantly decreased ASCA IgG and IgA and anti-E. coli IgG. In the feces specific IgG levels against all antigens were higher in CD and AGE patients while specific IgA levels were higher in non-IBD patients. Anti-food IgG and IgA levels did not correlate with food intolerance.
Summary: In contrast to anti-microbial Abs, we found only minor changes in serum anti-food Ab levels in specific subgroups of IBD patients. Fecal Ab levels towards microbial and food antigens show distinct patterns in controls, CD and UC patients.
Conflict of interest statement
Competing Interests: Gernot Sellge is a PLOS ONE Editorial Board member. This does not alter the authors' adherence to PLOS ONE Editorial policies and criteria.
Figures
![Figure 1. Serum IgG and IgA levels…](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4162554/bin/pone.0106750.g001.jpg)
![Figure 2. Anti-food and anti-microbial serum IgG…](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4162554/bin/pone.0106750.g002.jpg)
Figure 3. Anti-food and anti-microbial serum IgG…
Figure 3. Anti-food and anti-microbial serum IgG and IgA levels in CD patients with or…
Figure 4. Anti-food and anti-microbial serum IgG…
Figure 4. Anti-food and anti-microbial serum IgG and IgA levels in CD patients with or…
Figure 5. Fecal IgG and IgA levels…
Figure 5. Fecal IgG and IgA levels specific for food and microbial antigens in IBD…
- Anti-food and anti-microbial IgG subclass antibodies in inflammatory bowel disease.Jansen A, Mandić AD, Bennek E, Frehn L, Verdier J, Tebrügge I, Lutz H, Streetz K, Trautwein C, Sellge G. Jansen A, et al. Scand J Gastroenterol. 2016 Dec;51(12):1453-1461. doi: 10.1080/00365521.2016.1205130. Epub 2016 Jul 25. Scand J Gastroenterol. 2016. PMID: 27455092
- Clinical significance of soluble immunoglobulins A and G and their coated bacteria in feces of patients with inflammatory bowel disease.Lin R, Chen H, Shu W, Sun M, Fang L, Shi Y, Pang Z, Wu W, Liu Z. Lin R, et al. J Transl Med. 2018 Dec 17;16(1):359. doi: 10.1186/s12967-018-1723-0. J Transl Med. 2018. PMID: 30558634 Free PMC article.
- Higher titers of anti-Saccharomyces cerevisiae antibodies IgA and IgG are associated with more aggressive phenotypes in Romanian patients with Crohn's disease.Gologan S, Iacob R, Preda C, Vadan R, Cotruta B, Catuneanu AM, Iacob S, Constantinescu I, Gheorghe L, Iobagiu S, Gheorghe C, Diculescu M. Gologan S, et al. J Gastrointestin Liver Dis. 2012 Mar;21(1):39-44. J Gastrointestin Liver Dis. 2012. PMID: 22457858
- Reappraisal of antibodies against Saccharomyces cerevisiae (ASCA) as persistent biomarkers in quiescent Crohn's disease.Duarte-Silva M, Afonso PC, de Souza PR, Peghini BC, Rodrigues-Júnior V, de Barros Cardoso CR. Duarte-Silva M, et al. Autoimmunity. 2019 Feb;52(1):37-47. doi: 10.1080/08916934.2019.1588889. Epub 2019 Mar 19. Autoimmunity. 2019. PMID: 30884988 Clinical Trial.
- Dynamic immunoglobulin responses to gut bacteria during inflammatory bowel disease.Rengarajan S, Vivio EE, Parkes M, Peterson DA, Roberson EDO, Newberry RD, Ciorba MA, Hsieh CS. Rengarajan S, et al. Gut Microbes. 2020 May 3;11(3):405-420. doi: 10.1080/19490976.2019.1626683. Epub 2019 Jun 16. Gut Microbes. 2020. PMID: 31203722 Free PMC article.
- Salivary IgA and IgG Antibody Responses against Periodontitis-Associated Bacteria in Crohn's Disease.Gürsoy M, Rautava J, Pussinen P, Kristoffersen AK, Enersen M, Loimaranta V, Gürsoy UK. Gürsoy M, et al. Int J Mol Sci. 2023 Jan 25;24(3):2385. doi: 10.3390/ijms24032385. Int J Mol Sci. 2023. PMID: 36768711 Free PMC article.
- Fcα Receptor-1-Activated Monocytes Promote B Lymphocyte Migration and IgA Isotype Switching.Bos AV, van Gool MMJ, Breedveld AC, van der Mast R, Marsman C, Bouma G, van de Wiel MA, van Ham SM, Mebius RE, van Egmond M. Bos AV, et al. Int J Mol Sci. 2022 Sep 22;23(19):11132. doi: 10.3390/ijms231911132. Int J Mol Sci. 2022. PMID: 36232432 Free PMC article.
- Preclinical stage abundance and nuclear antigen reactivity of faecal Immunoglobulin A vary among males and females of lupus-prone mouse models.Gudi R, Roy S, Sun W, Vasu C. Gudi R, et al. Immunology. 2022 Apr;165(4):497-507. doi: 10.1111/imm.13459. Epub 2022 Mar 1. Immunology. 2022. PMID: 35138645
- Irisin attenuates inflammation in a mouse model of ulcerative colitis by altering the intestinal microbiota.Huangfu LX, Cai XT, Yang JN, Wang HC, Li YX, Dai ZF, Yang RL, Lin XH. Huangfu LX, et al. Exp Ther Med. 2021 Dec;22(6):1433. doi: 10.3892/etm.2021.10868. Epub 2021 Oct 11. Exp Ther Med. 2021. PMID: 34707714 Free PMC article.
- Integrated Analysis of Multiple Microarray Studies to Identify Novel Gene Signatures in Ulcerative Colitis.Chen ZA, Sun YF, Wang QX, Ma HH, Ma ZZ, Yang CJ. Chen ZA, et al. Front Genet. 2021 Jul 9;12:697514. doi: 10.3389/fgene.2021.697514. eCollection 2021. Front Genet. 2021. PMID: 34306038 Free PMC article.
-
- Ruel J, Ruane D, Mehandru S, Gower-Rousseau C, Colombel JF (2014) IBD across the age spectrum-is it the same disease? Nat Rev Gastroenterol Hepatol 11: 88–98. - PubMed
- Research Support, Non-U.S. Gov't
- Antigens / immunology*
- Case-Control Studies
- Crohn Disease / blood
- Crohn Disease / immunology
- Feces / microbiology*
- Food*
- Humans
- Immunoglobulin A / blood*
- Immunoglobulin G / blood*
- Inflammatory Bowel Diseases / blood
- Inflammatory Bowel Diseases / immunology*
- Inflammatory Bowel Diseases / microbiology
- Serum / microbiology*
- Tumor Necrosis Factor-alpha / antagonists & inhibitors
- Tumor Necrosis Factor-alpha / metabolism
- Antigens
- Immunoglobulin A
- Immunoglobulin G
- Tumor Necrosis Factor-alpha
- Full Text Sources
- Other Literature Sources
- Medical
- Miscellaneous
NCBI Literature Resources
The PubMed wordmark and PubMed logo are registered trademarks of the U.S. Department of Health and Human Services (HHS). Unauthorized use of these marks is strictly prohibited.
National Library of Medicine
8600 Rockville Pike
Bethesda, MD 20894
![Figure 3. Anti-food and anti-microbial serum IgG…](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4162554/bin/pone.0106750.g003.jpg)
Figure 4. Anti-food and anti-microbial serum IgG…
Figure 4. Anti-food and anti-microbial serum IgG and IgA levels in CD patients with or…
Figure 5. Fecal IgG and IgA levels…
Figure 5. Fecal IgG and IgA levels specific for food and microbial antigens in IBD…
- Anti-food and anti-microbial IgG subclass antibodies in inflammatory bowel disease.Jansen A, Mandić AD, Bennek E, Frehn L, Verdier J, Tebrügge I, Lutz H, Streetz K, Trautwein C, Sellge G. Jansen A, et al. Scand J Gastroenterol. 2016 Dec;51(12):1453-1461. doi: 10.1080/00365521.2016.1205130. Epub 2016 Jul 25. Scand J Gastroenterol. 2016. PMID: 27455092
- Clinical significance of soluble immunoglobulins A and G and their coated bacteria in feces of patients with inflammatory bowel disease.Lin R, Chen H, Shu W, Sun M, Fang L, Shi Y, Pang Z, Wu W, Liu Z. Lin R, et al. J Transl Med. 2018 Dec 17;16(1):359. doi: 10.1186/s12967-018-1723-0. J Transl Med. 2018. PMID: 30558634 Free PMC article.
- Higher titers of anti-Saccharomyces cerevisiae antibodies IgA and IgG are associated with more aggressive phenotypes in Romanian patients with Crohn's disease.Gologan S, Iacob R, Preda C, Vadan R, Cotruta B, Catuneanu AM, Iacob S, Constantinescu I, Gheorghe L, Iobagiu S, Gheorghe C, Diculescu M. Gologan S, et al. J Gastrointestin Liver Dis. 2012 Mar;21(1):39-44. J Gastrointestin Liver Dis. 2012. PMID: 22457858
- Reappraisal of antibodies against Saccharomyces cerevisiae (ASCA) as persistent biomarkers in quiescent Crohn's disease.Duarte-Silva M, Afonso PC, de Souza PR, Peghini BC, Rodrigues-Júnior V, de Barros Cardoso CR. Duarte-Silva M, et al. Autoimmunity. 2019 Feb;52(1):37-47. doi: 10.1080/08916934.2019.1588889. Epub 2019 Mar 19. Autoimmunity. 2019. PMID: 30884988 Clinical Trial.
- Dynamic immunoglobulin responses to gut bacteria during inflammatory bowel disease.Rengarajan S, Vivio EE, Parkes M, Peterson DA, Roberson EDO, Newberry RD, Ciorba MA, Hsieh CS. Rengarajan S, et al. Gut Microbes. 2020 May 3;11(3):405-420. doi: 10.1080/19490976.2019.1626683. Epub 2019 Jun 16. Gut Microbes. 2020. PMID: 31203722 Free PMC article.
- Salivary IgA and IgG Antibody Responses against Periodontitis-Associated Bacteria in Crohn's Disease.Gürsoy M, Rautava J, Pussinen P, Kristoffersen AK, Enersen M, Loimaranta V, Gürsoy UK. Gürsoy M, et al. Int J Mol Sci. 2023 Jan 25;24(3):2385. doi: 10.3390/ijms24032385. Int J Mol Sci. 2023. PMID: 36768711 Free PMC article.
- Fcα Receptor-1-Activated Monocytes Promote B Lymphocyte Migration and IgA Isotype Switching.Bos AV, van Gool MMJ, Breedveld AC, van der Mast R, Marsman C, Bouma G, van de Wiel MA, van Ham SM, Mebius RE, van Egmond M. Bos AV, et al. Int J Mol Sci. 2022 Sep 22;23(19):11132. doi: 10.3390/ijms231911132. Int J Mol Sci. 2022. PMID: 36232432 Free PMC article.
- Preclinical stage abundance and nuclear antigen reactivity of faecal Immunoglobulin A vary among males and females of lupus-prone mouse models.Gudi R, Roy S, Sun W, Vasu C. Gudi R, et al. Immunology. 2022 Apr;165(4):497-507. doi: 10.1111/imm.13459. Epub 2022 Mar 1. Immunology. 2022. PMID: 35138645
- Irisin attenuates inflammation in a mouse model of ulcerative colitis by altering the intestinal microbiota.Huangfu LX, Cai XT, Yang JN, Wang HC, Li YX, Dai ZF, Yang RL, Lin XH. Huangfu LX, et al. Exp Ther Med. 2021 Dec;22(6):1433. doi: 10.3892/etm.2021.10868. Epub 2021 Oct 11. Exp Ther Med. 2021. PMID: 34707714 Free PMC article.
- Integrated Analysis of Multiple Microarray Studies to Identify Novel Gene Signatures in Ulcerative Colitis.Chen ZA, Sun YF, Wang QX, Ma HH, Ma ZZ, Yang CJ. Chen ZA, et al. Front Genet. 2021 Jul 9;12:697514. doi: 10.3389/fgene.2021.697514. eCollection 2021. Front Genet. 2021. PMID: 34306038 Free PMC article.
-
- Ruel J, Ruane D, Mehandru S, Gower-Rousseau C, Colombel JF (2014) IBD across the age spectrum-is it the same disease? Nat Rev Gastroenterol Hepatol 11: 88–98. - PubMed
- Research Support, Non-U.S. Gov't
- Antigens / immunology*
- Case-Control Studies
- Crohn Disease / blood
- Crohn Disease / immunology
- Feces / microbiology*
- Food*
- Humans
- Immunoglobulin A / blood*
- Immunoglobulin G / blood*
- Inflammatory Bowel Diseases / blood
- Inflammatory Bowel Diseases / immunology*
- Inflammatory Bowel Diseases / microbiology
- Serum / microbiology*
- Tumor Necrosis Factor-alpha / antagonists & inhibitors
- Tumor Necrosis Factor-alpha / metabolism
- Antigens
- Immunoglobulin A
- Immunoglobulin G
- Tumor Necrosis Factor-alpha
- Full Text Sources
- Other Literature Sources
- Medical
- Miscellaneous
NCBI Literature Resources
The PubMed wordmark and PubMed logo are registered trademarks of the U.S. Department of Health and Human Services (HHS). Unauthorized use of these marks is strictly prohibited.
National Library of Medicine
8600 Rockville Pike
Bethesda, MD 20894
![Figure 4. Anti-food and anti-microbial serum IgG…](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4162554/bin/pone.0106750.g004.jpg)
Figure 5. Fecal IgG and IgA levels…
Figure 5. Fecal IgG and IgA levels specific for food and microbial antigens in IBD…
- Anti-food and anti-microbial IgG subclass antibodies in inflammatory bowel disease.Jansen A, Mandić AD, Bennek E, Frehn L, Verdier J, Tebrügge I, Lutz H, Streetz K, Trautwein C, Sellge G. Jansen A, et al. Scand J Gastroenterol. 2016 Dec;51(12):1453-1461. doi: 10.1080/00365521.2016.1205130. Epub 2016 Jul 25. Scand J Gastroenterol. 2016. PMID: 27455092
- Clinical significance of soluble immunoglobulins A and G and their coated bacteria in feces of patients with inflammatory bowel disease.Lin R, Chen H, Shu W, Sun M, Fang L, Shi Y, Pang Z, Wu W, Liu Z. Lin R, et al. J Transl Med. 2018 Dec 17;16(1):359. doi: 10.1186/s12967-018-1723-0. J Transl Med. 2018. PMID: 30558634 Free PMC article.
- Higher titers of anti-Saccharomyces cerevisiae antibodies IgA and IgG are associated with more aggressive phenotypes in Romanian patients with Crohn's disease.Gologan S, Iacob R, Preda C, Vadan R, Cotruta B, Catuneanu AM, Iacob S, Constantinescu I, Gheorghe L, Iobagiu S, Gheorghe C, Diculescu M. Gologan S, et al. J Gastrointestin Liver Dis. 2012 Mar;21(1):39-44. J Gastrointestin Liver Dis. 2012. PMID: 22457858
- Reappraisal of antibodies against Saccharomyces cerevisiae (ASCA) as persistent biomarkers in quiescent Crohn's disease.Duarte-Silva M, Afonso PC, de Souza PR, Peghini BC, Rodrigues-Júnior V, de Barros Cardoso CR. Duarte-Silva M, et al. Autoimmunity. 2019 Feb;52(1):37-47. doi: 10.1080/08916934.2019.1588889. Epub 2019 Mar 19. Autoimmunity. 2019. PMID: 30884988 Clinical Trial.
- Dynamic immunoglobulin responses to gut bacteria during inflammatory bowel disease.Rengarajan S, Vivio EE, Parkes M, Peterson DA, Roberson EDO, Newberry RD, Ciorba MA, Hsieh CS. Rengarajan S, et al. Gut Microbes. 2020 May 3;11(3):405-420. doi: 10.1080/19490976.2019.1626683. Epub 2019 Jun 16. Gut Microbes. 2020. PMID: 31203722 Free PMC article.
- Salivary IgA and IgG Antibody Responses against Periodontitis-Associated Bacteria in Crohn's Disease.Gürsoy M, Rautava J, Pussinen P, Kristoffersen AK, Enersen M, Loimaranta V, Gürsoy UK. Gürsoy M, et al. Int J Mol Sci. 2023 Jan 25;24(3):2385. doi: 10.3390/ijms24032385. Int J Mol Sci. 2023. PMID: 36768711 Free PMC article.
- Fcα Receptor-1-Activated Monocytes Promote B Lymphocyte Migration and IgA Isotype Switching.Bos AV, van Gool MMJ, Breedveld AC, van der Mast R, Marsman C, Bouma G, van de Wiel MA, van Ham SM, Mebius RE, van Egmond M. Bos AV, et al. Int J Mol Sci. 2022 Sep 22;23(19):11132. doi: 10.3390/ijms231911132. Int J Mol Sci. 2022. PMID: 36232432 Free PMC article.
- Preclinical stage abundance and nuclear antigen reactivity of faecal Immunoglobulin A vary among males and females of lupus-prone mouse models.Gudi R, Roy S, Sun W, Vasu C. Gudi R, et al. Immunology. 2022 Apr;165(4):497-507. doi: 10.1111/imm.13459. Epub 2022 Mar 1. Immunology. 2022. PMID: 35138645
- Irisin attenuates inflammation in a mouse model of ulcerative colitis by altering the intestinal microbiota.Huangfu LX, Cai XT, Yang JN, Wang HC, Li YX, Dai ZF, Yang RL, Lin XH. Huangfu LX, et al. Exp Ther Med. 2021 Dec;22(6):1433. doi: 10.3892/etm.2021.10868. Epub 2021 Oct 11. Exp Ther Med. 2021. PMID: 34707714 Free PMC article.
- Integrated Analysis of Multiple Microarray Studies to Identify Novel Gene Signatures in Ulcerative Colitis.Chen ZA, Sun YF, Wang QX, Ma HH, Ma ZZ, Yang CJ. Chen ZA, et al. Front Genet. 2021 Jul 9;12:697514. doi: 10.3389/fgene.2021.697514. eCollection 2021. Front Genet. 2021. PMID: 34306038 Free PMC article.
-
- Ruel J, Ruane D, Mehandru S, Gower-Rousseau C, Colombel JF (2014) IBD across the age spectrum-is it the same disease? Nat Rev Gastroenterol Hepatol 11: 88–98. - PubMed
- Research Support, Non-U.S. Gov't
- Antigens / immunology*
- Case-Control Studies
- Crohn Disease / blood
- Crohn Disease / immunology
- Feces / microbiology*
- Food*
- Humans
- Immunoglobulin A / blood*
- Immunoglobulin G / blood*
- Inflammatory Bowel Diseases / blood
- Inflammatory Bowel Diseases / immunology*
- Inflammatory Bowel Diseases / microbiology
- Serum / microbiology*
- Tumor Necrosis Factor-alpha / antagonists & inhibitors
- Tumor Necrosis Factor-alpha / metabolism
- Antigens
- Immunoglobulin A
- Immunoglobulin G
- Tumor Necrosis Factor-alpha
- Full Text Sources
- Other Literature Sources
- Medical
- Miscellaneous
![Figure 5. Fecal IgG and IgA levels…](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4162554/bin/pone.0106750.g005.jpg)
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Source: PubMed