Practical considerations for large-scale gut microbiome studies

FEMS Microbiology Reviews

Volumn 41, Issue , 2017, Pages S154-S167

  Vandeputte, Doris ^a,b,c   Tito, Raul Y ^a,b,c   Vanleeuwen, Rianne ^d   Falony, Gwen ^a,b   Raes, Jeroen ^a,b  

^a REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^d UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

cold chain management; faecal sample preservation; gut microbiome; user experience faecal sampling

Indexed keywords

COLD STRESS; CROSS-SECTIONAL STUDY; CRYOPRESERVATION; FECES; FLORA; FREEZING; GASTROINTESTINAL TRACT; GOLD STANDARD; HUMAN; MICROBIOME; NONHUMAN; REVIEW; STANDARDIZATION; INTESTINE; INTESTINE FLORA; MICROBIOLOGY; PHYSIOLOGY; PROCEDURES;

CRYOPROTECTIVE AGENT;

CRYOPRESERVATION; CRYOPROTECTIVE AGENTS; FECES; GASTROINTESTINAL MICROBIOME; HUMANS; INTESTINES;

EID: 85037376418     PISSN: 01686445     EISSN: 15746976     Source Type: Journal    
DOI: 10.1093/FEMSRE/FUX027     Document Type: Review

References (75)

1. Aagaard K, Petrosino J, Keitel W et al. The Human Microbiome Project strategy for comprehensive sampling of the human microbiome and why it matters. FASEB J 2013;27:1012–22.
2. Anderson EL, Li W, Klitgord N et al. A robust ambient temperature collection and stabilization strategy: Enabling worldwide functional studies of the human microbiome. Sci Rep 2016;6:31731.
3. Bahl MI, Bergström A, Licht TR. Freezing fecal samples prior to DNA extraction affects the Firmicutes to Bacteroidetes ratio determined by downstream quantitative PCR analysis. FEMS Microbiol Lett 2012;329:193–7.
4. Bai G, Gajer P, Nandy M et al. Comparison of storage conditions for human vaginal microbiome studies. PLoS One 2012;7:e36934.
5. Blekhman R, Tang K, Archie E et al. Common methods for fecal sample storage in field studies yield consistent signatures of individual identity in microbiome sequencing data. Sci Rep 2016;6:31519.
6. Cani PD, Bibiloni R, Knauf C et al. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 2008;57:147081.
7. Caporaso JG, Lauber CL, Costello EK et al. Moving pictures of the human microbiome. Genome Biol 2011;12:R50.
8. Cardona S, Eck A, Cassellas M et al. Storage conditions of intestinal microbiota matter in metagenomic analysis. BMC Microbiol 2012;12:158.
9. Carroll IM, Ringel-Kulka T, Siddle JP et al. Characterization of the fecal microbiota using high-throughput sequencing reveals a stable microbial community during storage. PLoS One 2012;7:e46953.
10. Cho I, Blaser MJ. The human microbiome: at the interface of health and disease. Nat Rev Genet 2012;13:260–70.
11. Choo JM, Leong LE, Rogers GB. Sample storage conditions significantly influence faecal microbiome profiles. Sci Rep 2015;5:16350.
12. Claesson MJ, Jeffery IB, Conde S et al. Gut microbiota composition correlates with diet and health in the elderly. Nature 2012;488:178–84.
13. Cryan JF, Dinan TG. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci 2012;13:701–12.
14. Debelius J, Song SJ, Vazquez-Baeza Y et al. Tiny microbes, enormous impacts: what matters in gut microbiome studies? Genome Biol 2016;17:217.
15. Dominianni C, Wu J, Hayes RB et al. Comparison of methods for fecal microbiome biospecimen collection. BMC Microbiol 2014;14:103.
16. Donaldson GP, Lee SM, Mazmanian SK. Gut biogeography of the bacterial microbiota. Nat Rev Microbiol 2015;14:20–32.
17. Dubilier N, Mcfall-ngai M, Zhou L. Create a global microbiome effort. Nature 2015;526:631–4.
18. Falony G, Joossens M, Vieira-Silva S et al. Population-level analysis of gut microbiome variation. Science (80-) 2016;352:560–4.
19. Finucane MM, Sharpton TJ, Laurent TJ et al. A taxonomic signature of obesity in the microbiome? Getting to the Guts of the matter. PLoS One 2014;9:e84689.
20. Flores R, Shi J, Gail MH et al. Assessment of the human faecal microbiota: I. Measurement and reproducibility of selected enzymatic activities. Eur J Clin Invest 2012; 42:848–54.
21. Flores R, Shi J, Yu G et al. Collection media and delayed freezing effects on microbial composition of human stool. Microbiome 2015;3:33.
22. Fouhy F, Deane J, Rea MC et al. The effects of freezing on faecal microbiota as determined using miseq sequencing and culture-based investigations. PLoS One 2015;10:1–12.
23. Frank DN, Robertson CE, Hamm CM et al. Disease phenotype and genotype are associated with shifts in intestinal-associated microbiota in inflammatory bowel diseases. Inflamm Bowel Dis 2011;17:179–84.
24. Franzosa EA, Morgan XC, Segata N et al. Relating the metatranscriptome and metagenome of the human gut. P Natl Acad Sci USA 2014;111:2329–38.
25. Gevers D, Knight R, Petrosino JF et al. The Human Microbiome Project: a community resource for the healthy human microbiome. PLoS Biol 2012;10:e1001377.
26. Gorzelak MA, Gill SK, Tasnim N et al. Methods for improving human gut microbiome data by reducing variability through sample processing and storage of stool. PLoS One 2015;10:1–14.
27. Gratton J, Phetcharaburanin J, Mullish BH et al. Optimized sample handling strategy for metabolic profiling of human feces. Anal Chem 2016;88:4661–8.
28. Guo Y, Li S-H, Kuang Y-S et al. Effect of short-term room temperature storage on the microbial community in infant fecal samples. Sci Rep 2016;6:26648.
29. Hale VL, Tan CL, Knight R et al. Effect of preservation method on spider monkey (Ateles geoffroyi) fecal microbiota over 8 weeks. J Microbiol Methods 2015;113:16–26.
30. Hamilton MJ, Weingarden AR, Sadowsky MJ et al. Standardized Frozen preparation for transplantation of fecal microbiota for recurrent clostridium difficile infection. Am J Gastroenterol 2012;107:761–7.
31. Hill C, Brown JR, Lynch D et al. Effect of room temperature transport vials on DNA quality and phylogenetic composition of faecal microbiota of elderly adults and infants. Microbiome 2016;4:26.
32. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature 2012;486:207–14.
33. Jordan S, Watkins A, Storey M et al. Volunteer bias in recruitment, retention, and blood sample donation in a randomised controlled trial involving mothers and their children at six months and two years: a longitudinal analysis. PLoS One 2013;8:e67912.
34. Kau AL, Ahern PP, Griffin NW et al. Human nutrition, the gut microbiome and the immune system. Nature 2011;474: 327–36.
35. Kerckhof FM, Courtens ENP, Geirnaert A et al. Optimized cryopreservation of mixed microbial communities for conserved functionality and diversity. PLoS One 2014;9, DOI: 10.1371/journal.pone.0099517.
36. Khan MZ, Altmann J, Isani SS et al. A matter of time: evaluation the storage of fecal samples for steroid analysis. Gen Comp Endocrinol 2002;128:57–64.
37. Kia E, Wagner Mackenzie B, Middleton D et al. Integrity of the human faecal microbiota following long-term sample storage. PLoS One 2016;11:e0163666.
38. Koboziev I, Reinoso Webb C, Furr KL et al. Role of the enteric microbiota in intestinal homeostasis and inflammation. Free Radic Biol Med 2014;68:122–33.
39. Koren O, Knights D, Gonzalez A et al. A guide to enterotypes across the human body: meta-analysis of microbial community structures in human microbiome datasets. PLoS Comput Biol 2013;9:e1002863.
40. Laurin V, Labbé N, Juteau P et al. Long-term storage conditions for carriers with denitrifying biomass of the fluidized, methanol-fed denitrification reactor of the Montreal Biodome, and the impact on denitrifying activity and bacterial population. Water Res 2006;40:1836–40.
41. Le Chatelier E, Nielsen T, Qin J et al. Richness of human gut microbiome correlates with metabolic markers. Nature 2013;500:541–6.
42. Leddin DJ, Enns R, Hilsden R et al. Canadian Association of Gastroenterology position statement on screening individuals at average risk for developing colorectal cancer: 2010. Can J Gastroenterol 2010;24:705–14.
43. Lindahl T. Instability and decay of the primary structure of DNA. Nature 1993;362:709–15.
44. Loftfield E, Vogtmann E, Sampson JN et al. Comparison of collection methods for fecal samples for discovery metabolomics in epidemiologic studies. Cancer Epidemiol Biomarkers Prev 2016;25:1483–90.
45. Lozupone CA, Stombaugh JI, Gordon JI et al. Diversity, stability and resilience of the human gut microbiota. Nature 2012;489:220–30.
46. McKain N, Genc B, Snelling TJ et al. Differential recovery of bacterial and archaeal 16S rRNA genes from ruminal digesta in response to glycerol as cryoprotectant. J Microbiol Methods 2013;95:381–3.
47. Mas S, Crescenti A, Gassó P et al. DNA cards: Determinants of DNA yield and quality in collecting genetic samples for pharmacogenetic studies. Basic Clin Pharmacol 2007;101:132–7.
48. Mondot S, Kang S, Furet JP et al. Highlighting new phylogenetic specificities of Crohn’s disease microbiota. Inflamm Bowel Dis 2011;17:185–92.
49. Murphy M. Minimizing attrition in longitudinal studies: Means or end? In: Magnusson D, Bergman L (eds). Data Quality in Longitudinal Research. New York: Cambridge University Press, 1990, 148–56.
50. Nagy ZT. A hands-on overview of tissue preservation methods for molecular genetic analyses. Org Divers Evol 2010;10:91–105.
51. Nechvatal JM, Ram JL, Basson MD et al. Fecal collection, ambient preservation, and DNA extraction for PCR amplification of bacterial and human markers from human feces. J Microbiol Methods 2008;72:124–32.
52. Nsubuga AM, Robbins MM, Roeder AD et al. Factors affecting the amount of genomic DNA extracted from ape faeces and the identification of an improved sample storage method. Mol Ecol 2004;13:2089–94.
53. Prendini L, Hanner R, DeSalle R. Obtaining, storing and archiving specimens and tissue samples for use in molecular studies. In: DeSalle R, Giribet G, Wheeler W (eds). Techniques in Molecular Systematics and Evolution. Basle: Birkhäuser, 2002, 176–248.
54. Qin J, Li R, Raes J et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 2010;464:59–65.
55. Raes J, Foerstner KU, Bork P. Get the most out of your metagenome: computational analysis of environmental sequence data. Curr Opin Microbiol 2007;10:490–8.
56. Reck M, Tomasch J, Deng Z et al. Stool metatranscriptomics: A technical guideline for mRNA stabilisation and isolation. BMC Genomics 2015;16:494.
57. Sackett DL. Bias in analytic research. J Chronic Dis 1979;32:51–63.
58. Santiago A, Panda S, Mengels G et al. Processing faecal samples: a step forward for standards in microbial community analysis. BMC Microbiol 2014;14:112.
59. Shaw AG, Sim K, Powell E et al. Latitude in sample handling and storage for infant faecal microbiota studies: the elephant in the room? Microbiome 2016;4:40.
60. Sinha R, Chen J, Amir A et al. Collecting fecal samples for microbiome analyses in epidemiology studies. Cancer Epidemiol Biomarkers Prev 2015;33:395–401.
61. Smith LM, Burgoyne LA. Collecting, archiving and processing DNA from wildlife samples using FTA databasing paper. BMC Ecol 2004;4:4.
62. Song SJ, Amir A, Metcalf JL et al. Preservation methods differ in fecal microbiome stability, affecting suitability for field studies. mSystems 2016;1:1–12.
63. Tapani E, Taavitsainen M, Lindros K et al. Toxicity of ethanol in low concentrations. Acta Radiol 1996;37:923–6.
64. Tedjo DI, Jonkers DM, Savelkoul PH et al. The effect of sampling and storage on the fecal microbiota composition in healthy and diseased subjects. PLoS One 2015;10:e0126685.
65. The International Human Microbiome Consortium. Final Report Summary – IHMS (International Human Microbiome Standards, Project ID: 261376 Funded under: FP7-HEALTH, France), 2015.
66. Tigchelaar EF, Zhernakova A, Dekens JAM et al. Cohort profile: LifeLines DEEP, a prospective, general population cohort study in the northern Netherlands: study design and baseline characteristics. BMJ Open 2015;5:e006772.
67. Vandeputte D, Falony G, Vieira-Silva S et al. Stool consistency is strongly associated with gut microbiota richness and composition, enterotypes and bacterial growth rates. Gut 2016;65: 57–62.
68. Vlaeminck SE, Terada A, Smets BF et al. Aggregate size and architecture determine microbial activity balance for one-stage partial nitritation and anammox. Appl Environ Microb 2010;76:900–9.
69. Vogtmann E, Chen J, Amir A et al. Comparison of collection methods for fecal samples in microbiome studies. Am J Epidemiol 2016, DOI: 10.1093/aje/kww177.
70. Vuckovic D. Current trends and challenges in sample preparation for global metabolomics using liquid chromatography-mass spectrometry. Anal Bioanal Chem 2012; 403:1523–48.
71. Wada A, Kono M, Kawauchi S et al. Rapid discrimination of Gram-Positive and Gram-Negative bacteria in liquid samples by using naoh-sodium dodecyl sulfate solution and flow cytometry. PLoS One 2012;7:e47093.
72. Waite DW, Deines P, Taylor MW. Quantifying the impact of storage procedures for faecal bacteriotherapy in the critically endangered New Zealand Parrot, the Kakapo (Strigops habroptilus). Zoo Biol 2013;32:620–5.
73. Wehrspann P. Comparison of diverse methods for the cultivation of anaerobians, with special reference to the GASPAK system. Zentralbl Bakteriol Orig A 1976;234:121–8.
74. Wu GD, Chen J, Hoffmann C et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 2011;334: 105–8.
75. Yatsunenko T, Rey FE, Manary MJ et al. Human gut microbiome viewed across age and geography. Nature 2012;486:222–7.