Skip to main content
SpringerLink
Log in

Meal ingestion provokes entry of lipoproteins containing fat from the previous meal: possible metabolic implications

  • ORIGINAL CONTRIBUTION
  • Published:
European Journal of Nutrition Aims and scope Submit manuscript

Summary

Background

Prolonged and exaggerated postprandial plasma triacylglycerol (TAG) concentrations are considered as an independent risk factor for coronary artery disease. Western populations eat many meals at regular intervals, and can be in a postprandial state for at least 17h of a 24h period. After consuming 2 meals an early plasma TAG peak has been observed after the second meal, the origin of which is unclear.

Aim of the study

To test the hypothesis that the early TAG peak observed following sequential meals was of intestinal origin and represented fat derived from the previous meal.

Methods

Postprandial plasma lipaemic responses of 17 healthy postmenopausal women were studied by giving a test breakfast followed by a lunch. Watermiscible retinyl palmitate (RP) was added to the breakfast, but not the lunch test meal. Plasma TAG, retinyl esters (RE) and apo B–48 were determined for a 10h period following breakfast.

Results

In response to the test meals, RE, apo B–48 and TAG showed multiple peaks. Despite omission of RP from the lunch, RE showed an early peak response after ingestion of lunch in 15 of 17 subjects. The peak response after lunch of all three markers appeared significantly earlier compared with their respective peak responses after the breakfast (P < 0.0001). The area of RE response after lunch was significantly correlated with the RE lipaemic response to the breakfast (r = 0.67; P < 0.004) and to the fasting TAG concentration (r = 0.48; P < 0.05).

Conclusions

Since the lunch did not contain RP, the distinctive second influx of RE after lunch was believed to have originated from the breakfast. This, together with the fact that all three markers showed an earlier response to the lunch than the breakfast, supports the view that ingestion of a second meal provokes entry of fat from the previous meal, from an as yet unidentified site (gut, enterocytes, lymph). The results indicate that the degree of TAG “storage” from previous meals might be a function of TAG tolerance and provide a possible site of regulation of the entry of fat into the systemic circulation.

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

Similar content being viewed by others

References

  1. Hokanson J, Austin MA (1996) Plasma triglyceride level is a risk factor for cardiovascular disease independent of high density lipoprotein cholesterol: a meta-analysis of population-based prospective studies. J Cardiovasc Risk 3:213–219

    PubMed  Google Scholar 

  2. Sethi S, Gibney MJ, Williams CM (1993) Postprandial lipoprotein metabolism. Nutr Res Rev 6:161–183

    Google Scholar 

  3. Patsch JR (1994) Triglyceride-rich lipoproteins and atherosclerosis. Atherosclerosis 110(Suppl):S23–S26

    Article  PubMed  Google Scholar 

  4. Karpe F, Hamsten A (1995) Postprandial lipoprotein metabolism and atherosclerosis. Curr Opin Lipidol 6:123–129

    PubMed  Google Scholar 

  5. Krasinski SD, Cohn JS, Russell RM, Schaefer EJ (1990) Postprandial plasma vitamin A metabolism in humans: A reassessment of the use of plasma retinyl esters as markers for intestinally derived chylomicrons and their remnants. Metabolism 39:357–365

    Article  PubMed  Google Scholar 

  6. Karpe F, Steiner G, Olivecrona T, Calson LA, Hamsten A (1993) Metabolism of triglyceride-rich lipoproteins during alimentary lipemia. J Clin Invest 91:748–758

    PubMed  Google Scholar 

  7. Lovegrove JA, Jackson KG, Murphy MC, Brookes CN, Zampelas A, Knapper JME, Wright JW, Gould BJ, Williams CM (1999) Markers of intestinally-derived lipoproteins: application to studies of altered diet and meal fatty acid composition. Nutr Metab Cardiovasc Dis 9: 9–18

    PubMed  Google Scholar 

  8. Williams CM (1997) Postprandial lipid metabolism: effects of dietary fatty acids. Proc Nutr Soc 56:679–692

    Article  PubMed  Google Scholar 

  9. Cohn JS, McNamara JR, Krasinski SD, Russell RM, Schaefer EJ (1989) Role of triglyceride-rich lipoproteins from the liver and intestine in the etiology of postprandial peaks in plasma triglyceride concentration. Metabolism 38:484–490

    Article  PubMed  Google Scholar 

  10. Williams CM, Moore F, Morgan L, Wright J (1992) Effects of n-3 fatty acids on postprandial triacylglycerol and hormone concentrations in normal subjects. Br J Nutr 68:655–666

    PubMed  Google Scholar 

  11. Peel AS, Zampelas A, Williams CM, Gould BJ (1993) A novel antiserum specific to apolipoprotein B-48: application in the investigation of postprandial lipidaemia in humans. Clin Sci 85:521–524

    PubMed  Google Scholar 

  12. Fielding BA,Callow J, Owen RM, Samra JS, Matthews DR, Frayn KN (1996) Postprandial lipemia: the origin of an early peak studied by specific dietary fatty acid during sequential meals. AmJ Clin Nutr 63:36–41

    Google Scholar 

  13. Coppack SW, Frayn KN, Humphreys SM (1989) Plasma triglycerol extraction in human adipose tissue in vivo: effects of glucose ingestion and insulin infusion. Eur J Clin Nutr 43:493–496

    PubMed  Google Scholar 

  14. Silva KDRR, Williams CM, Lovegrove JA (2001) Use of water-miscible retinyl palmitate as markers of chylomicrons gives earlier peak response of plasma retinyl esters compared with oil-soluble retinyl palmitate. Brit J Nutr 86:427–432

    PubMed  Google Scholar 

  15. Edelstein C, Scanu AM (1986) Precautionary measures for collecting blood destined for lipoprotein isolation. Methods Enzymol 128:151–155

    PubMed  Google Scholar 

  16. McNamara JR, Huang C, Massov T, Leary ET, Warnick GR, Rubins HB, Robins SJ, Schefer EJ (1994) Modification of the Dextran-Mg+2 high-density lipoprotein cholesterol precipitation method for use with previously frozen plasma. Clin Chem 40:233–239

    PubMed  Google Scholar 

  17. Friedewald WT, Levey RI (1972) Estimation of the concentration of lowdensity lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 18:499–502

    PubMed  Google Scholar 

  18. Ruotolo G, Zhang H, Bentsianov V, Le NA (1992) Protocol for the study of the metabolism of retinyl esters in plasma lipoproteins during postprandial lipaemia. J Lipid Res 33:1541–1549

    PubMed  Google Scholar 

  19. Lovegrove JA, Isherwood SG, Jackson KG, Williams CM, Gould BJ (1996) Quantitation of apolipoprotein B-48 in triacylglycerol-rich lipoproteins by a specific enzyme-linked immunosorbant assay. Biochim Biophys Acta 1301:221–229

    PubMed  Google Scholar 

  20. Matthews JNS, Altman DG, Campbell MJ, Royston P (1990) Analysis of serial measurements in medical research. Br Med J 300:230–235

    Google Scholar 

  21. Littell RC, Milliken GA, Stroup WW, Wolfinger RD (1996) SAS® system for Mixed Models. SAS Inst. Inc., Cary, NC, USA

  22. Jackson KG, Robertson MD, Fielding BA, Frayn KN, Williams CM (2002) Olive oil increases the number of triacylglycerol- rich chylomicron particles compared with other oils: an effect retained when a second meal is fed. Am J Clin Nutr 76:942–949

    PubMed  Google Scholar 

  23. Borgström B, Laurell CB (1953) Studies on lymph and lymph-proteins during absorption of fat and saline by rats. Acta Physiol Scan 29:264

    Google Scholar 

  24. Evans K, Kuusela PJ, Cruz ML, Wilhelmova I, Fielding BA, Frayn KN (1998) Rapid chylomicron appearance following sequential meals: effects of second meal composition. Brit J Nutr 79:425–429

    PubMed  Google Scholar 

  25. Griffiths JA, Humphreys SM, Clark MOL, Fielding BA, Frayn KN (1994) Immediate metabolic availability of dietary fat in combination with carbohydrate. Am J Clin Nutr 59:53–59

    PubMed  Google Scholar 

  26. Robertson MD, Parkes M, Warren BF, Ferguson DJP, Jackson KG, Jewell DP, Frayn KN (2003) Mobilisation of enterocyte fat stores by oral glucose in humans. Gut 52:834–839

    Article  PubMed  Google Scholar 

  27. Mendeloff AI (1954) The effects of eating and of sham feeding upon the absorption of vitamin A palmitate in man. J Clin Investigation 33:1015–1021

    Google Scholar 

  28. Mattes RD (2002) Oral fat exposure increases the first phase triacylglycerol concentration due to release of stored lipids in humans. J Nutr 132:3656–3662

    PubMed  Google Scholar 

  29. Jackson KG, Robertson MD, Fielding BA, Frayn KN, Williams CM (2001) Second meal effect:modified sham feeding does not provoke the release of stored triacylglycerol from a previous high-fat meal. Brit J Nutr 85:149–156

    PubMed  Google Scholar 

  30. Mattes RD (1993) Oral fat exposure alters postprandial lipid metabolism in humans. Am J Clin Nutr 63:911–917

    Google Scholar 

  31. Lovegrove JA, Silva KDRR, Wright JW, Williams CM (2002) Adiposity, insulin levels and lipid metabolism in postmenopausal women. Int J Obesity 26:475–486

    Article  Google Scholar 

  32. Robertson MD, Jackson KG, Fielding BA, Williams CM, Frayn KN (2002) Acute affects of meal fatty acid composition on insulin sensitivity in healthy post-menopausal women. Br J Nutr 88:635–640

    Article  PubMed  Google Scholar 

  33. Hollander D (1981) Intestinal absorption of vitamins A, E,D and K. J Lab Clin Med 97:449–462

    PubMed  Google Scholar 

  34. Ross AC (1982) Retinol esterification by rat liver microsomes. Evidence for a fatty acyl coenzyme A: choleterolacyltransferase. J Biol Chem 257:2453–2459

    PubMed  Google Scholar 

  35. Humayun MA, Jones AE, Bennoson J, Wootton SA (2000) Impaired postprandial lipid metabolism in middle-aged men. Proc Nutr Soc 59:20A (abstract)

    Google Scholar 

  36. Karpe F, Hultin M (1995) Endogenous triglyceride-rich lipoproteins accumulate in rat plasma when competing with a chylomicron-like triglyceride emulsion for a common lipolytic pathway. J Lipid Res 36:1557–1566

    PubMed  Google Scholar 

  37. Jackson KG, Zampelas A, Knapper JME, Culverwell CC, Wright J, Gould BJ, Williams CM (1999) Lack of influence of meal fatty acid composition on the contribution of intestinally derived lipoproteins to postprandial lipaemia. Br J Nutr 81:51–57

    PubMed  Google Scholar 

  38. Ong DE (1994) Cellular transport and metabolism of vitamin A: Roles of cellular retinoid-binding proteins. Nutr Rev 52:S24–S31

    Google Scholar 

  39. Demacker PNM, Reijnen IGM, Katan MB, Stuyt PMJ, Stalenhoef AFH (1991) Increased removal of remnants of triglyceride-rich lipoproteins on a diet rich in polyunsaturated fatty acids. Eur J Clin Invest 21:197–203

    PubMed  Google Scholar 

  40. Schrezenmeir J, Weber JP, Probst R, Biesalski HK, Luley E, Prellwitz W (1991) Postprandial pattern of triglyceride- rich lipoprotein in normalweight humans after an oral fat load: Exaggerated triglycerides and altered insulin response in some subjects. Ann Nutr Metab 36:186–196

    Google Scholar 

  41. Wilson DE, Chan IF, Ball M (1983) Plasma lipoprotein retinoids after vitamin A feeding in normal man: Minimal appearance of retinyl esters among low density lipoproteins. Metabolism 32:514–517

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Hugh Sinclair Unit of Human Nutrition, School of Food Biosciences, University of Reading, 226, Whiteknights Reading (Berks.) RG6 6AP, UK

    K. D. R. R. Silva, J. W. Wright, C. M. Williams & J. A. Lovegrove

Authors
  1. K. D. R. R. Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. W. Wright
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. C. M. Williams
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. A. Lovegrove
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. A. Lovegrove.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Silva, K.D.R.R., Wright, J.W., Williams, C.M. et al. Meal ingestion provokes entry of lipoproteins containing fat from the previous meal: possible metabolic implications. Eur J Nutr 44, 377–383 (2005). https://doi.org/10.1007/s00394-004-0538-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00394-004-0538-3

Key words

Search

Navigation