Advertisement

European Journal of Nutrition

, Volume 56, Issue 7, pp 2245–2253 | Cite as

Probiotics modulate gut microbiota and health status in Japanese cedar pollinosis patients during the pollen season

  • Gaku HarataEmail author
  • Himanshu Kumar
  • Fang HeEmail author
  • Kenji Miyazawa
  • Kazutoyo Yoda
  • Manabu Kawase
  • Akira Kubota
  • Masaru Hiramatsu
  • Samuli Rautava
  • Seppo Salminen
Original Contribution

Abstract

Background

Japanese cedar pollinosis (JCP) is a challenging public health problem in Japan. Altered gut microbiota is associated with several diseases, including allergic diseases. However, only a few studies have focused on JCP and the underlying mechanisms for probiotic effects remain unclear. In addition, this study is the first observation of the correlation between the gut microbiota and blood lipid in JCP.

Methods

Faecal samples from JCP subjects were collected before and after treatment with (n = 14) and without (n = 11) LGG–TMC0356-fermented milk for 10 weeks. Gut microbiota composition was characterized from faecal DNA using sequencing of 16S rRNA genes.

Results

16S rRNA-based operational taxonomic unit clustering of the microbiota revealed that LGG–TMC0356-fermented milk significantly altered gut microbiota after 10 weeks of milk consumption, and eight dominant genera of microbes were detected. During the JCP season, the Bacteroidetes/Firmicutes ratio, when compared to baseline, was significantly decreased in subjects at end of the study. Bacteroidetes showed positive correlation with LDL- and HDL-cholesterol levels, whereas Firmicutes showed negative correlation with total cholesterol, LDL- and HDL- cholesterol.

Conclusions

The altered gut microbiota through supplementation of fermented milk containing the study probiotics may be a prospective target for protection against JCP, with beneficial effects on blood lipid levels.

Keywords

JCP Gut microbiota Blood lipid Lactobacillus rhamnosus GG Lactobacillus gasseri TMC0356 Probiotic Allergy 

Notes

Acknowledgments

This work supported by Takanashi milk Company Limited. We thank Dr. Juha-Pekka Pursiheimo (Turku Clinical Sequencing Laboratory, Institute of Biomedicine, University of Turku) for his assistance and technique of next-generation sequencing. Thanks also to Enago (www.enago.jp) for the English language review.

Funding

This work was supported by Takanashi Milk Products Co., Ltd.

Compliance with ethical standards

Conflict of interest

G. Harata, F. He, K. Miyazawa, K. Yoda, M. Kawase, A. Kubota and M. Hiramatsu are employees of Takanashi Milk Products Co., Ltd.; H. Kumar, S. Rautava and S. Salminen declare no conflicts of interest.

References

  1. 1.
    Fiocchi A, Pawankar R, Cuello-Garcia C, Ahn K, Al-Hammadi S, Agarwal A, Beyer K, Burks W, Canonica GW, Ebisawa M et al (2015) World Allergy Organization-McMaster University Guidelines for Allergic Disease Prevention (GLAD-P): Probiotics. World Allergy Organ J 8:4. doi: 10.1186/s40413-016-0102-7 CrossRefGoogle Scholar
  2. 2.
    Okuda M, Ohkubo K, Gotoh M, Hiroshima K, Ishida Y, Hori K (2005) Dynamics of airborne pollen particles from inhalation to allergic reaction in the nose. Rhinology 43:29–33Google Scholar
  3. 3.
    Kalliomäki M, Salminen S, Arvilommi H, Kero P, Koskinen P, Isolauri E (2001) Probiotics in primary prevention of atopic disease: a randomized placebo-controlled trial. Lancet 357:1076–1079CrossRefGoogle Scholar
  4. 4.
    Björkstén B, Naaber P, Sepp E, Mikelsaar M (1999) The intestinal microflora in allergic Estonian and Swedish 2-year-old children. Clin Exp Allergy 29:342–346CrossRefGoogle Scholar
  5. 5.
    Björkstén B, Sepp E, Julge K, Voor T, Mikelsaar M (2001) Allergy development and the intestinal microflora during the first year of life. J Allergy Clin Immunol 108:516–520CrossRefGoogle Scholar
  6. 6.
    Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S et al (2014) Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol 11:506–514. doi: 10.1038/nrgastro.2014.66 CrossRefGoogle Scholar
  7. 7.
    Rautava S, Kainonen E, Salminen S, Isolauri E (2012) Maternal probiotic supplementation during pregnancy and breast-feeding reduces the risk of eczema in the infant. J Allergy Clin Immunol 130:1355–1360. doi: 10.1016/j.jaci.2012.09.003 CrossRefGoogle Scholar
  8. 8.
    Kawase M, He F, Kubota A, Hiramatsu M, Saito H, Ishii T, Yasueda H, Akiyama KE (2009) Effect of fermented milk prepared with two probiotic strains on Japanese cedar pollinosis in a double-blind placebo-controlled clinical study. Int J Food Microbiol 128:429–434. doi: 10.1016/j.ijfoodmicro.2008.09.017 CrossRefGoogle Scholar
  9. 9.
    Vinding RK, Stokholm J, Chawes BL, Bisgaard H (2016) Blood lipid levels associate with childhood asthma, airway obstruction, bronchial hyperresponsiveness, and aeroallergen sensitization. J Allergy Clin Immunol 137:68–74.e4. doi: 10.1016/j.jaci.2015.05.033 CrossRefGoogle Scholar
  10. 10.
    Robertson AK, Zhou X, Strandvik B, Hansson GK (2004) Severe hypercholesterolaemia leads to strong Th2 responses to an exogenous antigen. Scand J Immunol 59(3):285–293CrossRefGoogle Scholar
  11. 11.
    Cottrell L, Neal WA, Ice C, Perez MK, Piedimonte A (2011) Metabolic abnormalities in children with asthma. Am J Respir Crit Care Med 183:441–448. doi: 10.1164/rccm.201004-0603OC (Epub 2010 Sep 17) CrossRefGoogle Scholar
  12. 12.
    Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the Miseq Illumina sequencing platform james. Appl Environ Microbiol 79:5112–5120CrossRefGoogle Scholar
  13. 13.
    Brandt K, Alatossava T (2003) Specific identification of certain probiotic Lactobacillus rhamnosus strains with PCR primers based on phagerelated sequences. Int J Food Microbiol 84:189–196CrossRefGoogle Scholar
  14. 14.
    Collado MC, Laitinen K, Salminen S, Isolauri E (2012) Maternal weight and excessive weight gain during pregnancy modify the immunomodulatory potential of breast milk. Pediatr Res 72:77–85. doi: 10.1038/pr.2012.42 CrossRefGoogle Scholar
  15. 15.
    Salminen S, Endo A, Isolauri E, Scalabrin D (2016) Early gut colonization with lactobacilli and staphylococcus in infants: the hygiene hypothesis extended. J Pediatr Gastroenterol Nutr 62:80–86. doi: 10.1097/MPG.0000000000000925 CrossRefGoogle Scholar
  16. 16.
    Tamura M, Shikina T, Morihana T, Hayama M, Kajimoto O, Sakamoto A, Kajimoto Y, Watanabe O, Nonaka C, Shida K et al (2007) Effects of probiotics on allergic rhinitis induced by Japanese cedar pollen: randomized double-blind, placebo-controlled clinical trial. Int Arch Allergy Immunol 143:75–82CrossRefGoogle Scholar
  17. 17.
    Yonekura S, Okamoto Y, Okawa T, Hisamitsu M, Chazono H, Kobayashi K, Sakurai D, Horiguchi S, Hanazawa T (2009) Effects of daily intake of Lactobacillus paracasei strain KW3110 on Japanese cedar pollinosis. Allergy Asthma Proc 30:397–405. doi: 10.2500/aap.2009.30.3256 CrossRefGoogle Scholar
  18. 18.
    West CE, Jenmalm MC, Prescott SL (2015) The gut microbiota and its role in the development of allergic disease: a wider perspective. Clin Exp Allergy 45:43–53. doi: 10.1111/cea.12332 CrossRefGoogle Scholar
  19. 19.
    McCoy KD, Köller Y (2015) New developments providing mechanistic insight into the impact of the microbiota on allergic disease. Clin Immunol 159:170–176. doi: 10.1016/j.clim.2015.05.007 CrossRefGoogle Scholar
  20. 20.
    Abrahamsson TR, Jakobsson HE, Andersson AF, Björkstén B, Engstrand L, Jenmalm MC (2012) Low diversity of the gut microbiota in infants with atopic eczema. J Allergy Clin Immunol 129:434–440. doi: 10.1016/j.jaci.2011.10.025 CrossRefGoogle Scholar
  21. 21.
    Nylund L, Satokari R, Nikkilä J, Rajilić-Stojanović M, Kalliomäki M, Isolauri E, Salminen S, de Vos WM (2013) Microarray analysis reveals marked intestinal microbiota aberrancy in infants having eczema compared to healthy children in at-risk for atopic disease. BMC Microbiol 23(13):12. doi: 10.1186/1471-2180-13-12 CrossRefGoogle Scholar
  22. 22.
    Kubota A, He F, Kawase M, Harata G, Hiramatsu M, Salminen S, Iino H (2009) Lactobacillus strains stabilize intestinal microbiota in Japanese cedar pollinosis patients. Microbiol Immunol 53:198–205CrossRefGoogle Scholar
  23. 23.
    Burger-van Paassen N, Vincent A, Puiman PJ, van der Sluis M, Bouma J, Boehm G, van Goudoever JB, van Seuningen I, Renes IB (2009) The regulation of intestinal mucin MUC2 expression by short-chain fatty acids: implications for epithelial protection. Biochem J 420:211–219. doi: 10.1042/BJ20082222 CrossRefGoogle Scholar
  24. 24.
    Finnie IA, Dwarakanath AD, Taylor BA, Rhodes JM (1995) Colonic mucin synthesis is increased by sodium-butyrate. Gut 36:93–99CrossRefGoogle Scholar
  25. 25.
    Peng L, He Z, Chen W, Holzman IR, Lin J (2007) Effects of butyrate on intestinal barrier function in a Caco-2 cell monolayer model of intestinal barrier. Pediatr Res 61:37–41CrossRefGoogle Scholar
  26. 26.
    Peng L, Li ZR, Green RS, Holzman IR, Lin J (2009) Butyrate enhances the intestinal barrier by facilitating tight junction assembly via activation of AMP activated protein kinase in Caco-2 cell monolayers. J Nutr 139:1619–1625. doi: 10.3945/jn.109.104638 CrossRefGoogle Scholar
  27. 27.
    Larsen N, Vogensen FK, van den Berg FW, Nielsen DS, Andreasen AS, Pedersen BK, Al-Soud WA, Sørensen SJ, Hansen LH, Jakobsen M (2010) Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. Plos One 5:e9085. doi: 10.1371/journal.pone.0009085 CrossRefGoogle Scholar
  28. 28.
    Atarashi K, Tanoue T, Shima T, Imaoka A, Kuwahara T, Momose Y, Cheng G, Yamasaki S, Saito T, Ohba Y et al (2011) Induction of colonic regulatory T cells by indigenous Clostridium species. Science 331:337–341. doi: 10.1126/science.1198469 CrossRefGoogle Scholar
  29. 29.
    Atarashi K, Tanoue T, Oshima K, Suda W, Nagano Y, Nishikawa H, Fukuda S, Saito T, Narushima S, Hase K et al (2013) Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature 500:232–236. doi: 10.1038/nature12331 CrossRefGoogle Scholar
  30. 30.
    Berni Canani R, Sangwan N, Stefka AT, Nocerino R, Paparo L, Aitoro R, Calignano A, Khan AA, Gilbert JA, Nagler CR (2016) Lactobacillus rhamnosus GG-supplemented formula expands butyrate-producing bacterial strains in food allergic infants. ISME J 10:742–750. doi: 10.1038/ismej.2015.151 CrossRefGoogle Scholar
  31. 31.
    Feleszko W, Jaworska J, Rha RD, Steinhausen S, Avagyan A, Jaudszus A, Ahrens B, Groneberg DA, Wahn U, Hamelmann E (2007) Probiotic-induced suppression of allergic sensitization and airway inflammation is associated with an increase of T regulatory-dependent mechanisms in a murine model of asthma. Clin Exp Allergy 37:498–505CrossRefGoogle Scholar
  32. 32.
    Tremaroli V, Bäckhed F (2012) Functional interactions between the gut microbiota and host metabolism. Nature 489:242–249. doi: 10.1038/nature11552 CrossRefGoogle Scholar
  33. 33.
    Ley RE, Bäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI (2005) Obesity alters gut microbial ecology. Proc Natl Acad Sci USA 102:11070–11075CrossRefGoogle Scholar
  34. 34.
    Ling Z, Li Z, Liu X, Cheng Y, Luo Y, Tong X, Yuan L, Wang Y, Sun J, Li L et al (2014) Altered fecal microbiota composition associated with food allergy in infants. Appl Environ Microbiol 80:2546–2554. doi: 10.1128/AEM.00003-14 CrossRefGoogle Scholar
  35. 35.
    Maksimoval OV, Zaitseva EV, Mazurina SA, Revyakina VA, Gervazieva VB (2015) Intestine microbiota in children with obesity and allergic diseases. Zh Mikrobiol Epidemiol Immunobiol 3(53–8):32Google Scholar
  36. 36.
    Fu J, Bonder MJ, Cenit MC, Tigchelaar EF, Maatman A, Dekens JA, Brandsma E, Marczynska J, Imhann F, Weersma RK et al (2015) The gut microbiome contributes to a substantial proportion of the variation in blood lipids. Circ Res 117:817–824. doi: 10.1161/CIRCRESAHA.115.306807 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Gaku Harata
    • 1
    • 2
    Email author
  • Himanshu Kumar
    • 2
  • Fang He
    • 1
    Email author
  • Kenji Miyazawa
    • 1
  • Kazutoyo Yoda
    • 1
  • Manabu Kawase
    • 1
  • Akira Kubota
    • 1
  • Masaru Hiramatsu
    • 1
  • Samuli Rautava
    • 2
  • Seppo Salminen
    • 2
  1. 1.Technical Research LaboratoryTakanashi Milk Products Co., Ltd.YokohamaJapan
  2. 2.Functional Foods ForumUniversity of TurkuTurkuFinland

Personalised recommendations