Applied Microbiology and Biotechnology

, Volume 102, Issue 19, pp 8275–8289 | Cite as

Origination, change, and modulation of geriatric disease-related gut microbiota during life

  • Muhammad Shahid Riaz Rajoka
  • Haobin Zhao
  • Na Li
  • Yao Lu
  • Ziyang Lian
  • Dongyan Shao
  • Mingliang Jin
  • Qi Li
  • Liqing Zhao
  • Junling ShiEmail author


The age-related changes in the diversity and composition of the gut microbiota are well described in recent studies. These changes have been suggested to be influenced by age-associated weakening of the immune system and low-grade chronic inflammation, resulting in numerous age-associated pathological conditions. Gut microbiota homeostasis is important throughout the life of the host by providing vital functions to regulate various immunological functions and homeostasis. Based on published results, we summarize the relationship between the gut microbiota and aging-related diseases, especially Parkinson’s disease, immunosenescence, rheumatoid arthritis, bone loss, and metabolic syndrome. The change in composition of the gut microbiota and gut ecosystem during life and its influence on the host immunologic and metabolic phenotype are also analyzed to determine factors that affect aging-related diseases. Approaches to maintain host health and prevent or cure geriatric diseases are also discussed.


Gut microbiota Immunity Dysbiosis Disorder Health span Aging Elderly 



This study was supported by the National Key Technology R&D Program (grant number 2015BAD16B02), the Modern Agricultural Industry Technology System (CARS-30), Key Research and Development Plan of Shaanxi Province (2017ZDXL-NY-0304), and National Natural Science Foundation of China (NSFC) (grant Number 31701722 and 3147171).

Author’s contributions

Muhammad Shahid Riaz Rajoka and Junling Shi wrote the review. All authors reviewed the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.


  1. Abrahamsson TR, Jakobsson HE, Andersson AF, Bjorksten B, Engstrand L, Jenmalm MC (2014) Low gut microbiota diversity in early infancy precedes asthma at school age. Clin Exper Allergy 44(6):842–850. CrossRefGoogle Scholar
  2. Adlerberth I, Wold AE (2009) Establishment of the gut microbiota in Western infants. Acta Paediatr 98(2):229–238. CrossRefPubMedGoogle Scholar
  3. Ai L, Tian H, Chen Z, Chen H, Xu J, Fang JY (2017) Systematic evaluation of supervised classifiers for fecal microbiota-based prediction of colorectal cancer. Oncotarget 8(6):9546–9556. CrossRefPubMedPubMedCentralGoogle Scholar
  4. Aura AM, Mattila I, Hyotylainen T, Gopalacharyulu P, Bounsaythip C, Oresic M, Oksman-Caldentey KM (2011) Drug metabolome of the simvastatin formed by human intestinal microbiota in vitro. Mol BioSyst 7(2):437–446. CrossRefPubMedGoogle Scholar
  5. Azad MB, Konya T, Maughan H, Guttman DS, Field CJ, Chari RS, Sears MR, Becker AB, Scott JA, Kozyrskyj AL (2013) Gut microbiota of healthy Canadian infants: profiles by mode of delivery and infant diet at 4 months. CMAJ 185(5):385–394. CrossRefPubMedPubMedCentralGoogle Scholar
  6. Backhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatcheva-Datchary P, Li Y, Xia Y, Xie H, Zhong H, Khan MT, Zhang J, Li J, Xiao L, Al-Aama J, Zhang D, Lee YS, Kotowska D, Colding C, Tremaroli V, Yin Y, Bergman S, Xu X, Madsen L, Kristiansen K, Dahlgren J, Wang J (2015) Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe 17(6):852. CrossRefPubMedGoogle Scholar
  7. Barik A, Das K, Chowdhury A, Rai RK (2018) Metabolic syndrome among rural Indian adults. Clin Nutr ESPEN 23:129–135. CrossRefPubMedGoogle Scholar
  8. Bartosch S, Fite A, Macfarlane GT, McMurdo ME (2004) Characterization of bacterial communities in feces from healthy elderly volunteers and hospitalized elderly patients by using real-time PCR and effects of antibiotic treatment on the fecal microbiota. Appl Environ Microbiol 70(6):3575–3581. CrossRefPubMedPubMedCentralGoogle Scholar
  9. Besdine R, Boult C, Brangman S, Coleman EA, Fried LP, Gerety M, Johnson JC, Katz PR, Potter JF, Reuben DB, Sloane PD, Studenski S, Warshaw G (2005) Caring for older Americans: the future of geriatric medicine. J Am Geriatr Soc 53(6 Suppl):S245–S256. CrossRefPubMedGoogle Scholar
  10. Biagi E, Candela M, Fairweather-Tait S, Franceschi C, Brigidi P (2012) Ageing of the human metaorganism: the microbial counterpart. AGE 34(1):247–267. CrossRefPubMedGoogle Scholar
  11. Biagi E, Candela M, Turroni S, Garagnani P, Franceschi C, Brigidi P (2013) Ageing and gut microbes: perspectives for health maintenance and longevity. Pharmacol Res 69(1):11–20. CrossRefPubMedGoogle Scholar
  12. Bischoff SC (2016) Microbiota and aging. Curr Opin Clin Nutr Metab Care 19(1):26–30. CrossRefPubMedGoogle Scholar
  13. Bisgaard H, Li N, Bonnelykke K, Chawes BL, Skov T, Paludan-Muller G, Stokholm J, Smith B, Krogfelt KA (2011) Reduced diversity of the intestinal microbiota during infancy is associated with increased risk of allergic disease at school age. J Allergy Clin Immunol 128(3):646–652. e1-5. CrossRefPubMedGoogle Scholar
  14. Britton RA, Irwin R, Quach D, Schaefer L, Zhang J, Lee T, Parameswaran N, McCabe LR (2014) Probiotic L. reuteri treatment prevents bone loss in a menopausal ovariectomized mouse model. J Cell Physiol 229(11):1822–1830. CrossRefPubMedPubMedCentralGoogle Scholar
  15. Camci G, Oguz S (2016) Association between Parkinson's disease and Helicobacter Pylori. J Clin Neurol 12(2):147–150. CrossRefPubMedPubMedCentralGoogle Scholar
  16. Candela M, Turroni S, Biagi E, Carbonero F, Rampelli S, Fiorentini C, Brigidi P (2014) Inflammation and colorectal cancer, when microbiota-host mutualism breaks. World J Gastroenterol 20(4):908–922. CrossRefPubMedPubMedCentralGoogle Scholar
  17. Cardwell CR, Stene LC, Joner G, Cinek O, Svensson J, Goldacre MJ, Parslow RC, Pozzilli P, Brigis G, Stoyanov D, Urbonaite B, Sipetic S, Schober E, Ionescu-Tirgoviste C, Devoti G, de Beaufort CE, Buschard K, Patterson CC (2008) Caesarean section is associated with an increased risk of childhood-onset type 1 diabetes mellitus: a meta-analysis of observational studies. Diabetologia 51(5):726–735. CrossRefPubMedGoogle Scholar
  18. Carlson AL, Xia K, Azcarate-Peril MA, Goldman BD, Ahn M, Styner MA, Thompson AL, Geng X, Gilmore JH, Knickmeyer RC (2017) Infant gut microbiome associated with cognitive development. Biol Psychiatry 83(2):148–159. CrossRefPubMedGoogle Scholar
  19. Charbonneau MR, O'Donnell D, Blanton LV, Totten SM, Davis JC, Barratt MJ, Cheng J, Guruge J, Talcott M, Bain JR, Muehlbauer MJ, Ilkayeva O, Wu C, Struckmeyer T, Barile D, Mangani C, Jorgensen J, Fan YM, Maleta K, Dewey KG, Ashorn P, Newgard CB, Lebrilla C, Mills DA, Gordon JI (2016) Sialylated milk oligosaccharides promote microbiota dependent growth in models of infant undernutrition. Cell 164(5):859–871. CrossRefPubMedPubMedCentralGoogle Scholar
  20. Chen JJ, Zheng P, Liu YY, Zhong XG, Wang HY, Guo YJ, Xie P (2018) Sex differences in gut microbiota in patients with major depressive disorder. Neuropsychiatr Dis Treat 14:647–655. CrossRefPubMedPubMedCentralGoogle Scholar
  21. Chi HH, Hua KF, Lin YC, Chu CL, Hsieh CY, Hsu YJ, Ka SM, Tsai YL, Liu FC, Chen A (2017) IL-36 signaling facilitates activation of the NLRP3 inflammasome and IL-23/IL-17 axis in renal inflammation and fibrosis. J Am Society Nephrol 28(7):2022–2037. CrossRefGoogle Scholar
  22. Claesson MJ, Cusack S, O'Sullivan O, Greene-Diniz R, de Weerd H, Flannery E, Marchesi JR, Falush D, Dinan T, Fitzgerald G, Stanton C, van Sinderen D, O'Connor M, Harnedy N, O'Connor K, Henry C, O'Mahony D, Fitzgerald AP, Shanahan F, Twomey C, Hill C, Ross RP, O'Toole PW (2011) Composition, variability, and temporal stability of the intestinal microbiota of the elderly. Proc Natl Acad Sci U S A 108(Suppl 1):4586–4591. CrossRefPubMedGoogle Scholar
  23. Claesson MJ, Jeffery IB, Conde S, Power SE, O'Connor EM, Cusack S, Harris HM, Coakley M, Lakshminarayanan B, O'Sullivan O, Fitzgerald GF, Deane J, O'Connor M, Harnedy N, O'Connor K, O'Mahony D, van Sinderen D, Wallace M, Brennan L, Stanton C, Marchesi JR, Fitzgerald AP, Shanahan F, Hill C, Ross RP, O'Toole PW (2012) Gut microbiota composition correlates with diet and health in the elderly. Nature 488(7410):178–184. CrossRefPubMedGoogle Scholar
  24. Collins SM, Surette M, Bercik P (2012) The interplay between the intestinal microbiota and the brain. Nat Rev Microbiol 10(11):735–742. CrossRefPubMedGoogle Scholar
  25. Cui M, Xiao H, Li Y, Dong J, Luo D, Li H, Feng G, Wang H, Fan S (2017) Total abdominal irradiation exposure impairs cognitive function involving miR-34a-5p/BDNF axis. Biochim Biophys Acta 1863(9):2333–2341. CrossRefPubMedPubMedCentralGoogle Scholar
  26. Damms-Machado A, Mitra S (2015) Effects of surgical and dietary weight loss therapy for obesity on gut microbiota composition and nutrient absorption. Biomed Res Int 2015:806248–806212. CrossRefPubMedPubMedCentralGoogle Scholar
  27. Dillin A, Gottschling DE, Nystrom T (2014) The good and the bad of being connected: the integrons of aging. Curr Opin Cell Biol 26:107–112. CrossRefPubMedGoogle Scholar
  28. Dinan TG, Cryan JF (2017) Gut instincts: microbiota as a key regulator of brain development, ageing and neurodegeneration. J Physiol 595(2):489–503. CrossRefPubMedGoogle Scholar
  29. Dominguez-Bello MG, Blaser MJ, Ley RE, Knight R (2011) Development of the human gastrointestinal microbiota and insights from high-throughput sequencing. Gastroenterol 140(6):1713–1719. CrossRefGoogle Scholar
  30. Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G, Fierer N, Knight R (2010) Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci U S A 107(26):11971–11975. CrossRefPubMedPubMedCentralGoogle Scholar
  31. Donaldson GP, Lee SM, Mazmanian SK (2016) Gut biogeography of the bacterial microbiota. Nat Rev Microbiol 14(1):20–32. CrossRefPubMedGoogle Scholar
  32. Drouin-Chartier JP, Cote JA, Labonte ME, Brassard D, Tessier-Grenier M, Desroches S, Couture P, Lamarche B (2016) Comprehensive review of the impact of dairy foods and dairy fat on cardiometabolic risk. Adv Nutr 7(6):1041–1051. CrossRefPubMedPubMedCentralGoogle Scholar
  33. Ege MJ, Mayer M, Normand AC, Genuneit J, Cookson WO, Braun-Fahrlander C, Heederik D, Piarroux R, von Mutius E (2011) Exposure to environmental microorganisms and childhood asthma. N Engl J Med 364(8):701–709. CrossRefPubMedGoogle Scholar
  34. Eloe-Fadrosh EA, Brady A, Crabtree J, Drabek EF, Ma B, Mahurkar A, Ravel J, Haverkamp M, Fiorino AM, Botelho C, Andreyeva I, Hibberd PL, Fraser CM (2015) Functional dynamics of the gut microbiome in elderly people during probiotic consumption. mBio 6(2):e00231–e00215. CrossRefPubMedPubMedCentralGoogle Scholar
  35. Faa G, Gerosa C, Fanni D, Nemolato S, van Eyken P, Fanos V (2013) Factors influencing the development of a personal tailored microbiota in the neonate, with particular emphasis on antibiotic therapy. J Matern Fetal Neonatal Med 26(Suppl 2):35–43. CrossRefPubMedGoogle Scholar
  36. Faderl M, Noti M, Corazza N, Mueller C (2015) Keeping bugs in check: the mucus layer as a critical component in maintaining intestinal homeostasis. IUBMB Life 67(4):275–285. CrossRefPubMedGoogle Scholar
  37. Fairhall N, Langron C, Sherrington C, Lord SR, Kurrle SE, Lockwood K, Monaghan N, Aggar C, Gill L, Cameron ID (2011) Treating frailty—a practical guide. BMC Med 9:83. CrossRefPubMedPubMedCentralGoogle Scholar
  38. Felice VD, Quigley EM, Sullivan AM, O'Keeffe GW, O'Mahony SM (2016) Microbiota-gut-brain signalling in Parkinson's disease: implications for non-motor symptoms. Parkinsonism Relat Disord 27:1–8. CrossRefPubMedGoogle Scholar
  39. Ferder IC, Wang N (2015) Hypermaintenance and hypofunction of aged spermatogonia: insight from age-related increase of Plzf expression. Oncotarget 6(18):15891–15901. CrossRefPubMedPubMedCentralGoogle Scholar
  40. Fransen F, van Beek AA, Borghuis T, Aidy SE, Hugenholtz F, van der Gaast-de Jongh C, Savelkoul HFJ, De Jonge MI, Boekschoten MV, Smidt H, Faas MM, de Vos P (2017) Aged gut microbiota contributes to Systemical Inflammaging after transfer to germ-free mice. Front Immunol 8:1385. CrossRefPubMedPubMedCentralGoogle Scholar
  41. Fulop T, McElhaney J, Pawelec G, Cohen AA, Morais JA, Dupuis G, Baehl S, Camous X, Witkowski JM, Larbi A (2015) Frailty, inflammation and Immunosenescence. Interdiscip Top Gerontol Geriatr 41:26–40. CrossRefPubMedGoogle Scholar
  42. Green-Johnson JM (2012) Immunological responses to gut bacteria. J AOAC Int 95(1):35–49CrossRefPubMedGoogle Scholar
  43. Gruber J, Kennedy BK (2017) Microbiome and longevity: gut microbes send signals to host mitochondria. Cell 169(7):1168–1169. CrossRefPubMedGoogle Scholar
  44. Hippe B, Zwielehner J, Liszt K, Lassl C, Unger F, Haslberger AG (2011) Quantification of butyryl CoA:acetate CoA-transferase genes reveals different butyrate production capacity in individuals according to diet and age. FEMS Microbiol Lett 316(2):130–135. CrossRefPubMedGoogle Scholar
  45. Hooper LV, Macpherson AJ (2010) Immune adaptations that maintain homeostasis with the intestinal microbiota. Nat Rev Immunol 10(3):159–169. CrossRefPubMedGoogle Scholar
  46. Human-Microbiome-Project-Consortium (2012) A framework for human microbiome research. Nature 486(7402):215–221. CrossRefGoogle Scholar
  47. Hwang JS, Im CR, Im SH (2012) Immune disorders and its correlation with gut microbiome. Immune Netw 12(4):129–138. CrossRefPubMedPubMedCentralGoogle Scholar
  48. Ijssennagger N, Belzer C, Hooiveld GJ (2015) Gut microbiota facilitates dietary heme-induced epithelial hyperproliferation by opening the mucus barrier in colon. Proc Natl Acad Sci U S A 112(32):10038–10043. CrossRefPubMedPubMedCentralGoogle Scholar
  49. Inouye SK, Studenski S, Tinetti ME, Kuchel GA (2007) Geriatric syndromes: clinical, research, and policy implications of a core geriatric concept. J Am Geriatr Soc 55(5):780–791. CrossRefPubMedPubMedCentralGoogle Scholar
  50. Jacob F, Melachio TT, Njitchouang GR, Gimonneau G, Njiokou F, Abate L, Christen R, Reveillaud J, Geiger A (2017) Intestinal bacterial communities of trypanosome-infected and uninfected Glossina palpalis palpalis from three human African Trypanomiasis foci in Cameroon. Front Microbiol 8:1464. CrossRefPubMedPubMedCentralGoogle Scholar
  51. Jakobsson HE, Abrahamsson TR, Jenmalm MC, Harris K, Quince C, Jernberg C, Bjorksten B, Engstrand L, Andersson AF (2014) Decreased gut microbiota diversity, delayed Bacteroidetes colonisation and reduced Th1 responses in infants delivered by caesarean section. Gut 63(4):559–566. CrossRefPubMedGoogle Scholar
  52. Janssen AW, Kersten S (2015) The role of the gut microbiota in metabolic health. FASEB J 29(8):3111–3123. CrossRefPubMedGoogle Scholar
  53. Jeffery IB, Lynch DB, O'Toole PW (2016) Composition and temporal stability of the gut microbiota in older persons. Isme J 10(1):170–182. CrossRefPubMedGoogle Scholar
  54. Jeong JJ, Kim KA, Hwang YJ, Han MJ, Kim DH (2016) Anti-inflammaging effects of Lactobacillus brevis OW38 in aged mice. Benef Microbes 7(5):707–718. CrossRefPubMedGoogle Scholar
  55. Jiang S, Xie S, Lv D, Zhang Y, Deng J, Zeng L, Chen Y (2016) A reduction in the butyrate producing species Roseburia spp. and Faecalibacterium prausnitzii is associated with chronic kidney disease progression. Antonie Van Leeuwenhoek 109(10):1389–1396. CrossRefPubMedGoogle Scholar
  56. Jie Z, Xia H, Zhong SL, Feng Q, Li S, Liang S, Zhong H (2017) The gut microbiome in atherosclerotic cardiovascular disease. Nat Commun 8(1):845. CrossRefPubMedPubMedCentralGoogle Scholar
  57. Jimenez E, Fernandez L, Marin ML, Martin R, Odriozola JM, Nueno-Palop C, Narbad A, Olivares M, Xaus J, Rodriguez JM (2005) Isolation of commensal bacteria from umbilical cord blood of healthy neonates born by cesarean section. Curr Microbiol 51(4):270–274. CrossRefPubMedGoogle Scholar
  58. Jimenez E, Marin ML, Martin R, Odriozola JM, Olivares M, Xaus J, Fernandez L, Rodriguez JM (2008) Is meconium from healthy newborns actually sterile? Res Microbiol 159(3):187–193. CrossRefPubMedGoogle Scholar
  59. Jost T, Lacroix C, Braegger C, Chassard C (2015) Impact of human milk bacteria and oligosaccharides on neonatal gut microbiota establishment and gut health. Nutr Rev 73(7):426–437. CrossRefPubMedGoogle Scholar
  60. Kamiya T, Watanabe Y, Makino S, Kano H, Tsuji NM (2016) Improvement of intestinal immune cell function by lactic acid bacteria for dairy products. Microorganisms 5(1) CrossRefPubMedCentralGoogle Scholar
  61. Keenan MJ, Marco ML, Ingram DK, Martin RJ (2015) Improving healthspan via changes in gut microbiota and fermentation. Age 37(5):98. CrossRefPubMedPubMedCentralGoogle Scholar
  62. Kelly TN, Bazzano LA, Ajami NJ, He H, Zhao J, Petrosino JF, Correa A, He J (2016) Gut microbiome associates with lifetime cardiovascular disease risk profile among bogalusa heart study participants. Circ Res 119(8):956–964. CrossRefPubMedPubMedCentralGoogle Scholar
  63. Keshavarzian A, Green SJ, Engen PA, Voigt RM, Naqib A, Forsyth CB, Mutlu E, Shannon KM (2015) Colonic bacterial composition in Parkinson's disease. Mov Disord 30(10):1351–1360. CrossRefPubMedGoogle Scholar
  64. Killeen SD, Wang JH, Andrews EJ, Redmond HP (2009) Bacterial endotoxin enhances colorectal cancer cell adhesion and invasion through TLR-4 and NF-kappaB-dependent activation of the urokinase plasminogen activator system. Br J Cancer 100(10):1589–1602. CrossRefPubMedPubMedCentralGoogle Scholar
  65. Kim HM, Lee DE, Park SD, Kim YT, Kim YJ, Jeong JW, Jang SS, Ahn YT, Sim JH, Huh CS, Chung DK, Lee JH (2014) Oral administration of Lactobacillus plantarum HY7714 protects hairless mouse against ultraviolet B-induced photoaging. J Microbiol Biotechnol 24(11):1583–1591CrossRefPubMedGoogle Scholar
  66. Kim MH, Kang SG, Park JH, Yanagisawa M, Kim CH (2013) Short-chain fatty acids activate GPR41 and GPR43 on intestinal epithelial cells to promote inflammatory responses in mice. Gastroenterol 145(2):396–406.e1-10. CrossRefGoogle Scholar
  67. Kimoto-Nira H, Suzuki C, Kobayashi M, Sasaki K, Kurisaki J, Mizumachi K (2007) Anti-ageing effect of a lactococcal strain: analysis using senescence-accelerated mice. Br J Nutr 98(6):1178–1186. CrossRefPubMedGoogle Scholar
  68. Koh A, De Vadder F, Kovatcheva-Datchary P, Backhed F (2016) From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cell 165(6):1332–1345. CrossRefPubMedGoogle Scholar
  69. Kulecka M, Paziewska A, Zeber-Lubecka N, Ambrozkiewicz F, Kopczynski M, Kuklinska U, Pysniak K, Gajewska M, Mikula M, Ostrowski J (2016) Prolonged transfer of feces from the lean mice modulates gut microbiota in obese mice. Nutr Metab 13(1):57. CrossRefGoogle Scholar
  70. Kumar A (2011) Long-term potentiation at CA3-CA1 hippocampal synapses with special emphasis on aging, disease, and stress. Frontiers aging Neurosci 3:7. CrossRefGoogle Scholar
  71. Kumbhare SV, Kumar H, Chowdhury SP, Dhotre DP, Endo A, Matto J, Ouwehand AC, Rautava S, Joshi R, Patil NP, Patil RH, Isolauri E, Bavdekar AR, Salminen S, Shouche YS (2017) A cross-sectional comparative study of gut bacterial community of Indian and Finnish children. Sci Rep 7(1):10555. CrossRefPubMedPubMedCentralGoogle Scholar
  72. Kwon G, Lee J, Lim YH (2016) Dairy Propionibacterium extends the mean lifespan of Caenorhabditis elegans via activation of the innate immune system. Sci Rep 6:31713. CrossRefPubMedPubMedCentralGoogle Scholar
  73. La Fata G, Weber P, Mohajeri MH (2017) Probiotics and the gut immune system: indirect regulation. Probiotics Antimicrob Proteins 10(1):11–21. CrossRefPubMedCentralGoogle Scholar
  74. Landete JM, Gaya P, Rodriguez E, Langa S (2017) Probiotic bacteria for healthier aging: immunomodulation and metabolism of phytoestrogens. Biomed Res Int 2017:5939818–5939810. CrossRefPubMedPubMedCentralGoogle Scholar
  75. Laursen MF, Zachariassen G, Bahl MI, Bergstrom A, Host A, Michaelsen KF, Licht TR (2015) Having older siblings is associated with gut microbiota development during early childhood. BMC Microbiol 15:154. CrossRefPubMedPubMedCentralGoogle Scholar
  76. Lippert K, Kedenko L, Antonielli L, Kedenko I, Gemeier C, Leitner M, Kautzky-Willer A, Paulweber B, Hackl E (2017) Gut microbiota dysbiosis associated with glucose metabolism disorders and the metabolic syndrome in older adults. Benef Microbes 8(4):545–556. CrossRefPubMedGoogle Scholar
  77. Liu X, Zou Q, Zeng B, Fang Y, Wei H (2013) Analysis of fecal Lactobacillus community structure in patients with early rheumatoid arthritis. Curr Microbiol 67(2):170–176. CrossRefPubMedGoogle Scholar
  78. Liu Y, Gibson GR, Walton GE (2016) An in vitro approach to study effects of prebiotics and probiotics on the faecal microbiota and selected immune parameters relevant to the elderly. PLoS One 11(9):e0162604. CrossRefPubMedPubMedCentralGoogle Scholar
  79. Loper HB, La Sala M, Dotson C, Steinle N (2015) Taste perception, associated hormonal modulation, and nutrient intake. Nutr Rev 73(2):83–91. CrossRefPubMedPubMedCentralGoogle Scholar
  80. Macia L, Thorburn AN, Binge LC, Marino E, Rogers KE, Maslowski KM, Vieira AT, Kranich J, Mackay CR (2012) Microbial influences on epithelial integrity and immune function as a basis for inflammatory diseases. Immunol Rev 245(1):164–176. CrossRefPubMedGoogle Scholar
  81. Maidji E, Somsouk M, Rivera JM (2017) Replication of CMV in the gut of HIV-infected individuals and epithelial barrier dysfunction. Plos Pathlog 13(2):e1006202. CrossRefGoogle Scholar
  82. Makivuokko H, Tiihonen K, Tynkkynen S, Paulin L, Rautonen N (2010) The effect of age and non-steroidal anti-inflammatory drugs on human intestinal microbiota composition. Br J Nutr 103(2):227–234. CrossRefPubMedGoogle Scholar
  83. Man AL, Gicheva N, Nicoletti C (2014) The impact of ageing on the intestinal epithelial barrier and immune system. Cell Immunol 289(1–2):112–118. CrossRefPubMedGoogle Scholar
  84. Mariat D, Firmesse O, Levenez F, Guimaraes V, Sokol H, Dore J, Corthier G, Furet JP (2009) The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age. BMC Microbiol 9:123. CrossRefPubMedPubMedCentralGoogle Scholar
  85. Marizzoni M, Provasi S, Cattaneo A, Frisoni GB (2017) Microbiota and neurodegenerative diseases. Curr Opin Neurol 30:630–638. CrossRefPubMedGoogle Scholar
  86. Martin R, Makino H, Cetinyurek Yavuz A, Ben-Amor K, Roelofs M, Ishikawa E, Kubota H, Swinkels S, Sakai T, Oishi K, Kushiro A, Knol J (2016) Early life events, including mode of delivery and type of feeding, siblings and gender, shape the developing gut microbiota. PLoS One 11(6):e0158498. CrossRefPubMedPubMedCentralGoogle Scholar
  87. Martin R, Nauta AJ, Ben Amor K, Knippels LM, Knol J, Garssen J (2010) Early life: gut microbiota and immune development in infancy. Benef Microbes 1(4):367–382. CrossRefPubMedGoogle Scholar
  88. Mathur R, Barlow GM (2015) Obesity and the microbiome. Exp Rev Gastroenterol Hepatol 9(8):1087–1099. CrossRefGoogle Scholar
  89. Matsumoto M, Kurihara S, Kibe R, Ashida H, Benno Y (2011) Longevity in mice is promoted by probiotic-induced suppression of colonic senescence dependent on upregulation of gut bacterial polyamine production. PLoS One 6(8):e23652. CrossRefPubMedPubMedCentralGoogle Scholar
  90. McCabe L, Britton RA, Parameswaran N (2015) Prebiotic and probiotic regulation of bone health: role of the intestine and its microbiome. Curr Osteoporos Rep 13(6):363–371. CrossRefPubMedPubMedCentralGoogle Scholar
  91. Mello AM, Paroni G, Daragjati J, Pilotto A (2016) Gastrointestinal microbiota and their contribution to healthy aging. Dig Dis 34(3):194–201. CrossRefPubMedGoogle Scholar
  92. Miller MS, Toth MJ (2013) Myofilament protein alterations promote physical disability in aging and disease. Exerc Sport Sci Rev 41(2):93–99. CrossRefPubMedPubMedCentralGoogle Scholar
  93. Mu C, Zhang L, He X, Smidt H, Zhu W (2017) Dietary fibres modulate the composition and activity of butyrate-producing bacteria in the large intestine of suckling piglets. Antonie Van Leeuwenhoek 110(5):687–696. CrossRefPubMedGoogle Scholar
  94. Mueller S, Saunier K, Hanisch C, Norin E, Alm L, Midtvedt T, Cresci A, Silvi S, Orpianesi C, Verdenelli MC, Clavel T, Koebnick C, Zunft HJ, Dore J, Blaut M (2006) Differences in fecal microbiota in different European study populations in relation to age, gender, and country: a cross-sectional study. Appl Environ Microbiol 72(2):1027–1033. CrossRefPubMedPubMedCentralGoogle Scholar
  95. Nakayama J, Watanabe K, Jiang J, Matsuda K, Chao SH, Haryono P, La-Ongkham O, Sarwoko MA, Sujaya IN, Zhao L, Chen KT, Chen YP, Chiu HH, Hidaka T, Huang NX, Kiyohara C, Kurakawa T, Sakamoto N, Sonomoto K, Tashiro K, Tsuji H, Chen MJ, Leelavatcharamas V, Liao CC, Nitisinprasert S, Rahayu ES, Ren FZ, Tsai YC, Lee YK (2015) Diversity in gut bacterial community of school-age children in Asia. Sci Rep 5:8397. CrossRefPubMedPubMedCentralGoogle Scholar
  96. Nguyen NT, Vafin RR, Rzhanov IV, Kolpakov AI, Gataullin IG, Tyulkin SV, Sinyagina MN, Grigoryeva TV, Ilinskaya ON (2016) Molecular genetic analysis of microorganisms with interaepithelial invasion isolated from patients with colorectal cancer. Mol Gen Mikrobiol Virusol 34(1):13–18CrossRefPubMedGoogle Scholar
  97. Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, Pettersson S (2012) Host-gut microbiota metabolic interactions. Sci 336(6086):1262–1267. CrossRefGoogle Scholar
  98. Nogacka AM, Salazar N, Arboleya S, Suarez M, Fernandez N, Solis G, de Los Reyes-Gavilan CG, Gueimonde M (2017) Early microbiota, antibiotics and health. Cell Mol Life Sci 75:83–91. CrossRefPubMedGoogle Scholar
  99. O'Mahony SM, Clarke G, Borre YE, Dinan TG, Cryan JF (2015) Serotonin, tryptophan metabolism and the brain-gut-microbiome axis. Behav Brain Res 277:32–48. CrossRefPubMedGoogle Scholar
  100. Org E, Blum Y, Kasela S, Mehrabian M, Kuusisto J, Kangas AJ, Soininen P, Wang Z, Ala-Korpela M, Hazen SL, Laakso M, Lusis AJ (2017) Relationships between gut microbiota, plasma metabolites, and metabolic syndrome traits in the METSIM cohort. Genome Biol 18(1):70. CrossRefPubMedPubMedCentralGoogle Scholar
  101. Ostan R, Bucci L, Capri M, Salvioli S, Scurti M, Pini E, Monti D, Franceschi C (2008) Immunosenescence and immunogenetics of human longevity. Neuroimmunomodulation 15(4–6):224–240. CrossRefPubMedGoogle Scholar
  102. Ostojic SM (2018) Inadequate production of H2 by gut microbiota and Parkinson disease. Trends Endocrinol Metab S1043-2760(18):30027–30024. CrossRefGoogle Scholar
  103. Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO (2007) Development of the human infant intestinal microbiota. PLoS Biol 5(7):e177. CrossRefPubMedPubMedCentralGoogle Scholar
  104. Pararajasingam A, Uwagwu J (2017) Lactobacillus: the not so friendly bacteria. BMJ Case Reports 2017
  105. Parashar A, Udayabanu M (2017) Gut microbiota: implications in Parkinson's disease. Parkinsonism Relat Disord 38:1–7. CrossRefGoogle Scholar
  106. Park MR, Oh S, Son SJ, Park DJ, Oh S, Kim SH, Jeong DY, Oh NS, Lee Y, Song M, Kim Y (2015) Bacillus licheniformis isolated from traditional Korean food resources enhances the longevity of Caenorhabditis elegans through serotonin signaling. J Agric Food Chem 63(47):10227–10233. CrossRefPubMedGoogle Scholar
  107. Penders J, Thijs C, Vink C, Stelma FF, Snijders B, Kummeling I, van den Brandt PA, Stobberingh EE (2006) Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics 118(2):511–521. CrossRefPubMedGoogle Scholar
  108. Perez-Pardo P, Kliest T, Dodiya HB, Broersen LM, Garssen J, Keshavarzian A, Kraneveld AD (2017) The gut-brain axis in Parkinson's disease: possibilities for food-based therapies. Eur J Pharmacol 817:86–95. CrossRefPubMedGoogle Scholar
  109. Petra AI, Panagiotidou S, Hatziagelaki E, Stewart JM, Conti P, Theoharides TC (2015) Gut microbiota brain axis and its effect on neuropsychiatric disorders with suspected immune dysregulation. Clin Ther 37(5):984–995. CrossRefPubMedPubMedCentralGoogle Scholar
  110. Potempa J, Mydel P, Koziel J (2017) The case for periodontitis in the pathogenesis of rheumatoid arthritis. Nat Rev Rheumatol 13:606–620. CrossRefPubMedGoogle Scholar
  111. Qian Y, Yang X, Xu S, Wu C, Song Y, Qin N, Chen SD, Xiao Q (2018) Alteration of the fecal microbiota in Chinese patients with Parkinson's disease. Brain Behav Immun 70:194–202. CrossRefPubMedGoogle Scholar
  112. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T, Mende DR, Li J, Xu J, Li S, Li D, Cao J, Wang B, Liang H, Zheng H, Xie Y, Tap J, Lepage P, Bertalan M, Batto JM, Hansen T, Le Paslier D, Linneberg A, Nielsen HB, Pelletier E, Renault P, Sicheritz-Ponten T, Turner K, Zhu H, Yu C, Li S, Jian M, Zhou Y, Li Y, Zhang X, Li S, Qin N, Yang H, Wang J, Brunak S, Dore J, Guarner F, Kristiansen K, Pedersen O, Parkhill J, Weissenbach J, Bork P, Ehrlich SD, Wang J (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464(7285):59–65. CrossRefPubMedPubMedCentralGoogle Scholar
  113. Rajilic-Stojanovic M, Heilig HG, Molenaar D, Kajander K, Surakka A, Smidt H, de Vos WM (2009) Development and application of the human intestinal tract chip, a phylogenetic microarray: analysis of universally conserved phylotypes in the abundant microbiota of young and elderly adults. Environ Microbiol 11(7):1736–1751. CrossRefPubMedPubMedCentralGoogle Scholar
  114. Rajoka MSR, Shi J, Mehwish HM, Zhu J, Li Q, Shao D, Huang Q, Yang H (2017a) Interaction between diet composition and gut microbiota and its impact on gastrointestinal tract health. Food Sci Human Wellness CrossRefGoogle Scholar
  115. Remely M, Tesar I, Hippe B, Gnauer S, Rust P, Haslberger AG (2015) Gut microbiota composition correlates with changes in body fat content due to weight loss. Benef Microbes 6(4):431–439. CrossRefPubMedGoogle Scholar
  116. Rajoka MSR, Mehwish HM, Siddiq M, Haobin Z, Zhu J, Yan L, Shao D, Xu X, Shi J (2017b) Identification, characterization, and probiotic potential of Lactobacillus rhamnosus isolated from human milk. Food Sci Technol 84:271–280. CrossRefGoogle Scholar
  117. Riggs BL, Melton Iii LJ 3rd, Robb RA, Camp JJ, Atkinson EJ, Peterson JM, Rouleau PA, McCollough CH, Bouxsein ML, Khosla S (2004) Population-based study of age and sex differences in bone volumetric density, size, geometry, and structure at different skeletal sites. J Bone Miner Res 19(12):1945–1954. CrossRefPubMedGoogle Scholar
  118. Rogers GB (2015) Germs and joints: the contribution of the human microbiome to rheumatoid arthritis. Nature Medi 21(8):839–841. CrossRefGoogle Scholar
  119. Rogier EW, Frantz AL, Bruno ME, Wedlund L, Cohen DA, Stromberg AJ, Kaetzel CS (2014) Lessons from mother: long-term impact of antibodies in breast milk on the gut microbiota and intestinal immune system of breastfed offspring. Gut Microbes 5(5):663–668. CrossRefPubMedPubMedCentralGoogle Scholar
  120. Roth GA, Forouzanfar MH, Moran AE, Barber R, Nguyen G, Feigin VL, Naghavi M, Mensah GA, Murray CJ (2015) Demographic and epidemiologic drivers of global cardiovascular mortality. N Engl J Med 372(14):1333–1341. CrossRefPubMedPubMedCentralGoogle Scholar
  121. Rutayisire E, Huang K, Liu Y, Tao F (2016) The mode of delivery affects the diversity and colonization pattern of the gut microbiota during the first year of infants' life: a systematic review. BMC Gastroenterol 16(1):86. CrossRefPubMedPubMedCentralGoogle Scholar
  122. Saraswati S, Sitaraman R (2014) Aging and the human gut microbiota-from correlation to causality. Front Microbiol 5:764. CrossRefPubMedGoogle Scholar
  123. Satoh T, Murata M, Iwabuchi N, Odamaki T, Wakabayashi H, Yamauchi K, Abe F, Xiao JZ (2015) Effect of Bifidobacterium breve B-3 on skin photoaging induced by chronic UV irradiation in mice. Benef Microbes 6(4):497–504. CrossRefPubMedGoogle Scholar
  124. Satokari R, Gronroos T, Laitinen K, Salminen S, Isolauri E (2009) Bifidobacterium and Lactobacillus DNA in the human placenta. Lett Appl Microbiol 48(1):8–12. CrossRefPubMedGoogle Scholar
  125. Scheperjans F, Aho V, Pereira PA, Koskinen K, Paulin L, Pekkonen E, Haapaniemi E, Kaakkola S, Eerola-Rautio J, Pohja M, Kinnunen E, Murros K, Auvinen P (2015) Gut microbiota are related to Parkinson's disease and clinical phenotype. Mov Disord Off J Mov Disord Soc 30(3):350–358. CrossRefPubMedGoogle Scholar
  126. Scher JU, Joshua V, Artacho A, Abdollahi-Roodsaz S, Ockinger J, Kullberg S, Skold M, Eklund A, Grunewald J, Clemente JC, Ubeda C, Segal LN, Catrina AI (2016) The lung microbiota in early rheumatoid arthritis and autoimmunity. Microbiome 4(1):60. CrossRefPubMedPubMedCentralGoogle Scholar
  127. Sepova HK, Dudik B, Bilkova A (2018) Gut microbiota: its development and relation to certain diseases. Ceska Slov 66(6):267–273Google Scholar
  128. Shale M, Schiering C, Powrie F (2013) CD4(+) T-cell subsets in intestinal inflammation. Immunol Rev 252(1):164–182. CrossRefPubMedPubMedCentralGoogle Scholar
  129. Shanley DP, Aw D, Manley NR, Palmer DB (2009) An evolutionary perspective on the mechanisms of immunosenescence. Trends Immunol 30(7):374–381. CrossRefPubMedGoogle Scholar
  130. Sharma AK, Jaiswal SK, Chaudhary N, Sharma VK (2017) A novel approach for the prediction of species-specific biotransformation of xenobiotic/drug molecules by the human gut microbiota. Sci Rep 7(1):9751. CrossRefPubMedPubMedCentralGoogle Scholar
  131. Sun Y, Xu Z, Lin H, Lu X, Huang Y, Huang S, Wang X, Chi P (2017) Impact of body mass index on treatment outcome of neoadjuvant chemoradiotherapy in locally advanced rectal cancer. Eur J Surg Oncol 43:1828–1834. CrossRefPubMedGoogle Scholar
  132. Takahashi A, Flanigan ME, McEwen BS, Russo SJ (2018) Aggression, social stress, and the immune system in humans and animal models. Front Behav Neurosci 12:56. CrossRefPubMedPubMedCentralGoogle Scholar
  133. Takahashi M, Suzuki M, Fukuoka M, Fujikake N, Watanabe S, Murata M, Wada K, Nagai Y, Hohjoh H (2015) Normalization of overexpressed alpha-synuclein causing Parkinson's disease by a moderate gene silencing with RNA interference. Mol Ther Nucleic acids 4:e241. CrossRefPubMedGoogle Scholar
  134. Tang MS, Bowcutt R, Leung JM, Wolff MJ, Gundra UM, Hudesman D, Malter LB, Poles MA, Chen LA, Pei Z, Neto AG, Abidi WM, Ullman T, Mayer L, Bonneau RA, Cho I, Loke P (2017) Integrated analysis of biopsies from inflammatory bowel disease patients identifies SAA1 as a link between mucosal microbes with TH17 and TH22 cells. Inflamm Bowel Dis 23(9):1544–1554. CrossRefPubMedPubMedCentralGoogle Scholar
  135. Thanabalasuriar A, Kubes P (2014) Neonates, antibiotics and the microbiome. Nat Med 20(5):469–470. CrossRefPubMedGoogle Scholar
  136. Thomas F, Hehemann JH, Rebuffet E, Czjzek M, Michel G (2011) Environmental and gut bacteroidetes: the food connection. Front Microbiol 2:93. CrossRefPubMedPubMedCentralGoogle Scholar
  137. Thushara RM, Gangadaran S, Solati Z, Moghadasian MH (2016) Cardiovascular benefits of probiotics: a review of experimental and clinical studies. Food Funct 7(2):632–642. CrossRefPubMedGoogle Scholar
  138. Tinetti ME, Inouye SK, Gill TM, Doucette JT (1995) Shared risk factors for falls, incontinence, and functional dependence. Unifying the approach to geriatric syndromes. Jama 273(17):1348–1353CrossRefPubMedGoogle Scholar
  139. Tomkovich S, Yang Y, Winglee K, Gauthier J, Muhlbauer M, Sun X, Mohamadzadeh M, Liu X, Martin P, Wang GP, Oswald E, Fodor AA, Jobin C (2017) Locoregional effects of microbiota in a preclinical model of colon carcinogenesis. Cancer Res 77(10):2620–2632. CrossRefPubMedPubMedCentralGoogle Scholar
  140. Urbaniak C, Angelini M, Gloor GB, Reid G (2016) Human milk microbiota profiles in relation to birthing method, gestation and infant gender. Microbiome 4:1. CrossRefPubMedPubMedCentralGoogle Scholar
  141. Vaahtovuo J, Munukka E, Korkeamaki M, Luukkainen R, Toivanen P (2008) Fecal microbiota in early rheumatoid arthritis. J Rheumatol 35(8):1500–1505Google Scholar
  142. Vaiserman AM, Koliada AK, Marotta F (2017) Gut microbiota: a player in aging and a target for anti-aging intervention. Ageing Res Rev 35(supplement C):36–45. CrossRefPubMedGoogle Scholar
  143. Vallejo-Vaz AJ, Robertson M, Catapano AL, Watts GF, Kastelein JJ, Packard CJ, Ford I, Ray KK (2017) LDL-cholesterol lowering for the primary prevention of cardiovascular disease among men with primary elevations of LDL-cholesterol levels of 190 mg/dL or above: analyses from the WOSCOPS 5-year randomised trial and 20-year observational follow-up. Circulation 136:1878–1891. CrossRefPubMedGoogle Scholar
  144. van Tongeren SP, Slaets JP, Harmsen HJ, Welling GW (2005) Fecal microbiota composition and frailty. Appl Environ Microbiol 71(10):6438–6442. CrossRefPubMedPubMedCentralGoogle Scholar
  145. Vrieze A, Van Nood E, Holleman F, Salojarvi J, Kootte RS, Bartelsman JF, Dallinga-Thie GM, Ackermans MT, Serlie MJ, Oozeer R, Derrien M, Druesne A, Van Hylckama Vlieg JE, Bloks VW, Groen AK, Heilig HG, Zoetendal EG, Stroes ES, de Vos WM, Hoekstra JB, Nieuwdorp M (2012) Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterol 143(4):913–916.e7. CrossRefGoogle Scholar
  146. Walker AW, Duncan SH, Louis P, Flint HJ (2014) Phylogeny, culturing, and metagenomics of the human gut microbiota. Trends Microbiol 22(5):267–274. CrossRefPubMedGoogle Scholar
  147. Waring RH, Harris RM, Mitchell SC (2017) Drug metabolism in the elderly: a multifactorial problem? Maturitas 100:27–32. CrossRefPubMedGoogle Scholar
  148. Wong SH, Zhao L, Zhang X, Nakatsu G, Han J, Xu W, Xiao X, Kwong TN, Tsoi H, Wu WK, Benhua Z, Chan FK, Sung JJ, Wei H, Yu J (2017) Gavage of fecal samples from patients with colorectal cancer promotes intestinal carcinogenesis in germ-free and conventional mice. Gastroenterol 153:1621–1633.e6. CrossRefGoogle Scholar
  149. Xiao Y, Yan H, Diao H, Yu B, He J, Yu J, Zheng P, Mao X, Luo Y, Chen D (2017) Early gut microbiota intervention suppresses DSS-induced inflammatory responses by deactivating TLR/NLR signalling in pigs. Sci Rep 7(1):3224. CrossRefPubMedPubMedCentralGoogle Scholar
  150. Zhang C, Li S, Yang L, Huang P, Li W, Wang S, Zhao G, Zhang M, Pang X, Yan Z, Liu Y, Zhao L (2013) Structural modulation of gut microbiota in life-long calorie-restricted mice. Nat Commun 4:2163. CrossRefPubMedPubMedCentralGoogle Scholar
  151. Zhao Q, Harbour SN, Kolde R, Latorre IJ (2017) Selective induction of homeostatic Th17 cells in the murine intestine by cholera toxin interacting with the microbiota. J Immunol 199(1):312–322. CrossRefPubMedPubMedCentralGoogle Scholar
  152. Zwielehner J, Liszt K, Handschur M, Lassl C, Lapin A, Haslberger AG (2009) Combined PCR-DGGE fingerprinting and quantitative-PCR indicates shifts in fecal population sizes and diversity of Bacteroides, bifidobacteria and Clostridium cluster IV in institutionalized elderly. Exp Gerontol 44(6–7):440–446. CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Muhammad Shahid Riaz Rajoka
    • 1
    • 2
  • Haobin Zhao
    • 1
  • Na Li
    • 1
  • Yao Lu
    • 1
  • Ziyang Lian
    • 1
  • Dongyan Shao
    • 1
  • Mingliang Jin
    • 1
  • Qi Li
    • 1
  • Liqing Zhao
    • 2
  • Junling Shi
    • 1
    Email author
  1. 1.Key Laboratory for Space Bioscience and Space Biotechnology, School of Life SciencesNorthwestern Polytechnical UniversityXi’anPeople’s Republic of China
  2. 2.Department of Food Science and Engineering, College of Chemistry and Chemical EngineeringShenzhen UniversityShenzhenPeople’s Republic of China

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