Independent positive association of plasma β-carotene concentrations with adiponectin among non-diabetic obese subjects

Abstract

Purpose

Many epidemiological studies find an inverse correlation between carotenoids intake or carotenoids plasma concentrations and body mass index (BMI), insulin resistance or metabolic syndrome in the general population. However, it is not clear whether these relationships occur in obese population.

Methods

We conducted a cross-sectional study in 108 obese non-diabetic patients.

Results

There was an inverse correlation between plasma levels of pro-vitamin A carotenoids (α-carotene, β-carotene and β-cryptoxanthin) and both BMI and insulin resistance (estimated by the HOMA-IR). No correlation between plasma concentrations of lycopene or lutein/zeaxanthin and BMI or insulin resistance was found. The inverse association between the three pro-vitamin A carotenoids and HOMA-IR disappeared after adjustment for BMI and waist circumference. Interestingly, we identified a positive association between concentrations of β-carotene and adiponectin in plasma that was independent of sex, age, smoking status, BMI and waist circumference. To our knowledge, such association has never been described in obese patients.

Conclusion

These results suggest the existence of a favourable effect of β-carotene on insulin sensitivity in obese individuals that could involve a positive regulation of adiponectin, either directly or via its pro-vitamin A activity. The demonstration of the potential benefits of β-carotene towards insulin sensitivity would open the way to dietary strategies to prevent metabolic syndrome.

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References

  1. 1.

    de Heredia FP, Gomez-Martinez S, Marcos A (2012) Obesity, inflammation and the immune system. Proc Nutr Soc 71(2):332–338

    Article  Google Scholar 

  2. 2.

    Leal Vde O, Mafra D (2013) Adipokines in obesity. Clin Chim Acta 419:87–94

    Article  Google Scholar 

  3. 3.

    Grattagliano I, Palmieri VO, Portincasa P, Moschetta A, Palasciano G (2008) Oxidative stress-induced risk factors associated with the metabolic syndrome: a unifying hypothesis. J Nutr Biochem 19(8):491–504

    Article  CAS  Google Scholar 

  4. 4.

    Bisbal C, Lambert K, Avignon A (2010) Antioxidants and glucose metabolism disorders. Curr Opin Clin Nutr Metab Care 13(4):439–446

    Article  CAS  Google Scholar 

  5. 5.

    Calder PC, Ahluwalia N, Brouns F, Buetler T, Clement K, Cunningham K, Esposito K, Jonsson LS, Kolb H, Lansink M, Marcos A, Margioris A, Matusheski N, Nordmann H, O’Brien J, Pugliese G, Rizkalla S, Schalkwijk C, Tuomilehto J, Warnberg J, Watzl B, Winklhofer-Roob BM (2011) Dietary factors and low-grade inflammation in relation to overweight and obesity. Br J Nutr 106(Suppl 3):S5–78

    Article  CAS  Google Scholar 

  6. 6.

    Landrier JF, Marcotorchino J, Tourniaire F (2012) Lipophilic micronutrients and adipose tissue biology. Nutrients 4(11):1622–1649

    Article  Google Scholar 

  7. 7.

    Rao AV, Rao LG (2007) Carotenoids and human health. Pharmacol Res 55(3):207–216

    Article  CAS  Google Scholar 

  8. 8.

    Namitha KK, Negi PS (2010) Chemistry and biotechnology of carotenoids. Crit Rev Food Sci Nutr 50(8):728–760

    Article  CAS  Google Scholar 

  9. 9.

    Ford ES, Will JC, Bowman BA, Narayan KM (1999) Diabetes mellitus and serum carotenoids: findings from the Third National Health and Nutrition Examination Survey. Am J Epidemiol 149(2):168–176

    Article  CAS  Google Scholar 

  10. 10.

    Ylonen K, Alfthan G, Groop L, Saloranta C, Aro A, Virtanen SM (2003) Dietary intakes and plasma concentrations of carotenoids and tocopherols in relation to glucose metabolism in subjects at high risk of type 2 diabetes: the Botnia Dietary Study. Am J Clin Nutr 77(6):1434–1441

    Google Scholar 

  11. 11.

    Ford ES, Mokdad AH, Giles WH, Brown DW (2003) The metabolic syndrome and antioxidant concentrations: findings from the Third National Health and Nutrition Examination Survey. Diabetes 52(9):2346–2352

    Article  CAS  Google Scholar 

  12. 12.

    Coyne T, Ibiebele TI, Baade PD, Dobson A, McClintock C, Dunn S, Leonard D, Shaw J (2005) Diabetes mellitus and serum carotenoids: findings of a population-based study in Queensland, Australia. Am J Clin Nutr 82(3):685–693

    CAS  Google Scholar 

  13. 13.

    Galan P, Viteri FE, Bertrais S, Czernichow S, Faure H, Arnaud J, Ruffieux D, Chenal S, Arnault N, Favier A, Roussel AM, Hercberg S (2005) Serum concentrations of beta-carotene, vitamins C and E, zinc and selenium are influenced by sex, age, diet, smoking status, alcohol consumption and corpulence in a general French adult population. Eur J Clin Nutr 59(10):1181–1190

    Article  CAS  Google Scholar 

  14. 14.

    Andersen LF, Jacobs DR Jr, Gross MD, Schreiner PJ, Dale Williams O, Lee DH (2006) Longitudinal associations between body mass index and serum carotenoids: the CARDIA study. Br J Nutr 95(2):358–365

    Article  CAS  Google Scholar 

  15. 15.

    Hozawa A, Jacobs DR Jr, Steffes MW, Gross MD, Steffen LM, Lee DH (2006) Associations of serum carotenoid concentrations with the development of diabetes and with insulin concentration: interaction with smoking: the Coronary Artery Risk Development in Young Adults (CARDIA) Study. Am J Epidemiol 163(10):929–937

    Article  Google Scholar 

  16. 16.

    Hozawa A, Jacobs DR Jr, Steffes MW, Gross MD, Steffen LM, Lee DH (2007) Relationships of circulating carotenoid concentrations with several markers of inflammation, oxidative stress, and endothelial dysfunction: the Coronary Artery Risk Development in Young Adults (CARDIA)/Young Adult Longitudinal Trends in Antioxidants (YALTA) study. Clin Chem 53(3):447–455

    Article  CAS  Google Scholar 

  17. 17.

    Sugiura M, Nakamura M, Ogawa K, Ikoma Y, Matsumoto H, Ando F, Shimokata H, Yano M (2008) Associations of serum carotenoid concentrations with the metabolic syndrome: interaction with smoking. Br J Nutr 100(6):1297–1306

    Article  CAS  Google Scholar 

  18. 18.

    Wang L, Gaziano JM, Norkus EP, Buring JE, Sesso HD (2008) Associations of plasma carotenoids with risk factors and biomarkers related to cardiovascular disease in middle-aged and older women. Am J Clin Nutr 88(3):747–754

    CAS  Google Scholar 

  19. 19.

    Sluijs I, Beulens JW, Grobbee DE, van der Schouw YT (2009) Dietary carotenoid intake is associated with lower prevalence of metabolic syndrome in middle-aged and elderly men. J Nutr 139(5):987–992

    Article  CAS  Google Scholar 

  20. 20.

    Coyne T, Ibiebele TI, Baade PD, McClintock CS, Shaw JE (2009) Metabolic syndrome and serum carotenoids: findings of a cross-sectional study in Queensland, Australia. Br J Nutr 102(11):1668–1677

    Article  CAS  Google Scholar 

  21. 21.

    Czernichow S, Vergnaud AC, Galan P, Arnaud J, Favier A, Faure H, Huxley R, Hercberg S, Ahluwalia N (2009) Effects of long-term antioxidant supplementation and association of serum antioxidant concentrations with risk of metabolic syndrome in adults. Am J Clin Nutr 90(2):329–335

    Article  CAS  Google Scholar 

  22. 22.

    Arnlov J, Zethelius B, Riserus U, Basu S, Berne C, Vessby B, Alfthan G, Helmersson J (2008) Serum and dietary beta-carotene and alpha-tocopherol and incidence of type 2 diabetes mellitus in a community-based study of Swedish men: report from the Uppsala Longitudinal Study of Adult Men (ULSAM) study. Diabetologia 52(1):97–105

  23. 23.

    Chai W, Conroy SM, Maskarinec G, Franke AA, Pagano IS, Cooney RV (2010) Associations between obesity and serum lipid-soluble micronutrients among premenopausal women. Nutr Res 30(4):227–232

    Article  CAS  Google Scholar 

  24. 24.

    Beydoun MA, Shroff MR, Chen X, Beydoun HA, Wang Y, Zonderman AB (2011) Serum antioxidant status is associated with metabolic syndrome among U.S. adults in recent national surveys. J Nutr 141(5):903–913

    Article  CAS  Google Scholar 

  25. 25.

    Suzuki K, Ito Y, Inoue T, Hamajima N (2011) Inverse association of serum carotenoids with prevalence of metabolic syndrome among Japanese. Clin Nutr 30(3):369–375

    Article  CAS  Google Scholar 

  26. 26.

    Osth M, Ost A, Kjolhede P, Stralfors P (2014) The concentration of beta-carotene in human adipocytes, but not the whole-body adipocyte stores, is reduced in obesity. PLoS ONE 9(1):e85610

    Article  Google Scholar 

  27. 27.

    Kimmons JE, Blanck HM, Tohill BC, Zhang J, Khan LK (2006) Associations between body mass index and the prevalence of low micronutrient levels among US adults. MedGenMed 8(4):59

    Google Scholar 

  28. 28.

    Garcia OP, Long KZ, Rosado JL (2009) Impact of micronutrient deficiencies on obesity. Nutr Rev 67(10):559–572

    Article  Google Scholar 

  29. 29.

    Chung HY, Ferreira AL, Epstein S, Paiva SA, Castaneda-Sceppa C, Johnson EJ (2009) Site-specific concentrations of carotenoids in adipose tissue: relations with dietary and serum carotenoid concentrations in healthy adults. Am J Clin Nutr 90(3):533–539

    Article  CAS  Google Scholar 

  30. 30.

    Borel P, Moussa M, Reboul E, Lyan B, Defoort C, Vincent-Baudry S, Maillot M, Gastaldi M, Darmon M, Portugal H, Planells R, Lairon D (2007) Human plasma levels of vitamin E and carotenoids are associated with genetic polymorphisms in genes involved in lipid metabolism. J Nutr 137(12):2653–2659

    CAS  Google Scholar 

  31. 31.

    Reboul E, Borel P (2011) Proteins involved in uptake, intracellular transport and basolateral secretion of fat-soluble vitamins and carotenoids by mammalian enterocytes. Prog Lipid Res 50(4):388–402

    Article  CAS  Google Scholar 

  32. 32.

    Villaca Chaves G, Pereira SE, Saboya CJ, Ramalho A (2008) Non-alcoholic fatty liver disease and its relationship with the nutritional status of vitamin A in individuals with class III obesity. Obes Surg 18(4):378–385

    Article  Google Scholar 

  33. 33.

    Villaca Chaves G, Goncalves de Souza G, Cardoso de Matos A, Abrantes Peres W, Pereira SE, Saboya CJ, D’Almeida CA, Ramalho A (2010) Serum retinol and beta-carotene levels and risk factors for cardiovascular disease in morbid obesity. Int J Vitam Nutr Res 80(3):159–167

    Article  Google Scholar 

  34. 34.

    Suzuki K, Inoue T, Hashimoto S, Ochiai J, Kusuhara Y, Ito Y, Hamajima N (2010) Association of serum carotenoids with high molecular weight adiponectin and inflammation markers among Japanese subjects. Clin Chim Acta 411(17–18):1330–1334

    Article  CAS  Google Scholar 

  35. 35.

    Turer AT, Scherer PE (2012) Adiponectin: mechanistic insights and clinical implications. Diabetologia 55(9):2319–2326

    Article  CAS  Google Scholar 

  36. 36.

    Tourniaire F, Gouranton E, von Lintig J, Keijer J, Luisa Bonet M, Amengual J, Lietz G, Landrier JF (2009) Beta-carotene conversion products and their effects on adipose tissue. Genes Nutr 4(3):179–187

    Article  CAS  Google Scholar 

  37. 37.

    Bonet ML, Ribot J, Palou A (2012) Lipid metabolism in mammalian tissues and its control by retinoic acid. Biochim Biophys Acta 1821(1):177–189

    Article  CAS  Google Scholar 

  38. 38.

    Kawada T, Aoki N, Kamei Y, Maeshige K, Nishiu S, Sugimoto E (1990) Comparative investigation of vitamins and their analogues on terminal differentiation, from preadipocytes to adipocytes, of 3T3-L1 cells. Comp Biochem Physiol A 96(2):323–326

    Article  CAS  Google Scholar 

  39. 39.

    Kuri-Harcuch W (1982) Differentiation of 3T3-F442A cells into adipocytes is inhibited by retinoic acid. Differentiation 23(2):164–169

    Article  CAS  Google Scholar 

  40. 40.

    Kameji H, Mochizuki K, Miyoshi N, Goda T (2010) Beta-carotene accumulation in 3T3-L1 adipocytes inhibits the elevation of reactive oxygen species and the suppression of genes related to insulin sensitivity induced by tumor necrosis factor-alpha. Nutrition 26(11–12):1151–1156

    Article  CAS  Google Scholar 

  41. 41.

    Ziouzenkova O, Orasanu G, Sukhova G, Lau E, Berger JP, Tang G, Krinsky NI, Dolnikowski GG, Plutzky J (2007) Asymmetric cleavage of beta-carotene yields a transcriptional repressor of retinoid X receptor and peroxisome proliferator-activated receptor responses. Mol Endocrinol 21(1):77–88

    Article  CAS  Google Scholar 

  42. 42.

    Amengual J, Gouranton E, van Helden YG, Hessel S, Ribot J, Kramer E, Kiec-Wilk B, Razny U, Lietz G, Wyss A, Dembinska-Kiec A, Palou A, Keijer J, Landrier JF, Bonet ML, von Lintig J (2011) Beta-carotene reduces body adiposity of mice via BCMO1. PLoS ONE 6(6):e20644

    Article  CAS  Google Scholar 

  43. 43.

    Lobo GP, Amengual J, Li HN, Golczak M, Bonet ML, Palczewski K, von Lintig J (2010) Beta, beta-carotene decreases peroxisome proliferator receptor gamma activity and reduces lipid storage capacity of adipocytes in a beta, beta-carotene oxygenase 1-dependent manner. J Biol Chem 285(36):27891–27899

    Article  CAS  Google Scholar 

  44. 44.

    Feng D, Ling WH, Duan RD (2010) Lycopene suppresses LPS-induced NO and IL-6 production by inhibiting the activation of ERK, p38MAPK, and NF-kappaB in macrophages. Inflamm Res 59(2):115–121

    Article  CAS  Google Scholar 

  45. 45.

    Gouranton E, Thabuis C, Riollet C, Malezet-Desmoulins C, El Yazidi C, Amiot MJ, Borel P, Landrier JF (2011) Lycopene inhibits proinflammatory cytokine and chemokine expression in adipose tissue. J Nutr Biochem 22(7):642–648

    Article  CAS  Google Scholar 

  46. 46.

    Marcotorchino J, Romier B, Gouranton E, Riollet C, Gleize B, Malezet-Desmoulins C, Landrier JF (2012) Lycopene attenuates LPS-induced TNF-alpha secretion in macrophages and inflammatory markers in adipocytes exposed to macrophage-conditioned media. Mol Nutr Food Res 56(5):725–732

    Article  CAS  Google Scholar 

  47. 47.

    Gouranton E, Aydemir G, Reynaud E, Marcotorchino J, Malezet C, Caris-Veyrat C, Blomhoff R, Landrier JF, Ruhl R (2011) Apo-10′-lycopenoic acid impacts adipose tissue biology via the retinoic acid receptors. Biochim Biophys Acta 1811(12):1105–1114

    Article  CAS  Google Scholar 

  48. 48.

    Al-Delaimy WK, Ferrari P, Slimani N, Pala V, Johansson I, Nilsson S, Mattisson I, Wirfalt E, Galasso R, Palli D, Vineis P, Tumino R, Dorronsoro M, Pera G, Ocke MC, Bueno-de-Mesquita HB, Overvad K, Chirlaque M, Trichopoulou A, Naska A, Tjonneland A, Olsen A, Lund E, Alsaker EH, Barricarte A, Kesse E, Boutron-Ruault MC, Clavel-Chapelon F, Key TJ, Spencer E, Bingham S, Welch AA, Sanchez-Perez MJ, Nagel G, Linseisen J, Quiros JR, Peeters PH, van Gils CH, Boeing H, van Kappel AL, Steghens JP, Riboli E (2005) Plasma carotenoids as biomarkers of intake of fruits and vegetables: individual-level correlations in the European Prospective Investigation into Cancer and Nutrition (EPIC). Eur J Clin Nutr 59(12):1387–1396

    Article  CAS  Google Scholar 

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Acknowledgments

The authors thank Catherine Clement, dietitian, for her expertise in managing and analysing the nutrition-related data. This study was supported by INRA, Aix-Marseille University and AP-HM.

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

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Correspondence to J. F. Landrier or P. Darmon.

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J. F. Landrier and P. Darmon have contributed equally to this work.

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Ben Amara, N., Tourniaire, F., Maraninchi, M. et al. Independent positive association of plasma β-carotene concentrations with adiponectin among non-diabetic obese subjects. Eur J Nutr 54, 447–454 (2015). https://doi.org/10.1007/s00394-014-0728-6

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Keywords

  • Carotenoids
  • Adiponectin
  • β-Carotene
  • Lycopene
  • HOMA-IR