The Journal of Allergy and Clinical Immunology
Volume 121, Issue 1 , Pages 129-134 , January 2008

Reduced diversity in the early fecal microbiota of infants with atopic eczema

  • Mei Wang, PhD

      Affiliations

    • Department of Food Technology, Engineering and Nutrition, Lund University, Lund, Sweden
  • ,
  • Caroline Karlsson, MSc

      Affiliations

    • Department of Food Technology, Engineering and Nutrition, Lund University, Lund, Sweden
  • ,
  • Crister Olsson, PhD

      Affiliations

    • Department of Food Technology, Engineering and Nutrition, Lund University, Lund, Sweden
  • ,
  • Ingegerd Adlerberth, MD, PhD

      Affiliations

    • Department of Clinical Bacteriology, Göteborg University, Göteborg, Sweden
  • ,
  • Agnes E. Wold, MD, PhD

      Affiliations

    • Department of Clinical Bacteriology, Göteborg University, Göteborg, Sweden
  • ,
  • David P. Strachan, MD, PhD

      Affiliations

    • Division of Community Health Sciences, St George's, University of London, London, United Kingdom
  • ,
  • Paolo M. Martricardi, MD

      Affiliations

    • Department of Pediatric Pneumology and Immunology, Charité Medical University, Berlin, Germany
  • ,
  • Nils Åberg, MD, PhD

      Affiliations

    • Department of Paediatrics, Göteborg University, Göteborg, Sweden
  • ,
  • Michael R. Perkin, MD, PhD

      Affiliations

    • Division of Community Health Sciences, St George's, University of London, London, United Kingdom
  • ,
  • Salvatore Tripodi, MD

      Affiliations

    • Pediatric Allergology Unit, Sandro Pertini Hospital, Rome, Italy
  • ,
  • Anthony R. Coates, MD, PhD

      Affiliations

    • Medical Microbiology, Department of Cellular and Molecular Medicine, St George's, University of London, London, United Kingdom
  • ,
  • Bill Hesselmar, MD, PhD

      Affiliations

    • Department of Paediatrics, Göteborg University, Göteborg, Sweden
  • ,
  • Robert Saalman, MD, PhD

      Affiliations

    • Department of Paediatrics, Göteborg University, Göteborg, Sweden
  • ,
  • Göran Molin, PhD

      Affiliations

    • Department of Food Technology, Engineering and Nutrition, Lund University, Lund, Sweden
  • ,
  • Siv Ahrné, PhD

      Affiliations

    • Department of Food Technology, Engineering and Nutrition, Lund University, Lund, Sweden
    • Corresponding Author InformationReprint requests: Siv Ahrné, PhD, Applied Nutrition, PO Box 124, SE-22100 Lund, Sweden.

Received 4 June 2007 ,Revised 5 September 2007 ,Accepted 10 September 2007.

References 

  1. Eichenfield LF, Hanifin JM, Beck LA, Lemanske RF, Sampson HA, Weiss ST, et al. Atopic dermatitis and asthma: parallels in the evolution of treatment. Pediatrics. 2003;111:608–616
  2. Strachan DP. Hay fever, hygiene and household size. BMJ. 1989;289:1259–1260
  3. Bach JF. The effects on infections on suspectibility to autoimmune and allergic diseases. N Engl J Med. 2002;347:911–920
  4. Bauer H, Horowitz RE, Levenson SM, Popper H. The response of the lymphatic tissue to microbial flora. Studies on germfree mice. Am J Pathol. 1963;42:471–483
  5. Maeda Y, Noda S, Tanaka K, Sawamura SA, Alba Y, Ishikawa H, et al. The failure of oral tolerance induction is functionally coupled to the absence of T-cells in Peyers patches under germfree conditions. Immunobiology. 2001;204:442–457
  6. Sudo N, Sawamura S, Tanaka K, Aiba Y, Kubo C, Koga Y. The requirement of intestinal bacterial flora for the development of an IgE production system fully susceptible to oral tolerance induction. J Immunol. 1977;159:1739–1745
  7. Matricardi PM, Rosmini F, Riondino S, Fortini M, Ferrigno L, Rapicetta M, et al. Exposure to foodborne and orofaecal microbes versus airborne viruses in relation to atopy and allergic asthma: epidemiological study. BMJ. 2000;320:412–417
  8. Adlerberth I, Carlsson B, deMan P, Jalil F, Khan SR, Larsson P, et al. Intestinal colonization with Enterobacteriacae in Pakistani and Swedish hospital-delivered infants. Acta Paediatr Scand. 1991;80:602–610
  9. Adlerberth I, Jalil F, Hansson LÅ, Carlsson B, Mellander L, Larsson P, et al. High turn-over rate of Escherichia coli strains in the intestinal flora of infantas in Pakistan. Epidemiol Infect. 1998;12:587–598
  10. Wold AE. The hygiene hypothesis revised: is the rising frequency of allergy due to changes in the intestinal flora?. Allergy. 1998;53(suppl):20–25
  11. Kalliomäki M, Kirjavainen P, Eerola E, Pentti K, Salmimen S, Isolari E. Distinct patterns of neonatal gut microflora in infants in whom atopy was and was not developing. J Allergy Clin Immunol. 2001;107:129–134
  12. Kirjavainen PV, Arvola T, Salminen SJ, Isolari E. Aberrant composition of gut microbiota of allergic infants: a target of bifidobacterial therapy at weaning. Gut. 2002;51:51–55
  13. Watnabe S, Narisawa Y, Arase S. Differences in faecal microflora between patients with atopic dermatitis and healthy control subjects. J Allergy Clin Immunol. 2003;111:587–591
  14. Penders J, Thijs C, van den Brandt PA, Kummeling I, Snijders B, Stelma F, et al. Gut microbiota composition and development of atopic manifestations in infancy: the KOALA birth cohort study. Gut. 2007;56:661–667
  15. Adlerberth I, Strachan DP, Matricardi PM, Ahrné S, Orfei L, Åberg N, et al. Gut microbiota and development of atopic eczema in three European birth cohorts. J Allergy Clin Immunol. 2007;120:343–350
  16. Wang X, Heazlewood SP, Krause DO, Florin TH. Molecular characterization of microbial species that colonize human ileal and colonic mucosa by using 16S rDNA sequence analysis. J Appl Microbiol. 2003;95:508–520
  17. Wang M, Ahrné S, Jeppsson B, Molin G. Comparison of bacterial diversity along the human intestinal tract by direct cloning and sequencing of 16S rRNA genes. FEMS Microbiol Ecol. 2005;54:219–231
  18. Schwieger F, Tebbe CT. A new approach to utilize PCR-single-strand conformation polymorphism for 16S rRNA gene-based microbial community analysis. Appl Environ Microbiol. 1998;64:4870–4876
  19. Marsh TL. Terminal restriction fragment length polymorphism (T-RFLP): an emerging method for characterizing diversity among homologous populations of amplification products. Curr Opin Microbiol. 1999;2:323–327
  20. Valinski L, Della Vedova G, Jiang T, Borneman J. Oligonucleotide fingerprinting of rRNA genes for analysis of fungal community composition. Appl Environ Microbiol. 2002;68:5999–6004
  21. Ott SJ, Musfeldt M, Wenderoth DF, Hampe J, Brant O, Fölsch UR, et al. Reduction in diversity of the colonic mucosa associated bacterial microflora in patients with active inflammatory disease. Gut. 2004;53:685–693
  22. Wang M, Ahrné S, Antonsson M, Molin G. T-RFLP combined with principal component analysis and 16S rRNA gene sequencing: an effective strategy for comparison of faecal microbiota in infants of different ages. J Microbiol Methods. 2004;59:53–69
  23. Zoetendal EG, Akkermans ADL, de Vos WM. Temperature gradient gel electrophoresis analysis of 16S rRNA from human faecal samples reveals stable and host-specific communities of active bacteria. Appl Environ Microbiol. 1998;64:3854–3859
  24. Murray CS, Tannock GW, Simon MA, Harmsen HJM, Wellin GW, Custovic A, et al. Faecal microbiota in sensitized wheezy and non-sensitized non-wheezy children: a nested case control study. Clin Exp Allergy. 2005;35:741–745
  25. Williams HC. Diagnostic criteria for atopic dermatitis. Lancet. 1996;348:1391–1392
  26. Asher MI, Keil U, Anderson HR, Beasley R, Crane J, Martinez F, et al. International Study of Asthma and Allergies in Childhood (ISAAC): rationale and methods. Eur Respir J. 1995;8:483–491
  27. Tripodi S, Panetta V, Pelosi S, Pelosi U, Boner AL. Measurement of body surface area in atopic dermatitis using specific PC software (ScoradCard). Pediatr Allergy Immunol. 2004;15:96–101
  28. Bennet R, Nord CE. Development of the faecal anaerobic microflora after caesarean section and treatment with antibiotics in newborn infants. Infection. 1987;15:332–336
  29. Bezirtzoglou E. The intestinal microflora during the first weeks of life. Anaerobe. 1997;3:173–177
  30. Nübel U, Engelen B, Felske A, Snaidr J, Weishuber A, Amann RI, et al. Sequence heterogeneities of genes encoding 16S rRNAs in Paenibacillus polymyxa detected by temperature gradient gel electrophoresis. J Bacteriol. 1996;178:5636–5643
  31. Heuer H, Krsek M, Baker P, Smalla K, Wellington EMH. Analysis of Actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients. Appl Environ Microbiol. 1997;63:3233–3241
  32. Magurran AE. An index of diversity. In: Measuring biological diversity. Oxford: Blackwell Science Ltd; 2004;p. 100–133
  33. StataCorp . Stata Statistical Software: release 8.2. College Station (Tex): Stata Corp; 2005;
  34. Langendijk PS, Schaf F, Jansen GJ, Raangs GC, Kamphuis GR, Wilkinson MH, et al. Quantitative fluorescence in situ hybridization of Bifidobacterium spp. With genus-specific 16S rRNA-targeted probes and its application in faecal samples. Appl Environ Microbiol. 1995;61:3069–3075
  35. Suau A, Bonnet R, Sutren M. Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut. Appl Environ Microbiol. 1999;65:4799–4807
  36. Wintzingerode FV, Hoebel UB, Stackebrandt E. Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis. FEMS Microbiol Rev. 1997;21:213–229
  37. Dunbar J, Ticknor LO, Kuske CR. Assessment of microbial diversity in four southwestern United States soils by 16S rRNA gene terminal restriction fragment analysis. Appl Environ Microbiol. 2000;66:2943–2950
  38. Zoetendal EG, Collier CT, Koike S, Mackie RI, Gaskins HR. Molecular ecological analysis of the gastrointestinal microbiota: a review. J Nutr. 2004;134:465–472
  39. Olsson C, Ahrné S, Pettersson B, Molin G. DNA based classification of food associated Enterobacteriacae previously identified by Biolog GN Microplates. System Appl Microbiol. 2004;27:219–228
  40. Stark PL, Lee A. The microbial ecology of the large bowel of breast-fed and formula-fed infants during the first year of life. J Med Microbiol. 1982;15:189–203
  41. Penders J, Thijs C, Vink C, Stelma FF, Snijders B, Kummeling I, et al. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics. 2006;118:511–521

 Supported by the European Framework Programme 5 (QLRT-2000-00538) and by an unrestricted grant from Probi AB, Lund, Sweden.

 Disclosure of potential conflict of interest: C. Olsson owns stock in Probi AB. The rest of the authors have declared that they have no conflict of interest.

PII: S0091-6749(07)01767-8

doi: 10.1016/j.jaci.2007.09.011

The Journal of Allergy and Clinical Immunology
Volume 121, Issue 1 , Pages 129-134 , January 2008