The obese gut microbiome across the epidemiologic transition

Emerging Themes in Epidemiology

Volumn 13, Issue 1, 2016, Pages

  Dugas, Lara R ^a   Fuller, Miles ^b   Gilbert, Jack ^c,d,e,f   Layden, Brian T ^b,g  

^a LOYOLA UNIVERSITY CHICAGO   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c ARGONNE NATIONAL LABORATORY   (United States)

^d UNIVERSITY OF CHICAGO   (United States)

^e MARINE BIOLOGICAL LABORATORY   (United States)

^f ZHEJIANG UNIVERSITY   (China)

^g JESSE BROWN VA MEDICAL CENTER   (United States)

Author keywords

Geographical differences; Gut microbiome; Obesity

Indexed keywords

DIETARY INTAKE; DISEASE ASSOCIATION; ENVIRONMENTAL FACTOR; GEOGRAPHIC DISTRIBUTION; HUMAN; INTESTINE FLORA; NONHUMAN; OBESITY; OUTCOME ASSESSMENT; PHENOTYPE; PHYSICAL ACTIVITY; PREVALENCE; REVIEW;

EID: 84954108649     PISSN: None     EISSN: 17427622     Source Type: Journal    
DOI: 10.1186/s12982-015-0044-5     Document Type: Review

References (95)

1. Global Status Report on noncommunicable diseases 2014. World Health Organization. http://apps.who.int/iris/bitstream/10665/148114/1/9789241564854-eng.pdf.
2. Luke A, Bovet P, Plange-Rhule J, Forrester TE, Lambert EV, Schoeller DA, Dugas LR, Durazo-Arvizu RA, Shoham DA, Cao G, et al. A mixed ecologic-cohort comparison of physical activity and weight among young adults from five populations of African origin. BMC Public Health. 2014;14:397.
3. Popkin BM, Adair LS, Ng SW. Global nutrition transition and the pandemic of obesity in developing countries. Nutr Rev. 2012;70(1):3-21.
4. Farni K, Shoham DA, Cao G, Luke AH, Layden J, Cooper RS, Dugas LR. Physical activity and pre-diabetes - an unacknowledged mid-life crisis: findings from NHANES 2003-2006. PeerJ. 2014;2:e499.
5. Peer N, Steyn K, Lombard C, Lambert EV, Vythilingum B, Levitt NS. Rising diabetes prevalence among urban-dwelling black South Africans. PLoS One. 2012;7(9):e43336.
6. Dietrich P, Hellerbrand C. Non-alcoholic fatty liver disease, obesity and the metabolic syndrome. Best Pract Res Clin Gastroenterol. 2014;28(4):637-53.
7. Pettitt DJ, Talton J, Dabelea D, Divers J, Imperatore G, Lawrence JM, Liese AD, Linder B, Mayer-Davis EJ, Pihoker C, et al. Prevalence of diabetes in U.S. youth in 2009: the SEARCH for diabetes in youth study. Diabetes Care. 2014;37(2):402-8.
8. Saydah S, Bullard KM, Cheng Y, Ali MK, Gregg EW, Geiss L, Imperatore G. Trends in cardiovascular disease risk factors by obesity level in adults in the United States, NHANES 1999-2010. Obesity. 2014;22(8):1888-95.
9. Swinburn B, Sacks G, Ravussin E. Increased food energy supply is more than sufficient to explain the US epidemic of obesity. Am J Clin Nutr. 2009;90(6):1453-6.
10. Hall KD, Sacks G, Chandramohan D, Chow CC, Wang YC, Gortmaker SL, Swinburn BA. Quantification of the effect of energy imbalance on bodyweight. Lancet. 2011;378(9793):826-37.
11. Chaput JP, Perusse L, Despres JP, Tremblay A, Bouchard C. Findings from the Quebec Family Study on the etiology of obesity: genetics and environmental highlights. Curr Obes Rep. 2014;3:54-66.
12. Locke AE, Kahali B, Berndt SI, Justice AE, Pers TH, Day FR, Powell C, Vedantam S, Buchkovich ML, Yang J, et al. Genetic studies of body mass index yield new insights for obesity biology. Nature. 2015;518(7538):197-206.
13. Luke A, Cooper RS, Prewitt TE, Adeyemo AA, Forrester TE. Nutritional consequences of the African diaspora. Annu Rev Nutr. 2001;21:47-71.
14. De Bourdeaudhuij I, Van Dyck D, Salvo D, Davey R, Reis RS, Schofield G, Sarmiento OL, Mitas J, Christiansen LB, MacFarlane D, et al. International study of perceived neighbourhood environmental attributes and body mass index: IPEN adult study in 12 countries. Int J Behav Nutr Phys Act. 2015;12:62.
15. Raymond SU, Leeder S, Greenberg HM. Obesity and cardiovascular disease in developing countries: a growing problem and an economic threat. Curr Opinion Clin Nutr Metab Care. 2006;9(2):111-6.
16. Karalius VP, Harbison JE, Plange-Rhule J, van Breemen RB, Li G, Huang K, Durazo-Arvizu RA, Mora N, Dugas LR, Vail L, et al. Bisphenol A (BPA) found in humans and water in three geographic regions with distinctly different levels of economic development. Environ Health Insights. 2014;8:1-3.
17. Kramer H, Dugas L, Shoham D. Obesity as an effect modifier of the risk of death in chronic kidney disease. Nephrol Dial Transpl. 2013;28(Suppl 4):iv65-72.
18. Desai M, Jellyman JK, Ross MG. Epigenomics, gestational programming and risk of metabolic syndrome. Int J Obes. 2015;39(4):633-41.
19. Rosenquist JN, Lehrer SF, O'Malley AJ, Zaslavsky AM, Smoller JW, Christakis NA. Cohort of birth modifies the association between FTO genotype and BMI. Proc Natl Acad Sci USA. 2015;112(2):354-9.
20. Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature. 2006;444(7122):1022-3.
21. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444(7122):1027-31.
22. Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE, Kau AL, Griffin NW, Lombard V, Henrissat B, Bain JR, et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science. 2013;341(6150):1241214.
23. Turnbaugh PJ, Backhed F, Fulton L, Gordon JI. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe. 2008;3(4):213-23.
24. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, Sogin ML, Jones WJ, Roe BA, Affourtit JP, et al. A core gut microbiome in obese and lean twins. Nature. 2009;457(7228):480-4.
25. Turnbaugh PJ, Gordon JI. The core gut microbiome, energy balance and obesity. J Physiol. 2009;587(Pt 17):4153-8.
26. Ley RE. Obesity and the human microbiome. Curr Opin Gastroenterol. 2010;26(1):5-11.
27. Sonnenburg ED, Sonnenburg JL. Starving our microbial self: the deleterious consequences of a diet deficient in microbiota-accessible carbohydrates. Cell Metab. 2014;20(5):779-86.
28. Karlsson F, Tremaroli V, Nielsen J, Backhed F. Assessing the human gut microbiota in metabolic diseases. Diabetes. 2013;62(10):3341-9.
29. Karlsson FH, Nookaew I, Nielsen J. Metagenomic data utilization and analysis (MEDUSA) and construction of a global gut microbial gene catalogue. PLoS Comput Biol. 2014;10(7):e1003706.
30. Ley RE, Peterson DA, Gordon JI. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell. 2006;124(4):837-48.
31. Tyler AD, Smith MI, Silverberg MS. Analyzing the human microbiome: a "how to" guide for physicians. Am J Gastroenterol. 2014;109(7):983-93.
32. Smith M.I., Turpin W., Tyler A.D., Silverberg M.S., Croitoru K. Microbiome analysis - From technical advances to biological relevance 2014 F1000 Prime Rep 6, 51.
33. Lax S, Smith DP, Hampton-Marcell J, Owens SM, Handley KM, Scott NM, Gibbons SM, Larsen P, Shogan BD, Weiss S, et al. Longitudinal analysis of microbial interaction between humans and the indoor environment. Science. 2014;345(6200):1048-52.
34. Kelley ST, Gilbert JA. Studying the microbiology of the indoor environment. Genome Biol. 2013;14(2):202.
35. Cox LM, Yamanishi S, Sohn J, Alekseyenko AV, Leung JM, Cho I, Kim SG, Li H, Gao Z, Mahana D, et al. Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences. Cell. 2014;158(4):705-21.
36. Ng M, Fleming T, Robinson M, Thomson B, Graetz N, Margono C, Mullany EC, Biryukov S, Abbafati C, Abera SF, et al. Global, regional, and national prevalence of overweight and obesity in children and adults during 1980-2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet. 2014;384(9945):766-81.
37. Stevens GA, Singh GM, Lu Y, Danaei G, Lin JK, Finucane MM, Bahalim AN, McIntire RK, Gutierrez HR, Cowan M, et al. National, regional, and global trends in adult overweight and obesity prevalences. Popul Health Metr. 2012;10(1):22.
38. United Nations Development Programme. Human Development Index (HDI). http://hdr.undp.org/en/content/human-development-index-hdi.
39. Kaufman JS, Tracy JA, Durazo-Arvizu RA, Cooper RS. Lifestyle, education, and prevalence of hypertension in populations of African origin. Results from the International Collaborative Study on Hypertension in Blacks. Ann Epidemiol. 1997;7(1):22-7.
40. Kaufman JS, Durazo-Arvizu RA, Rotimi CN, McGee DL, Cooper RS. Obesity and hypertension prevalence in populations of African origin. The Investigators of the International Collaborative Study on Hypertension in Blacks. Epidemiology. 1996;7(4):398-405.
41. Cooper R, Forrester T, Ogunbiyi O, Muffinda J. Angiotensinogen levels and obesity in four black populations. ICSHIB Investigators. J Hypertens. 1998;16(5):571-5.
42. Cooper R, Rotimi C, Ataman S, McGee D, Osotimehin B, Kadiri S, Muna W, Kingue S, Fraser H, Forrester T, et al. The prevalence of hypertension in seven populations of west African origin. Am J Public Health. 1997;87(2):160-8.
43. Ezzati M, Vander Hoorn S, Lawes CM, Leach R, James WP, Lopez AD, Rodgers A, Murray CJ. Rethinking the "diseases of affluence" paradigm: global patterns of nutritional risks in relation to economic development. PLoS Med. 2005;2(5):e133.
44. Durazo-Arvizu RA, Luke A, Cooper RS, Cao G, Dugas L, Adeyemo A, Boyne M, Forrester T. Rapid increases in obesity in Jamaica, compared to Nigeria and the United States. BMC Public Health. 2008;8:133.
45. Cooper R, Rotimi C. Hypertension in blacks. Am J Hypertens. 1997;10(7 Pt 1):804-12.
46. Rotimi CN, Cooper RS, Marcovina SM, McGee D, Owoaje E, Ladipo M. Serum distribution of lipoprotein(a) in African Americans and Nigerians: potential evidence for a genotype-environmental effect. Genet Epidemiol. 1997;14(2):157-68.
47. Okosun IS, Liao Y, Rotimi CN, Choi S, Cooper RS. Predictive values of waist circumference for dyslipidemia, type 2 diabetes and hypertension in overweight White, Black, and Hispanic American adults. J Clin Epidemiol. 2000;53(4):401-8.
48. Okosun IS, Liao Y, Rotimi CN, Prewitt TE, Cooper RS. Abdominal adiposity and clustering of multiple metabolic syndrome in White, Black and Hispanic americans. Ann Epidemiol. 2000;10(5):263-70.
49. Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, Magris M, Hidalgo G, Baldassano RN, Anokhin AP, et al. Human gut microbiome viewed across age and geography. Nature. 2012;486(7402):222-7.
50. Lee S, Sung J, Lee J, Ko G. Comparison of the gut microbiotas of healthy adult twins living in South Korea and the United States. Appl Environ Microbiol. 2011;77(20):7433-7.
51. David LA, Materna AC, Friedman J, Campos-Baptista MI, Blackburn MC, Perrotta A, Erdman SE, Alm EJ. Host lifestyle affects human microbiota on daily timescales. Genome Biol. 2014;15(7):R89.
52. Backhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, Semenkovich CF, Gordon JI. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci USA. 2004;101(44):15718-23.
53. Le Chatelier E, Nielsen T, Qin J, Prifti E, Hildebrand F, Falony G, Almeida M, Arumugam M, Batto JM, Kennedy S, et al. Richness of human gut microbiome correlates with metabolic markers. Nature. 2013;500(7464):541-6.
54. Ferrer M, Ruiz A, Lanza F, Haange SB, Oberbach A, Till H, Bargiela R, Campoy C, Segura MT, Richter M, et al. Microbiota from the distal guts of lean and obese adolescents exhibit partial functional redundancy besides clear differences in community structure. Environ Microbiol. 2013;15(1):211-26.
55. Patil DP, Dhotre DP, Chavan SG, Sultan A, Jain DS, Lanjekar VB, Gangawani J, Shah PS, Todkar JS, Shah S, et al. Molecular analysis of gut microbiota in obesity among Indian individuals. J Biosci. 2012;37(4):647-57.
56. Murphy EF, Cotter PD, Healy S, Marques TM, O'Sullivan O, Fouhy F, Clarke SF, O'Toole PW, Quigley EM, Stanton C, et al. Composition and energy harvesting capacity of the gut microbiota: relationship to diet, obesity and time in mouse models. Gut. 2010;59(12):1635-42.
57. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, Fernandes GR, Tap J, Bruls T, Batto JM, et al. Enterotypes of the human gut microbiome. Nature. 2011;473(7346):174-80.
58. Bell DS. Changes seen in gut bacteria content and distribution with obesity: causation or association? Postgrad Med. 2015;127(8):863-8.
59. Vrieze A, Van Nood E, Holleman F, Salojarvi J, Kootte RS, Bartelsman JF, Dallinga-Thie GM, Ackermans MT, Serlie MJ, Oozeer R et al. Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology. 2012;143(4):913-16.e917.
60. Everard A, Lazarevic V, Gaia N, Johansson M, Stahlman M, Backhed F, Delzenne NM, Schrenzel J, Francois P, Cani PD. Microbiome of prebiotic-treated mice reveals novel targets involved in host response during obesity. ISME J. 2014;8(10):2116-30.
61. Cani PD, Possemiers S, Van de Wiele T, Guiot Y, Everard A, Rottier O, Geurts L, Naslain D, Neyrinck A, Lambert DM, et al. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut. 2009;58(8):1091-103.
62. Bleau C, Karelis AD, St-Pierre DH, Lamontagne L. Crosstalk between intestinal microbiota, adipose tissue and skeletal muscle as an early event in systemic low-grade inflammation and the development of obesity and diabetes. Diabetes Metab Res Rev. 2015;31(6):545-61.
63. Ding S, Chi MM, Scull BP, Rigby R, Schwerbrock NM, Magness S, Jobin C, Lund PK. High-fat diet: bacteria interactions promote intestinal inflammation which precedes and correlates with obesity and insulin resistance in mouse. PLoS One. 2010;5(8):e12191.
64. Backhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI. Host-bacterial mutualism in the human intestine. Science. 2005;307(5717):1915-20.
65. Bakker GJ, Zhao J, Herrema H, Nieuwdorp M. Gut microbiota and energy expenditure in health and obesity. J Clin Gastroenterol. 2015;49(Suppl 1):S13-9.
66. Lopez-Cepero AA, Palacios C. Association of the intestinal microbiota and obesity. P R Health Sci J. 2015;34(2):60-4.
67. Janssen AW, Kersten S. The role of the gut microbiota in metabolic health. Faseb J. 2015;29(8):3111-23.
68. Suzuki TA, Worobey M. Geographical variation of human gut microbial composition. Biol Lett. 2014;10(2):20131037.
69. Schnorr SL, Candela M, Rampelli S, Centanni M, Consolandi C, Basaglia G, Turroni S, Biagi E, Peano C, Severgnini M, et al. Gut microbiome of the Hadza hunter-gatherers. Nat Commun. 2014;5:3654.
70. Voreades N, Kozil A, Weir TL. Diet and the development of the human intestinal microbiome. Front Microbiol. 2014;5:494.
71. Petriz BA, Castro AP, Almeida JA, Gomes CP, Fernandes GR, Kruger RH, Pereira RW, Franco OL. Exercise induction of gut microbiota modifications in obese, non-obese and hypertensive rats. BMC Genom. 2014;15:511.
72. Clarke SF, Murphy EF, O'Sullivan O, Lucey AJ, Humphreys M, Hogan A, Hayes P, O'Reilly M, Jeffery IB, Wood-Martin R, et al. Exercise and associated dietary extremes impact on gut microbial diversity. Gut. 2014;63(12):1913-20.
73. Evans CC, LePard KJ, Kwak JW, Stancukas MC, Laskowski S, Dougherty J, Moulton L, Glawe A, Wang Y, Leone V, et al. Exercise prevents weight gain and alters the gut microbiota in a mouse model of high fat diet-induced obesity. PLoS One. 2014;9(3):e92193.
74. Matsumoto M, Inoue R, Tsukahara T, Ushida K, Chiji H, Matsubara N, Hara H. Voluntary running exercise alters microbiota composition and increases n-butyrate concentration in the rat cecum. Biosci Biotechnol Biochem. 2008;72(2):572-6.
75. Queipo-Ortuno MI, Seoane LM, Murri M, Pardo M, Gomez-Zumaquero JM, Cardona F, Casanueva F, Tinahones FJ. Gut microbiota composition in male rat models under different nutritional status and physical activity and its association with serum leptin and ghrelin levels. PLoS One. 2013;8(5):e65465.
76. Albenberg LG, Wu GD. Diet and the intestinal microbiome: associations, functions, and implications for health and disease. Gastroenterology. 2014;146(6):1564-72.
77. De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, Collini S, Pieraccini G, Lionetti P. 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):14691-6.
78. Walker AW, Ince J, Duncan SH, Webster LM, Holtrop G, Ze X, Brown D, Stares MD, Scott P, Bergerat A, et al. Dominant and diet-responsive groups of bacteria within the human colonic microbiota. ISME J. 2011;5(2):220-30.
79. Lin A, Bik EM, Costello EK, Dethlefsen L, Haque R, Relman DA, Singh U. Distinct distal gut microbiome diversity and composition in healthy children from Bangladesh and the United States. PLoS One. 2013;8(1):e53838.
80. Ou J, Carbonero F, Zoetendal EG, DeLany JP, Wang M, Newton K, Gaskins HR, O'Keefe SJ. Diet, microbiota, and microbial metabolites in colon cancer risk in rural Africans and African Americans. Am J Clin Nutr. 2013;98(1):111-20.
81. Tyakht AV, Kostryukova ES, Popenko AS, Belenikin MS, Pavlenko AV, Larin AK, Karpova IY, Selezneva OV, Semashko TA, Ospanova EA, et al. Human gut microbiota community structures in urban and rural populations in Russia. Nat Commun. 2013;4:2469.
82. Bermon S, Petriz B, Kajeniene A, Prestes J, Castell L, Franco OL. The microbiota: an exercise immunology perspective. Exerc Immunol Rev. 2015;21:70-9.
83. Cooper RS, Amoah AG, Mensah GA. High blood pressure: the foundation for epidemic cardiovascular disease in African populations. Ethn Dis. 2003;13(2 Suppl 2):S48-52.
84. Cooper RS, Rotimi CN, Kaufman JS, Owoaje EE, Fraser H, Forrester T, Wilks R, Riste LK, Cruickshank JK. Prevalence of NIDDM among populations of the African diaspora. Diabetes Care. 1997;20(3):343-8.
85. Cooper RS, Wolf-Maier K, Luke A, Adeyemo A, Banegas JR, Forrester T, Giampaoli S, Joffres M, Kastarinen M, Primatesta P, et al. An international comparative study of blood pressure in populations of European vs. African descent. BMC Med. 2005;3:2.
86. Kaufman JS, Owoaje EE, James SA, Rotimi CN, Cooper RS. Determinants of hypertension in West Africa: contribution of anthropometric and dietary factors to urban-rural and socioeconomic gradients. Am J Epidemiol. 1996;143(12):1203-18.
87. Dugas LR, Bovet P, Forrester TE, Lambert EV, Plange-Rhule J, Durazo-Arvizu RA, Shoham D, Kroff J, Cao G, Cooper RS, et al. Comparisons of intensity-duration patterns of physical activity in the US, Jamaica and 3 African countries. BMC Public Health. 2014;14(1):882.
88. Luke AH, Rotimi CN, Cooper RS, Long AE, Forrester TE, Wilks R, Bennett FI, Ogunbiyi O, Compton JA, Bowsher RR. Leptin and body composition of Nigerians, Jamaicans, and US blacks. Am J Clin Nutr. 1998;67(3):391-6.
89. Luke A, Rotimi CN, Adeyemo AA, Durazo-Arvizu RA, Prewitt TE, Moragne-Kayser L, Harders R, Cooper RS. Comparability of resting energy expenditure in Nigerians and U.S. blacks. Obes Res. 2000;8(5):351-9.
90. Luke A, Guo X, Adeyemo AA, Wilks R, Forrester T, Lowe W Jr, Comuzzie AG, Martin LJ, Zhu X, Rotimi CN, et al. Heritability of obesity-related traits among Nigerians, Jamaicans and US black people. Int J Obes Relat Metab Disord. 2001;25(7):1034-41.
91. Luke A, Durazo-Arvizu RA, Rotimi CN, Iams H, Schoeller DA, Adeyemo AA, Forrester TE, Wilks R, Cooper RS. Activity energy expenditure and adiposity among black adults in Nigeria and the United States. Am J Clin Nutr. 2002;75(6):1045-50.
92. Luke A, Durazo-Arvizu R, Rotimi C, Prewitt TE, Forrester T, Wilks R, Ogunbiyi OJ, Schoeller DA, McGee D, Cooper RS. Relation between body mass index and body fat in black population samples from Nigeria, Jamaica, and the United States. Am J Epidemiol. 1997;145(7):620-8.
93. Luke A, Dugas LR, Ebersole K, Durazo-Arvizu RA, Cao G, Schoeller DA, Adeyemo A, Brieger WR, Cooper RS. Energy expenditure does not predict weight change in either Nigerian or African American women. Am J Clin Nutr. 2009;89(1):169-76.
94. Luke A, Bovet P, Forrester TE, Lambert EV, Plange-Rhule J, Schoeller DA, Dugas LR, Durazo-Arvizu RA, Shoham D, Cooper RS, et al. Protocol for the modeling the epidemiologic transition study: a longitudinal observational study of energy balance and change in body weight, diabetes and cardiovascular disease risk. BMC Public Health. 2012;11:927.
95. Luke A, Adeyemo AA, Tayo B, Durazo-Arvizu RA, Schoeller DA, Leman C, Cooper RS. Energy expenditure, adiposity and weight gain in Yoruba and African-American women. Obes Rev. 2006;7(Supplement 2):AOP0183.