Skip to main content
SpringerLink
Log in

Study of the diversity and short-chain fatty acids production by the bacterial community in overweight and obese Mexican children

  • Article
  • Published:
European Journal of Clinical Microbiology & Infectious Diseases Aims and scope Submit manuscript

Abstract

Obesity and overweight are health problems of multifactorial etiology, which may include changes in the microbiome. In Mexico, more than 30 % of the child population between 5 and 11 years of age suffer from being overweight or are obese, which makes it a public health issue in progress. The purpose of this work was to measure the short-chain fatty acid concentration by high-performance liquid chromatography (HPLC), and to characterize the bacterial diversity by ion torrent semiconductor sequencing, of 16S rDNA libraries prepared from stools collected from a sample of well-characterized Mexican children for normal weight, overweight, and obese conditions by anthropometric and biochemical criteria. We found that triglyceride levels are increased in overweight and obese children, who presented altered propionic and butyric acid concentrations in feces. In addition, although the colon microbiota did not show a clear bacterial dysbiosis among the three conditions, the abundance of some particular bacteria was changed with respect to normal controls. We conclude from our results that the imbalance in the abundance of at least nine different bacteria as well as altered short-chain fatty acid concentration in feces is associated to the overweight and obese conditions of Mexican children.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

SCFAs:

Short-chain fatty acids

NGS:

Next-generation sequencing

nt:

Nucleotides

References

  1. Waalen J (2014) The genetics of human obesity. Transl Res 164(4):293–301

    Article  CAS  PubMed  Google Scholar 

  2. James WPT (2008) The epidemiology of obesity: the size of the problem. J Intern Med 263(4):336–352

    Article  CAS  PubMed  Google Scholar 

  3. Ng M, Fleming T, Robinson M, Thomson B, Graetz N, Margono C et al (2014) 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 384(9945):766–781

    Article  PubMed  Google Scholar 

  4. Holub CK, Elder JP, Arredondo EM, Barquera S, Eisenberg CM, Sánchez Romero LM et al (2013) Obesity control in Latin American and U.S. Latinos: a systematic review. Am J Prev Med 44(5):529–537

    Article  PubMed  Google Scholar 

  5. World Health Organization (WHO) (2008) The global burden of disease: 2004 update. WHO, Geneva, Switzerland

  6. Latnovic L, Rodriguez Cabrera L (2013) Public health strategy against overweight and obesity in Mexico’s national agreement for nutritional health. Int J Obes Supp 3:S12–S14

    Article  Google Scholar 

  7. Encuesta Nacional de Salud y Nutrición. Resultados Nacionales 2012. Instituto Nacional de Salud Pública. Available online at: http://ensanut.insp.mx/informes/ENSANUT2012ResultadosNacionales.pdf

  8. Kannel WB, D’Agostino RB, Cobb JL (1996) Effect of weight on cardiovascular disease. Am J Clin Nutr 63(3 Suppl):419S–422S

    CAS  PubMed  Google Scholar 

  9. Carey VJ, Walters EE, Colditz GA, Solomon CG, Willett WC, Rosner BA et al (1997) Body fat distribution and risk of non-insulin-dependent diabetes mellitus in women. The Nurses’ Health Study. Am J Epidemiol 145(7):614–619

    Article  CAS  PubMed  Google Scholar 

  10. Wild SH, Byrne CD (2006) ABC of obesity. Risk factors for diabetes and coronary heart disease. BMJ 333:1009–1011

    Article  PubMed Central  PubMed  Google Scholar 

  11. Devaraj S, Hemarajata P, Versalovic J (2013) The human gut microbiome and body metabolism: implications for obesity and diabetes. Clin Chem 59(4):617–628

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  12. Ursell LK, Metcalf JL, Parfrey LW, Knight R (2012) Defining the human microbiome. Nutr Rev 70(Suppl 1):S38–S44

    Article  PubMed Central  PubMed  Google Scholar 

  13. Ley RE (2010) Obesity and the human microbiome. Curr Opin Gastroenterol 26(1):5–11

    Article  PubMed  Google Scholar 

  14. Caricilli AM, Castoldi A, Câmara NOS (2014) Intestinal barrier: a gentlemen’s agreement between microbiota and immunity. World J Gastrointest Pathophysiol 5(1):18–32

    Article  PubMed Central  PubMed  Google Scholar 

  15. Michelsen KS, Arditi M (2007) Toll-like receptors and innate immunity in gut homeostasis and pathology. Curr Opin Hematol 14(1):48–54

    Article  CAS  PubMed  Google Scholar 

  16. Rooks MG, Garrett WS (2011) Bacteria, food, and cancer. F1000 Biol Rep 3:12

    Article  PubMed Central  PubMed  Google Scholar 

  17. Whelan K, Judd PA, Preedy VR, Taylor MA (2004) Enteral feeding: the effect on faecal output, the faecal microflora and SCFA concentrations. Proc Nutr Soc 63(1):105–113

    Article  CAS  PubMed  Google Scholar 

  18. Segain J-P, Raingeard de la Blétière D, Bourreille A, Leray V, Gervois N, Rosales C et al (2000) Butyrate inhibits inflammatory responses through NFκB inhibition: implications for Crohn’s disease. Gut 47:397–403

  19. Dengler F, Rackwitz R, Benesch F, Pfannkuche H, Gäbel G (2014) Both butyrate incubation and hypoxia upregulate genes involved in the ruminal transport of SCFA and their metabolites. J Anim Physiol Anim Nutr (Berl). doi:10.1111/jpn.12201

    Google Scholar 

  20. Clemente JC, Ursell LK, Parfrey LW, Knight R (2012) The impact of the gut microbiota on human health: an integrative view. Cell 148(6):1258–1270

    Article  CAS  PubMed  Google Scholar 

  21. Bäckhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A et al (2004) The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci U S A 101(44):15718–15723

    Article  PubMed Central  PubMed  Google Scholar 

  22. DiBaise JK, Zhang H, Crowell MD, Krajmalnik-Brown R, Decker GA, Rittmann BE (2008) Gut microbiota and its possible relationship with obesity. Mayo Clin Proc 83(4):460–469

    Article  PubMed  Google Scholar 

  23. Flint HJ (2011) Obesity and the gut microbiota. J Clin Gastroenterol 45(Suppl):S128–S132

    Article  CAS  PubMed  Google Scholar 

  24. Gill SR, Pop M, DeBoy RT, Eckburg PB, Turnbaugh PJ, Samuel BS et al (2006) Metagenomic analysis of the human distal gut microbiome. Science 312(5778):1355–1359

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  25. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M et al (2005) Diversity of the human intestinal microbial flora. Science 308(5728):1635–1638

    Article  PubMed Central  PubMed  Google Scholar 

  26. Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO (2007) Development of the human infant intestinal microbiota. PLoS Biol 5(7):e177

    Article  PubMed Central  PubMed  Google Scholar 

  27. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C et al (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464(7285):59–65

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  28. Tremaroli V, Bäckhed F (2012) Functional interactions between the gut microbiota and host metabolism. Nature 489(7415):242–249

    Article  CAS  PubMed  Google Scholar 

  29. de Onis M, Onyango AW, Borghi E, Siyam A, Nishida C, Siekmann J (2007) Development of a WHO growth reference for school-aged children and adolescents. Bull World Health Organ 85(9):660–667

    Article  PubMed Central  PubMed  Google Scholar 

  30. Arimond M, Ruel MT (2004) Dietary diversity is associated with child nutritional status: evidence from 11 demographic and health surveys. J Nutr 134(10):2579–2585

    CAS  PubMed  Google Scholar 

  31. García Cuartero B, García Lacalle C, Jiménez Lobo C, González Vergaz A, Calvo Rey C, Alcázar Villar MJ et al (2007) Índice HOMA y QUICKI, insulina y péptido C en niños sanos. Puntos de corte de riesgo cardiovascular. An Pediatr (Barc) 66(5):481–490

    Article  Google Scholar 

  32. Fierer N, Hamady M, Lauber CL, Knight R (2008) The influence of sex, handedness, and washing on the diversity of hand surface bacteria. Proc Natl Acad Sci U S A 105(46):17994–17999

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  33. Whiteley AS, Jenkins S, Waite I, Kresoje N, Payne H, Mullan B et al (2012) Microbial 16S rRNA Ion Tag and community metagenome sequencing using the Ion Torrent (PGM) Platform. J Microbiol Methods 91(1):80–88

    Article  CAS  PubMed  Google Scholar 

  34. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  35. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460–2461

    Article  CAS  PubMed  Google Scholar 

  36. Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos G et al (2011) Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res 21:494–504

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  37. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K et al (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72(7):5069–5072

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  38. Vázquez-Baeza Y, Pirrung M, Gonzalez A, Knight R (2013) EMPeror: a tool for visualizing high-throughput microbial community data. Gigascience 2:16

    Article  PubMed Central  PubMed  Google Scholar 

  39. De Baere S, Eeckhaut V, Steppe M, De Maesschalck C, De Backer P, Van Immerseel F et al (2013) Development of a HPLC-UV method for the quantitative determination of four short-chain fatty acids and lactic acid produced by intestinal bacteria during in vitro fermentation. J Pharm Biomed Anal 80:107–115

    Article  PubMed  Google Scholar 

  40. Samuel BS, Gordon JI (2006) A humanized gnotobiotic mouse model of host–archaeal–bacterial mutualism. Proc Natl Acad Sci U S A 103(26):10011–10016

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  41. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444(7122):1027–1031

    Article  PubMed  Google Scholar 

  42. Larsen N, Vogensen FK, van den Berg FW, Nielsen DS, Andreasen AS, Pedersen BK et al (2010) Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS One 5(2):e9085

    Article  PubMed Central  PubMed  Google Scholar 

  43. Turnbaugh PJ, Gordon JI (2009) The core gut microbiome, energy balance and obesity. J Physiol 587(Pt 17):4153–4158

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  44. Turnbaugh PJ, Ridaura VK, Faith JJ, Rey FE, Knight R, Gordon JI (2009) The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med 1(6):6ra14

    Article  PubMed Central  PubMed  Google Scholar 

  45. Scheppach W (1994) Effects of short chain fatty acids on gut morphology and function. Gut 35(1 Suppl):S35–S38

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  46. Kotzampassi K, Giamarellos-Bourboulis EJ, Stavrou G (2014) Obesity as a consequence of gut bacteria and diet interactions. ISRN Obes 2014:651895. doi:10.1155/2014/651895

    PubMed Central  PubMed  Google Scholar 

  47. Wolever TMS, Spadafora P, Eshuis H (1991) Interaction between colonic acetate and propionate in humans. Am J Clin Nutr 53(3):681–687

    CAS  PubMed  Google Scholar 

  48. Vogt JA, Wolever TMS (2003) Fecal acetate is inversely related to acetate absorption from the human rectum and distal colon. J Nutr 133:3145–3148

    CAS  PubMed  Google Scholar 

  49. Frost G, Sleeth ML, Sahuri-Arisoylu M, Lizarbe B, Cerdan S, Brody L et al (2014) The short-chain fatty acid acetate reduces appetite via a central homeostatic mechanism. Nat Commun 5:3611. doi:10.1038/ncomms4611

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  50. Duncan SH, Belenguer A, Holtrop G, Johnstone AM, Flint HJ, Lobley GE (2007) Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces. Appl Environ Microbiol 73(4):1073–1078

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  51. Gostner A, Blaut M, Schäffer V, Kozianowski G, Theis S, Klingeberg M et al (2006) Effect of isomalt consumption on faecal microflora and colonic metabolism in healthy volunteers. Br J Nutr 95(1):40–50

    Article  CAS  PubMed  Google Scholar 

  52. Goodrich JK, Waters JL, Poole AC, Sutter JL, Koren O, Blekhman R et al (2014) Human genetics shape the gut microbiome. Cell 159:789–799

    Article  CAS  PubMed  Google Scholar 

  53. David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE et al (2014) Diet rapidly and reproducibly alters the human gut microbiome. Nature 505(7484):559–563

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  54. Looft T, Johnson TA, Allen HK, Bayles DO, Alt DP, Stedtfeld RD et al (2012) In-feed antibiotic effects on the swine intestinal microbiome. Proc Natl Acad Sci U S A 109(5):1691–1696

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  55. Truesdell SJ, Sims JC, Boerman PA, Seymour JL, Lazarus RA (1991) Pathways for metabolism of ketoaldonic acids in an Erwinia sp. J Bacteriol 173(21):6651–6656

    CAS  PubMed Central  PubMed  Google Scholar 

  56. Tims S, Derom C, Jonkers DM, Vlietinck R, Saris WH, Kleerebezem M et al (2013) Microbiota conservation and BMI signatures in adult monozygotic twins. ISME J 7(4):707–717

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  57. Balamurugan R, George G, Kabeerdoss J, Hepsiba J, Chandragunasekaran AMS, Ramakrishna BS (2010) Quantitative differences in intestinal Faecalibacterium prausnitzii in obese Indian children. Br J Nutr 103(3):335–338

    Article  CAS  PubMed  Google Scholar 

  58. Sotos M, Nadal I, Marti A, Martínez A, Martin-Matillas M, Campoy C et al (2008) Gut microbes and obesity in adolescents. Proc Nutr Soc 67(OCE):E20. doi:10.1017/S0029665108006290

    Article  Google Scholar 

  59. Ravussin Y, Koren O, Spor A, LeDuc C, Gutman R, Stombaugh J et al (2012) Responses of gut microbiota to diet composition and weight loss in lean and obese mice. Obesity (Silver Spring) 20(4):738–747

    Article  CAS  Google Scholar 

  60. Kameyama K, Itoh K (2014) Intestinal colonization by a lachnospiraceae bacterium contributes to the development of diabetes in obese mice. Microbes Environ. 2014 Oct 4. [Epub ahead of print]

  61. Zhao L (2013) The gut microbiota and obesity: from correlation to causality. Nat Rev Microbiol 11(9):639–647

    Article  CAS  PubMed  Google Scholar 

  62. Becker N, Kunath J, Loh G, Blaut M (2011) Human intestinal microbiota: characterization of a simplified and stable gnotobiotic rat model. Gut Microbes 2(1):25–33

    Article  PubMed  Google Scholar 

  63. Lee SM, Han HW, Yim SY (2015) Beneficial effects of soy milk and fiber on high cholesterol diet-induced alteration of gut microbiota and inflammatory gene expression in rats. Food Funct 6(2):492–500

    Article  CAS  PubMed  Google Scholar 

  64. Reichardt N, Duncan SH, Young P, Belenguer A, McWilliam Leitch C, Scott KP et al (2014) Phylogenetic distribution of three pathways for propionate production within the human gut microbiota. ISME J 8(6):1323–1335

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  65. Karlsson CLJ, Önnerfält J, Xu J, Molin G, Ahrné S, Thorngren-Jerneck K (2012) The microbiota of the gut in preschool children with normal and excessive body weight. Obesity 20:2257–2261

    Article  PubMed  Google Scholar 

  66. Xu P, Li M, Zhang J, Zhang T (2012) Correlation of intestinal microbiota with overweight and obesity in Kazakh school children. BMC Microbiol 12:283

    Article  PubMed Central  PubMed  Google Scholar 

  67. Abdallah Ismail N, Ragab SH, Abd Elbaky A, Shoeib AR, Alhosary Y, Fekry D (2011) Frequency of Firmicutes and Bacteroidetes in gut microbiota in obese and normal weight Egyptian children and adults. Arch Med Sci 7(3):501–507

    Article  PubMed Central  PubMed  Google Scholar 

  68. Martinez-Marignac VL, Valladares A, Cameron E, Chan A, Perera A, Globus-Goldberg R et al (2007) Admixture in Mexico City: implications for admixture mapping of type 2 diabetes genetic risk factors. Hum Genet 120:807–819

    Article  PubMed  Google Scholar 

  69. Silva-Zolezzi I, Hidalgo-Miranda A, Estrada-Gil J, Fernandez-Lopez JC, Uribe-Figueroa L, Contreras A et al (2009) Analysis of genomic diversity in Mexican Mestizo populations to develop genomic medicine in Mexico. Proc Natl Acad Sci U S A 106:8611–8616

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by Cinvestav-IPN, Estimulos a Investigaciones Médicas, Fundación Miguel Alemán A. C., and FONSEC SS/IMSS/ISSSTE-CONACYT-233361 granted to JGM. We thank Mario Arturo Cruz Montiel, Angel Antonio Martínez Gomez, Jakeline Leon Bernal, Jessica Jazmín Bárcenas García, and Rodrigo García Gutiérrez for technical assistance in the laboratory; Antonia López Salazar for administrative assistance; Suresh Thenozhi for technical assistance in bioinformatics analysis; and Caterina R. Venturelli as well as Sathish Kumar Kamaraj for the careful reading and correction of this text. The authors are deeply indebted to all parents and children who participated in this study.

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

The authors declare that all procedures were performed in accordance with the ethical standards approved by the Local Ethical Committee Board of Health from the Instituto Mexicano del Seguro Social R-2011–1402 1402–10, Mexico City, and with the Helsinki Declaration revised in 2000.

Informed consent

The authors declare that informed consent was signed by all parents and children in accordance with the Helsinki Declaration revised in 2000.

Author information

Authors and Affiliations

  1. Departamento de Genética y Biología Molecular, Cinvestav-IPN Unidad Zacatenco, México, DF, 07360, Mexico

    S. Murugesan, M. Ulloa-Martínez, A. Piña-Escobedo & J. García-Mena

  2. Departamento de Farmacología, Cinvestav-IPN, México, DF, Mexico

    S. Murugesan, F. M. Galván-Rodríguez & C. Hoyo-Vadillo

  3. Departamento de Nutrición, Instituto Nacional de Perinatología, México, DF, Mexico

    M. L. Pizano-Zárate

  4. Escuela Superior de Medicina del Instituto Politécnico Nacional, México, DF, Mexico

    H. Martínez-Rojano

  5. Departamento de Fisiología Biofísica y Neurociencias, Cinvestav-IPN, México, DF, Mexico

    C. Miranda-Brito & M. C. Romano

Authors
  1. S. Murugesan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Ulloa-Martínez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. H. Martínez-Rojano
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. F. M. Galván-Rodríguez
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. C. Miranda-Brito
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. M. C. Romano
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. A. Piña-Escobedo
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. M. L. Pizano-Zárate
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. C. Hoyo-Vadillo
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. J. García-Mena
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. García-Mena.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Table S1

(DOCX 38 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Murugesan, S., Ulloa-Martínez, M., Martínez-Rojano, H. et al. Study of the diversity and short-chain fatty acids production by the bacterial community in overweight and obese Mexican children. Eur J Clin Microbiol Infect Dis 34, 1337–1346 (2015). https://doi.org/10.1007/s10096-015-2355-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-015-2355-4

Keywords

Search

Navigation