The Association of Dietary Micronutrient Intake and Systemic Inflammation among Patients with Type 2 Diabetes: A Cross-Sectional Study
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Design and Setting
2.2. Inclusion/Exclusion Criteria
2.3. Study Procedures
2.4. Biomarker Assessment
2.5. Statistical Analysis
3. Results
3.1. Descriptive Statistics
3.2. Bivariate Statistics
3.3. Regression Analysis
3.4. Logistic Regression Analysis for Micronutrients
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Crea, F. The burden of cardiovascular risk factors: A global perspective. Eur. Heart J. 2022, 43, 2817–2820. [Google Scholar] [CrossRef] [PubMed]
- Vaduganathan, M.; Mensah, G.A.; Turco, J.V.; Fuster, V.; Roth, G.A. The Global Burden of Cardiovascular Diseases and Risk: A Compass for Future Health. J. Am. Coll. Cardiol. 2022, 80, 2361–2371. [Google Scholar] [CrossRef] [PubMed]
- Chen, W.; Zhang, S.; Hu, X.; Chen, F.; Li, D. A Review of Healthy Dietary Choices for Cardiovascular Disease: From Individual Nutrients and Foods to Dietary Patterns. Nutrients 2023, 15, 4898. [Google Scholar] [CrossRef]
- Szczepańska, E.; Białek-Dratwa, A.; Janota, B.; Kowalski, O. Dietary Therapy in Prevention of Cardiovascular Disease (CVD)-Tradition or Modernity? A Review of the Latest Approaches to Nutrition in CVD. Nutrients 2022, 14, 2649. [Google Scholar] [CrossRef] [PubMed]
- Fung, T.T.; Willett, W.C.; Stampfer, M.J.; Manson, J.E.; Hu, F.B. Dietary patterns and the risk of coronary heart disease in women. Arch. Intern. Med. 2001, 161, 1857–1862. [Google Scholar] [CrossRef]
- Bermingham, K.M.; Mazidi, M.; Franks, P.W.; Maher, T.; Valdes, A.M.; Linenberg, I.; Wolf, J.; Hadjigeorgiou, G.; Spector, T.D.; Menni, C.; et al. Characterisation of Fasting and Postprandial NMR Metabolites: Insights from the ZOE PREDICT 1 Study. Nutrients 2023, 15, 2638. [Google Scholar] [CrossRef]
- Grosso, G.; Mistretta, A.; Frigiola, A.; Gruttadauria, S.; Biondi, A.; Basile, F.; Vitaglione, P.; D’Orazio, N.; Galvano, F. Mediterranean diet and cardiovascular risk factors: A systematic review and meta-analysis. J. Am. Coll. Cardiol. 2018, 71, 927–939. [Google Scholar] [CrossRef]
- Norlander, A.E.; Madhur, M.S.; Harrison, D.G. The immunology of hypertension. J. Exp. Med. 2018, 215, 21–33. [Google Scholar] [CrossRef]
- Hong, N.; Lin, Y.; Ye, Z.; Yang, C.; Huang, Y.; Duan, Q.; Xie, S. The relationship between dyslipidemia and inflammation among adults in east coast China: A cross-sectional study. Front. Immunol. 2022, 13, 937201. [Google Scholar] [CrossRef]
- Mahemuti, N.; Jing, X.; Zhang, N.; Liu, C.; Li, C.; Cui, Z.; Liu, Y.; Chen, J. Association between Systemic Immunity-Inflammation Index and Hyperlipidemia: A Population-Based Study from the NHANES (2015–2020). Nutrients 2023, 15, 1177. [Google Scholar] [CrossRef]
- Sharif, S.; Cramer, M.J.; de Borst, G.J.; Visseren, F.L.J.; Westerink, J.; the SMART study group; van Petersen, R.; Dinther, B.G.F.; Algra, A.; van der Graaf, Y.; et al. Low-grade inflammation as a risk factor for cardiovascular events and all-cause mortality in patients with type 2 diabetes. Cardiovasc. Diabetol. 2021, 20, 220. [Google Scholar] [CrossRef] [PubMed]
- Dregan, A.; Charlton, J.; Chowienczyk, P.; Gulliford, M.C. Chronic inflammatory disorders and risk of type 2 diabetes mellitus, coronary heart disease, and stroke: A population-based cohort study. Circulation 2014, 130, 837–844. [Google Scholar] [CrossRef] [PubMed]
- Kim, K.; Vance, T.M.; Chun, O.K. Greater Total Antioxidant Capacity from Diet and Supplements Is Associated with a Less Atherogenic Blood Profile in U.S. Adults. Nutrients 2016, 8, 15. [Google Scholar] [CrossRef] [PubMed]
- Basu, A.; Izuora, K.; Hooyman, A.; Scofield, H.R.; Ebersole, J.L. Dietary Strawberries Improve Serum Metabolites of Cardiometabolic Risks in Adults with Features of the Metabolic Syndrome in a Randomized Controlled Crossover Trial. Int. J. Mol. Sci. 2023, 24, 2051. [Google Scholar] [CrossRef]
- Bagherniya, M.; Khayyatzadeh, S.S.; Bakavoli, A.R.H.; Ferns, A.G.; Ebrahimi, M.; Safarian, M.; Nematy, M.; Ghayour-Mobarhan, M. Serum high-sensitive C-reactive protein is associated with dietary intakes in diabetic patients with and without hypertension: A cross-sectional study. Ann. Clin. Biochem. 2018, 55, 422–429. [Google Scholar] [CrossRef]
- Gao, S.; Zhao, D.; Qi, Y.; Wang, W.; Wang, M.; Sun, J.; Liu, J.; Li, Y.; Liu, J. Circulating Oxidized Low-Density Lipoprotein Levels Independently Predict 10-Year Progression of Subclinical Carotid Atherosclerosis: A Community-Based Cohort Study. J. Atheroscler. Thromb. 2018, 25, 1032–1043. [Google Scholar] [CrossRef]
- Hess, J.M.; Stephensen, C.B.; Kratz, M.; Bolling, B.W. Exploring the Links between Diet and Inflammation: Dairy Foods as Case Studies. Adv. Nutr. 2021, 12 (Suppl. S1), 1S–13S. [Google Scholar] [CrossRef]
- Estruch, R.; Ros, E.; Salas-Salvadó, J.; Covas, M.-I.; Corella, D.; Arós, F.; Gómez-Gracia, E.; Ruiz-Gutiérrez, V.; Fiol, M.; Lapetra, J.; et al. Primary Prevention of Cardiovascular Disease with a Mediterranean Diet Supplemented with Extra-Virgin Olive Oil or Nuts. N. Engl. J. Med. 2018, 378, e34. [Google Scholar] [CrossRef]
- Richardson, L.A.; Izuora, K.; Basu, A. Mediterranean Diet and Its Association with Cardiovascular Disease Risk Factors: A Scoping Review. Int. J. Environ. Res. Public Health 2022, 19, 2762. [Google Scholar] [CrossRef]
- Hart, M.J.; Torres, S.J.; McNaughton, S.A.; Milte, C.M. Dietary patterns and associations with biomarkers of inflammation in adults: A systematic review of observational studies. Nutr. J. 2021, 20, 24. [Google Scholar] [CrossRef]
- Leong, X.F. Lipid Oxidation Products on Inflammation-Mediated Hypertension and Atherosclerosis: A Mini Review. Front. Nutr. 2021, 8, 717740. [Google Scholar] [CrossRef]
- Le Gresley, A.; Ampem, G.; De Mars, S.; Grootveld, M.; Naughton, D.P. “Real-World” Evaluation of Lipid Oxidation Products and Trace Metals in French Fries from Two Chain Fast-Food Restaurants. Front. Nutr. 2021, 8, 620952. [Google Scholar] [CrossRef] [PubMed]
- Defagó, M.D.; Elorriaga, N.; Irazola, V.E.; Rubinstein, A.L. Influence of food patterns on endothelial biomarkers: A systematic review. J. Clin. Hypertens. 2014, 16, 907–913. [Google Scholar] [CrossRef]
- Ottaviani, J.I.; Sagi-Kiss, V.; Schroeter, H.; Kuhnle, G.G.C. Reliance on self-reports and estimated food composition data in nutrition research introduces significant bias that can only be addressed with biomarkers. eLife 2024, 13, RP92941. [Google Scholar] [CrossRef]
- Zhao, J.; Li, Z.; Gao, Q.; Zhao, H.; Chen, S.; Huang, L.; Wang, W.; Wang, T. A review of statistical methods for dietary pattern analysis. Nutr. J. 2021, 20, 37. [Google Scholar] [CrossRef] [PubMed]
- Heart Outcomes Prevention Evaluation Study Investigators; Yusuf, S.; Dagenais, G.; Pogue, J.; Bosch, J.; Sleight, P. Vitamin E supplementation and cardiovascular events in high-risk patients. N. Engl. J. Med. 2000, 342, 154–160. [Google Scholar] [CrossRef]
- An, P.; Wan, S.; Luo, Y.; Luo, J.; Zhang, X.; Zhou, S.; Xu, T.; He, J.; Mechanick, J.I.; Wu, W.-C.; et al. Micronutrient Supplementation to Reduce Cardiovascular Risk. J. Am. Coll. Cardiol. 2022, 80, 2269–2285. [Google Scholar] [CrossRef] [PubMed]
- Bazzano, L.A.; He, J.; Ogden, L.G.; Loria, C.M.; Vupputuri, S.; Myers, L.; Whelton, P.K. Agreement on nutrient intake between the databases of the First National Health and Nutrition Examination Survey and the ESHA Food Processor. Am. J. Epidemiol. 2002, 156, 78–85. [Google Scholar] [CrossRef] [PubMed]
- Ludden, T.M.; Beal, S.L.; Sheiner, L.B. Comparison of the Akaike Information Criterion, the Schwarz criterion and the F test as guides to model selection. J. Pharmacokinet. Biopharm. 1994, 22, 431–445. [Google Scholar] [CrossRef]
- Takata, S.; Wada, H.; Tamura, M.; Koide, T.; Higaki, M.; Mikura, S.-I.; Yasutake, T.; Hirao, S.; Nakamura, M.; Honda, K.; et al. Kinetics of c-reactive protein (CRP) and serum amyloid A protein (SAA) in patients with community-acquired pneumonia (CAP), as presented with biologic half-life times. Biomarkers 2011, 16, 530–535. [Google Scholar] [CrossRef]
- Cetinkaya, M.; Ozkan, H.; Köksal, N.; Akaci, O.; Ozgür, T. Comparison of the efficacy of serum amyloid A, C-reactive protein, and procalcitonin in the diagnosis and follow-up of necrotizing enterocolitis in premature infants. J. Pediatr. Surg. 2011, 46, 1482–1489. [Google Scholar] [CrossRef] [PubMed]
- Tekin, I.O.; Pocan, B.; Borazan, A.; Ucar, E.; Kuvandik, G.; Ilikhan, S.; Demircan, N.; Ozer, C.; Kadayifci, S. Positive correlation of CRP and fibrinogen levels as cardiovascular risk factors in early stage of continuous ambulatory peritoneal dialysis patients. Ren. Fail. 2008, 30, 219–225. [Google Scholar] [CrossRef] [PubMed]
- Calder, P.C. Omega-3 fatty acids and inflammatory processes: Nutrition or pharmacology? Br. J. Nutr. 2013, 110, 873–881. [Google Scholar] [CrossRef] [PubMed]
- Grant, A.J.; de Groh, E.M.B.M. Vitamin D and its role in immune function: A review of the literature. Nutrients 2020, 12, 2640. [Google Scholar] [CrossRef]
- Haase, H.R.; Wessels, L.R. The role of zinc in the regulation of inflammation and immunity. Int. J. Mol. Sci. 2017, 18, 2618. [Google Scholar] [CrossRef]
- Gombart, A.F.; Pierre, A.; Maggini, S. A Review of Micronutrients and the Immune System-Working in Harmony to Reduce the Risk of Infection. Nutrients 2020, 12, 236. [Google Scholar] [CrossRef]
- Barone, M.; D’Amico, F.; Brigidi, P.; Turroni, S. Gut microbiome-micronutrient interaction: The key to controlling the bioavailability of minerals and vitamins? Biofactors 2022, 48, 307–314. [Google Scholar] [CrossRef]
- Shenkin, A. Micronutrients in health and disease. Postgrad Med. J. 2006, 82, 559–567. [Google Scholar] [CrossRef]
- Jin, M.; Pan, T.; Tocher, D.R.; Betancor, M.B.; Monroig, Ó.; Shen, Y.; Zhu, T.; Sun, P.; Jiao, L.; Zhou, Q. Dietary choline supplementation attenuated high-fat diet-induced inflammation through regulation of lipid metabolism and suppression of NFκB activation in juvenile black seabream (Acanthopagrus schlegelii). J. Nutr. Sci. 2019, 8, e38. [Google Scholar] [CrossRef]
- Zargarzadeh, N.; Severo, J.S.; Pizarro, A.B.; Persad, E.; Mousavi, S.M. The Effects of Folic Acid Supplementation on Pro-inflammatory Mediators: A Systematic Review and Dose-Response Meta-Analysis of Randomized Controlled Trials. Clin. Ther. 2021, 43, e346–e363. [Google Scholar] [CrossRef]
- Asbaghi, O.; Sadeghian, M.; Nazarian, B.; Sarreshtedari, M.; Mozaffari-Khosravi, H.; Maleki, V.; Alizadeh, M.; Shokri, A.; Sadeghi, O. The effect of vitamin E supplementation on selected inflammatory biomarkers in adults: A systematic review and meta-analysis of randomized clinical trials. Sci. Rep. 2020, 10, 17234. [Google Scholar] [CrossRef]
- Mohammadi, H.; Talebi, S.; Ghavami, A.; Rafiei, M.; Sharifi, S.; Faghihimani, Z.; Ranjbar, G.; Miraghajani, M.; Askari, G. Effects of zinc supplementation on inflammatory biomarkers and oxidative stress in adults: A systematic review and meta-analysis of randomized controlled trials. J. Trace Elem. Med. Biol. 2021, 68, 126857. [Google Scholar] [CrossRef] [PubMed]
- Wagener, F.A.D.T.G.; Volk, H.-D.; Willis, D.; Abraham, N.G.; Soares, M.P.; Adema, G.J.; Figdor, C.G. Different faces of the heme-heme oxygenase system in inflammation. Pharmacol. Rev. 2003, 55, 551–571. [Google Scholar] [CrossRef]
- Wessling-Resnick, M. Iron homeostasis and the inflammatory response. Annu. Rev. Nutr. 2010, 30, 105–122. [Google Scholar] [CrossRef] [PubMed]
- Cornelissen, A.; Guo, L.; Sakamoto, A.; Virmani, R.; Finn, A.V. New insight into the role of iron in inflammation and atherosclerosis. eBioMedicine 2019, 47, 598–606. [Google Scholar] [CrossRef] [PubMed]
- Kahaer, A.; Chen, R.; Maitusong, M.; Mijiti, P.; Rexiti, P. Zero-profile implant versus conventional cage-plate construct in anterior cervical discectomy and fusion for the treatment of single-level degenerative cervical spondylosis: A systematic review and meta-analysis. J. Orthop. Surg. Res. 2022, 17, 506. [Google Scholar] [CrossRef]
- Shi, W.; Huang, X.; Schooling, C.M.; Zhao, J.V. Red meat consumption, cardiovascular diseases, and diabetes: A systematic review and meta-analysis. Eur. Heart J. 2023, 44, 2626–2635. [Google Scholar] [CrossRef]
- Misra, R.; Balagopal, P.; Raj, S.; Patel, T.G. Red Meat Consumption (Heme Iron Intake) and Risk for Diabetes and Comorbidities? Curr. Diabetes Rep. 2018, 18, 100. [Google Scholar] [CrossRef]
Variable | Characteristics | Mean ± SD | n (%) | 95% CI (LCL, UCL) |
---|---|---|---|---|
Age (years) | - | 64.10 ± 10.3 | - | 61.6, 66.5 |
BMI (kg/m2) | - | 34.0 ± 8.3 | - | 32.0, 36.0 |
BMI Status | Normal (18.5–24.9) | - | 11 (15.5) | 8.0, 26.0 |
Overweight (25.0–29.9) | - | 12 (16.9) | 9.1, 27.6 | |
Obese (≥30.0) | - | 48 (67.6) | 55.5, 78.2 | |
Gender | Female | - | 43 (60.6) | 48.3, 72.0 |
Male | - | 28 (39.4) | 28.0, 51.8 | |
Race/ethnicity | White | - | 26 (36.6) | 25.5, 48.9 |
Non-white | - | 45 (63.4) | 51.1, 74.5 | |
Duration of T2DM (years) | 15.80 ± 9.1 | - | 13.7, 18.0 | |
Average A1c over last 3 years (%) | - | 7.80 ± 1.5 | - | 7.5, 8.2 |
CRP (ng/mg) | - | 0.74 ± 0.19 | - | 0.70, 0.80 |
Microvascular complications | Yes | - | 42 (59.2) | 46.8, 70.7 |
No | - | 29 (40.8) | 29.3, 53.2 | |
Macrovascular complications | Yes | - | 16 (22.5) | 13.5, 34.0 |
No | - | 55 (77.5) | 66.0, 86.5 |
Micronutrient | Mean ± SD | Mean ± SD (Males) | Mean ± SD (Females) | RDA * (Male) | RDA (Female) |
---|---|---|---|---|---|
Vitamin E (mg) | 4.27 ± 3.83 | 4.71 ± 5.23 | 3.97 ± 2.59 | 11 | 15 |
Vitamin B6 (mg) | 0.95 ± 0.47 | 1.15 ± 0.62 | 0.81 ± 0.29 | 1 | 1.2 |
Vitamin B9 (mcg) | 245.3 ± 163.63 | 287.68 ± 226.40 | 216.96 ± 99.05 | 400 | 400 |
Vitamin B12 (mcg) | 2.50 ± 1.58 | 3.20 ± 2.09 | 1.97 ± 0.87 | 1.8 | 2.4 |
Zinc (mg) | 5.42 ± 2.90 | 6.34 ± 3.58 | 4.84 ± 2.22 | 8 | 9 |
Iron (mg) | 9.75 ± 4.51 | 11.31 ± 5.68 | 8.72 ± 3.24 | 8 | 18 |
Choline (mg) | 173.02 ± 87.64 | 198.96 ± 92.85 | 155.99 ± 81.03 | 375 | 400 |
Variables | CRP | Fibrinogen | SAA | Vitamin E | Vitamin B6 | Folate | Vitamin B12 | Iron |
---|---|---|---|---|---|---|---|---|
CRP | 1 | 0.289 * | 0.678 ** | 0.068 | 0.222 | 0.207 | 0.125 | 0.302 ** |
Fibrinogen | 0.289 * | 1 | 0.301 * | 0.061 | 0.125 | 0.140 | 0.088 | 0.180 |
SAA | 0.678 ** | 0.301 * | 1 | 0.174 | 0.194 | 0.118 | 0.048 | 0.216 |
Vitamin E | 0.068 | 0.061 | 0.174 | 1 | 0.218 | 0.181 | −0.019 | 0.273 * |
Vitamin B6 | 0.222 | 0.125 | 0.194 | 0.218 | 1 | 0.828 ** | 0.882 ** | 0.863 ** |
Vitamin B9 | 0.207 | 0.140 | 0.118 | 0.181 | 0.828 ** | 1 | 0.769 ** | 0.877 ** |
Vitamin B12 | 0.125 | 0.088 | 0.048 | −0.019 | 0.882 ** | 0.769 ** | 1 | 0.759 ** |
Iron | 0.302 * | 0.180 | 0.216 | 0.273 * | 0.863 ** | 0.877 ** | 0.759 ** | 1 |
Variable | Unstandardized Coefficient | Standardized Coefficient Beta | Coefficients Standard Error | 95% CI (LCL, UCL) | p Value | |
---|---|---|---|---|---|---|
Constant | −2.284 | - | 1.851 | −6.017 | 1.449 | 0.2 |
Age | 0.001 | 0.002 | 0.019 | −0.038 | 0.039 | 0.9 |
Gender (Ref: Females) | 0.138 | 0.056 | 0.388 | −0.645 | 0.920 | 0.7 |
Body mass index | 0.047 | 0.303 | 0.024 | −0.001 | 0.096 | 0.06 |
Duration of diabetes (years) | −0.014 | −0.106 | 0.022 | −0.058 | 0.030 | 0.5 |
HbA1c (%) | 0.119 | 0.134 | 0.130 | −0.143 | 0.382 | 0.4 |
Complications (Ref: No) | 0.206 | 0.081 | 0.369 | −0.538 | 0.950 | 0.6 |
Vitamin E | 0.002 | 0.006 | 0.053 | −0.106 | 0.110 | 0.9 |
Vitamin B6 | 0 | 0.204 | 1.012 | −1.514 | 2.569 | 0.6 |
Vitamin B9 | −0.002 | −0.315 | 0.002 | −0.007 | 0.002 | 0.3 |
Vitamin B12 | −0.188 | −0.248 | 0.252 | −0.696 | 0.320 | 0.5 |
Iron | 0.139 | 0.499 | 0.092 | −0.047 | 0.324 | 0.3 |
Variable | Adjusted Odds Ratio | 95% CI (LCL, UCL) | p Value | |
---|---|---|---|---|
Age | 0.993 | 0.916 | 1.077 | 0.9 |
Gender (Ref: Females) | 4.117 | 0.665 | 25.505 | 0.1 |
Body mass index | 1.232 | 1.063 | 1.426 | 0.005 |
Duration of diabetes (in years) | 1.052 | 0.949 | 1.167 | 0.3 |
HbA1c | 2.349 | 1.123 | 4.912 | 0.023 |
Complications (Ref: No) | 0.312 | 0.050 | 1.959 | 0.2 |
Vitamin E | 1.150 | 0.894 | 1.478 | 0.3 |
Vitamin B6 | 0.078 | 0.001 | 6.757 | 0.2 |
Vitamin B9 | 0.990 | 0.978 | 1.001 | 0.08 |
Vitamin B12 | 1.819 | 0.605 | 5.464 | 0.3 |
Iron | 1.250 | 0.855 | 1.827 | 0.2 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Izuora, K.; Alver, A.; Basu, A.; Batra, K.; Williams, S.J.; Ebersole, J.L. The Association of Dietary Micronutrient Intake and Systemic Inflammation among Patients with Type 2 Diabetes: A Cross-Sectional Study. Healthcare 2024, 12, 1804. https://doi.org/10.3390/healthcare12181804
Izuora K, Alver A, Basu A, Batra K, Williams SJ, Ebersole JL. The Association of Dietary Micronutrient Intake and Systemic Inflammation among Patients with Type 2 Diabetes: A Cross-Sectional Study. Healthcare. 2024; 12(18):1804. https://doi.org/10.3390/healthcare12181804
Chicago/Turabian StyleIzuora, Kenneth, Amalie Alver, Arpita Basu, Kavita Batra, Shelley J. Williams, and Jeffrey L. Ebersole. 2024. "The Association of Dietary Micronutrient Intake and Systemic Inflammation among Patients with Type 2 Diabetes: A Cross-Sectional Study" Healthcare 12, no. 18: 1804. https://doi.org/10.3390/healthcare12181804