Skip to main content
Log in

Dietary fat quality in regular fat diets has minor effects on biomarkers of inflammation in obese Zucker rats

  • Original Contribution
  • Published:
European Journal of Nutrition Aims and scope Submit manuscript

Abstract

Purpose

Adipose tissue-associated chronic inflammation is involved in the pathogenesis of obesity-related diseases. Dietary fatty acids are known to influence inflammatory processes. The aim of this study was to investigate, whether diets with regular fat contents but variable fat qualities affect adipose tissue-associated inflammation through the fatty acid composition of mesenteric adipose tissue (MAT).

Methods

Obese Zucker rats were fed diets containing 7 % wt:wt rapeseed oil, corn oil, or lard for 10 weeks. Fatty acid composition and endocrine function regarding adipokines and cytokines of MAT, number of total CD3+ T cells, and cytokine secretion of mesenteric lymph node (MLN)-derived lymphocytes were determined. Local effects in MAT and MLN were compared to systemic effects assessed in serum and peripheral blood mononuclear cells.

Results

Fatty acid composition of MAT reflected dietary fatty acid intake, without affecting endocrine function. Feeding the lard diet for 10 weeks increased the serum adiponectin and TNF-α secretion of blood lymphocytes, whereas CD3+ T cells in blood were decreased. No effects were seen for the secretion of adipokines and cytokines from MAT, the amount of T cells in MLN, and cytokine secretion of MLN lymphocytes.

Conclusions

In conclusion, feeding obese rats a diet with regular fat content but variable fat sources for 10 weeks, changed the fatty acid composition of MAT but not its secretory properties or MLN functions. Although the local immune system was not influenced, lard-feeding induced minor changes in systemic immune function.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

AA:

Arachidonic acid

ALA:

α-Linolenic acid

AT:

Adipose tissue

RSO:

Rapeseed oil

COO:

Corn oil

CRP:

C-reactive protein

FITC:

Fluorescein isothiocyanate

HFD:

High-fat diet

LA:

Linoleic acid

MAT:

Mesenteric adipose tissue

MCP-1:

Monocyte chemotactic protein-1

MLN:

Mesenteric lymph node

MUFA:

Monounsaturated fatty acids

PAI-1:

Plasminogen activator inhibitor-1

PBMC:

Peripheral blood mononuclear cells

PE:

Phycoerythrin

PUFA:

Polyunsaturated fatty acids

SFA:

Saturated fatty acids

TMSH:

Trimethylsulfonium hydroxide

References

  1. Galic S, Oakhill JS, Steinberg GR (2010) Adipose tissue as an endocrine organ. Mol Cell Endocrinol 316:129–139

    Article  CAS  Google Scholar 

  2. Yu R, Kim CS, Kang JH (2009) Adipose tissue as an endocrine organ as target for treatment of metabolic syndrome. Forum Nutr 61:95–103

    Article  CAS  Google Scholar 

  3. Hotamisligil GS, Erbay E (2008) Nutrient sensing and inflammation in metabolic diseases. Nat Rev Immunol 8:923–934

    Article  CAS  Google Scholar 

  4. Hotamisligil GS (2006) Inflammation and metabolic disorders. Nature 444:860–867

    Article  CAS  Google Scholar 

  5. Gregor MF, Hotamisligil GS (2011) Inflammatory mechanisms in obesity. Annu Rev Immunol 29:415–445

    Article  CAS  Google Scholar 

  6. Kintscher U, Hartge M, Hess K, Foryst-Ludwig A, Clemenz M et al (2008) T-lymphocyte infiltration in visceral adipose tissue—a primary event in adipose tissue inflammation and the development of obesity-mediated insulin resistance. Arteriosc Thromb Vasc Biol 28:1304–1310

    Article  CAS  Google Scholar 

  7. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr (2003) Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112:1796–1808

    CAS  Google Scholar 

  8. Wronska A, Kmiec Z (2012) Structural and biochemical characteristics of various white adipose tissue depots. Acta Physiol (Oxf) 205:194–208

    Article  CAS  Google Scholar 

  9. Catalano KJ, Stefanovski D, Bergman RN (2010) Critical role of the mesenteric depot versus other intra-abdominal adipose depots in the development of insulin resistance in young rats. Diabetes 59:1416–1423

    Article  CAS  Google Scholar 

  10. Gillingham LG, Gustafson JA, Han SY, Jassal DS, Jones PJ (2011) High-oleic rapeseed (canola) and flaxseed oils modulate serum lipids and inflammatory biomarkers in hypercholesterolaemic subjects. Br J Nutr 105:417–427

    Article  CAS  Google Scholar 

  11. Riccardi G, Giacco R, Rivellese AA (2004) Dietary fat, insulin sensitivity and the metabolic syndrome. Clin Nutr 23:447–456

    Article  CAS  Google Scholar 

  12. Djousse L, Biggs ML, Lemaitre RN, King IB, Song X, Ix JH, Mukamal KJ, Siscovick DS, Mozaffarian D (2011) Plasma omega-3 fatty acids and incident diabetes in older adults. Am J Clin Nutr 94:527–533

    Article  CAS  Google Scholar 

  13. Brostow DP, Odegaard AO, Koh WP, Duval S, Gross MD, Yuan JM, Pereira MA (2011) Omega-3 fatty acids and incident type 2 diabetes: the Singapore Chinese Health Study. Am J Clin Nutr 94:520–526

    Article  CAS  Google Scholar 

  14. Bradley RL, Fisher FF, Maratos-Flier E (2008) Dietary fatty acids differentially regulate production of TNF-alpha and IL-10 by murine 3T3-L1 adipocytes. Obesity (Silver Spring) 16:938–944

    Article  CAS  Google Scholar 

  15. Lo CJ, Chiu KC, Fu M, Lo R, Helton S (1999) Fish oil decreases macrophage tumor necrosis factor gene transcription by altering the NF kappa B activity. J Surg Res 82:216–221

    Article  CAS  Google Scholar 

  16. Masson CJ, Mensink RP (2011) Exchanging saturated fatty acids for (n-6) polyunsaturated fatty acids in a mixed meal may decrease postprandial lipemia and markers of inflammation and endothelial activity in overweight men. J Nutr 141:816–821

    Article  CAS  Google Scholar 

  17. Vijay-Kumar M, Vanegas SM, Patel N, Aitken JD, Ziegler TR, Ganji V (2011) Fish oil rich diet in comparison to saturated fat rich diet offered protection against lipopolysaccharide-induced inflammation and insulin resistance in mice. Nutr Metab 8:16

    Google Scholar 

  18. Laugerette F, Furet JP, Debard C, Daira P, Loizon E, Geloen A, Soulage CO, Simonet C, Lefils-Lacourtablaise J, Bernoud-Hubac N, Bodennec J, Peretti N, Vidal H, Michalski MC (2012) Oil composition of high-fat diet affects metabolic inflammation differently in connection with endotoxin receptors in mice. Am J Physiol Endocrinol Metab 302:E374–E386

    Article  CAS  Google Scholar 

  19. Caughey GE, Mantzioris E, Gibson RA, Cleland LG, James MJ (1996) The effect on human tumor necrosis factor alpha and interleukin 1 beta production of diets enriched in n-3 fatty acids from vegetable oil or fish oil. Am J Clin Nutr 63:116–122

    CAS  Google Scholar 

  20. Gillingham LG, Harris-Janz S, Jones PJ (2011) Dietary monounsaturated fatty acids are protective against metabolic syndrome and cardiovascular disease risk factors. Lipids 46:209–228

    Article  CAS  Google Scholar 

  21. Bueno AA, Oyama LM, de Oliveira C, Pisani LP, Ribeiro EB, Silveira VL, Oller do Nascimento CM (2008) Effects of different fatty acids and dietary lipids on adiponectin gene expression in 3T3-L1 cells and C57BL/6J mice adipose tissue. Pflugers Arch 455:701–709

    Article  CAS  Google Scholar 

  22. Todoric J, Loffler M, Huber J, Bilban M, Reimers M, Kadl A, Zeyda M, Waldhausl W, Stulnig TM (2006) Adipose tissue inflammation induced by high-fat diet in obese diabetic mice is prevented by n-3 polyunsaturated fatty acids. Diabetologia 49:2109–2119

    Article  CAS  Google Scholar 

  23. Kalupahana NS, Claycombe K, Newman SJ, Stewart T, Siriwardhana N, Matthan N, Lichtenstein AH, Moustaid-Moussa N (2010) Eicosapentaenoic acid prevents and reverses insulin resistance in high-fat diet-induced obese mice via modulation of adipose tissue inflammation. J Nutr 140:1915–1922

    Article  CAS  Google Scholar 

  24. Ruth MR, Proctor SD, Field CJ (2009) Effects of feeding fish oil on mesenteric lymph node cytokine responses in obese leptin receptor-deficient JCR:LA-cp rats. Int J Obes 33:96–103

    Article  CAS  Google Scholar 

  25. Kim CS, Lee SC, Kim YM, Kim BS, Choi HS, Kawada T, Kwon BS, Yu R (2008) Visceral fat accumulation induced by a high-fat diet causes the atrophy of mesenteric lymph nodes in obese mice. Obesity (Silver Spring) 16:1261–1269

    Article  CAS  Google Scholar 

  26. Paul G, Schaffler A, Neumeier M, Furst A, Bataillle F, Buechler C, Muller-Ladner U, Scholmerich J, Rogler G, Herfarth H (2006) Profiling adipocytokine secretion from creeping fat in Crohn’s disease. Inflamm Bowel Dis 12:471–477

    Article  Google Scholar 

  27. Watzl B, Kulling SE, Moseneder J, Barth SW, Bub A (2005) A 4-wk intervention with high intake of carotenoid-rich vegetables and fruit reduces plasma C-reactive protein in healthy, nonsmoking men. Am J Clin Nutr 82:1052–1058

    CAS  Google Scholar 

  28. Hara A, Radin NS (1978) Lipid extraction of tissues with a low-toxicity solvent. Anal Biochem 90:420–426

    Article  CAS  Google Scholar 

  29. Ostwald R, Okey R, Shannon A, Joan T (1962) Changes in tissue lipids in response to diet. 1. Fatty acids of subcutaneous, mesenteric and interscapular fat. J Nutr 76:341–352

    CAS  Google Scholar 

  30. Garaulet M, Perez-Llamas F, Perez-Ayala M, Martinez P, de Medina FS, Tebar FJ, Zamora S (2001) Site-specific differences in the fatty acid composition of abdominal adipose tissue in an obese population from a Mediterranean area: relation with dietary fatty acids, plasma lipid profile, serum insulin, and central obesity. Am J Clin Nutr 74:585–591

    CAS  Google Scholar 

  31. Pond CM, Mattacks CA (2003) The source of fatty acids incorporated into proliferating lymphoid cells in immune-stimulated lymph nodes. Br J Nutr 89:375–382

    Article  CAS  Google Scholar 

  32. Nishimura S, Manabe I, Nagasaki M, Eto K, Yamashita H, Ohsugi M, Otsu M, Hara K, Ueki K, Sugiura S, Yoshimura K, Kadowaki T, Nagai R (2009) CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nat Med 15:914–920

    Article  CAS  Google Scholar 

  33. Bjermo H, Iggman D, Kullberg J, Dahlman I, Johansson L, Persson L, Berglund J, Pulkki K, Basu S, Uusitupa M, Rudling M, Arner P, Cederholm T, Ahlstrom H, Riserus U (2012) Effects of n-6 PUFAs compared with SFAs on liver fat, lipoproteins, and inflammation in abdominal obesity: a randomized controlled trial. Am J Clin Nutr 95:1003–1012

    Article  CAS  Google Scholar 

  34. Mukaro VR, Costabile M, Murphy KJ, Hii CS, Howe PR, Ferrante A (2008) Leukocyte numbers and function in subjects eating n-3 enriched foods: selective depression of natural killer cell levels. Arthritis Res Ther 10:R57

    Google Scholar 

  35. Miles EA, Banerjee T, Wells SJ, Calder PC (2006) Limited effect of eicosapentaenoic acid on T-lymphocyte and natural killer cell numbers and functions in healthy young males. Nutrition 22:512–519

    Article  CAS  Google Scholar 

  36. Wu D, Meydani SN, Meydani M, Hayek MG, Huth P, Nicolosi RJ (1996) Immunologic effects of marine- and plant-derived n-3 polyunsaturated fatty acids in nonhuman primates. Am J Clin Nutr 63:273–280

    CAS  Google Scholar 

  37. Ouchi N, Parker JL, Lugus JJ, Walsh K (2011) Adipokines in inflammation and metabolic disease. Nat Rev Immunol 11:85–97

    Google Scholar 

Download references

Acknowledgments

We thank M. Giorgi, C. Hoffmann, S. Merkel, G. Schultheiss, L. Uhlmann, and A. Waldheim for their excellent technical assistance. This work was supported in part by the German Federal Ministry of Research and Education [0315379G].

Conflict of interest

All authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Bernhard Watzl.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 27 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Graf, D., Barth, S.W., Bub, A. et al. Dietary fat quality in regular fat diets has minor effects on biomarkers of inflammation in obese Zucker rats. Eur J Nutr 53, 211–219 (2014). https://doi.org/10.1007/s00394-013-0518-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00394-013-0518-6

Keywords

Navigation