1887

Abstract

Purpose. The microbiome from nursing home (NH) residents is marked by a loss in diversity that is associated with increased frailty. Our objective was to explore the associations of NH environment, frailty, nutritional status and residents’ age to microbiome composition and potential metabolic function.

Methodology. We conducted a prospective longitudinal cohort study of 23 residents, 65 years or older, from one NH that had four floors: two separate medical intensive floors and two floors with active elders. Residents were assessed using the mini nutritional assessment tool and clinical frailty scale. Bacterial composition and metabolic potential of residents' stool samples was determined by metagenomic sequencing. We performed traditional unsupervised correspondence analysis and linear mixed effect modelling regression to assess the bacteria and functional pathways significantly affected by these covariates.

Results/Key findings. NH resident microbiomes demonstrated temporal stability (PERMANOVA P=0.001) and differing dysbiotic associations with increasing age, frailty and malnutrition scores. As residents aged, the abundance of microbiota-encoded genes and pathways related to essential amino acid, nitrogenous base and vitamin B production declined. With increasing frailty, residents had lower abundances of butyrate-producing organisms, which are associated with increased health and higher abundances of known dysbiotic species. As residents became malnourished, butyrate-producing organisms declined and dysbiotic bacterial species increased. Finally, the microbiome of residents living in proximity shared similar species and, as demonstrated for Escherichia coli, similar strains.

Conclusion. These findings support the conclusion that a signature ‘NH’ microbiota may exist that is affected by the residents' age, frailty, nutritional status and physical location.

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2017-11-14
2019-10-20
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References

  1. Claesson MJ, Jeffery IB, Conde S, Power SE, O'Connor EM et al. Gut microbiota composition correlates with diet and health in the elderly. Nature 2012; 488: 178– 184 [CrossRef] [PubMed]
    [Google Scholar]
  2. Lee DC, Barlas D, Ryan JG, Ward MF, Sama AE et al. Methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci: prevalence and predictors of colonization in patients presenting to the emergency department from nursing homes. J Am Geriatr Soc 2002; 50: 1463– 1465 [CrossRef] [PubMed]
    [Google Scholar]
  3. Pop-Vicas A, Tacconelli E, Gravenstein S, Lu B, D'Agata EM. Influx of multidrug-resistant, gram-negative bacteria in the hospital setting and the role of elderly patients with bacterial bloodstream infection. Infect Control Hosp Epidemiol 2009; 30: 325– 331 [CrossRef] [PubMed]
    [Google Scholar]
  4. Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG et al. Human gut microbiome viewed across age and geography. Nature 2012; 486: 222– 227 [CrossRef] [PubMed]
    [Google Scholar]
  5. Cassone M, Mody L. Colonization with multi-drug resistant organisms in nursing homes: scope, importance, and management. Curr Geriatr Rep 2015; 4: 87– 95 [CrossRef] [PubMed]
    [Google Scholar]
  6. Buffie CG, Pamer EG. Microbiota-mediated colonization resistance against intestinal pathogens. Nat Rev Immunol 2013; 13: 790– 801 [CrossRef] [PubMed]
    [Google Scholar]
  7. Rampelli S, Candela M, Turroni S, Biagi E, Collino S et al. Functional metagenomic profiling of intestinal microbiome in extreme ageing. Aging 2013; 5: 902– 912 [CrossRef] [PubMed]
    [Google Scholar]
  8. O'Toole PW, Jeffery IB. Gut microbiota and aging. Science 2015; 350: 1214– 1215 [CrossRef] [PubMed]
    [Google Scholar]
  9. Rehman A, Rausch P, Wang J, Skieceviciene J, Kiudelis G et al. Geographical patterns of the standing and active human gut microbiome in health and IBD. Gut 2016; 65: 238– 248 [CrossRef] [PubMed]
    [Google Scholar]
  10. Rockwood K, Song X, Macknight C, Bergman H, Hogan DB et al. A global clinical measure of fitness and frailty in elderly people. CMAJ 2005; 173: 489– 495 [CrossRef] [PubMed]
    [Google Scholar]
  11. Jackson MA, Jackson M, Jeffery IB, Beaumont M, Bell JT et al. Signatures of early frailty in the gut microbiota. Genome Med 2016; 8: 8 [CrossRef] [PubMed]
    [Google Scholar]
  12. Milani C, Ticinesi A, Gerritsen J, Nouvenne A, Lugli GA et al. Gut microbiota composition and Clostridium difficile infection in hospitalized elderly individuals: a metagenomic study. Sci Rep 2016; 6: 25945 [CrossRef] [PubMed]
    [Google Scholar]
  13. Rubenstein LZ, Harker JO, Salvà A, Guigoz Y, Vellas B. Screening for undernutrition in geriatric practice: developing the short-form mini-nutritional assessment (MNA-SF). J Gerontol A Biol Sci Med Sci 2001; 56: M366– M372 [CrossRef] [PubMed]
    [Google Scholar]
  14. Saarela RK, Lindroos E, Soini H, Hiltunen K, Muurinen S et al. Dentition, nutritional status and adequacy of dietary intake among older residents in assisted living facilities. Gerodontology 2016; 33: 225– 232 [CrossRef] [PubMed]
    [Google Scholar]
  15. Guigoz Y. The mini nutritional assessment (MNA) review of the literature–what does it tell us?. J Nutr Health Aging 2006; 10: 485– 487 [PubMed]
    [Google Scholar]
  16. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30: 2114– 2120 [CrossRef] [PubMed]
    [Google Scholar]
  17. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012; 9: 1– 3 [CrossRef] [PubMed]
    [Google Scholar]
  18. Truong DT, Franzosa EA, Tickle TL, Scholz M, Weingart G et al. MetaPhlAn2 for enhanced metagenomic taxonomic profiling. Nat Methods 2015; 12: 902– 903 [CrossRef] [PubMed]
    [Google Scholar]
  19. Abubucker S, Segata N, Goll J, Schubert AM, Izard J et al. Metabolic reconstruction for metagenomic data and its application to the human microbiome. PLoS Comput Biol 2012; 8: e1002358 [CrossRef] [PubMed]
    [Google Scholar]
  20. Truong DT, Tett A, Pasolli E, Huttenhower C, Segata N. Microbial strain-level population structure and genetic diversity from metagenomes. Genome Res 2017; 27: 626– 638 [CrossRef] [PubMed]
    [Google Scholar]
  21. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32: 1792– 1797 [CrossRef] [PubMed]
    [Google Scholar]
  22. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30: 1312– 1313 [CrossRef] [PubMed]
    [Google Scholar]
  23. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J et al. BLAST+: architecture and applications. BMC Bioinformatics 2009; 10: 421 [CrossRef] [PubMed]
    [Google Scholar]
  24. Kostic AD, Gevers D, Siljander H, Vatanen T, Hyötyläinen T et al. The dynamics of the human infant gut microbiome in development and in progression toward type 1 diabetes. Cell Host Microbe 2015; 17: 260– 273 [CrossRef] [PubMed]
    [Google Scholar]
  25. Collado MC, Derrien M, Isolauri E, de Vos WM, Salminen S. Intestinal integrity and Akkermansia muciniphila, a mucin-degrading member of the intestinal microbiota present in infants, adults, and the elderly. Appl Environ Microbiol 2007; 73: 7767– 7770 [CrossRef] [PubMed]
    [Google Scholar]
  26. Morgan XC, Tickle TL, Sokol H, Gevers D, Devaney KL et al. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol 2012; 13: 2– 18 [CrossRef] [PubMed]
    [Google Scholar]
  27. Takahashi K, Nishida A, Fujimoto T, Fujii M, Shioya M et al. Reduced abundance of butyrate-producing bacteria species in the fecal microbial community in crohn's disease. Digestion 2016; 93: 59– 65 [CrossRef] [PubMed]
    [Google Scholar]
  28. Rivière A, Selak M, Lantin D, Leroy F, de Vuyst L. Bifidobacteria and butyrate-producing colon bacteria: importance and strategies for their stimulation in the human gut. Front Microbiol 2016; 7: 979 [CrossRef] [PubMed]
    [Google Scholar]
  29. Vital M, Howe AC, Tiedje JM. Revealing the bacterial butyrate synthesis pathways by analyzing (meta)genomic data. MBio 2014; 5: e00889-14 [CrossRef] [PubMed]
    [Google Scholar]
  30. van den Abbeele P, Belzer C, Goossens M, Kleerebezem M, de Vos WM et al. Butyrate-producing Clostridium cluster XIVa species specifically colonize mucins in an in vitro gut model. Isme J 2013; 7: 949– 961 [CrossRef] [PubMed]
    [Google Scholar]
  31. Meehan CJ, Beiko RG. A phylogenomic view of ecological specialization in the Lachnospiraceae, a family of digestive tract-associated bacteria. Genome Biol Evol 2014; 6: 703– 713 [CrossRef] [PubMed]
    [Google Scholar]
  32. Abdel Hadi L, di Vito C, Riboni L. Fostering inflammatory bowel disease: sphingolipid strategies to join forces. Mediators Inflamm 2016; 2016: 1– 13 [CrossRef] [PubMed]
    [Google Scholar]
  33. Leclercq S, de Saeger C, Delzenne N, de Timary P, Stärkel P. Role of inflammatory pathways, blood mononuclear cells, and gut-derived bacterial products in alcohol dependence. Biol Psychiatry 2014; 76: 725– 733 [CrossRef] [PubMed]
    [Google Scholar]
  34. Whalen JG. Spontaneous Citrobacter freundii infection in an immunocompetent patient. Arch Dermatol 2007; 143: 115– 125 [CrossRef]
    [Google Scholar]
  35. Hidron AI, Edwards JR, Patel J, Horan TC, Sievert DM et al. NHSN annual update: antimicrobial-resistant pathogens associated with healthcare-associated infections: annual summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2006–2007. Infect Control Hosp Epidemiol 2008; 29: 996– 1011 [CrossRef] [PubMed]
    [Google Scholar]
  36. Polansky O, Sekelova Z, Faldynova M, Sebkova A, Sisak F et al. Important metabolic pathways and biological processes expressed by chicken cecal microbiota. Appl Environ Microbiol 2015; 82: 1569– 1576 [CrossRef] [PubMed]
    [Google Scholar]
  37. Finegold SM, Song Y, Liu C, Hecht DW, Summanen P et al. Clostridium clostridioforme: a mixture of three clinically important species. Eur J Clin Microbiol Infect Dis 2005; 24: 319– 324 [CrossRef] [PubMed]
    [Google Scholar]
  38. Lozupone C, Faust K, Raes J, Faith JJ, Frank DN et al. Identifying genomic and metabolic features that can underlie early successional and opportunistic lifestyles of human gut symbionts. Genome Res 2012; 22: 1974– 1984 [CrossRef] [PubMed]
    [Google Scholar]
  39. Schirmer M, Smeekens SP, Vlamakis H, Jaeger M, Oosting M et al. Linking the human gut microbiome to inflammatory cytokine production capacity. Cell 2016; 167: e1128 [Crossref]
    [Google Scholar]
  40. Lin YP, Thibodeaux CH, Peña JA, Ferry GD, Versalovic J. Probiotic Lactobacillus reuteri suppress proinflammatory cytokines via c-Jun. Inflamm Bowel Dis 2008; 14: 1068– 1083 [CrossRef] [PubMed]
    [Google Scholar]
  41. Biagi E, Nylund L, Candela M, Ostan R, Bucci L et al. Through ageing, and beyond: gut microbiota and inflammatory status in seniors and centenarians. PLoS One 2010; 5: e10667 [CrossRef] [PubMed]
    [Google Scholar]
  42. Kumar M, Babaei P, Ji B, Nielsen J. Human gut microbiota and healthy aging: recent developments and future prospective. Nutr Healthy Aging 2016; 4: 3– 16 [CrossRef] [PubMed]
    [Google Scholar]
  43. Biagi E, Candela M, Turroni S, Garagnani P, Franceschi C et al. Ageing and gut microbes: perspectives for health maintenance and longevity. Pharmacol Res 2013; 69: 11– 20 [CrossRef] [PubMed]
    [Google Scholar]
  44. Fujita S, Volpi E. Amino acids and muscle loss with aging. J Nutr 2006; 136: 277S– 280 [PubMed]
    [Google Scholar]
  45. Volpi E, Kobayashi H, Sheffield-Moore M, Mittendorfer B, Wolfe RR. Essential amino acids are primarily responsible for the amino acid stimulation of muscle protein anabolism in healthy elderly adults. Am J Clin Nutr 2011; 78: 250– 258 [PubMed]
    [Google Scholar]
  46. Morgan XC, Tickle TL, Sokol H, Gevers D, Devaney KL et al. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol 2012; 13: R79 [CrossRef] [PubMed]
    [Google Scholar]
  47. Basson A, Trotter A, Rodriguez-Palacios A, Cominelli F. Mucosal interactions between genetics, diet, and microbiome in inflammatory bowel disease. Front Immunol 2016; 7: 290 [CrossRef] [PubMed]
    [Google Scholar]
  48. Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermúdez-Humarán LG et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci USA 2008; 105: 16731– 16736 [CrossRef] [PubMed]
    [Google Scholar]
  49. Joossens M, Huys G, Cnockaert M, de Preter V, Verbeke K et al. Dysbiosis of the faecal microbiota in patients with Crohn's disease and their unaffected relatives. Gut 2011; 60: 631– 637 [CrossRef] [PubMed]
    [Google Scholar]
  50. Miyake S, Kim S, Suda W, Oshima K, Nakamura M et al. Dysbiosis in the gut microbiota of patients with multiple sclerosis, with a striking depletion of species belonging to clostridia XIVa and IV clusters. PLoS One 2015; 10: e0137429 [CrossRef] [PubMed]
    [Google Scholar]
  51. Galland L. The gut microbiome and the brain. J Med Food 2014; 17: 1261– 1272 [CrossRef] [PubMed]
    [Google Scholar]
  52. Li J, Zhao F, Wang Y, Chen J, Tao J et al. Gut microbiota dysbiosis contributes to the development of hypertension. Microbiome 2017; 5: 14 [CrossRef] [PubMed]
    [Google Scholar]
  53. Boulangé CL, Neves AL, Chilloux J, Nicholson JK, Dumas ME. Impact of the gut microbiota on inflammation, obesity, and metabolic disease. Genome Med 2016; 8: 42 [CrossRef] [PubMed]
    [Google Scholar]
  54. Sommer F, Bäckhed F. The gut microbiota–masters of host development and physiology. Nat Rev Microbiol 2013; 11: 227– 238 [CrossRef] [PubMed]
    [Google Scholar]
  55. Boursier J, Mueller O, Barret M, Machado M, Fizanne L et al. The severity of nonalcoholic fatty liver disease is associated with gut dysbiosis and shift in the metabolic function of the gut microbiota. Hepatology 2016; 63: 764– 775 [CrossRef] [PubMed]
    [Google Scholar]
  56. Hansen SG, Skov MN, Justesen US. Two cases of Ruminococcus gnavus bacteremia associated with diverticulitis. J Clin Microbiol 2013; 51: 1334– 1336 [CrossRef] [PubMed]
    [Google Scholar]
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