Association Analysis of Dietary Inflammatory Index and Gestational Diabetes Mellitus: Based on National Health and Nutrition Examination Survey Database

Abstract

Objective This study focused on the association of the Dietary Inflammatory Index (DII) with the risk of gestational diabetes mellitus (GDM) using data from the National Health and Nutrition Examination Survey (NHANES).

Methods Data from two cycles of NHANES (2007–2010) were analyzed. Weighted logistic regression models were constructed to explore the relationship between DII and GDM. Stratified and subgroup analyses with adjustment for confounding factors were carried out to explore the association between DII and GDM. Mediation analysis was conducted to investigate potential mediating factors.

Results A total of 1,421 samples were analyzed. Based on the weighted logistic regression model, a strong positive association was observed between DII score and GDM risk (OR: 1.14, 95%CI: 1.02–1.26, P<0.01), suggesting that a pro-inflammatory diet could considerably increase the likelihood of GDM occurrence. This positive association was particularly significant in populations who consume alcohol (OR:1.17, 95%CI: 1.03–1.34, P<0.01) and have a body mass index>30 kg/m² (OR: 1.18, 95% CI: 1.01–1.38, P<0.05). Mediation analysis indicated that the white blood cell count mediated the association between DII and GDM, with an indirect effect of 0.000828 (95% CI: 0.000226–0.001347, P=0.001) and a mediation proportion of 8.01%. Specifically, the neutrophil count as a component contributed to this mediation effect (0.000774, 95% CI: 0.00014–0.001063, P=0.001), with a mediation proportion of 7.59%.

Conclusion A pro-inflammatory diet in women elevates the likelihood of GDM occurrence. An anti-inflammatory dietary pattern may be a protective intervention for GDM.

Keywords

gestational diabetes mellitus - dietary inflammatory index - neutrophil count - cross-sectional study - National Health and Nutrition Examination Survey

Publication History

Received: 22 November 2023
Received: 13 March 2024

Accepted: 18 March 2024

Article published online:
25 April 2024

• References

• 1 Kautzky-Willer A, Winhofer Y, Kiss H. et al. Gestational diabetes mellitus (Update 2023). Wien Klin Wochenschr 2023; 135: 115-128
• 2 Kim KS, Hong S, Han K. et al. The clinical characteristics of gestational diabetes mellitus in Korea: A National Health Information Database Study. Endocrinol Metab (Seoul) 2021; 36: 628-636
• 3 Han Q, Shao P, Leng J. et al. Interactions between general and central obesity in predicting gestational diabetes mellitus in Chinese pregnant women: A prospective population-based study in Tianjin, China. J Diabetes 2018; 10: 59-67
• 4 Torloni MR, Betran AP, Horta BL. et al. Prepregnancy BMI and the risk of gestational diabetes: A systematic review of the literature with meta-analysis. Obes Rev 2009; 10: 194-203
• 5 Magliano DJ, Boyko EJ. IDF Diabetes Atlas, 10th Ed. Brussels: International Diabetes Federation; 2021
• 6 You H, Hu J, Liu Y. et al. Risk of type 2 diabetes mellitus after gestational diabetes mellitus: A systematic review & meta-analysis. Indian J Med Res 2021; 154: 62-77
• 7 Sweeting A, Wong J, Murphy HR. et al. A clinical update on gestational diabetes mellitus. Endocr Rev 2022; 43: 763-793
• 8 Parikh NI, Gonzalez JM, Anderson CAM. et al. Adverse pregnancy outcomes and cardiovascular disease risk: Unique opportunities for cardiovascular disease prevention in women: A scientific statement from the American Heart Association. Circulation 2021; 143: e902-e916
• 9 Kramer CK, Campbell S, Retnakaran R. Gestational diabetes and the risk of cardiovascular disease in women: A systematic review and meta-analysis. Diabetologia 2019; 62: 905-914
• 10 Dall TM, Yang W, Gillespie K. et al. The economic burden of elevated blood glucose levels in 2017: Diagnosed and undiagnosed diabetes, gestational diabetes mellitus, and prediabetes. Diabetes Care 2019; 42: 1661-1668
• 11 Plows JF, Stanley JL, Baker PN. et al. The pathophysiology of gestational diabetes mellitus. Int J Mol Sci 2018; 19: 3342
• 12 Cinkajzlova A, Anderlova K, Simjak P. et al. Subclinical inflammation and adipose tissue lymphocytes in pregnant females with gestational diabetes mellitus. J Clin Endocrinol Metab 2020; 105: dgaa528
• 13 Xuan Nguyen K, Bui Minh T, Dinh HT. et al. Low-grade inflammation in gestational diabetes mellitus and its correlation with maternal insulin resistance and fetal growth indices. Int J Gen Med 2023; 16: 1429-1436
• 14 Lyu X, Jia J, Yang H. et al. Hematological parameters in the first trimester and the risk of gestational diabetes mellitus – Beijing, China, 2017-2020. China CDC Wkly 2023; 5: 194-200
• 15 Galland L. Diet and inflammation. Nutr Clin Pract 2010; 25: 634-640
• 16 Beam A, Clinger E, Hao L. Effect of diet and dietary components on the composition of the gut microbiota. Nutrients 2021; 13: 2795
• 17 Bonaccio M, Costanzo S, Di Castelnuovo A. et al. Increased adherence to a mediterranean diet is associated with reduced low-grade inflammation after a 12.7-year period: Results from the Moli-sani Study. J Acad Nutr Diet 2023; 123: 783-95 e7
• 18 Pajunen L, Korkalo L, Koivuniemi E. et al. A healthy dietary pattern with a low inflammatory potential reduces the risk of gestational diabetes mellitus. Eur J Nutr 2022; 61: 1477-1490
• 19 Mohtashaminia F, Hosseini F, Jayedi A. et al. Adherence to the Mediterranean diet and risk of gestational diabetes: A prospective cohort study. BMC Pregnancy Childbirth 2023; 23: 647
• 20 Sedaghat F, Akhoondan M, Ehteshami M. et al. Maternal dietary patterns and gestational diabetes risk: A case-control study. J Diabetes Res 2017; 2017: 5173926
• 21 Shivappa N, Steck SE, Hurley TG. et al. Designing and developing a literature-derived, population-based dietary inflammatory index. Public Health Nutr 2014; 17: 1689-1696
• 22 Denova-Gutierrez E, Munoz-Aguirre P, Shivappa N. et al. Dietary inflammatory index and type 2 diabetes mellitus in adults: The diabetes mellitus survey of Mexico City. Nutrients 2018; 10: 385
• 23 Laouali N, Mancini FR, Hajji-Louati M. et al. Dietary inflammatory index and type 2 diabetes risk in a prospective cohort of 70,991 women followed for 20 years: The mediating role of BMI. Diabetologia 2019; 62: 2222-2232
• 24 Shivappa N, Hebert JR, Akhoundan M. et al. Association between inflammatory potential of diet and odds of gestational diabetes mellitus among Iranian women. J Matern Fetal Neonatal Med 2019; 32: 3552-3558
• 25 Sen S, Rifas-Shiman SL, Shivappa N. et al. Dietary inflammatory potential during pregnancy is associated with lower fetal growth and breastfeeding failure: Results from Project Viva. J Nutr 2016; 146: 728-736
• 26 Zhang Z, Wu Y, Zhong C. et al. Association between dietary inflammatory index and gestational diabetes mellitus risk in a prospective birth cohort study. Nutrition 2021; 87-88: 111193
• 27 Zhang J, Jia J, Lai R. et al. Association between dietary inflammatory index and atherosclerosis cardiovascular disease in U.S. adults. Front Nutr 2022; 9: 1044329
• 28 Chen J, Sun B, Zhang D. Association of dietary n3 and n6 fatty acids intake with hypertension: NHANES 2007-2014. Nutrients 2019; 11: 1232
• 29 Casagrande SS, Linder B, Cowie CC. Prevalence of gestational diabetes and subsequent Type 2 diabetes among U.S. women. Diabetes Res Clin Pract 2018; 141: 200-208
• 30 Knippen KL, Sheu JJ, Oza-Frank R. et al. Predictors of health-protective behavior and glycemia after gestational diabetes, NHANES 2007-2014. Diabetes Educ 2019; 45: 408-419
• 31 Tian X, Xue B, Wang B. et al. Physical activity reduces the role of blood cadmium on depression: A cross-sectional analysis with NHANES data. Environ Pollut 2022; 304: 119211
• 32 Zhang Y, Liu W, Zhang W. et al. Association between blood lead levels and hyperlipidemiais: Results from the NHANES (1999-2018). Front Public Health 2022; 10: 981749
• 33 Dong X, Li S, Sun J. et al. Association of coffee, decaffeinated coffee and caffeine intake from coffee with cognitive performance in older adults: National Health and Nutrition Examination Survey (NHANES) 2011-2014. Nutrients 2020; 12: 840
• 34 Li C, Shang S. Relationship between sleep and hypertension: Findings from the NHANES (2007-2014). Int J Environ Res Public Health 2021; 18: 7867
• 35 Miao H, Liu Y, Tsai TC. et al. Association between blood lead level and uncontrolled hypertension in the US population (NHANES 1999-2016). J Am Heart Assoc 2020; 9: e015533
• 36 Liao S, Zhang J, Shi S. et al. Association of aldehyde exposure with cardiovascular disease. Ecotoxicol Environ Saf 2020; 206: 111385
• 37 Mao Y, Hu W, Xia B. et al. Association between history of gestational diabetes mellitus and the risk of arthritis in women. Front Public Health 2022; 10: 878845
• 38 Liu B, Wang J, Li YY. et al. The association between systemic immune-inflammation index and rheumatoid arthritis: Evidence from NHANES 1999-2018. Arthritis Res Ther 2023; 25: 34
• 39 Pereira SS, Alvarez-Leite JI. Low-grade inflammation, obesity, and diabetes. Curr Obes Rep 2014; 3: 422-431
• 40 Zatterale F, Longo M, Naderi J. et al. Chronic adipose tissue inflammation linking obesity to insulin resistance and type 2 diabetes. Front Physiol 2019; 10: 1607
• 41 Powe CE. Early pregnancy biochemical predictors of gestational diabetes mellitus. Curr Diab Rep 2017; 17: 12
• 42 Aleksandrova K, Koelman L, Rodrigues CE. Dietary patterns and biomarkers of oxidative stress and inflammation: A systematic review of observational and intervention studies. Redox Biol 2021; 42: 101869
• 43 Minihane AM, Vinoy S, Russell WR. et al. Low-grade inflammation, diet composition and health: Current research evidence and its translation. Br J Nutr 2015; 114: 999-1012
• 44 Abell SK, De Courten B, Boyle JA. et al. Inflammatory and other biomarkers: Role in pathophysiology and prediction of gestational diabetes mellitus. Int J Mol Sci 2015; 16: 13442-13473
• 45 Farrar D, Duley L, Dowswell T. et al. Different strategies for diagnosing gestational diabetes to improve maternal and infant health. Cochrane Database Syst Rev 2017; 8: CD007122
• 46 Goran MI, Plows JF, Ventura EE. Effects of consuming sugars and alternative sweeteners during pregnancy on maternal and child health: Evidence for a secondhand sugar effect. Proc Nutr Soc 2019; 78: 262-271
• 47 Lorenzo PI, Martin-Montalvo A, Cobo Vuilleumier N. et al. Molecular modelling of islet beta-cell adaptation to inflammation in pregnancy and gestational diabetes mellitus. Int J Mol Sci 2019; 20: 6171
• 48 Jaworsky K, DeVillez P, Alexander JM. et al. Effects of an eating pattern including colorful fruits and vegetables on management of gestational diabetes: A randomized controlled trial. Nutrients 2023; 15: 3624
• 49 Kahleova H, Tura A, Hill M. et al. A plant-based dietary intervention improves beta-cell function and insulin resistance in overweight adults: A 16-week randomized clinical trial. Nutrients 2018; 10: 189
• 50 Christ A, Lauterbach M, Latz E. Western diet and the immune System: An inflammatory connection. Immunity 2019; 51: 794-811
• 51 Quan W, Zeng M, Jiao Y. et al. Western dietary patterns, foods, and risk of gestational diabetes mellitus: A systematic review and meta-analysis of prospective cohort studies. Adv Nutr 2021; 12: 1353-1364
• 52 Mahjoub F, Ben Jemaa H, Ben Sabeh F. et al. Impact of nutrients and Mediterranean diet on the occurrence of gestational diabetes. Libyan J Med 2021; 16: 1930346
• 53 Assaf-Balut C, Garcia de la Torre N, Duran A. et al. A Mediterranean diet with additional extra virgin olive oil and pistachios reduces the incidence of gestational diabetes mellitus (GDM): A randomized controlled trial: The St. Carlos GDM prevention study. PLoS One 2017; 12: e0185873
• 54 Gepner Y, Golan R, Harman-Boehm I. et al. Effects of initiating moderate alcohol intake on cardiometabolic risk in adults with type 2 diabetes: A 2-year randomized, controlled trial. Ann Intern Med 2015; 163: 569-579
• 55 Abraham KA, Kearney ML, Reynolds LJ. et al. Red wine enhances glucose-dependent insulinotropic peptide (GIP) and insulin responses in type 2 diabetes during an oral glucose tolerance test. Diabetol Int 2016; 7: 173-180
• 56 Butts M, Sundaram VL, Murughiyan U. et al. The influence of alcohol consumption on intestinal nutrient absorption: A comprehensive review. Nutrients 2023; 15: 1571
• 57 van der Heide FCT, Eussen S, Houben A. et al. Alcohol consumption and microvascular dysfunction: A J-shaped association: The Maastricht Study. Cardiovasc Diabetol 2023; 22: 67
• 58 Hendriks HFJ. Alcohol and human health: What is the evidence? . Annu Rev Food Sci Technol 2020; 11: 1-21
• 59 Wechsler H, Davenport A, Dowdall G. et al. Health and behavioral consequences of binge drinking in college. A national survey of students at 140 campuses. JAMA 1994; 272: 1672-1677
• 60 Pearson MR, Kirouac M, Witkiewitz K. Questioning the validity of the 4+/5+ binge or heavy drinking criterion in college and clinical populations. Addiction 2016; 111: 1720-1726
• 61 Agriculture. USDoHaHSaUSDo. 2015 – 2020 Dietary Guidelines for Americans, 8th Edition. 2015 https://health.gov/our-work/food-nutrition/previous-dietary-guidelines/2015
• 62 Toulis KA, Nirantharakumar K, Pourzitaki C. et al. Glucokinase activators for type 2 diabetes: Challenges and future developments. Drugs 2020; 80: 467-475
• 63 Kim JY, Lee DY, Lee YJ. et al. Chronic alcohol consumption potentiates the development of diabetes through pancreatic beta-cell dysfunction. World J Biol Chem 2015; 6: 1-15
• 64 Breslow RA, Chen CM, Graubard BI. et al. Diets of drinkers on drinking and nondrinking days: NHANES 2003-2008. Am J Clin Nutr 2013; 97: 1068-1075
• 65 Schrieks IC, Stafleu A, Griffioen-Roose S. et al. Moderate alcohol consumption stimulates food intake and food reward of savoury foods. Appetite 2015; 89: 77-83
• 66 Cains S, Blomeley C, Kollo M. et al. Agrp neuron activity is required for alcohol-induced overeating. Nat Commun 2017; 8: 14014
• 67 Sterneder S, Stoeger V, Dugulin CA. et al. Astringent gallic acid in red wine regulates mechanisms of gastric acid secretion via activation of bitter taste sensing receptor TAS2R4. J Agric Food Chem 2021; 69: 10550-10561
• 68 Laniewska-Dunaj M, Jelski W, Szmitkowski M. The effect of ethanol on the stomach. Pol Merkur Lekarski 2012; 32: 194-197
• 69 Brenes JC, Gomez G, Quesada D. et al. Alcohol contribution to total energy intake and its association with nutritional status and diet quality in eight Latina American countries. Int J Environ Res Public Health 2021; 18: 13130
• 70 Butler L, Popkin BM, Poti JM. Associations of alcoholic beverage consumption with dietary intake, waist circumference, and body mass index in US adults: National Health and Nutrition Examination Survey 2003-2012. J Acad Nutr Diet 2018; 118: 409-20 e3
• 71 Ganguly A, Devaskar SU. High-fat diet affects pregestational adiposity and glucose tolerance perturbing gestational placental macronutrient transporters culminating in an obese offspring in wild-type and glucose transporter isoform 3 heterozygous null mice. J Nutr Biochem 2018; 62: 192-201
• 72 Ye YX, Wang Y, Wu P. et al. Blood cell parameters from early to middle pregnancy and risk of gestational diabetes mellitus. J Clin Endocrinol Metab 2023; 108: e1702-e1711
• 73 Hessami K, Tabrizi R, Homayoon N. et al. Gestational diabetes mellitus and inflammatory biomarkers of neutrophil-lymphocyte ratio and platelet-lymphocyte ratio: A systematic review and meta-analysis. Biomarkers 2021; 26: 491-498
• 74 Liu W, Lou X, Zhang Z. et al. Association of neutrophil to lymphocyte ratio, platelet to lymphocyte ratio, mean platelet volume with the risk of gestational diabetes mellitus. Gynecol Endocrinol 2021; 37: 105-107
• 75 Sun T, Meng F, Zhao H. et al. Elevated first-trimester neutrophil count is closely associated with the development of maternal gestational diabetes mellitus and adverse pregnancy outcomes. Diabetes 2020; 69: 1401-1410
• 76 Zhang R, Chen J, Xiong Y. et al. Increased neutrophil count Is associated with the development of chronic kidney disease in patients with diabetes. J Diabetes 2022; 14: 442-454
• 77 Gimeno-Molina B, Muller I, Kropf P. et al. The role of neutrophils in pregnancy, term and preterm labour. Life (Basel) 2022; 12: 1512
• 78 Stoikou M, Grimolizzi F, Giaglis S. et al. Gestational diabetes mellitus is associated with altered neutrophil activity. Front Immunol 2017; 8: 702
• 79 Zhang J, Chi H, Xiao H. et al. Interleukin 6 (IL-6) and tumor necrosis factor alpha (TNF-alpha) single nucleotide polymorphisms (SNPs), inflammation and metabolism in gestational diabetes mellitus in inner Mongolia. Med Sci Monit 2017; 23: 4149-4157
• 80 Hocaoglu C, Kural B, Aliyazicioglu R. et al. IL-1beta, IL-6, IL-8, IL-10, IFN-gamma, TNF-alpha and its relationship with lipid parameters in patients with major depression. Metab Brain Dis 2012; 27: 425-430
• 81 Li QY, Xu HY, Yang HJ. Effect of proinflammatory factors TNF-alpha,IL-1beta, IL-6 on neuropathic pain. Zhongguo Zhong Yao Za Zhi 2017; 42: 3709-3712
• 82 Kaneko Y, Takeuchi T. An update on the pathogenic role of IL-6 in rheumatic diseases. Cytokine 2021; 146: 155645
• 83 Akash MSH, Rehman K, Liaqat A. Tumor necrosis factor-alpha: Role in development of insulin resistance and pathogenesis of type 2 diabetes mellitus. J Cell Biochem 2018; 119: 105-110
• 84 Kong M, Zhang H, Liu X. et al. Association of maternal neutrophil count in early pregnancy with the development of gestational diabetes mellitus: A prospective cohort study in China. Gynecol Endocrinol 2022; 38: 258-262