Modern View on Microbiocenosis, Immune Response and Factors Influencing on Their Formation. Fundamental and Applied Aspects
https://doi.org/10.15690/vsp.v12i4.726
Abstract
This review of current literature summarizes results of scientific studies on the structure of the intestinal microbiota both of adults and infants. It is shown, that all intestinal microbiota of an adult consists of 395 phylogenetically isolated groups of microorganisms, among them 244 are absolutely new. Based on the RNA-sequencing of genes the most common among Caucasians enterotypes were detected. It was demonstrated, that specific structure of intestinal microbiota of an adult individual is unique and stable and that genetic background of the macroorganism is a base of intestinal microbiome formation. The article covers the issues of special characteristics of microbiocenosis development at the early stages of ontogenesis. It is emphasized, that prevalence of «infantile» species of bifidobacteria in the structure of intestinal microbiota of breast-fed infants is due to the presence of certain nutritive substances in the milk: oligosaccharides of the breast milk, which are natural prebiotics. The authors give criteria for including the nutrients into the group of prebiotics and show new experimental and clinical data on influence of prebiotics on different levels of immunological defense system.
Key words: intestinal microbiota, enterotypes, prebiotics, oligosaccharides, inulin, immune response.
About the Authors
N. M. Bogdanova
St. Petersburg State Pediatric Medical University, Russian Federation
Russian Federation
Bogdanova Natal’ya Mikhailovna, MD, assistant professor of the Department of Propedeutics of Child Diseases >
Russian Federation
Bogdanova Natal’ya Mikhailovna, MD, assistant professor of the Department of Propedeutics of Child Diseases >
E. M. Bulatova
St. Petersburg State Pediatric Medical University, Russian Federation
Russian Federation
Russian Federation
M. N. Wasia
St. Petersburg State Pediatric Medical University, Russian Federation
Russian Federation
Mary Nechesa Wasia
Russian Federation
Mary Nechesa Wasia
References
1. Shenderov B. A. Meditsinskaya mikrobnaya ekologiya i funktsional'noe pitanie. Tom II: «Sotsial'no-ekologicheskie i klinicheskie posledstviya disbalansa mikrobnoi ekologii cheloveka i zhivotnykh [Medical Bacterial Environmental Science and Functional Nutrition. Volume 2: Social, Ecological and Clinical Consequences of Microbial Misbalance of People and Animals]. Moscow, GRANT, 1998. 416 p.
2. Suau A., Bonnet R., Sutren M., Godon J. J., Gibson G. R., Collins M. D., Dore J. Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut. Appl. Environ. Microbiol. 1999; 65 (11): 4799–4807.
3. Egert M., de Graaf A. A., Smidt H., de Vos W. M., Venema K. Beyond diversity: functional microbiomics of the human colon. Trends Microbiol. 2006; 14: 86–91.
4. Qin J., Li R., Raes J., Arumugam M., Burgdorf K. S., Manichanh C. et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010; 464 (7285): 59–65.
5. Zhu B., Wang X., Li L. Human gut microbiome: the second genome of human body. Protein Cell. 2010; 1 (8): 718–725;
6. Eckburg P. B., Bik E. M., Bernstein C. N., Purdom E., Dethlefsen L., Sargent M., Gill S. R., Nelson K. E., Relman D. A. Science. 2005; 308 (5728): 1635–1638.
7. Arumugam M., Raes J., Pelletier E., Le Paslier D. Enterotypes of the human gut microbiome. Nature. 2011; 473 (7346): 174–180.
8. Zoetendal E. G., Akkermans A. D., De Vos W. M. Temperature gradient gel electrophoresis analysis of 16S rRNA from human fecal samples reveals stable and host-specific communities of active bacteria. Appl. Environ. Microbiol. 1998; 64 (10): 3854–3859.
9. Seksik P., Rigottier-Gois L., Gramet G. et al. Alterations of the dominant faecal bacterial groups in patients with Crohn’s disease of the colon. Gut. 2003; 52: 237–242.
10. Ly N. P., Litonjua A., Gold D. R., Celedon J. C. Gut microbiota, probiotics, and vitamin D: interrelated exposures influencing allergy, asthma, and obesity? J. Allergy Clin. Immunol. 2011; 127 (5): 1087–1094.
11. Sin D. D., Sutherland E. R. Obesity and the lung: 4. Obesity and asthma. Thorax. 2008; 63 (11): 1018–1023.
12. Koenig J. E., Spor A., Scalfone N., Fricker A. D., Stombaugh J., Knight R., Angenent L. T., Ley R. E. Succession of microbial consortia in the developing infant gut microbiome. Proc. Natl. Acad. Sci. USA. 2011; Mar 15; 108 (Suppl. 1): 4578–4585.
13. Palmer C., Bik E. M., DiGiulio D. B., Relman D. A., Brown P. O. Development of the human infant intestinal microbiota. PLoS Biol. 2007; 5 (7): 177.
14. Hummelen R., Vos A. P., van't Land B., van Norren K., Reid G. Altered host-microbe interaction in HIV: a target for intervention with pro- and prebiotics. Int. Rev. Immunol. 2010; 29 (5): 485–513.
15. Turnbaugh P. J., Hamady M., Yatsunenko T., Cantarel B. L., Duncan A., Ley R. E., Sogin M. L., Jones W. J., Roe B. A., Affourtit J. P., Egholm M., Henrissat B., Heath A. C., Knight R., Gordon J. I. A core gut microbiome in obese and lean twins. Nature. 2009; 457 (7228): 480–484.
16. de Filippo C. et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc. Natl. Acad. Sci. USA. 2010; 107 (33): 14691–14696.
17. Maslowski K. M., Mackay C. R. Diet, gut microbiota and immune responses. Nat. Immunol. 2011; 12 (1): 5–9.
18. Guarino A., Wudy A., Basile F., Ruberto E., Buccigrossi V. Composition and roles of intestinal microbiota in children. J. Matern. Fetal Neonatal Med. 2012; 25 (Suppl.1): 63–66.
19. Biasucci G., Rubini M., Riboni S., Morelli L., Bessi E., Retetangos C. Mode of delivery affects the bacterial community in the newborn gut. Early Hum. Dev. 2010; 86 (Suppl. 1): 13–15.
20. Bezirtzoglou E., Stavropoulou E. Immunology and probiotic impact of the newborn and young children intestinal microflora. Anaerobe. 2011; 17 (6): 369–374.
21. Guemonde M., LaitinenK., Salminen S. Breast milk: a sourse of bifidobacteria for infant gut development and maturation. Neonatology. 2007; 92: 64–66.
22. Mitsou E. K., Kirtzalidou E., Oikonomou I., Liosis G., Kyriacou A. Fecal microflora of Greek healthy neonates. Anaerobe. 2008; 14 (2): 94–101.
23. Bulatova E. M., Gabrusskaya T. V., Netrebenko O. K. Pediatrija im. G. N. Speranskogo — PEDIATRIYA. 2007; 111 (3): 84–89.
24. Bulatova E. M., Volkova I. S., Netrebenko O. K. Pediatrija im. G. N. Speranskogo — PEDIATRIYA. 2008; 87 (5): 82–86.
25. Roberfroid M. B. Prebiotics and probiotics: are they functional foods? Am. J. Clin. Nutr. 2000; 71 (6) Suppl.: 1682–1687.
26. Jirillo E., Jirillo F., Magrone T. Healthy effects exerted by prebiotics, probiotics, and symbiotics with special reference to their impact on the immune system. Int. J. Vitam. Nutr. Res. 2012; 82 (3): 200–208.
27. Morrow A. L., Ruiz-Palacios G. M., Altaye M., Jiang X., Guerrero M. L., Meinzen-Derr J. K., Farkas T., Chaturvedi P., Pickering L. K., Newburg D. S. Human milk oligosaccharides are associated with protection against diarrhea in breast-fed infants. J. Pediatr. 2004; 145 (3): 297–303.
28. O'Connell Motherway M., Kinsella M. Transcriptional and functional characterization of genetic elements involved in galactooligosaccharide utilization by Bifidobacterium breve UCC2003. Microb. Biotechnol. 2013; 6 (1): 67–79.
29. Garrido D., Ruiz-Moyano S. Utilization of galactooligosaccharides by Bifidobacterium longum subsp. infantis isolates. Food Microbiol. 2013; 33 (2): 262–270.
30. Satoh T., Odamaki T. In vitro comparative evaluation of the impact of lacto-N-biose I, a major building block of human milk oligosaccharides, on the fecal microbiota of infants. Anaerobe. 2013; 19: 50–57.
31. Vandenplas Y. Oligosaccharides in infant formula. Brit. J. Nutr. 2002; 87 (Suppl. 2): 293–296.
32. Boehm G., Stahl B. Oligosaccharides. In: T. Mattila-Sandholm (ed.). Functional Dairy products. Cambridge: Woodhead Publ. 2003. P. 203–243.
33. Bode L., Kunz C., Strobel S., Klein N. Human milk oligosaccharides reduce plat Rudloff Selet-neutrophil complex formation leading to a decrease in neutrophil beta 2 integrin expression. J. Leukoc. Biol. 2004; 76 (4): 820–826.
34. Field C. J. The immunological components of human milk and their effect on immune development in infants. J. Nutr. 2005; 135 (1): 1–4.
35. Masjedi M., Tivey D. R., Thompson F. M., Cummins A. G. Activa tion of the gut-associated lymphoid tissue with expression of interleukin-2 receptors that peaks during weaning in the rat. J. Pediatr. Gastroenterol. Nutr. 1999; 29 (5): 556–562.
36. Contor L., Asp N. G. Process for the assessment of scientific support for claims on foods (PASSCLAIM) phase two: moving forward. Eur. J. Nutr. 2004; 43 (Suppl. 2): 3–6.
37. Cummings J. H., Antoine J. M., Azpiroz F., Bourdet-Sicard R., Brandtzaeg P., Calder P. C., Gibson G. R., Guarner F., Isolauri E., Pannemans D., Shortt C., Tuijtelaars S., Watzl B. PASSCLAIM — gut health and immunity. Eur. J. Nutr. 2004; 43 (Suppl. 2): 118–173.
38. Gibson G. R., Roberfroid M. B. Dietary modulation of the human colonic microbiota: Introducing the concept of prebiotics. J. Nutr. 1995; 125: 1401–1412.
39. Leach J. D., Sobolik K. D. High dietaryintake of prebiotic inulintype fructans in the prehistoric Chihauhuan desert. Brit. J. Nutr. 2010; 103: 1158–1561.
40. Van Loo J., Coussement P., de Leenheer L., Hoebregs H., Smits G. On the presence of inulin and oligofructose as natural ingredients in the western diet. Crit. Rev. Food Sci. Nutr. 1995; 35: 525–552.
41. Langlands S. J., Hopkins M. J., Coleman N., Cumming J. H. Prebiotic carbohydrates modify the mucosa associated microflora of the human large bowel. Gut. 2004; 53: 1610–1616.
42. Cumming J. H., Christie S., Cole T. J. A study of fructo-oligosaccharides in the prevention of traveller's diarrhoea. Aliment. Pharmacol. Ther. 2001; 15: 1139–1145.
43. Gibson G. R., Beatty E. R., Wang X., Cummings J. Selective stimulation of bifidobacteria in the human colon by oligofructose and inulin. Gastroenterology. 1995; 108: 975–982.
44. Geier M., Butler R., Howarth G. Inflammatory bowel disease: current insights into pathogenesis and new therapeutic options; probiotics, prebiotics and symbiotics. Int. J. Food Microbiol. 2007; 115: 1–11.
45. Lindsay J. O., Whelan K., Stagg A. J., Gobin P., Al-Hassi H. O., Rayment N., Kamm M. A., Knight S. C., Forbes A. Clinical, micro biological and immunological effects of fructo-oligosaccharide in patients with Crohn's disease. Gut. 2006; 55: 348–355.
46. Welters C. F. M., Heineman E., Thunnissen B. J. M. Effect of dietary inulin supplementation on inflammation of pouch mucosa in patients with an ileal pouch-anal anastomosis. Dis. Colon Rectum. 2002; 45: 621–627.
47. Garcia-Peris P., Velasco C., Lozano M. A., Moreno Y., Paron L., de la Cuerda C., Breton I., Camblor M., Garcia-Hernandez J., Guarner F., Hernandez M. Effect of a mixture of inulin and fructooligosaccharide on lactobacillus and bifidobacterium intestinal microbiota of patients receiving radiotherapy; a randomised, double-blind, placebo-controlled trial. Nutr. Hosp. 2012; 27 (6): 1908–1915.
48. Kon' I.Ya., Abramova T. V., Pustgraev N. N., Konovalova T. S., Kiseleva E. S. Voprosi prakticheskoi pediatrii — Problems of Practical Pediatrics. 2008; 3 (4): 76–81.
49. Kon' I.Ya., Kurkova V. I., Abramova T. V., Gul'tikova O. S. Voprosi prakticheskoi pediatrii — Problems of Practical Pediatrics. 2010; 5 (2): 29–37.
50. Phoem A. N., Voravuthikunchai S. P. Eleutherine americana as a growth promotor for infant intestinal microbiota. Anaerobe. 2013; 20: 14–19.
51. di Bartolomeo F., Startek J. B., van den Ende W. Prebiotics to fight diseases: reality or fiction? Phytother. Res. 2012; doi: 10.1002/ptr.4901.
52. Pratt V. C., Tappenden K. A., McBurney M. I., Field C. J. Shortchain fatty acid-supplemented total parenteral nutrition improves nonspecific immunity after intestinal resection in rats. JPEN J. Parenter. Enteral. Nutr. 1996; 20 (4): 264–271.
53. Inan M. S., Rasoulpour R. J., Yin L., Hubbard A. K., Rosenberg D. W., Giardina C. The luminal short-chain fatty acid butyrate modulates NF-kappaB activity in a human colonic epithelial cell line. Gastroenterology. 2000; 118 (4): 724–734.
54. Arslanoglu S., Moro G. E., Schmitt J., Tandoi L., Rizzardi S., Boehm G. Early dietary intervention with a mixture of prebiotic oligosaccharides reduces the incidence of allergic manifestations and infections during the first two years of life. J. Nutr. 2008; 138 (6): 1091–1095.
55. van de Pol M. A., Lutter R., Smids B. S., Weersink E. J., van der Zee J. S. Synbiotics reduce allergen-induced T-helper 2 response and improve peak expiratory flow in allergic asthmatics. Allergy. 2011; 66 (1): 39–47.
56. van Hoffen E., Ruiter B., Faber J., M'Rabet L., Knol E. F., Stahl B., Arslanoglu S., Moro G., Boehm G., Garssen J. A specific mixture of short-chain galacto-oligosaccharides and long-chain fructooligosaccharides induces a beneficial immunoglobulin profile in infants at high risk for allergy. Allergy. 2009; 64 (3): 484–487.
57. Gruber C., van Stuijvenberg M., Mosca F., Moro G., Chirico G., Braegger C. P., Riedler J., Boehm G., Wahn U. Reduced occurrence of early atopic dermatitis because of immunoactive prebiotics among low-atopy-risk infants. J. Allergy Clin. Immunol. 2010; 126 (4): 791–797.
58. Moro G., Arslanoglu S., Stahl B., Jelinek J., Wahn U., Boehm G. A mixture of prebiotic oligosaccharides reduces the incidence of atopic dermatitis during the first six months of age. Arch. Dis. Child. 2006; 91 (10): 814–819.
59. Arslanoglu S., Moro G. E., Schmitt J., Tandoi L., Rizzardi S., Boehm G. Early dietary intervention with a mixture of prebiotic oligosaccharides reduces the incidence of allergic manifestations and infections during the first two years of life. J. Nutr. 2008; 138: 1091–1095.
60. Scholtens P. A., Alliet P., Raes M., Alles M. S., Kroes H., Boehm G. et al. Fecal secretory immunoglobulin A is increased in healthy infants who receive a formula with short-chain galactooligosaccharides and long-chain fructo-oligosaccharides. J. Nutr. 2008; 138: 1141–1147.
61. Kukkonen K., Savilahti E., Haahtela T., Juntunen-Backman K., Korpela R., Poussa T. Probiotics and prebiotic galacto-oligosaccharides in the prevention of allergic diseases: a randomized, doubleblind, placebo-controlled trial. J. Allergy Clin. Immunol. 2007; 119 (1): 192–198.
62. Bruzzese E., Volpicelli M., Salvini F., Bisceglia M., Lio netti P., Cinquetti M. et al. Early administration of GOS/FOS prevents intestinal and respiratory infections in infants [abstract]. J. Pediatr. Gastroenterol. Nutr. 2006; 42: 95.
63. Arslanoglu S., Moro G. E., Boehm G. Early supplementation of prebiotic oligosaccharides protects formula-fed infants against infections during the first 6 months of life. J. Nutr. 2007; 137: 2420–2424.
64. Saavedra J. M., Tschernia A. Human studies with probiotics and prebiotics: clinical implications. Brit. J. Nutr. 2002; 87: 241–246.
65. Drakoularakou A., Tzortzis G., Rastall R. A., Gibson G. R. A double-blind, placebo-controlled, randomized human study assessing the capacity of a novel galacto-oligosaccharide mixture in reducing travellers‘ diarrhoea. Eur. J. Clin. Nutr. 2010; 64: 146–152.
66. Lukens M. V., Claassen E. A., de Graaff P. M., van Dijk M. E., Hoogerhout P., Toebes M., Schumacher T. N., van der Most R. G., Kimpen J. L., van Bleek G. M. Characterization of the CD8+ T cell responses directed against respiratory syncytial virus during primary and secondary infection in C57BL/6 mice. Virology. 2006; 15, 352 (1): 157–168.
67. Velez E., Castillo N., Meson O., Grau A., Bibas Bonet M. E., Perdigon G. Study of the effect exerted by fructo-oligosaccharides from yacon (Smallanthus sonchifolius) root flour in an intestinal infection model with Salmonella typhimurium. Brit. J. Nutr. 2013; 109 (11): 1971–1979.
68. Firmansyach A., Pramila G., Fassler A., Hashke F., LinkAmster H. Improvd humoral response to measles vaccine in infants receving infant cereal with fructo-oligosaccharides. J. Pediatr. Gastroenterol. Nutr. 2000; Abstract 521.
69. Schijf M. A., Kruijsen D., Bastiaans J., Coenjaerts F. E., Garssen J., van Bleek G. M., van't Land B. Specific dietary oligosaccharides increase Th1 responses in a mouse respiratory syncytial virus infection model. J Virol2012; 86 (21): 11472–11482.
Review
For citations:
Bogdanova N.M., Bulatova E.M., Wasia M.N. Modern View on Microbiocenosis, Immune Response and Factors Influencing on Their Formation. Fundamental and Applied Aspects. Current Pediatrics. 2013;12(4):18-25. (In Russ.) https://doi.org/10.15690/vsp.v12i4.726
Views:
862
Email this article 
