The impact of food order on postprandial glycaemic excursions in prediabetes
Open accessAbstract
Data suggest that nutrient order during a meal significantly impacts postprandial glucose and insulin excursions in type 2 diabetes, while its effects in prediabetes have not been reported. Fifteen participants with prediabetes consumed the same meal on 3 days in random order: carbohydrate first, followed 10 minutes later by protein and vegetables (CF); protein and vegetables first, followed 10 minutes later by carbohydrate (PVF); or vegetables first followed by protein and carbohydrate (VF). Blood was sampled for glucose and insulin measurements at 0, 30, 60, 90, 120, 150 and 180 minutes. Incremental glucose peaks were similarly attenuated by >40% in the PVF and VF meal conditions compared with CF. The incremental area under the curve for glucose was 38.8% lower following the PVF meal order, compared with CF, and postprandial insulin excursions were significantly lower in the VF meal condition compared with CF. The CF meal pattern showed marked glycaemic variability whereas glucose levels were stable in the PVF and VF meal conditions. Food order presents a novel, simple behavioural strategy to reduce glycaemic excursions in prediabetes.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
6 of 7 cited sources checked · 5 supported · 0 flagged · accuracy not yet measured
- Premisecitation
In a prior crossover study of metformin-treated type 2 diabetes patients, eating protein and vegetables before carbohydrate lowered postprandial glucose excursions over 180 minutes compared with the reverse order.
“In a previous crossover study of metformin-treated subjects with T2DM, we demonstrated that ingestion of protein plus vegetables before carbohydrate led to lower postprandial glucose excursions over 180 min, compared to eating the same foods in the reverse order (13).”
Quote in the paperSubstantial claim1 of 1 sources checked- cites [13] source
- Premisecitation
In type 2 diabetes, the order in which nutrients are eaten during a meal has a significant effect on postprandial glucose and insulin excursions.
“Data suggest that nutrient order during a meal significantly impacts postprandial glucose and insulin excursions in type 2 diabetes, while its’ effects in prediabetes have not been reported.”
- Also stated in: § Introduction · plain
“Sequential nutrient ingestion is a novel strategy to attenuate the glycemic effect of a meal researched by our group and others in patients with type 2 diabetes (11–14).”
Quote in the paperSubstantial claim4 of 4 sources checked- cites [11] source
- cites [12] sourceExperimental — accuracy not yet measured
- cites [13] sourceExperimental — accuracy not yet measured
- cites [14] source
The Results (Glucose control variables; page unavailable) report significant reductions in postprandial glucose excursions with the food-order intervention in patients with type 2 diabetes. The Study design describes glucose monitoring but not insulin measurement; the Introduction discusses insulin secretion in relation to earlier preload studies. This paper therefore does not establish a significant effect of its meal-order intervention on postprandial insulin excursions. (LLM, conf=0.88)
Experimental — accuracy not yet measured
- Also stated in: § Introduction · plain
- Premisecitation
In that prior study, the carbohydrate-last pattern produced a lower insulin response than carbohydrate-first.
“Furthermore, we showed that the carbohydrate-last meal pattern stimulated a lower insulin response compared to consuming carbohydrate first.”
Quote in the paperSubstantial claim1 of 1 sources checked- cites [13] source
- Findingown data
The glucose iAUC0-180 was 38.8% lower after PVF than after CF (114.9±22.87 vs 187.8±30.79 mmol/L×180 min, p=0.008).
“Postprandial glucose levels were significantly decreased at 30 and 60 min (Figure 1), respectively, and the iAUC0–180 was 38.8% lower (114.9±22.87 vs 187.8±30.79 mmol/L×180 min, p=0.008) following the PVF meal order, compared with CF, the reverse meal order.”
Quote in the paperSubstantial claim - Findingown data
Postprandial glucose levels were significantly lower at 30 and 60 minutes after the PVF meal order compared with CF.
“Postprandial glucose levels were significantly decreased at 30 and 60 min (Figure 1), respectively, and the iAUC0–180 was 38.8% lower (114.9±22.87 vs 187.8±30.79 mmol/L×180 min, p=0.008) following the PVF meal order, compared with CF, the reverse meal order.”
Quote in the paperSubstantial claim
- Findingown data
In individuals with prediabetes, consuming carbohydrate at the end of the meal after protein and vegetables reduced iAUC and IGP compared with the reverse order.
“Similar to our previously reported findings in patients with T2DM (12,13), we found that consuming carbohydrate at the end of the meal after protein and vegetables reduced iAUC and IGP compared with the reverse order in individuals with prediabetes.”
Quote in the paperSubstantial claim - Findingown data
The VF meal order stimulated the least insulin response among the three meal conditions.
“Notably, the VF meal order stimulated the least insulin response among the three meal conditions, while the reductions in IGP and glucose iAUC (0–180) vs the CF meal condition were similar to the PVF meal order.”
Quote in the paperSubstantial claim - Findingown data
The incremental glucose peak was 45.8% lower for PVF than for CF (1.56±0.24 vs 2.88±0.31 mmol/L, p<0.001).
“IGP was 45.8% lower for the PVF meal order compared with CF (1.56±0.24 vs 2.88±0.31 mmol/L, p<0.001) and 43.1% lower for VF compared with CF (1.64±0.32 vs 2.88±0.31 mmol/L, p<0.001).”
- Also stated in: § Abstract · plain
“Incremental glucose peaks were similarly attenuated by >40% in the PVF and VF meal conditions compared with CF.”
Quote in the paperSubstantial claim - Also stated in: § Abstract · plain
- Findingown data
The incremental glucose peak was 43.1% lower for VF than for CF (1.64±0.32 vs 2.88±0.31 mmol/L, p<0.001).
“IGP was 45.8% lower for the PVF meal order compared with CF (1.56±0.24 vs 2.88±0.31 mmol/L, p<0.001) and 43.1% lower for VF compared with CF (1.64±0.32 vs 2.88±0.31 mmol/L, p<0.001).”
- Also stated in: § Abstract · plain
“Incremental glucose peaks were similarly attenuated by >40% in the PVF and VF meal conditions compared with CF.”
Quote in the paperSubstantial claim - Also stated in: § Abstract · plain
- Findingown data
The glucose iAUC0-180 was 23.4% lower after VF than after CF (143.8±34.5 vs 187.8±30.79 mmol/L×180 min, p=0.205).
“The VF meal pattern also showed reduced postprandial glucose levels at 30 and 60 min compared with CF and a decrease in iAUC0–180 of 23.4%(143.8±34.5 vs 187.8± 30.79 mmol/L×180 min, p=0.205).”
Quote in the paperNot a substantial claim - Findingown data
The CF meal order provoked symptoms of hypoglycemia in one participant, an adverse event not seen in the other meal conditions.
“In fact, the CF meal order provoked symptoms of hypoglycemia in one participant, an adverse event that was not observed in the other meal conditions.”
Quote in the paperNot a substantial claim - Findingown data
The VF meal pattern reduced postprandial glucose levels at 30 and 60 minutes compared with CF.
“The VF meal pattern also showed reduced postprandial glucose levels at 30 and 60 min compared with CF and a decrease in iAUC0–180 of 23.4%(143.8±34.5 vs 187.8± 30.79 mmol/L×180 min, p=0.205).”
Quote in the paperSubstantial claim - Findingreasoning
The insulin response was not significantly different between the PVF and CF meal conditions.
“However, the insulin response, albeit lower, was not significantly different between these meal conditions, likely due to limitations of sample size and greater heterogeneity in insulin secretory patterns in individuals with prediabetes.”
Quote in the paperSubstantial claim - Findingown data
Mean glucose concentrations were significantly lower in the CF condition than in both PVF and VF at 120, 150, and 180 minutes.
“Mean glucose concentrations were significantly lower in the CF meal condition compared to both PVF and VF at 120, 150 and 180 mins.”
Quote in the paperSubstantial claim - Study design and conductnone given
Baseline fasting glucose concentrations were similar across the three meal conditions.
“Baseline fasting glucose concentrations were similar in the three meal conditions.”
Quote in the paperNot a substantial claim - Interpretationown data
The VF food order required the least insulin to dispose of the same amount of carbohydrate.
“Compared with the CF meal order, both VF and PVF meal orders attenuated postprandial glucose peaks similarly, with the VF food order requiring the least insulin to dispose the same amount of carbohydrate.”
Quote in the paperSubstantial claim- Rests on an assumption: Participants maintained their usual physical activity and diet throughout the study, especially the day before each visit.
- Rests on an assumption: The small amounts of spices, herbs, and vinegar in the test meal had only minor effects on postprandial glucose and insulin.
- Interpretationreasoning
The lack of a significant difference in insulin response is likely due to sample size limitations and greater heterogeneity in insulin secretory patterns in prediabetes.
“However, the insulin response, albeit lower, was not significantly different between these meal conditions, likely due to limitations of sample size and greater heterogeneity in insulin secretory patterns in individuals with prediabetes.”
Quote in the paperSubstantial claim - Interpretationown data
Food order is a novel, simple behavioral strategy to attenuate glycemic excursions in prediabetes.
“In conclusion, food order presents a novel, simple behavioral strategy to attenuate glycemic excursions in prediabetes.”
- Also stated in: § Abstract · plain
“Food order presents a novel, simple behavioral strategy to reduce glycemic excursions in prediabetes.”
Quote in the paperSubstantial claim- Rests on an assumption: Participants maintained their usual physical activity and diet throughout the study, especially the day before each visit.
- Rests on an assumption: The small amounts of spices, herbs, and vinegar in the test meal had only minor effects on postprandial glucose and insulin.
- Also stated in: § Abstract · plain
- Interpretationreasoning
The effects are plausibly mediated by slowed carbohydrate absorption due to fiber and fat in the VF meal order.
“These effects are plausibly mediated by slowed carbohydrate absorption due to the effects of fiber and fat in the VF meal order, although more work is needed to clearly delineate these mechanisms.”
Quote in the paperSubstantial claim - Interpretationcitation
Food order is an alternative strategy that could mitigate the metabolic effects of carbohydrate.
“Food order is an alternative strategy that could mitigate the metabolic effects of carbohydrate (15).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [15] source
- Rests on an assumption: Participants maintained their usual physical activity and diet throughout the study, especially the day before each visit.
- Rests on an assumption: The small amounts of spices, herbs, and vinegar in the test meal had only minor effects on postprandial glucose and insulin.
- Study design and conductreasoning
Because HbA1c was used as the inclusion diagnostic criterion, the effects of food order in individuals with impaired fasting glucose and/or impaired glucose tolerance cannot be distinguished.
“We used HbA1c as the diagnostic criteria for inclusion in the study, therefore the effects of food order in individuals with impaired fasting glucose (IFG) and/or impaired glucose tolerance (IGT) cannot be distinguished.”
Quote in the paperSubstantial claim - Interpretationown data
When calorie intake and macronutrient composition are controlled, changing the order of nutrient intake during a meal significantly affects postprandial glucose and insulin excursions in people with prediabetes.
“In this study, we demonstrate that controlling for calorie intake and macronutrient composition, manipulation of nutrient order during a meal significantly impacts postprandial glucose and insulin excursions in individuals with prediabetes.”
Quote in the paperSubstantial claim- Rests on an assumption: Participants maintained their usual physical activity and diet throughout the study, especially the day before each visit.
- Rests on an assumption: The small amounts of spices, herbs, and vinegar in the test meal had only minor effects on postprandial glucose and insulin.
- Interpretationown data
Compared with CF, both VF and PVF meal orders attenuated postprandial glucose peaks to a similar degree.
“Compared with the CF meal order, both VF and PVF meal orders attenuated postprandial glucose peaks similarly, with the VF food order requiring the least insulin to dispose the same amount of carbohydrate.”
Quote in the paperSubstantial claim- Rests on an assumption: Participants maintained their usual physical activity and diet throughout the study, especially the day before each visit.
- Rests on an assumption: The small amounts of spices, herbs, and vinegar in the test meal had only minor effects on postprandial glucose and insulin.
- May combine two claims. 9
- Classified as probably not a substantial claim. 10
- The quote only partly states this claim. 1
May combine two claims.
Findingown dataThe incremental glucose peak and glucose iAUC0-180 were similar between the PVF and VF meal conditions.
“IGP and iAUC0–180 were similar between the PVF and VF meal conditions.”
- Also stated in: § Conclusions · plain
“Notably, the VF meal order stimulated the least insulin response among the three meal conditions, while the reductions in IGP and glucose iAUC (0–180) vs the CF meal condition were similar to the PVF meal order.”
Quote in the paperSubstantial claim- Also stated in: § Conclusions · plain
May combine two claims.
Findingown dataThe VF meal produced lower insulin excursions, with insulin iAUC0-180 43.8% lower than CF (54,116.7±7310.6 vs 96,382.1±21,909.8 pmol/L×180 min, p=0.03).
“The VF meal resulted in lower insulin excursions; iAUC0–180 was 43.8% lower compared with CF (54,116.7±7310.6 vs 96,382.1±21,909.8 pmol/L×180 min, p=0.03).”
- Also stated in: § Abstract · plain
“postprandial insulin excursions were significantly lower in the VF meal condition compared to CF.”
Quote in the paperSubstantial claim- Also stated in: § Abstract · plain
May combine two claims.
Findingown dataThe CF meal pattern showed marked glycemic variability with a peak at 60 minutes and a nadir at 180 minutes, while glucose levels were stable in the other meal conditions.
“Overall, the CF meal pattern demonstrated marked glycemic variability with a peak at 60 min and a nadir at 180 min, whereas glucose levels were stable in other meal conditions.”
- Also stated in: § Abstract · plain
“The CF meal pattern demonstrated marked glycemic variability whereas glucose levels were stable in the PVF and VF meal conditions.”
Quote in the paperSubstantial claim- Also stated in: § Abstract · plain
May combine two claims.
Findingown dataThe insulin iAUC0-180 after PVF was lower but not significantly different from CF (74,428.5±10,739.3 vs 96,382.1±21,909.8 pmol/L×180 min, p=0.44).
“The iAUC0–180 in the PVF meal condition was lower, albeit not significantly different compared with CF (74,428.5±10,739.3 vs 96,382.1±21,909.8 pmol/L ×180 min, p=0.44).”
Quote in the paperNot a substantial claimClassified as probably not a substantial claim.
Study design and conductnone givenThe experimental meal conditions were randomly assigned using research randomizer.
“under the following experimental conditions that were randomly assigned using research randomizer”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductnone givenParticipants were closely monitored to ensure they consumed the test meals entirely within the allotted time.
“Participants were closely monitored to ensure that the test meals were consumed in their entirety within the allotted time.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing). The quote only partly states this claim.
Study design and conductown dataSensitivity analysis excluding the participant with missing VF data did not change the significance of the results.
“Furthermore, on performing sensitivity analyses by excluding this participant, the significance of the results did not change.”
Quote in the paperNot a substantial claimClassified as probably not a substantial claim.
Study design and conductreasoningWith 15 subjects, the study had 80% power to detect a mean paired difference of 0.84 mmol/L in incremental glucose peak at an alpha of 0.05, assuming a standard deviation of differences of 1.1 mmol/L.
“Therefore, with 15 subjects enrolled, we would have 80% power to detect a mean of paired differences of 0.84 mmol/L in IGP (30% of 2.8) at an alpha level of 0.05, assuming a standard deviation of differences of 1.1 mmol/L.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductnone givenPlasma insulin was measured with quantitative immunoradiometric assay kits from Millipore, with intra-assay and inter-assay coefficients of variation of ≤4.4% and ≤6.0%.
“The plasma concentrations of insulin were determined using quantitative immunoradiometric assay kits from Millipore (St. Charles, Missouri, USA). The intra-assay and inter-assay coefficients of variation were ≤4.4% and ≤6.0%.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
Study design and conductnone givenWhole-blood glucose was measured with a quantitative enzymatic photometry cassette from Alere, with intra-assay and inter-assay coefficients of variation of ≤6.2% and ≤5.0%.
“Glucose concentrations were assessed in whole blood using a quantitative enzymatic photometry cassette from Alere (San Diego, California, USA). The intra-assay and inter-assay coefficients of variation were ≤6.2% and ≤5.0%, respectively.”
Quote in the paperNot a substantial claimClassified as probably not a substantial claim. May combine two claims.
Study design and conductown dataThe study used a within-subjects crossover design in which all participants ate isocaloric meals of identical composition on three separate days, one week apart, after a 12-hour overnight fast.
“We used a within-subjects crossover design in which all participants consumed isocaloric meals (Table 1) with exactly the same composition, on three separate days, 1 week apart, after a 12 hour overnight fast.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing). May combine two claims.
Study design and conductnone givenThe stringent study design and the use of meals and meal interventions that simulate real-world eating behavior are strengths of the study.
“The stringent study design and the use of meals and meal interventions that simulate real world eating behavior are strengths of our study.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
Study design and conductreasoningSpices, herbs, and vinegar were added to the meal for palatability and to mimic a regularly consumed meal; although the amounts were small, they may have minor effects on postprandial glucose and insulin.
“In designing the meal we used spices, herbs and vinegar in addition to macronutrients to improve palatability and replicate a meal that people regularly consume. Although the amounts used were small, they may have effects on postprandial glucose and insulin, albeit minor.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
Study design and conductnone givenThe study has limitations including a small sample and unclear generalizability to postprandial meal conditions.
“Our study has limitations including the small sample and unclear generalizability to postprandial meal conditions.”
Quote in the paperNot a substantial claim
The paper relies on this without support.
Participants maintained their usual physical activity and diet throughout the study, especially the day before each visit.
“Participants were counseled to maintain their usual level of physical activity and diet throughout the study period and in particular the day prior to each study visit.”
The paper relies on this without support.
The small amounts of spices, herbs, and vinegar in the test meal had only minor effects on postprandial glucose and insulin.
“Although the amounts used were small, they may have effects on postprandial glucose and insulin, albeit minor.”
Cites
Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin
(2002) · New England Journal of Medicine · doi:10.1056/nejmoa012512 · Cited by 19,011 · see citing works
Lindström, J., Ilanne-Parikka, P., Peltonen, M., Aunola, S., Eriksson, J. G., Hemiö, K., Hämäläinen, H., Härkönen, P., Keinänen-Kiukaanniemi, S., Laakso, M., et al. (2006) · The Lancet · doi:10.1016/s0140-6736(06)69701-8 · Cited by 1,799 · see citing works
Li, G., Zhang, P., Wang, J., Gregg, E. W., Yang, W., Gong, Q., Li, H., Li, H., Jiang, Y., An, Y., et al. (2008) · The Lancet · doi:10.1016/s0140-6736(08)60766-7 · Cited by 1,600 · see citing works
Barr, E. L. M., Zimmet, P. Z., Welborn, T. A., Jolley, D., Magliano, D. J., Dunstan, D. W., Cameron, A. J., Dwyer, T., Taylor, H. R., Tonkin, A. M., et al. (2007) · Circulation · doi:10.1161/circulationaha.106.685628 · Cited by 719 · see citing works
Diabetes Prevention Program Research Group (2007) · Diabetic Medicine · doi:10.1111/j.1464-5491.2007.02043.x · Cited by 363 · see citing works
Relation between blood glucose and coronary mortality over 33 years in the Whitehall Study
Brunner, E. J., Shipley, M. J., Witte, D. R., Fuller, J. H., & Marmot, M. G. (2006) · Diabetes Care · doi:10.2337/diacare.29.01.06.dc05-1405 · Cited by 166 · see citing works
Food Order Has a Significant Impact on Postprandial Glucose and Insulin Levels
Shukla, A. P., Iliescu, R. G., Thomas, C. E., & Aronne, L. J. (2015) · Diabetes Care · doi:10.2337/dc15-0429 · Cited by 104 · see citing works
Self-citationWu, J.-S., Yang, Y.-C., Lin, T.-S., Huang, Y.-H., Chen, J.-J., Lu, F.-H., Wu, C.-H., & Chang, C.-J. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2006-2175 · Cited by 98 · see citing works
Carbohydrate-last meal pattern lowers postprandial glucose and insulin excursions in type 2 diabetes
Shukla, A. P., Andono, J., Touhamy, S. H., Casper, A., Iliescu, R. G., Mauer, E., Shan Zhu, Y., Ludwig, D. S., & Aronne, L. J. (2017) · BMJ Open Diabetes Research & Care · doi:10.1136/bmjdrc-2017-000440 · Cited by 96 · cited 1× · see citing works
“postprandial glucose excursions over 180 minutes, compared with eating the same foods in the reverse order.(13) Furthermore, we showed that the carbohydrate-last meal pattern stimulated a lower”
BackgroundSelf-citationNoninvasive evaluation of neural impairment in subjects with impaired glucose tolerance
Putz, Z., Tabák, A. G., Tóth, N., Istenes, I., Németh, N., Gandhi, R. A., Hermányi, Z., Keresztes, K., Jermendy, G., Tesfaye, S., et al. (2009) · Diabetes Care · doi:10.2337/dc08-1406 · Cited by 90 · see citing works
Imai, S., Fukui, M., & Kajiyama, S. (2014) · Journal of Clinical Biochemistry and Nutrition · doi:10.3164/jcbn.13-67 · Cited by 81 · see citing works
Tricò, D., Filice, E., Trifirò, S., & Natali, A. (2016) · Nutrition & Diabetes · doi:10.1038/nutd.2016.33 · Cited by 47 · see citing works
The challenge of meeting prescribed carbohydrate intake goals in low-carbohydrate diet studies
Orloff, J. N., Aronne, L. J., & Shukla, A. P. (2018) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/nqy023 · Cited by 2 · cited 1× · see citing works
“Food order is an alternative strategy that could mitigate the metabolic effects of carbohydrate.(15) Similar to our previously reported findings in patients with type 2 diabetes,(12,13) we found that consuming carbohydrate at the end of the meal after protein and vegetables reduced iAUC and IGP compared with the rever…”
ResultSelf-citation
Flagged first, then by citations
Research works printed but not linked: 2
- U.S. Department of Health and Human Services, 2014, Estimates of Diabetes and its Burden in the United States. Centers for Disease Control and Prevention National Diabetes Statistics Report
- Aguirre F, 2013, IDF Diabetes Atlas
Cited by
Sorted by citations
The carbohydrate-insulin model: A physiological perspective on the obesity pandemic
Ludwig, D. S., Aronne, L. J., Astrup, A., de Cabo, R., Cantley, L. C., Friedman, M. I., Heymsfield, S. B., Johnson, J. D., King, J. C., Krauss, R. M., et al. (2021) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/nqab270 · Cited by 292 · see citing works
“, fructose (49–52), protein and fatty acid type, fiber, food order within a meal (53)], behaviors [e.”
BackgroundSelf-citationGlycemic variability: adverse clinical outcomes and how to improve it?
Zhou, Z. G., Sun, B., Huang, S., Zhu, C., & Bian, M. (2020) · Cardiovascular Diabetology · doi:10.1186/s12933-020-01085-6 · Cited by 257 · see citing works
Effects of a personalized nutrition program on cardiometabolic health: a randomized controlled trial
Bermingham, K. M., Linenberg, I., Polidori, L., Asnicar, F., Arrè, A., Wolf, J., Badri, F., Bernard, H., Pujol, J. C., Bulsiewicz, W. J., et al. (2024) · Nature Medicine · doi:10.1038/s41591-024-02951-6 · Cited by 173 · see citing works
“Food and meal order, including consuming carbohydrates before protein and vegetables in a meal, contributes to elevated glycemic variability 42 .”
Competing paradigms of obesity pathogenesis: energy balance versus carbohydrate-insulin models
Ludwig, D. S., Apovian, C. M., Aronne, L. J., Astrup, A. V., Cantley, L. C., Ebbeling, C. B., Heymsfield, S. B., Johnson, J. D., King, J. C., Krauss, R. M., et al. (2022) · European Journal of Clinical Nutrition · doi:10.1038/s41430-022-01179-2 · Cited by 118 · see citing works
“In addition to GL, the CIM provides a conceptual framework for understanding how other dietary factors, behaviors and environmental exposures may affect body weight through metabolic mechanisms rather than primary effects on energy intake or expenditure; these include fructose [37–40], protein amount [41], fatty acid…”
BackgroundSelf-citationNutritional Strategies for the Management of Type 2 Diabetes Mellitus: A Narrative Review
Minari, T. P., Tácito, L. H. B., Yugar, L. B. T., Ferreira‐Melo, S. E., Manzano, C. F., Pires, A. C., Moreno, H., Vilela-Martin, J. F., Cosenso‐Martin, L. N., & Yugar‐Toledo, J. C. (2023) · Nutrients · doi:10.3390/nu15245096 · Cited by 75 · see citing works
“Therefore, individuality must be taken into consideration when creating a dietary prescription, especially for T2DM patients who continuously monitor their blood glucose levels [45,46].”
BackgroundGuideline for the Management of Diabetes Mellitus in the Elderly in China (2024 Edition)
Guo, L., & Xiao, X. (2024) · Aging Medicine · doi:10.1002/agm2.12294 · Cited by 65 · see citing works
“33 For older diabetes mellitus patients with long-term imbal - anced diet, attention should also be paid to supplementation of vitamins and minerals.”
BackgroundSun, L., Goh, H. J., Govindharajulu, P., Leow, M. K., & Henry, C. J. (2019) · Clinical Nutrition · doi:10.1016/j.clnu.2019.04.001 · Cited by 61 · see citing works
“[32] Shukla AP, Dickison M, Coughlin N, Karan A, Mauer E, Truong W, et al.”
Nesti, L., Mengozzi, A., & Tricò, D. (2019) · Frontiers in Endocrinology · doi:10.3389/fendo.2019.00144 · Cited by 53 · see citing works
“Furthermore, preload-based diets are of particular interest in clinical settings in which available pharmacological options are limited, including type 1 diabetes (47) and gestational diabetes (29), or not costeffective, such as in the large number of individuals at high risk to develop T2D (18, 43).”
BackgroundSignificance of Glycemic Variability in Diabetes Mellitus
Kusunoki, Y., Konishi, K., Tsunoda, T., & Koyama, H. (2022) · Internal Medicine · doi:10.2169/internalmedicine.8424-21 · Cited by 40 · see citing works
“and exercise therapies are useful for GV suppression (82, 83); however, drug therapy is also quite effective.”
BackgroundThe Future of Shift Work: Circadian Biology Meets Personalised Medicine and Behavioural Science
Potter, G. D., & Wood, T. R. (2020) · Frontiers in Nutrition · doi:10.3389/fnut.2020.00116 · Cited by 40 · see citing works
Kang, J., Shi, X., Fu, J., Li, H., Ma, E., & Chen, W. (2022) · Nutrients · doi:10.3390/nu14224734 · Cited by 35 · see citing works
“Behavioral interventions, such as going to sleep early [38,39], eating an average frequency of 5 times a day [40], avoiding prolonged periods of sitting [41] and eating vegetables and protein first [42], were also advised to develop healthy habits.”
BackgroundLeahy, J. L., Aleppo, G., Fonseca, V. A., Garg, S. K., Hirsch, I. B., McCall, A. L., McGill, J. B., & Polonsky, W. H. (2019) · Journal of the Endocrine Society · doi:10.1210/js.2019-00222 · Cited by 38 · see citing works
Hengist, A., Ong, J. A., McNeel, K., Guo, J., & Hall, K. D. (2024) · American Journal of Clinical Nutrition · doi:10.1016/j.ajcnut.2024.10.007 · Cited by 38 · see citing works
Manipulation of Post-Prandial Hyperglycaemia in Type 2 Diabetes: An Update for Practitioners
Shibib, L., Al-Qaisi, M., Guess, N. D., Miras, A. D., Greenwald, S. E., Pelling, M., & Ahmed, A. (2024) · Diabetes Metabolic Syndrome and Obesity · doi:10.2147/dmso.s458894 · Cited by 39 · see citing works
“Data from several studies 164–166 in patients with pre-diabetes and type 2 diabetes suggested that nutrient order and consuming carbohydrates last could reduce post-prandial glucose and insulin peaks by more than 40%.”
BackgroundImai, S., Kajiyama, S., Kitta, K., Miyawaki, T., Matsumoto, S., Ozasa, N., Kajiyama, S., Hashimoto, Y., & Fukui, M. (2023) · Nutrients · doi:10.3390/nu15051174 · Cited by 31 · see citing works
Dietary Control of Inflammation and Resolution
Sears, B., & Saha, A. (2021) · Frontiers in Nutrition · doi:10.3389/fnut.2021.709435 · Cited by 22 · see citing works
“Eating protein before consuming carbohydrates generates more significant glycemic control in type 2 diabetic subjects than consuming carbohydrates first before protein (82, 83).”
BackgroundChukir, T., Mandel, L., Tchang, B. G., Al-Mulla, N. A., Igel, L. I., Kumar, R. B., Waitman, J. A., Aronne, L. J., & Shukla, A. P. (2020) · Obesity Research & Clinical Practice · doi:10.1016/j.orcp.2020.12.005 · Cited by 28 · see citing works
Self-citationMinari, T. P., Manzano, C. F., Tácito, L. H. B., Yugar, L. B. T., Sedenho‐Prado, L. G., Rubio, T. D. A., Pires, A. C., Vilela-Martin, J. F., Cosenso‐Martin, L. N., Moreno, H., et al. (2024) · Nutrients · doi:10.3390/nu16091378 · Cited by 29 · see citing works
Iizuka, K. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222112058 · Cited by 32 · see citing works
Gut-Based Strategies to Reduce Postprandial Glycaemia in Type 2 Diabetes
Kamruzzaman, M., Horowitz, M., Jones, K. L., & Marathe, C. S. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2021.661877 · Cited by 23 · see citing works
“For example, initial ingestion of non-carbohydrate macronutrients and ingestion of carbohydrates last has been reported to be effective in reducing postprandial glucose excursions among individuals with type 2 diabetes and impaired or normal glucose tolerance (64, 89).”
BackgroundFive Evidence-Based Lifestyle Habits People With Diabetes Can Use
Chacko, E., & Signore, C. (2020) · Clinical Diabetes · doi:10.2337/cd19-0078 · Cited by 15 · see citing works
“Research has also provided data showing the glycemia benefit of eating protein or protein and vegetables before eating the carbohydrate portion of a meal (22,23).”
BackgroundImpact of low-starch high-fiber pasta on postprandial blood glucose
Oba‐Yamamoto, C., Takeuchi, J., Nakamura, A., Nomoto, H., Kameda, H., Cho, K. Y., Atsumi, T., & Miyoshi, H. (2021) · Nutrition Metabolism and Cardiovascular Diseases · doi:10.1016/j.numecd.2021.10.019 · Cited by 16 · see citing works
“A variety of methods to suppress increases in postprandial plasma glucose concentrations have been reported, including intake of vegetables and proteins/lipids before carbohydrates [13,17,18].”
BackgroundChanging Meal Sequence Affects Glucose Excursions in Gestational Diabetes Mellitus
Yong, G., Jing, Q., Yao, Q., Yang, K., & Ye, X. (2022) · Journal of Diabetes Research · doi:10.1155/2022/7083106 · Cited by 11 · see citing works
AGP and Nutrition – Analysing postprandial glucose courses with CGM
Kröger, J., Siegmund, T., Schubert-Olesen, O., Keuthage, W., Lettmann, M., Richert, K., & Pfeiffer, A. F. H. (2021) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2021.108738 · Cited by 11 · see citing works
Ordered Eating and Its Effects on Various Postprandial Health Markers: A Systematic Review
Ferguson, B. K., & Wilson, P. B. (2022) · Journal of the American Nutrition Association · doi:10.1080/27697061.2022.2161664 · Cited by 11 · see citing works
Qin, Y., Aqeel, M. M., Zhu, F. M., Delp, E. J., & Eicher‐Miller, H. A. (2021) · Nutrients · doi:10.3390/nu13041179 · Cited by 9 · see citing works
Tang, Y., Chen, Y., Zhou, Y., Wu, B., Zhang, S., Gong, Y., & Ni, Q. (2025) · Frontiers in Nutrition · doi:10.3389/fnut.2025.1557923 · Cited by 11 · see citing works
“Elderly diabetic patients are at higher risk of malnutrition, sarcopenia, and frailty compared to their non-diabetic peers (47).”
Dimova, R. B., Chakarova, N. Y., Prato, S. D., & Tankova, T. I. (2023) · Journal of Nutrition · doi:10.1016/j.tjnut.2023.03.007 · Cited by 9 · see citing works
Mishra, S. S., McLaughlin, A., & Monro, J. A. (2023) · Nutrients · doi:10.3390/nu15143269 · Cited by 8 · see citing works
“Recent studies have shown that the order in which foods are consumed in a meal affects the glycaemic response and appetite and conclude that the ingestion of foods high in available carbohydrates should be concentrated towards the end of a meal [12,13].”
BackgroundKida, S., Aoyama, N., Fujii, T., Taniguchi, K., Yata, T., Iwane, T., Yamamoto, T., Tamaki, K., Minabe, M., & Komaki, M. (2023) · Nutrients · doi:10.3390/nu15112602 · Cited by 8 · see citing works
“The meal sequence of eating vegetables and proteins before carbohydrates is gaining attention as a healthier eating habit for people with type 2 diabetes [2,3].”
BackgroundEfficacy of a meal sequence in patients with type 2 diabetes: a systematic review and meta-analysis
Okami, Y., Tsunoda, H., Watanabe, J., & Kataoka, Y. (2022) · BMJ Open Diabetes Research & Care · doi:10.1136/bmjdrc-2021-002534 · Cited by 9 · see citing works
Ashwini, K., Abirami, K., Gayathri, R., Sasikala, S., Sudha, V., Shobana, S., Jeevan, R. G., Krishnaswamy, K., Deepika, V., Rajalakshmi, M., et al. (2025) · Journal of Nutrition · doi:10.1016/j.tjnut.2024.12.005 · Cited by 7 · see citing works
A Randomized Controlled Pilot Study of the Food Order Behavioral Intervention in Prediabetes
Shukla, A. P., Karan, A., Hootman, K. C., Graves, M., Steller, I., Abel, B., Giannita, A., Tils, J., Hayashi, L., O’Connor, M., et al. (2023) · Nutrients · doi:10.3390/nu15204452 · Cited by 7 · see citing works
“Furthermore, the glycemic effects of a carbohydrate-last food order were replicated in a subsequent study in individuals with prediabetes [18].”
BackgroundSelf-citationHengist, A., Ong, J. A., McNeel, K., Guo, J., & Hall, K. D. (2023) · medRxiv · doi:10.1101/2023.06.14.23291406 · Cited by 5 · see citing works
Kesavadev, J., Mohan, V. B., Joshi, S., Saboo, B., Chawla, M. S., Unnikrishnan, A. G., Lakhani, O., Gupta, A., PARIKH, R. M., Bhograj, A., et al. (2026) · Diabetes Therapy · doi:10.1007/s13300-026-01842-y · Cited by 9 · see citing works
“The resulting sharp post-prandial glucose excursions and higher insulin doses can also pose a risk of hypoglycaemia, especially in people following traditional meal patterns [47].”
Indarto, D., Rochmah, D. N., Wiboworini, B., Pratama, Y. M., & Wibowo, Y. C. (2022) · International Journal of Preventive Medicine · doi:10.4103/ijpvm.ijpvm_704_20 · Cited by 6 · see citing works
“International Journal of Preventive Medicine 2022, 13: 144 2 [10‐12] Growing evidence also indicates that the consumption of vegetables before carbohydrate decreases post prandial glucose and insulin levels and up‐regulates GLP‐1 secretion in healthy people,[13] pre diabetes patients[14] and T2DM patients.”
BackgroundIndarto, D., Dwipajati, D., Dirgahayu, P., Wibowo, Y. C., & Pratama, Y. M. (2022) · Journal of Obesity · doi:10.1155/2022/4875993 · Cited by 5 · see citing works
Wang, S., Song, S., Gao, J., Wu, W., Fu, Y., Yuan, T., & Zhao, W. (2025) · Journal of Nutrition · doi:10.1016/j.tjnut.2025.09.023 · Cited by 4 · see citing works
Deguchi, K., Aoshima, M., Hiraiwa, E., Ono, C., Ushiroda, C., Yamamoto-Wada, R., Yoshida, M., & Iizuka, K. (2025) · Nutrients · doi:10.3390/nu17091576 · Cited by 3 · see citing works
Methods of lowering the glycemic index of food and their underlying mechanisms - a review
Sornek, P., Izdebska, W., Stanek, J., Perkowska, K., Kaźmierczak, A., Mich, A., Pawlak, I., Borkowska, A., Ciesielski, R., & Kiełb, A. (2024) · Quality in Sport · doi:10.12775/qs.2024.20.54118 · Cited by 3 · see citing works
Pafili, Z., & Dimosthenopoulos, C. (2021) · HORMONES · doi:10.1007/s42000-021-00314-1 · Cited by 4 · see citing works
Lee, C. L., Shyam, S., Lee, Z. Y., & Tan, J. L. (2020) · Nutrition and Health · doi:10.1177/0260106020975573 · Cited by 3 · see citing works
“…during a meal produced a steadier PPG excursion, as compared with using a carbohydrate first/ protein last or composite eating strategy during a meal (Imai et al., 2013; Kuwata et al., 2016; Nishino et al., 2018; Shukla et al., 2017; Shukla et al., 2019; Sun et al., 2019; Tricò et al., 2016).”
BackgroundMethodHiguchi, Y., Miyawaki, T., Kajiyama, S., Kitta, K., Kajiyama, S., Hashimoto, Y., Fukui, M., & Imai, S. (2025) · Nutrients · doi:10.3390/nu17203194 · Cited by 2 · see citing works
“The attenuated postprandial glucose excursions observed in this study are likely attributable to the prescribed food order: vegetables first, protein second, and carbohydrates last [4–8].”
Kurotobi, Y., Kuwata, H., Matsushiro, M., Omori, Y., Imura, M., Nakatani, S., Matsubara, M., Haraguchi, T., Moyama, S., Hamamoto, Y., et al. (2025) · Nutrients · doi:10.3390/nu17040658 · Cited by 3 · see citing works
“A previous study of prediabetics reported that eating chicken and vegetables for 10 min, followed by a 10 min rest interval and then eating bread (carbohydrates) elicited less post-meal glucose compared with the reverse order [21].”
Dietary Habit and Oral Condition
Aoyama, N., Kida, S., Yata, T., Takase, M., Fujii, T., Sugihara, S., Hirata, T., Taniguchi, K., & Komaki, M. (2024) · Current Oral Health Reports · doi:10.1007/s40496-024-00387-y · Cited by 2 · see citing works
“…of the various dietary habits that may be beneficial to health is the meal sequence of eating vegetables and proteins before carbohydrates, which control postpran‑ dial blood glucose elevation and reduces the incidence of obesity in patients with type 2 diabetes and healthy indi‑ viduals [20–22].”
Kwok, A., Dordevic, A. L., & Truby, H. (2023) · Food Science & Nutrition · doi:10.1002/fsn3.3902 · Cited by 2 · see citing works
“In adults with prediabetes, consumption of protein prior to carbohydrates decreases postprandial glucose iAUC compared with consuming carbohydrates first for the same meal composition (Shukla et al., 2019).”
BackgroundLiu, Y., Jiang, H., Ruan, B., Liu, Y., Le, S., Fu, X., & Wang, S. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2022.925870 · Cited by 2 · see citing works
Wu, Y., Fan, Z., Lou, X., Zhao, W., Lu, X., Hu, J., Han, Y., & Liu, A. (2022) · Nutrients · doi:10.3390/nu14071318 · Cited by 2 · see citing works
AGP und Ernährung – Mit CGM postprandiale Glukoseverläufe analysieren
Kroeger, J., Siegmund, T., Schubert, O., Keuthage, W., Lettmann, M., Richert, K., & Pfeiffer, A. F. H. (2021) · Diabetologie und Stoffwechsel · doi:10.1055/a-1310-2736 · Cited by 2 · see citing works
“[70] Shukla AP, Dickison M, Coughlin N et al.”
BackgroundSavkin, A. V., & Feng, X. (2026) · IET Control Theory and Applications · doi:10.1049/cth2.70113 · Cited by 2 · see citing works
Dwipajati, D., & Kaswari, S. R. T. (2024) · Amerta Nutrition · doi:10.20473/amnt.v8i1.2024.58-66 · Cited by 2 · see citing works
Akoko, S., & Nwaogwugwu, A. Q. (2023) · Saudi Journal of Biomedical Research · doi:10.36348/sjbr.2023.v08i07.003 · Cited by 1 · see citing works
Rice: Prevention and Management of Type 2 Diabetes and Coronary Heart Disease
Bergman, C. J. (2020) · Springer eBooks · doi:10.1007/978-3-030-37510-2_9 · Cited by 1 · see citing works
Effect of Nutrient Preload and Food Order on Glucose, Insulin, and Gut Hormones
Bae, J. H., & Cho, Y. M. (2018) · Journal of Korean Diabetes · doi:10.4093/jkd.2018.19.4.193 · Cited by 1 · see citing works
“당뇨병 전단계인 사람이 단백질과 채소 또는 채소만을 탄수화물보다 먼저 섭취하면 반대의 경우에 비해 식후 혈당 이 개선되었고, 채소만 먼저 섭취한 경우에는 식후 혈중 총 인슐린 수치도 감소하였다[39].”
Kampmann-Gongoll, K., Schlesinger, S., Noreik, M., Kuß, O., & Lang, A. (2026) · Clinical Nutrition · doi:10.1016/j.clnu.2026.106775
Choi, M., Lee, S. M., Bang, E., Seo, I., Lee, J., Joo, S., Kim, H., Ahn, S. V., Kim, Y., & Oh, J. (2026) · Diabetes Obesity and Metabolism · doi:10.1111/dom.71227
Channappa, M., Shukla, S., Damle, A., et al. (2026) · Cureus · doi:10.7759/cureus.111407
Modifiable Factors Affecting the Postprandial Glycemic Response
Wu, Y., McLaughlin, T., Gorgani, S., Scheideman, A. F., Shao, M. M., Hislop, B. D., Hoang, K., Perelman, D., McGinity, C., Rodgar, M., et al. (2026) · Journal of Diabetes Science and Technology · doi:10.1177/19322968261418614 · Cited by 1 · see citing works
“29,30 Behavioral factors, such as meal timing 31 and stress levels, 32 have also been shown to impact GE rate significantly, but interventional studies harnessing these factors remain limited.”
Wada, I. Y., Tanaka, S., Watanabe, C., Shimokawa, K., & Ishii, F. (2025) · Drug Discoveries & Therapeutics · doi:10.5582/ddt.2025.01099
Park, J., & Kim, M. S. (2025) · Journal of Korean Biological Nursing Science · doi:10.7586/jkbns.25.011
“Managing these variables for patients with obesity can prevent the progression of T2D in those at the prediabetic stage and vascular complications in those with diabetes [18,19].”
Indarto, D., Fitri, N., Umagapi, F., Kisnawaty, S. W., Wibowo, Y. C., & Mahanani, M. R. (2024) · Clinical Nutrition Open Science · doi:10.1016/j.nutos.2024.09.005
Marinescu, I. P., Marinescu, D., Vasiliu, O., et al. (2024) · Psihiatru ro · doi:10.26416/psih.76.1.2024.9461
Nutrient Involvement in Insulin Secretion and Blood Glucose Variability
Kanazawa, Y. (2024) · Nippon Eiyo Shokuryo Gakkaishi · doi:10.4327/jsnfs.77.345
Okami, Y., 角田, 秀., Tsunoda, H., Watanabe, J., & Kataoka, Y. (n.d.) · Institutional Repositories DataBase (IRDB)
- Authors
- Shukla, A. P., Dickison, M., Coughlin, N., Karan, A., Mauer, E., Truong, W., Casper, A., Emiliano, A. B., Kumar, R. B., Saunders, K. H., Igel, L. I., & Aronne, L. J.
- Affiliations
- Weill Cornell Medicine (US)
- Rockefeller University (US)
- Corresponding author
- Shukla, Alpana P.
- ORCID
- Venue
- Diabetes, Obesity and Metabolism
- Publisher
- Wiley
- Published
- 2018-09-10
- Volume
- 21
- Issue
- 2
- Pages
- 377-381
- ISSN
- 1462-8902 (ISSN-L)
- 1463-1326
- PMC
- PMC7398578
- OpenAlex
- W2886715128
- Semantic Scholar
- 5a55f302c8186a7c3e7471f37b5f080164228332
- Cited by
- 66
- References
- 13
- Citations by year
- 2026: 9 · 2025: 8 · 2024: 11 · 2023: 9 · 2022: 9 · 2021: 10 · 2020: 6 · 2019: 3 · 2018: 1
- FWCI
- 3.98
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Diabetes Obesity and Metabolism (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (UL1TR000457, UL1TR002384)
- NIH Clinical Center
- National Center for Advancing Translational Sciences
- Clinical and Translational Science Center, Weill Cornell Medical College
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes Management and Research
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes Treatment and Management
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes, Cardiovascular Risks, and Lipoproteins
- Keywords
- prediabetes, postprandial blood glucose, postprandial insulin, glycaemic excursions, glycemic variability
- MeSH terms
- Adult, Aged, Blood Glucose, Feeding Behavior, Female, Humans, Hyperglycemia, Insulin, Male, Middle Aged, Prediabetic State, Retrospective Studies, Cross-Over Studies, Postprandial Period, Meals
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-09-28.
Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-09-28.
Cited sources are checked by gpt-6-sol.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review