Skip to main content
×
Home
    • Aa
    • Aa

Diets rich in n-6 PUFA induce intestinal microbial dysbiosis in aged mice

  • Sanjoy Ghosh (a1), Erin Molcan (a1), Daniella DeCoffe (a1), Chaunbin Dai (a1) and Deanna L. Gibson (a1)...
Abstract

Controversies have emerged regarding the beneficial v. detrimental effects of dietary n-6 PUFA. The alteration of the intestinal microbiota, a phenomenon termed dysbiosis, occurs during several chronic inflammatory diseases, but has not been well studied in an aged population. With present ‘Western’ diets predominantly composed of n-6 PUFA, we hypothesised that PUFA-rich diets cause intestinal dysbiosis in an aged population. C57BL/6 mice (aged 2 years) were fed a high-fat (40 % energy), isoenergetic and isonitrogenous diet composed of rapeseed oil, maize oil or maize oil supplemented with fish oil. We examined ileal microbiota using fluorescence in situ hybridisation and stained tissues by immunofluorescence for the presence of immune cells and oxidative stress. We observed that feeding high-fat diets rich in n-6 PUFA promoted bacterial overgrowth but depleted microbes from the Bacteroidetes and Firmicutes phyla. This corresponded with increased body mass and infiltration of macrophages and neutrophils. Fish oil supplementation (rich in long-chain n-3 PUFA like DHA and EPA) restored the microbiota and inflammatory cell infiltration and promoted regulatory T-cell recruitment. However, fish oil supplementation was associated with increased oxidative stress, evident by the increased presence of 4-hydroxynonenal, a product of lipid peroxidation. These results suggest that an n-6 PUFA-rich diet can cause dysbiosis and intestinal inflammation in aged mice. However, while fish oil supplementation on an n-6 PUFA diet reverses dysbiosis, the combination of n-6 and n-3 PUFA, like DHA/EPA, leads to increased oxidative stress, which could exacerbate gastrointestinal disorders in the elderly.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Diets rich in n-6 PUFA induce intestinal microbial dysbiosis in aged mice
      Available formats
      ×
      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your Dropbox account. Find out more about sending content to Dropbox.

      Diets rich in n-6 PUFA induce intestinal microbial dysbiosis in aged mice
      Available formats
      ×
      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your Google Drive account. Find out more about sending content to Google Drive.

      Diets rich in n-6 PUFA induce intestinal microbial dysbiosis in aged mice
      Available formats
      ×
Copyright
Corresponding author
*Corresponding author: D. L. Gibson, fax +1 250 807 8000, email deanna.gibson@ubc.ca
Linked references
Hide All

This list contains references from the content that can be linked to their source. For a full set of references and notes please see the PDF or HTML where available.

1J Walter , RA Britton & S Roos (2011) Host–microbial symbiosis in the vertebrate gastrointestinal tract and the Lactobacillus reuteri paradigm. Proc Natl Acad Sci U S A 108, Suppl. 1, 46454652.

2M Arumugam , J Raes & E Pelletier (2011) Enterotypes of the human gut microbiome. Nature 473, 173180.

3A Korecka & V Arulampalam (2012) The gut microbiome: scourge, sentinel or spectator? J Oral Microbiol 4 (Epublication 21 February 2012).

4R Ley , M Hamady & C Lozupone (2008) Evolution of mammals and their gut microbes. Science 320, 16471651.

5R Ley , P Turnbaugh , S Klein , et al. (2006) Microbial ecology: human gut microbes assciated with obesity. Nature 444, 10221023.

6H Sokol , P Seksik , JP Furet , et al. (2009) Low counts of Faecalibacterium prausnitzii in colitis microbiota. Inflamm Bowel Dis 15, 11831189.

7D Mariat , O Firmesse , F Levenez , et al. (2009) The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age. BMC Microbiol 9, 123.

8L Wen , RE Ley , PY Volchkov , et al. (2008) Innate immunity and intestinal microbiota in the development of type 1 diabetes. Nature 455, 11091113.

9A Giongo , KA Gano , DB Crabb , et al. (2011) Toward defining the autoimmune microbiome for type 1 diabetes. ISME J 5, 8291.

11A Caricilli , P Picardi & L de Abreu (2011) Gut microbiota is a key modulatator of insulin resistance in TLR2 knockout mice. PLoS Biol 9, 121.

12TL Blasbalg , JR Hibbeln , CE Ramsden , et al. (2011) Changes in consumption of omega-3 and omega-6 fatty acids in the United States during the 20th century. Am J Clin Nutr 93, 950962.

14R Canete , M Gil-Campos , CM Aguilera , et al. (2007) Development of insulin resistance and its relation to diet in the obese child. Eur J Nutr 46, 181187.

15A Ramel , A Martinez , M Kiely , et al. (2008) Beneficial effects of long-chain n-3 fatty acids included in an energy-restricted diet on insulin resistance in overweight and obese European young adults. Diabetologia 51, 12611268.

18F Fernandez-Banares , M Esteve , E Navarro , et al. (1996) Changes of the mucosal n-3 and n-6 fatty acid status occur early in the colorectal adenoma–carcinoma sequence. Gut 38, 254259.

19A Nkondjock , B Shatenstein , P Maisonneuve , et al. (2003) Assessment of risk associated with specific fatty acids and colorectal cancer among French-Canadians in Montreal: a case–control study. Int J Epidemiol 32, 200209.

20A Nkondjock , D Krewski , KC Johnson , et al. (2005) Specific fatty acid intake and the risk of pancreatic cancer in Canada. Br J Cancer 92, 971977.

21A Belluzzi , C Brignola , M Campieri , et al. (1996) Effect of an enteric-coated fish-oil preparation on relapses in Crohn's disease. N Engl J Med 334, 15571560.

22SM Innis & K Jacobson (2007) Dietary lipids in early development and intestinal inflammatory disease. Nutr Rev 65, S188S193.

23MG Dominguez-Bello , MJ Blaser , RE Ley , et al. (2011) Development of the human gastrointestinal microbiota and insights from high-throughput sequencing. Gastroenterology 140, 17131719.

24E Biagi , L Hylund , M Candela , et al. (2010) Through ageing, and beyond gut microbiota and inflammatory status in seniors and centenarians. PLoS One 5, e10667.

27PM Kris-Etherton , WS Harris & LJ Appel (2002) Fish consumption, fish oil, omega-3 fatty acids, and cardiovascular disease. Circulation 106, 27472757.

29CT Hammer & ED Wills (1978) The role of lipid components of the diet in the regulation of the fatty acid composition of the rat liver endoplasmic reticulum and lipid peroxidation. Biochem J 174, 585593.

31S Ghosh , C Dai , K Brown , et al. (2011) Colonic microbiota alters host susceptibility to infectious colitis by modulating inflammation, redox status, and ion transporter gene expression. Am J Physiol Gastrointest Liver Physiol 301, G39G49.

33H Meier , R Amann , W Ludwig , et al. (1999) Specific oligonucleotide probes for in situ detection of a major group of gram-positive bacteria with low DNA G+C content. Syst Appl Microbiol 22, 186196.

34J Klaus , U Spaniol , G Adler , et al. (2009) Small intestinal bacterial overgrowth mimicking acute flare as a pitfall in patients with Crohn's disease. BMC Gastroenterol 9, 61.

35EF Murphy , PD Cotter , S Healy , et al. (2010) Composition and energy harvesting capacity of the gut microbiota: relationship to diet, obesity and time in mouse models. Gut 59, 16351642.

38PJ Turnbaugh , RE Ley , MA Mahowald , et al. (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444, 10271031.

39A Tursi , G Brandimarte , GM Giorgetti , et al. (2005) Assessment of small intestinal bacterial overgrowth in uncomplicated acute diverticulitis of the colon. World J Gastroenterol 11, 27732776.

40M Pimentel , EJ Chow & HC Lin (2000) Eradication of small intestinal bacterial overgrowth reduces symptoms of irritable bowel syndrome. Am J Gastroenterol 95, 35033506.

41CD Packey & RB Sartor (2009) Commensal bacteria, traditional and opportunistic pathogens, dysbiosis and bacterial killing in inflammatory bowel diseases. Curr Opin Infect Dis 22, 292301.

42M Vijay-Kumar , JD Aitken , FA Carvalho , et al. (2010) Metabolic syndrome and altered gut microbiota in mice lacking Toll-like receptor 5. Science 328, 228231.

43PD Cani , NM Delzenne , J Amar , et al. (2008) Role of gut microflora in the development of obesity and insulin resistance following high-fat diet feeding. Pathol Biol (Paris) 56, 305309.

44PJ Turnbaugh , F Backhed , L Fulton , et al. (2008) Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 3, 213223.

45H Tilg , AR Moschen & A Kaser (2009) Obesity and the microbiota. Gastroenterology 136, 14761483.

46K Atarashi , T Tanoue , T Shima , et al. (2011) Induction of colonic regulatory T cells by indigenous Clostridium species. Science 331, 337341.

47MB Geuking , J Cahenzli , MA Lawson , et al. (2011) Intestinal bacterial colonization induces mutualistic regulatory T cell responses. Immunity 34, 794806.

48H Esterbauer , RJ Schaur & H Zollner (1991) Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med 11, 81128.

Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

British Journal of Nutrition
  • ISSN: 0007-1145
  • EISSN: 1475-2662
  • URL: /core/journals/british-journal-of-nutrition
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords: