Skip to main content

Advertisement

SpringerLink
Log in

Salivary Microbiota Associated with Immunoglobulin A Nephropathy

  • Host Microbe Interactions
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

This study aimed at investigating the salivary microbiota of 28 patients affected by immunoglobulin A nephropathy (IgAN). Fourteen healthy volunteers (HC) were used as control. Compared to HC, the number of some cultivable bacteria groups (e.g., total anaerobes) significantly (P < 0.05) decreased in the salivary samples of IgAN patients. Total bacteria from salivary samples of IgAN patients and HC subjects were analyzed by pyrosequencing of 16S rRNA gene. Paired t test showed no significant (P > 0.05) differences of alpha-diversity parameters (OTU, ACE, Chao1, and Shannon index) between the salivary samples of HC and IgAN patients. The difference for the community structure was further analyzed using three phylogeny-based beta-diversity measures. Compared to HC, the ratio between Firmicutes/Proteobacteria markedly decreased in IgAN patients. Gemella haemolysins, Granulicatella adiacens, and Veillonella parvula were positively associated (P < 0.05) with HC. Within the phylum Bacteroidetes, Prevotella species (Prevotella nigrescens, Prevotella intermedia, Prevotella pallens, and Prevotella salivae) were the highest in HC. The only exception was for Prevotella aurantiaca. Compared to HC, the percentage of abundance of some species, belonging to Pasteurellaceae family (e.g., Haemophylus parainfluenzae), increased in IgAN patients. Fusobacteriaceae (Fusobacterium) and Corynebacterium sp. also differed between the salivary samples of HC and IgAN patients.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Sekirov I, Russel SL, Antunes LCM, Finlay BB (2010) Gut microbiota in health and disease. Physiol Rev 90:859–904

    Article  CAS  PubMed  Google Scholar 

  2. Maukonen J, Matto J, Suihko ML, Saarela M (2008) Intra-individual diversity and similarity of salivary and faecal microbiota. J Med Microbiol 57:1560–1568

    Article  CAS  PubMed  Google Scholar 

  3. Bik ME, Long CD, Armitage GC, Loomer P, Emerson J et al (2010) Bacterial diversity in the oral cavity of ten healthy individuals. ISME J 4:962–974

    Article  PubMed Central  PubMed  Google Scholar 

  4. Ling Z, Kong J, Jia P, Wei C, Wang Y et al (2010) Analysis of oral microbiota in children with dental caries by PCR-DGGE and barcoded pyrosequencing. Microb Ecol 60:677–690

    Article  CAS  PubMed  Google Scholar 

  5. Lockhart PB, Durak DT (1999) Oral microflora as a cause of endocarditis and other distant site infections. Infect Dis Clin N Am 13:833–850

    Article  CAS  Google Scholar 

  6. Beck JD, Eke P, Heiss G, Manadios P, Couper D et al (2005) Periodontal disease and coronary heart disease: a reappraisal of the exposure. Circulation 112:19–24

    Article  PubMed  Google Scholar 

  7. Ahn J, Chen CY, Hayes RB (2012) Oral microbiome and oral and gastrointestinal cancer risk. Cancer Causes Control 23:399–404

    Article  PubMed Central  PubMed  Google Scholar 

  8. Paju S, Scannapeico FA (2007) Oral biofilm, periodontitis, and pulmonary infections. Oral Dis 13:508–512

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  9. Koren O, Spor A, Felin J, Fak F, Stombaugh J et al (2011) Human oral, gut, and plaque microbiota in patients with atherosclerosis. Proc Natl Acad Sci U S A 108:4592–4598

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  10. Silva-Boghossian C, Castro GF, Teles RP, De Souza IP, Colombo AP (2008) Salivary microbiota of HIV-positive children and its correlation with HIV status, oral diseases, and total secretory IgA. Int J Pediatr Dent 18:205–216

    Article  Google Scholar 

  11. Boggess KA, Beck JD, Murtha AP, Moss K, Offenbacher S (2006) Maternal periodontal disease in early pregnancy and risk for a small-for-gestational-age infant. Am J Obstet Gynecol 194:1316–1322

    Article  PubMed  Google Scholar 

  12. Akar H, Akar GC, Carrero JJ, Stenvinkel P, Lindholm B (2011) Systemic consequences of poor oral health in chronic kidney disease patients. Clin J Am Soc Nephrol 6:218–226

    Article  PubMed  Google Scholar 

  13. Craig RG, Kotanko P, Kamer AR, Levin NW (2007) Periodontal diseases–a modifiable source of systemic inflammation for the end-stage renal disease patient on haemodialysis therapy? Nephrol Dial Transplant 22:312–315

    Article  PubMed  Google Scholar 

  14. Moriyama T, Nitta K (2011) Tonsilletomy and steroid pulse therapy for IgA nefropathy. Tohoku J Exp Med 224:243–250

    Article  CAS  PubMed  Google Scholar 

  15. Nagasawa Y, Iio K, Fukuda S, Date Y, Iwatani H et al (2014) Periodontal disease bacteria specific to tonsil in IgA nephropathy patients predicts the remission by the treatment. PLoS One 9:e81636. doi:10.1371/journal.pone.0081636

    Article  PubMed Central  PubMed  Google Scholar 

  16. Glassock RJ, Lee G (2009) Immunoglobulin A nephropathy. In: Ponticelli C, Glassock RJ (eds) Treatment of primary glomerulonephritis. Oxford University Press, Oxford, pp 313–361

    Chapter  Google Scholar 

  17. Manno C, Strippoli GF, D’Altri C, Torres D, Rossini M et al (2007) A novel simpler histological classification for renal survival in IgA nephropathy: a retrospective study. Am J Kidney Dis 49:763–775

    Article  PubMed  Google Scholar 

  18. Kiryluk K, Novak J, Gharavi AG (2013) Pathogenesis of immunoglobulin A nephropathy: recent insight from genetic studies. Annu Rev Med 64:339–356

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  19. Glassock RJ (2011) The pathogenesis of IgA nephropathy. Curr Opin Nephrol Hypertens 20:153–160

    Article  CAS  PubMed  Google Scholar 

  20. Yu HH, Chu KH, Yang YH, Lee JH, Wang LC et al (2011) Genetics and immunopathogenesis of IgA nephropathy. Clin Rev Allerg Immunol 41:198–213

    Article  CAS  Google Scholar 

  21. Soylu A, Kasap B, Soylu OB, Türkmen M, Kavukçu S (2007) Does feeding in infancy effect the development of IgA nephropathy? Pediatr Nephrol 22:1040–1044

    Article  PubMed  Google Scholar 

  22. McCarthy DD, Kujawa J, Wilson C, Papandile A, Poreci U et al (2011) Mice overexpressing BAFF develop a commensal flora-dependent, IgA-associated nephropathy. J Clin Investig 121:3991–4002

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  23. De Angelis M, Montemurno E, Piccolo M, Vannini L, Lauriero G et al (2014) Microbiota and metabolome associated with immunoglobulin A nephropathy (IgAN). PLoS One 9:e99006. doi:10.1371/journal.pone.0099006

    Article  PubMed Central  PubMed  Google Scholar 

  24. Meng H, Ohtake H, Ishida A, Ohta N, Kakehata S (2012) IgA production and tonsillar focal infection in IgA nephropathy. J Clin Exp Hematop 52:161–170

    Article  PubMed  Google Scholar 

  25. Sharmin S, Shimizu Y, Hagiwara M, Hirayama K, Koyama A (2004) Staphylococcus aureus antigens induce IgA-type glomerulonephritis in Balb/c mice. J Nephrol 17:504–511

    CAS  PubMed  Google Scholar 

  26. Yamamoto C, Suzuki S, Kimura H, Yoshida H, Gejyo F (2002) Experimental nephropathy induced by Haemophilus parainfluenzae antigens. Nephron 90:320–327

    Article  CAS  PubMed  Google Scholar 

  27. De Angelis M, Piccolo M, Vannini L, Siragusa S, De Giacomo A et al (2013) Fecal microbiota and metabolome of children with autism and pervasive developmental disorder not otherwise specified. PLoS One 8:e76993. doi:10.1371/journal.pone.0076993

    Article  PubMed Central  PubMed  Google Scholar 

  28. Suchodolski JS, Dowd SE, Wilke V, Steiner JM, Jergens AE (2012) 16S rRNA gene pyrosequencing reveals bacterial dysbiosis in the duodenum of dogs with idiopathic inflammatory bowel disease. PLoS One 7:e39333. doi:10.1371/journal.pone.0039333

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  29. Gontcharova V, Youn E, Wolcott RD, Hollister EB, Gentry TJ et al (2010) Black box chimera check (B2C2): a windows-based software for batch depletion of chimeras from bacterial 16S rRNA gene datasets. Open Microbiol J 4:47–52

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  30. Dowd SE, Zaragoza J, Rodriguez JR, Oliver MJ, Payton PR (2005) Windows.NET network distributed basic local alignment search toolkit (W.ND-BLAST). BMC Bioinf 6:93

    Article  Google Scholar 

  31. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461

    Article  CAS  PubMed  Google Scholar 

  32. Cole JR, Wang Q, Cardenas E, Fish J, Chai B et al (2009) The ribosomal database project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:D141–D145. doi:10.1093/nar/gkn879

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  33. Scannapieco FA (2013) The oral microbiome: its role in health and in oral and systemic infections. Clin Microbiol Newsl 35:163–169

    Article  Google Scholar 

  34. Kumar PS, Griffen AL, Moeschberger ML, Leys EJ (2005) Identification of candidate periodontal pathogens and beneficial species by quantitative 16S clonal analysis. J Clin Microbiol 43:3944–3955

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  35. Petersen PE (2003) The world oral health report 2003: continuous improvement of oral health in the 21st century-the approach of the WHO global oral health programme. Community Dent Oral Epidemiol 31:3–23

    Article  PubMed  Google Scholar 

  36. Ling Z, Xia L, Yuezhu W, Lanjuan L, Xiang C (2013) Pyrosequencing analysis of the salivary microbiota of healthy Chinese children and adults. Microb Ecol 65:487–495

    Article  PubMed  Google Scholar 

  37. Huttenhower C, Gevers D, Knight R, Abubucker S, Badger JH (2012) Structure, function and diversity of the healthy human microbiome. Nature 486:207–214

    Article  CAS  Google Scholar 

  38. Huse S, Ye Y, Zhou Y, Fodor AA (2012) A core human microbiome as viewed through 16S rRNA sequence clusters. PLoS One 7:e34242. doi:10.1371/journal.pone.0034242

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  39. Francavilla R, Ercolini D, Piccolo M, Vannini L, Siragusa S et al (2014) Salivary microbiota and metabolome associated with celiac desease. Appl Environ Microbiol 80:3416–3425

    Article  PubMed Central  PubMed  Google Scholar 

  40. Takeshita T, Nakano Y, Kumagai T, Yasui M, Kamio N et al (2009) The ecological proportion of indigenous bacterial populations in saliva is correlated with oral health status. ISME J 3:65–78

    Article  CAS  PubMed  Google Scholar 

  41. Eitner F, Floege J (2008) Bacterial protease for the treatment of IgA nephropathy. Nephrol Dial Transplant 23:2173–2175

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was partly supported by Immunonephrology Working Group ERA-EDTA. We thank Sonya Siragusa (Department of Soil, Plant and Food Sciences, University of Bari Aldo Moro, Bari, Italy) and Valentina Maranzano (DETO, Nephrology Unit–University of Bari Aldo Moro, Bari) for technical assistance.

Author information

Authors and Affiliations

  1. Department of Soil, Plant and Food Sciences, University of Bari Aldo Moro, via Amendola 165/a, 70126, Bari, Italy

    Maria Piccolo, Maria De Angelis, Raffaella Di Cagno & Marco Gobbetti

  2. Nephrology Unit, Department of Emergency and Organ Transplantation, University of Bari Aldo Moro, Bari, Italy

    Gabriella Lauriero, Eustacchio Montemurno & Loreto Gesualdo

Authors
  1. Maria Piccolo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maria De Angelis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gabriella Lauriero
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Eustacchio Montemurno
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Raffaella Di Cagno
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Loreto Gesualdo
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Marco Gobbetti
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maria De Angelis.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Piccolo, M., De Angelis, M., Lauriero, G. et al. Salivary Microbiota Associated with Immunoglobulin A Nephropathy. Microb Ecol 70, 557–565 (2015). https://doi.org/10.1007/s00248-015-0592-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-015-0592-9

Keywords

Search

Navigation