Skip to main content
Log in

Apple preload increased postprandial insulin sensitivity of a high glycemic rice meal only at breakfast

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

Abstract

Purpose

The possible impact of preload food on insulin sensitivity has yet been reported. This study aimed to investigate the glycemic and insulinemic effect of an apple preload before breakfast, lunch and early supper, based on high glycemic index (GI) rice meals.

Methods

Twenty-three healthy participants in Group 1 and 14 participants in Group 2 were served with the reference meal (white rice containing 50 g of available carbohydrate) or experimental meals (apple preload and rice, each containing 15 and 35 g of available carbohydrate). The meals were either served at 8:00 for breakfast, 12:30 for lunch or 17:00 for early supper to explore the possible effect of time factor. The group 1 assessed the postprandial and subsequent-meal glycemic effect of the test meals by continuous glucose monitoring (CGM), along with subjective appetite; The group 2 further investigated the glycemic and insulin effect by blood collection.

Results

The apple preload lowered the blood glucose peak value by 33.5%, 31.4% and 31.0% in breakfast, lunch and supper, respectively, while increased insulin sensitivity by 40.5% only at breakfast, compared with the rice reference. The early supper resulted significantly milder glycemic response than its breakfast and lunch counterparts did. The result of CGM tests was consistent with that of the fingertip blood tests.

Conclusion

Apple preload performed the best at breakfast in terms of enhancing the insulin sensitivity. The preload treatment could effectively attenuate postprandial GR without increasing the area under insulin response curve in any of the three meals.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

After publication, all data necessary to understand and assess the conclusions of the manuscript are available to any reader of the European Journal of Nutrition.

References

  1. Mone P, Gambardella J, Pansini A, de Donato A, Martinelli G, Boccalone E, Matarese A, Frullone S, Santulli G (2021) Cognitive impairment in frail hypertensive elderly patients: role of hyperglycemia. Cells-Basel 10:2115

    Article  CAS  Google Scholar 

  2. Skrha J, Soupal J, Skrha JJ, Prazny M (2016) Glucose variability, HbA1c and microvascular complications. Rev Endocr Metab Disord 17:103–110

    Article  CAS  PubMed  Google Scholar 

  3. Takao T, Suka M, Yanagisawa H, Iwamoto Y (2017) Impact of postprandial hyperglycemia at clinic visits on the incidence of cardiovascular events and all-cause mortality in patients with type 2 diabetes. J Diabetes Investig 8:600–608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Cavalot F, Pagliarino A, Valle M, Di Martino L, Bonomo K, Massucco P, Anfossi G, Trovati M (2011) Postprandial blood glucose predicts cardiovascular events and all-cause mortality in type 2 diabetes in a 14-year follow-up: lessons from the san luigi gonzaga diabetes study. Diabetes Care 34:2237–2243

    Article  PubMed  PubMed Central  Google Scholar 

  5. Loader J, Montero D, Lorenzen C, Watts R, Meziat C, Reboul C, Stewart S, Walther G (2015) Acute hyperglycemia impairs vascular function in healthy and cardiometabolic diseased subjects systematic review and meta-analysis. Arterioscl Throm Vas 35:2060–2072

    Article  CAS  Google Scholar 

  6. Arble DM, Bass J, Laposky AD, Vitaterna MH, Turek FW (2009) Circadian timing of food intake contributes to weight gain. Obesity (Silver Spring) 17:2100–2102

    Article  PubMed  Google Scholar 

  7. Poggiogalle E, Jamshed H, Peterson CM (2018) Circadian regulation of glucose, lipid, and energy metabolism in humans. Metabolism 84:11–27

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Leung G, Huggins CE, Ware RS, Bonham MP (2020) Time of day difference in postprandial glucose and insulin responses: systematic review and meta-analysis of acute postprandial studies. Chronobiol Int 37:311–326

    Article  CAS  PubMed  Google Scholar 

  9. Wee M, Henry CJ (2020) Reducing the glycemic impact of carbohydrates on foods and meals: strategies for the food industry and consumers with special focus on Asia. Compr Rev Food Sci Food Saf 19:670–702

    Article  CAS  PubMed  Google Scholar 

  10. Sun L, Tan K, Han C, Leow MK, Henry CJ (2017) Impact of preloading either dairy or soy milk on postprandial glycemia, insulinemia and gastric emptying in healthy adults. Eur J Nutr 56:77–87

    Article  CAS  PubMed  Google Scholar 

  11. Wu T, Little TJ, Bound MJ, Borg M, Zhang X, Deacon CF, Horowitz M, Jones KL, Rayner CK (2016) A protein preload enhances the glucose-lowering efficacy of vildagliptin in type 2 diabetes. Diabetes Care 39:511–517

    Article  CAS  PubMed  Google Scholar 

  12. Ma J, Stevens JE, Cukier K, Maddox AF, Wishart JM, Jones KL, Clifton PM, Horowitz M, Rayner CK (2009) Effects of a protein preload on gastric emptying, glycemia, and gut hormones after a carbohydrate meal in diet-controlled type 2 diabetes. Diabetes Care 32:1600–1602

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Lubransky A, Monro J, Mishra S, Yu H, Haszard JJ, Venn BJ (2018) Postprandial glycaemic, hormonal and satiety responses to rice and kiwifruit preloads in chinese adults: a randomised controlled crossover trial. Nutrients 10:1110

    Article  PubMed  PubMed Central  Google Scholar 

  14. Lu J, Zhao W, Wang L, Fan Z, Zhu R, Wu Y, Zhou Y (2019) Apple preload halved the postprandial glycaemic response of rice meal on in healthy subjects. Nutrients 11:2912

    Article  PubMed  PubMed Central  Google Scholar 

  15. Lu X, Lu J, Fan Z, Liu A, Zhao W, Wu Y, Zhu R (2021) Both isocarbohydrate and hypercarbohydrate fruit preloads curbed postprandial glycemic excursion in healthy subjects. Nutrients 13:2470

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Zhao W, Zhou Y, Yuan Y, Fan Z, Wu Y, Liu A, Lu X (2020) Potato preload mitigated postprandial glycemic excursion in healthy subjects: an acute randomized trial. Nutrients 12:2759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Zhao W, Ye T, Fan Z, Wu Y, Liu A, Lu X (2021) Yam paste in glycemic preloads curbs peak glycemia of rice meals in apparent healthy subjects. Asia Pac J Clin Nutr 30:436–445

    PubMed  Google Scholar 

  18. Saito Y, Nitta A, Imai S, Kajiyama S, Miyawaki T, Ozasa N, Kajiyama S, Hashimoto Y, Fukui M (2020) Tomato juice preload has a significant impact on postprandial glucose concentration in healthy women: a randomized cross-over trial. Asia Pac J Clin Nutr 29:491–497

    CAS  PubMed  Google Scholar 

  19. Zhao W, Wang L, Fan Z, Lu J, Zhu R, Wu Y, Lu X (2020) Co-ingested vinegar-soaked or preloaded dried apple mitigated acute postprandial glycemia of rice meal in healthy subjects under equicarbohydrate conditions. Nutr Res 83:108–118

    Article  CAS  PubMed  Google Scholar 

  20. Lopez-Minguez J, Saxena R, Bandin C, Scheer FA, Garaulet M (2018) Late dinner impairs glucose tolerance in MTNR1B risk allele carriers: a randomized, cross-over study. Clin Nutr 37:1133–1140

    Article  CAS  PubMed  Google Scholar 

  21. Nakamura K, Tajiri E, Hatamoto Y, Ando T, Shimoda S, Yoshimura E (2021) Eating dinner early improves 24-h blood glucose levels and boosts lipid metabolism after breakfast the next day: a randomized cross-over trial. Nutrients 13:2424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Shea SA, Hilton MF, Orlova C, Ayers RT, Mantzoros CS (2005) Independent circadian and sleep/wake regulation of adipokines and glucose in humans. J Clin Endocrinol Metab 90:2537–2544

    Article  CAS  PubMed  Google Scholar 

  23. Saad A, Dalla MC, Nandy DK, Levine JA, Bharucha AE, Rizza RA, Basu R, Carter RE, Cobelli C, Kudva YC, Basu A (2012) Diurnal pattern to insulin secretion and insulin action in healthy individuals. Diabetes 61:2691–2700

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Jamshed H, Beyl RA, Della MD, Yang ES, Ravussin E, Peterson CM (2019) Early time-restricted feeding improves 24-hour glucose levels and affects markers of the circadian clock, aging, and autophagy in humans. Nutrients 11:1234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Flint A, Raben A, Blundell JE, Astrup A (2000) Reproducibility, power and validity of visual analogue scares in assessment of appetite sensations in single test meal studies. Int J Obesity 24:38–48

    Article  CAS  Google Scholar 

  26. Blundell J, de Graaf C, Hulshof T, Jebb S, Livingstone B, Lluch A, Mela D, Salah S, Schuring E, van der Knaap H, Westerterp M (2010) Appetite control: methodological aspects of the evaluation of foods. Obes Rev 11:251–270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Service FJ, Nelson RL (1980) Characteristics of glycemic stability. Diabetes Care 3:58–62

    Article  CAS  PubMed  Google Scholar 

  28. McDonnell CM, Donath SM, Vidmar SI, Werther GA, Cameron FJ (2005) A novel approach to continuous glucose analysis utilizing glycemic variation. Diabetes Technol Ther 7:253–263

    Article  CAS  PubMed  Google Scholar 

  29. Wolever TM (2004) Effect of blood sampling schedule and method of calculating the area under the curve on validity and precision of glycaemic index values. Br J Nutr 91:295–301

    Article  CAS  PubMed  Google Scholar 

  30. Matsuda M, DeFronzo RA (1999) Insulin sensitivity indices obtained from oral glucose tolerance testing: comparison with the euglycemic insulin clamp. Diabetes Care 22:1462–1470

    Article  CAS  PubMed  Google Scholar 

  31. Mishra S, Edwards H, Hedderley D, Podd J, Monro J (2017) Kiwifruit non-sugar components reduce glycaemic response to co-ingested cereal in humans. Nutrients 9:1195

    Article  PubMed  PubMed Central  Google Scholar 

  32. Wu T, Zhao BR, Bound MJ, Checklin HL, Bellon M, Little TJ, Young RL, Jones KL, Horowitz M, Rayner CK (2012) Effects of different sweet preloads on incretin hormone secretion, gastric emptying, and postprandial glycemia in healthy humans. Am J Clin Nutr 95:78–83

    Article  CAS  PubMed  Google Scholar 

  33. Akhavan T, Luhovyy BL, Panahi S, Kubant R, Brown PH, Anderson GH (2014) Mechanism of action of pre-meal consumption of whey protein on glycemic control in young adults. J Nutr Biochem 25:36–43

    Article  CAS  PubMed  Google Scholar 

  34. Wiedemann SJ, Rachid L, Illigens B, Böni-Schnetzler M, Donath MY (2020) Evidence for cephalic phase insulin release in humans: a systematic review and meta-analysis. Appetite 155:104792

    Article  PubMed  Google Scholar 

  35. Yaribeygi H, Farrokhi FR, Butler AE, Sahebkar A (2019) Insulin resistance: review of the underlying molecular mechanisms. J Cell Physiol 234:8152–8161

    Article  CAS  PubMed  Google Scholar 

  36. de Oliveira RC, Dos SPE, Camargo TM, Vinholes J, Rombaldi CV, Vizzotto M, Nora L (2019) Apple phenolic extracts strongly inhibit alpha-glucosidase activity. Plant Foods Hum Nutr 74:430–435

    Article  Google Scholar 

  37. Hanhineva K, Torronen R, Bondia-Pons I, Pekkinen J, Kolehmainen M, Mykkanen H, Poutanen K (2010) Impact of dietary polyphenols on carbohydrate metabolism. Int J Mol Sci 11:1365–1402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Yu K, Ke MY, Li WH, Zhang SQ, Fang XC (2014) The impact of soluble dietary fibre on gastric emptying, postprandial blood glucose and insulin in patients with type 2 diabetes. Asia Pac J Clin Nutr 23:210–218

    CAS  PubMed  Google Scholar 

  39. Choo VL, Viguiliouk E, Blanco MS, Cozma AI, Khan TA, Ha V, Wolever T, Leiter LA, Vuksan V, Kendall C, de Souza RJ, Jenkins D, Sievenpiper JL (2018) Food sources of fructose-containing sugars and glycaemic control: systematic review and meta-analysis of controlled intervention studies. BMJ 363:k4644

    Article  PubMed  PubMed Central  Google Scholar 

  40. Petersen KF, Laurent D, Yu C, Cline GW, Shulman GI (2001) Stimulating effects of low-dose fructose on insulin-stimulated hepatic glycogen synthesis in humans. Diabetes 50:1263–1268

    Article  CAS  PubMed  Google Scholar 

  41. Geidl-Flueck B, Gerber PA (2017) Insights into the hexose liver metabolism-glucose versus fructose. Nutrients 9:1206

    Article  Google Scholar 

  42. Cozma AI, Sievenpiper JL, de Souza RJ, Chiavaroli L, Ha V, Wang DD, Mirrahimi A, Yu ME, Carleton AJ, Di Buono M, Jenkins AL, Leiter LA, Wolever TM, Beyene J, Kendall CW, Jenkins DJ (2012) Effect of fructose on glycemic control in diabetes: a systematic review and meta-analysis of controlled feeding trials. Diabetes Care 35:1611–1620

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Yajima T, Takahashi H, Yasuda K (2020) Comparison of interstitial fluid glucose levels obtained by continuous glucose monitoring and flash glucose monitoring in patients with type 2 diabetes mellitus undergoing hemodialysis. J Diabetes Sci Technol 14:1088–1094

    Article  CAS  PubMed  Google Scholar 

  44. Chlup R, Jelenova D, Kudlova P, Chlupova K, Bartek J, Zapletalova J, Langova K, Chlupova L (2006) Continuous glucose monitoring a novel approach to the determination of the glycaemic index of foods (DEGIF 1)—determination of the glycaemic index of foods by means of the CGMS. Exp Clin Endocr Diab 114:68–74

    Article  CAS  Google Scholar 

  45. Morgan LM, Aspostolakou F, Wright J, Gama R (1999) Diurnal variations in peripheral insulin resistance and plasma non-esterified fatty acid concentrations: a possible link? Ann Clin Biochem 36(Pt 4):447–450

    Article  CAS  PubMed  Google Scholar 

  46. Malherbe C, Gasparo MD, Hertogh RD, Hoet JJ (1969) Circadian variations of blood sugar and plasma insulinlevels in man. Diabetologia 5:397

    Article  CAS  PubMed  Google Scholar 

  47. Nitta A, Imai S, Kajiyama S, Miyawaki T, Matsumoto S, Ozasa N, Kajiyama S, Hashimoto Y, Tanaka M, Fukui M (2019) Impact of different timing of consuming sweet snack on postprandial glucose excursions in healthy women. Diabetes Metab 45:369–374

    Article  CAS  PubMed  Google Scholar 

  48. Leung G, Huggins CE, Bonham MP (2019) Effect of meal timing on postprandial glucose responses to a low glycemic index meal: a crossover trial in healthy volunteers. Clin Nutr 38:465–471

    Article  CAS  PubMed  Google Scholar 

  49. Gu C, Brereton N, Schweitzer A, Cotter M, Duan D, Borsheim E, Wolfe RR, Pham LV, Polotsky VY, Jun JC (2020) Metabolic effects of late dinner in healthy volunteers-a randomized crossover clinical trial. J Clin Endocrinol Metab 105:2789

    Article  PubMed  PubMed Central  Google Scholar 

  50. Pellegrini M, Cioffi I, Evangelista A, Ponzo V, Goitre I, Ciccone G, Ghigo E, Bo S (2020) Effects of time-restricted feeding on body weight and metabolism. A systematic review and meta-analysis. Rev Endocr Metab Disord 21:17–33

    Article  PubMed  Google Scholar 

  51. Xie Z, Sun Y, Ye Y, Hu D, Zhang H, He Z, Zhao H, Yang H, Mao Y (2022) Randomized controlled trial for time-restricted eating in healthy volunteers without obesity. Nat Commun 13:1003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Bornet FR, Jardy-Gennetier AE, Jacquet N, Stowell J (2007) Glycaemic response to foods: impact on satiety and long-term weight regulation. Appetite 49:535–553

    Article  CAS  PubMed  Google Scholar 

  53. Clark MJ, Slavin JL (2013) The effect of fiber on satiety and food intake: a systematic review. J Am Coll Nutr 32:200–211

    Article  CAS  PubMed  Google Scholar 

  54. Scheer FA, Morris CJ, Shea SA (2013) The internal circadian clock increases hunger and appetite in the evening independent of food intake and other behaviors. Obesity (Silver Spring) 21:421–423

    Article  PubMed  Google Scholar 

  55. Sargent C, Zhou X, Matthews RW, Darwent D, Roach GD (2016) Daily rhythms of hunger and satiety in healthy men during one week of sleep restriction and circadian misalignment. Int J Environ Res Public Health 13:170

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We sincerely thank all the volunteers who participated for their time and corporation.

Funding

This research received no external funding.

Author information

Authors and Affiliations

Authors

Contributions

ZF and WZ formulated the research question. ZF, WZ and ZL designed the study. WZ, ZL, YW, AL, XL and XL carried out the research. WZ and ZL analyzed the data. WZ wrote the original draft and ZF revised the article.

Corresponding author

Correspondence to Zhihong Fan.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Ethical approval

This study was approved by the Ethics Committee of China Agricultural University (ethics number CAUHR-2021011) and registered on the Chinese Clinical Trial Registry (ChiCTR2100050541) on August 28th.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhao, W., Liu, Z., Fan, Z. et al. Apple preload increased postprandial insulin sensitivity of a high glycemic rice meal only at breakfast. Eur J Nutr 62, 1427–1439 (2023). https://doi.org/10.1007/s00394-022-03079-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00394-022-03079-4

Keywords

Navigation