Skip to main content

Advertisement

Log in

Analysis of Fecal Lactobacillus Community Structure in Patients with Early Rheumatoid Arthritis

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

The objective of this study was to analyze human fecal Lactobacillus community and its relationship with rheumatoid arthritis. Samples taken from rheumatoid arthritis (RA) patients and healthy individuals were analyzed by quantitative real-time PCR. Bacterial DNA was extracted from feces, and amplicons of the Lactobacillus-specific regions of 16S rRNA were analyzed by denaturing gradient gel electrophoresis. The richness, Shannon-Wiener index, and evenness of gut microbiota of both groups were analyzed to compare fecal Lactobacillus community structures. Results of this study demonstrated that fecal microbiota of RA patients contained significantly more Lactobacillus (10.62 ± 1.72 copies/g) than the control group (8.93 ± 1.60 copies/g). Significant increases were observed in RA patients in terms of the richness, Shannon-Wiener, and evenness measures, indicating more bacterial species, and increased bacterial diversity and abundance. These results suggest a potential relationship between Lactobacillus communities and the development and progression of rheumatoid arthritis.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Abdollahi-Roodsaz S, Joosten LA, Koenders MI, Devesa I, Roelofs MF, Radstake TR, Heuvelmans-Jacobs M, Akira S, Nicklin MJ, Ribeiro-Dias F, van den Berg WB (2008) Stimulation of TLR2 and TLR4 differentially skews the balance of T cells in a mouse model of arthritis. J Clin Invest 118(1):205–216. doi:10.1172/JCI32639

    Article  PubMed  CAS  Google Scholar 

  2. Amdekar S, Singh V, Singh R, Sharma P, Keshav P, Kumar A (2011) Lactobacillus casei reduces the inflammatory joint damage associated with collagen-induced arthritis (CIA) by reducing the pro-inflammatory cytokines: Lactobacillus casei: COX-2 inhibitor. J Clin Immunol 31(2):147–154. doi:10.1007/s10875-010-9457-7

    Article  PubMed  Google Scholar 

  3. Baharav E, Mor F, Halpern M, Weinberger A (2004) Lactobacillus GG bacteria ameliorate arthritis in Lewis rats. J Nutr 134(8):1964–1969

    PubMed  CAS  Google Scholar 

  4. Brisbin JT, Gong J, Parvizi P, Sharif S (2010) Effects of lactobacilli on cytokine expression by chicken spleen and cecal tonsil cells. Clin Vaccin Immunol 17(9):1337–1343. doi:10.1128/CVI.00143-10

    Article  CAS  Google Scholar 

  5. Devillard E, Burton JP, Reid G (2005) Complexity of vaginal microflora as analyzed by PCR denaturing gradient gel electrophoresis in a patient with recurrent bacterial vaginosis. Infect Dis Obstet Gynecol 13(1):25–31. doi:10.1080/10647440400025504

    Article  PubMed  CAS  Google Scholar 

  6. Edwards CJ (2008) Commensal gut bacteria and the etiopathogenesis of rheumatoid arthritis. J Rheumatol 35(8):1477–14797

    PubMed  Google Scholar 

  7. Forde BM, Neville BA, O’Donnell MM, Riboulet-Bisson E, Claesson MJ, Coghlan A, Ross RP, O’Toole PW (2011) Genome sequences and comparative genomics of two Lactobacillus ruminis strains from the bovine and human intestinal tracts. Microb Cell Fact 10(Suppl 1):S13. doi:10.1186/1475-2859-10-S1-S13

    Article  PubMed  Google Scholar 

  8. Hatakka K, Martio J, Korpela M, Herranen M, Poussa T, Laasanen T, Saxelin M, Vapaatalo H, Moilanen E, Korpela R (2003) Effects of probiotic therapy on the activity and activation of mild rheumatoid arthritis—a pilot study. Scand J Rheumatol 32(4):211–215

    Article  PubMed  CAS  Google Scholar 

  9. Hooper LV, Wong MH, Thelin A, Hansson L, Falk PG, Gordon JI (2001) Molecular analysis of commensal host-microbial relationships in the intestine. Science 291(5505):881–884. doi:10.1126/science.291.5505.881

    Article  PubMed  CAS  Google Scholar 

  10. Janczyk P, Pieper R, Smidt H, Souffrant WB (2007) Changes in the diversity of pig ileal lactobacilli around weaning determined by means of 16S rRNA gene amplification and denaturing gradient gel electrophoresis. FEMS Microbiol Ecol 61(1):132–140. doi:10.1111/j.1574-6941.2007.00317.x

    Article  PubMed  CAS  Google Scholar 

  11. Kano H, Kaneko T, Kaminogawa S (2002) Oral intake of Lactobacillus delbrueckii subsp. bulgaricus OLL1073R-1 prevents collagen-induced arthritis in mice. J Food Prot 65(1):153–160

    PubMed  Google Scholar 

  12. Lee JH, Valeriano VD, Shin YR, Chae JP, Kim GB, Ham JS, Chun J, Kang DK (2012) Genome sequence of Lactobacillus mucosae LM1, isolated from piglet feces. J Bacteriol 194(17):4766. doi:10.1128/JB.01011-12

    Article  PubMed  CAS  Google Scholar 

  13. Lee YK, Mazmanian SK (2010) Has the microbiota played a critical role in the evolution of the adaptive immune system? Science 330(6012):1768–1773. doi:10.1126/science.1195568

    Article  PubMed  CAS  Google Scholar 

  14. Lorca GL, Wadstrom T, Valdez GF, Ljungh A (2001) Lactobacillus acidophilus autolysins inhibit Helicobacter pylori in vitro. Curr Microbiol 42(1):39–44. doi:10.1007/s002840010175

    Article  PubMed  CAS  Google Scholar 

  15. Macklaim JM, Gloor GB, Anukam KC, Cribby S, Reid G (2011) At the crossroads of vaginal health and disease, the genome sequence of Lactobacillus iners AB-1. Proc Natl Acad Sci USA 108(Suppl 1):4688–4695. doi:10.1073/pnas.1000086107

    Article  PubMed  CAS  Google Scholar 

  16. Murata K, Hoshina T, Saito M, Ohkusu K, Yamamura K, Tanoue Y, Ihara K, Hara T (2012) Bacterial pericarditis caused by Lactobacillus iners in an infant. Diagn Microbiol Infect Dis 74(2):181–182. doi:10.1016/j.diagmicrobio.2012.06.008

    Article  PubMed  Google Scholar 

  17. Muyzer G, de Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59(3):695–700

    PubMed  CAS  Google Scholar 

  18. Noujaim JC, Andreatti Filho RL, Lima ET, Okamoto AS, Amorim RL, Neto RT (2008) Detection of T lymphocytes in intestine of broiler chicks treated with Lactobacillus spp. and challenged with Salmonella enterica serovar Enteritidis. Poult Sci 87(5):927–933. doi:10.3382/ps.2007-00476

    Article  PubMed  CAS  Google Scholar 

  19. Ou CC, Lin SL, Tsai JJ, Lin MY (2011) Heat-killed lactic acid bacteria enhance immunomodulatory potential by skewing the immune response toward Th1 polarization. J Food Sci 76(5):M260–M267. doi:10.1111/j.1750-3841.2011.02161.x

    Article  PubMed  CAS  Google Scholar 

  20. Penders J, Vink C, Driessen C, London N, Thijs C, Stobberingh EE (2005) Quantification of Bifidobacterium spp., Escherichia coli and Clostridium difficile in faecal samples of breast-fed and formula-fed infants by real-time PCR. FEMS Microbiol Lett 243(1):141–147. doi:10.1016/j.femsle.2004.11.052

    Article  PubMed  CAS  Google Scholar 

  21. Petersen ER, Claesson MH, Schmidt EG, Jensen SS, Ravn P, Olsen J, Ouwehand AC, Kristensen NN (2012) Consumption of probiotics increases the effect of regulatory T cells in transfer colitis. Inflamm Bowel Dis 18(1):131–142. doi:10.1002/ibd.21709

    Article  PubMed  Google Scholar 

  22. De Pineda L, Thompson SF, Summers K, de Leon F, Pope J, Reid G (2011) A randomized, double-blinded, placebo-controlled pilot study of probiotics in active rheumatoid arthritis. Med Sci Monit 17(6):CR347–CR354

    Article  Google Scholar 

  23. Sierra S, Lara-Villoslada F, Sempere L, Olivares M, Boza J, Xaus J (2010) Intestinal and immunological effects of daily oral administration of Lactobacillus salivarius CECT5713 to healthy adults. Anaerobe 16(3):195–200. doi:10.1016/j.anaerobe.2010.02.001

    Article  PubMed  Google Scholar 

  24. Simelyte E, Rimpilainen M, Lehtonen L, Zhang X, Toivanen P (2000) Bacterial cell wall-induced arthritis: chemical composition and tissue distribution of four Lactobacillus strains. Infect Immun 68(6):3535–3540

    Article  PubMed  CAS  Google Scholar 

  25. Simelyte E, Rimpilainen M, Zhang X, Toivanen P (2003) Role of peptidoglycan subtypes in the pathogenesis of bacterial cell wall arthritis. Ann Rheum Dis 62(10):976–982

    Article  PubMed  CAS  Google Scholar 

  26. So JS, Kwon HK, Lee CG, Yi HJ, Park JA, Lim SY, Hwang KC, Jeon YH, Im SH (2008) Lactobacillus casei suppresses experimental arthritis by down-regulating T helper 1 effect or functions. Mol Immunol 45(9):2690–2699. doi:10.1016/j.molimm.2007.12.010

    Article  PubMed  CAS  Google Scholar 

  27. So JS, Lee CG, Kwon HK, Yi HJ, Chae CS, Park JA, Hwang KC, Im SH (2008) Lactobacillus casei potentiates induction of oral tolerance in experimental arthritis. Mol Immunol 46(1):172–180. doi:10.1016/j.molimm.2008.07.038

    Article  PubMed  CAS  Google Scholar 

  28. Vaahtovuo J, Munukka E, Korkeamaki M, Luukkainen R, Toivanen P (2008) Fecal microbiota in early rheumatoid arthritis. J Rheumatol 35(8):1500–1505

    PubMed  CAS  Google Scholar 

  29. Walter J, Hertel C, Tannock GW, Lis CM, Munro K, Hammes WP (2001) Detection of Lactobacillus, Pediococcus, Leuconostoc, and Weissella species in human feces by using group-specific PCR primers and denaturing gradient gel electrophoresis. Appl Environ Microbiol 67(6):2578–2585. doi:10.1128/AEM.67.6.2578-2585.2001

    Article  PubMed  CAS  Google Scholar 

  30. Yuan J, Wei H, Zeng B, Tang H, Li W, Zhang Z (2010) Impact of neonatal antibiotic treatment on the biodiversity of the murine intestinal Lactobacillus community. Curr Microbiol 60(1):6–11. doi:10.1007/s00284-009-9492-x

    Article  PubMed  CAS  Google Scholar 

  31. Zoetendal EG, Cheng B, Koike S, Mackie RI (2004) Molecular microbial ecology of the gastrointestinal tract: from phylogeny to function. Curr Issues Intest Microbiol 5(2):31–47

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by the Natural Science Foundation of China (81072921) and National Basic Research Program of China (2013CB531406).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yongfei Fang.

Additional information

Xiaofei Liu and Benhua Zeng contributed equally to this study.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liu, X., Zou, Q., Zeng, B. et al. Analysis of Fecal Lactobacillus Community Structure in Patients with Early Rheumatoid Arthritis. Curr Microbiol 67, 170–176 (2013). https://doi.org/10.1007/s00284-013-0338-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-013-0338-1

Keywords

Navigation