Review | Open | Published:
Does long-term coffee intake reduce type 2 diabetes mellitus risk?
Diabetology & Metabolic Syndromevolume 1, Article number: 6 (2009)
This review reports the evidence for a relation between long-term coffee intake and risk of type 2 diabetes mellitus. Numerous epidemiological studies have evaluated this association and, at this moment, at least fourteen out of eighteen cohort studies revealed a substantially lower risk of type 2 diabetes mellitus with frequent coffee intake. Moderate coffee intake (≥4 cups of coffee/d of 150 mL or ≥400 mg of caffeine/d) has generally been associated with a decrease in the risk of type 2 diabetes mellitus. Besides, results of most studies suggest a dose-response relation, with greater reductions in type 2 diabetes mellitus risk with higher levels of coffee consumption. Several mechanisms underlying this protective effect, as well as the coffee components responsible for this association are suggested. Despite positive findings, it is still premature to recommend an increase in coffee consumption as a public health strategy to prevent type 2 diabetes mellitus. More population-based surveys are necessary to clarify the long-term effects of decaffeinated and caffeinated coffee intake on the risk of type 2 diabetes mellitus.
Type 2 diabetes mellitus (DM2) is characterized by insulin resistance and/or abnormal insulin secretion, resulting in a decrease in whole-body glucose disposal. Individuals with chronic hyperglycemia, insulin resistance, and/or DM2 are at greater risk for hypertension, dyslipidemia, and cardiovascular disease .
Although genetic factors may play a role in the etiology of DM2 , there is now convincing evidence that DM2 is strongly associated with modifiable factors, such as diet. Interestingly, among the several factors present in diet, coffee, one of the most widely consumed non-alcoholic beverages in Western society [3, 4], is highlighted as a potent dietary-component associated with reduced risk of several chronic diseases, including DM2 and its complications [5–11]. Coffee is a complex mixture of more than a thousand substances, including caffeine (primary source), phenolic compounds (chlorogenic acid and quinides - primary source), minerals and vitamins (magnesium, potassium, manganese, chromium, niacin), and fibers  and several of these coffee constituents have a possible role in glucose metabolism.
The present review provides an overview of the role of long-term coffee intake on the risks of glucose tolerance, insulin sensitivity, and DM2.
Coffee intake and type 2 diabetes mellitus: a link between cohort and systematic review studies
The association between the coffee intake and the risk of developing DM2 has been examined by several researches. Cohort studies and a systematic review are summarized in Table 1. Data from a prospective study indicated an inverse association between coffee consumption and the risk of DM2 in men independently of race, age or serum concentration of magnesium. Individuals who drank at least seven cups of coffee daily had 50% lower risk to develop DM2 than those who drank two cups or fewer per day . However, this study has not differenced the intake of caffeinated and decaffeinated coffee and didn't evaluate other sources of caffeine.
Salazar-Martinez et al  evaluated the intake of coffee and caffeine from any sources and found an association between coffee intake and the risk of DM2. Besides, this association was found to be more prominent in women than in men and a protective effect of caffeine intake against DM2 was also revealed.
In the Nurses' Health Study II, the researchers observed, after adjustment for several variables, a lower risk of DM2 in women who consumed any dose of coffee when compared to those who did not have this habit. This association was similar in both caffeinated 0.87 (CI: 0.83-0.91), decaffeinated 0.81 (CI: 0.73-0.90) and filtered coffee 0.86 (CI: 0.82-0.90), suggesting that moderate, either caffeinated, decaffeinated or filtered, coffee consumption decreases (13-19%) the risk of DM2 in young and middle-aged women .
The 11-year prospective Iowa Women's Health Study, carried out with postmenopausal woman verified that the intake of both types of coffee, caffeinated and decaffeinated, was inversely associated to the risk of DM2 . In accordance to this, the Nurses' Health Study I (1989-1990) revealed a 16% lower concentration of C-peptide in individuals who ingested at least 4 cups of caffeinated or decaffeinated coffee per day, indicating that the chronic consumption of caffeinated/decaffeinated coffee might reduce insulin secretion since it decreases C-peptide secretion, a marker of insulin secretion  and reducing insulin secretion is consistent with increased insulin sensitivity. The results from these studies indicate that coffee constituents other than caffeine might have a protective role against DM2.
Additionally, an epidemiological study indicated that coffee processing seems to have an effect in the risk of DM2 and pointed an advantage of the filtered coffee over the boiled one (without filtering) in reducing the risk of DM2 . Since the lipidic substances from coffee grains, namely cafestol and kahweol, are removed in filtered coffee [16, 17], it is reasonable to suggest that these substances might act indirectly by increasing the risk of DM2. Moreover, another epidemiological study observed that the protective effect of coffee intake depended on the doses  and a prospective study reported that both current and former (~20 ago) coffee consumers had, respectively, 62% and 64% reduction in the risk of DM2 .
As verified, not all studies have observed an inverse association between coffee consumption and the risk of DM2. In fact, a Finnish cohort study didn't report this association . In addition, a study in Pima Indians, a population with high prevalence of DM2, didn't find different incidence of DM2 among coffee consumers and who those who never drink coffee . Nevertheless, a systematic review elaborated from nine cohort studies supports the inverse association between coffee consumption and the risk of DM2. The individuals who ingested 4-6 cups per day and those with higher intake (more than 6 cups of coffee per day) had 28% and 35% lower risks of DM2 when compared to the lowest ingestion category (less than 2 cups or none daily) .
Can caffeine reduce the risk of DM2?
Among coffee constituents, caffeine (1, 3, 7 trimethylxanthine) has received more attention due to its physiological and pharmacological properties, mainly regarding its effect on sleep reduction and stimulant properties .
Caffeine can be completely absorbed by the stomach and small intestine within 45 minutes after intake and it reaches maximum concentration in the bloodstream in 15-120 minutes . Once absorbed, caffeine is distributed all over the body . In line with this, Biaggioni et al  showed linear correlations between the concentrations of caffeine in plasma and brain (r = 0.86) and between concentrations in plasma and kidney (r = 0.91). Besides, Eskenazi  demonstrated that caffeine can cross the placenta and be found in the mother's milk.
Caffeine metabolization takes place in the liver, starting by the removal of the methyl 1 and 7 groups in a reaction catalyzed by cytochrome P450, enabling the formation of three methylxanthine groups: paraxantine (84%), theobromine (12%) e theophylline (4%). Each component has a different role in human physiology; in particular, paraxantine increases lypolisis; theobromine stimulates blood vessels dilatation and increases the urine volume; and theophylline controls the glucose metabolism .
Blood concentrations of caffeine or its metabolites reflect caffeine intake in the previous hours . However, caffeine intake may not correlate strongly with coffee intake, as it also depends on the intake of other sources of caffeine. Table 2 shows the caffeine/magnesium content of selected food and drink.
The mean per capita caffeine intake in the Western society is 300 mg/d, essentially consumed from dietary sources such as coffee, tea, cola drinks and chocolate . Data from the National Health and Nutrition Examination Surveys (NHANES III) showed that the American population consumes nearly 236 mg/d of caffeine from coffee and tea . In Brazil, literature about caffeine intake is scarce. A research carried out in Rio de Janeiro city among pregnant women under care at a maternal infant unit found out the caffeine consumption to be 56.2 mg/d, being coffee (~40 mg) the most significant food source, followed by tea (~11 mg) and chocolate powder (~5 mg) .
Human studies indicate that caffeine intake of ~500 mg/d does not lead to dehydration or water imbalance [31, 32]. Moreover, moderate caffeine intake (~400 mg/d) is not associated with increased risk of hypertension, heart disease, osteoporosis, or high plasma cholesterol .
The Canadian Clinical Practice Guidelines  reported that for the average adult, a daily caffeine intake of 400-450 mg is not associated with any adverse effects. The recommendation for pregnant women and those who are breastfeeding is reduced to 300 mg/day; and for children, it is limited to their age (Table 3).
Some of the above mentioned researches have examined the association between decaffeinated coffee intake and risk of DM2 [8, 13, 14, 35, 36]. Three out of five studies have found significantly positive association between decaffeinated coffee intake and risk of DM2 and in one of these studies decaffeinated coffee tended to be associated with a lower risk of DM2. Besides, Wu et al  reported similar associations with lower plasma C-peptide concentrations and the intake of caffeinated and decaffeinated coffee, suggesting that both types of coffee exert a beneficial effect on insulin sensitivity. It follows from this that coffee components other than caffeine may be responsible for these effects.
Mechanisms underlying the protective effects of coffee intake on DM2
Up to the moment, several mechanisms of action as well as the precise coffee constituent responsible for the association between coffee intake and DM2 have been proposed. Figure 1 is the summary of studies listed bellow in text.
The hypothesis that coffee consumption lowers the risk of DM2 involves several possible mechanisms as its likely effects on obesity and insulin sensitivity, which are important risk factors for DM2 . In accordance to this, Tagliabue et al  proposed that coffee consumption might stimulate thermogenesis. Some studies showed that caffeine intake is inversely associated with body weight gain and satiety. Lopez-Garcia et al , in his latest research of a 12-year follow-up assessing men and women showed that individuals who consumed coffee lost more weight than those who did not.
Besides, a randomized, placebo-controlled and double-blind study with overweight and moderately obese men and women noticed that the intake of a high-caffeine diet (~524 mg/d) reduces body weight, fat mass and waist circumference, and increases the satiety, when compared to a low-caffeine diet (~151 mg/d) . Accordingly, Kovacs et al  observed that high caffeine consumption (511 mg/d) led to higher satiety than low caffeine intake (149 mg/d).
Additionally, coffee influences the secretion of gastrointestinal peptides such as glucagon-like peptide-1 (GLP-1) and gastric inhibitory polypeptide (GIP), lowering glucose absorption in the small intestine [41, 42], and activating central anorexigenic peptides (POMC/CART) as well as inhibiting orexigenic peptides (AgRP/NPY) [43, 44]. In accordance to this, McCarty  reports a higher GLP-1 production after the intake of drinks containing chlorogenic acid, such as coffee. Another suggested mechanism is the direct stimulation of pancreatic beta cells by caffeine and theophylline .
The beneficial effects of coffee's constituents other than caffeine on insulin sensitivity should be considered. Coffee is a major source of the polyphenol chlorogenic acid in the human diet and may affect glucose metabolism by different mechanisms: increasing insulin sensitivity ; inhibiting glucose absorption ; inhibiting or retarding the action of α-glucosidase ; inhibiting glucose transporters at the intestinal stage ; reducing or inhibiting glucose-6-phosphatase hydrolysis at the hepatic stage, what may reduce plasma glucose output, leading to reduced plasma glucose concentration [51–54]. Moreover, this acid neutralizes the deleterious effects of free fatty acids over the function of beta cells in insulin-resistant overweight individuals, reducing the risk of DM2 . However, it is important to take into account potential confounding by other foods sources of chlorogenic acid, such as apples .
Furthermore, it has been suggested that the inhibition of iron absorption by polyphenol compounds present in coffee might be one of the mechanisms underlying the protective effects of coffee intake on glucose metabolism  as evidences points that higher body iron stores are associated with an increased risk for DM2 . In line with this, the induction of iron deficiency in impaired glucose tolerant subjects has improved insulin sensitivity .
Each cup (237 mL; 8 fl oz) of regular instant coffee has nearly 7 mg of magnesium (Table 2), a micronutrient involved in glucose homeostasis [58–60]. Preliminary data evidenced an association between low dietary magnesium intake and insulin resistance . Accordingly, low plasma magnesium concentrations were found in the Pima Indians, probably due to their high degree of insulin resistance .
For many years, diet has been noticed as an important modifiable determinant of chronic diseases such as DM2. The association between coffee intake and reduction in the risk of DM2 development is plausible and has been consistently demonstrated in longitudinal studies in diverse populations.
The majority of epidemiological studies, as well as the systematic review about the issue, indicate that the long-term intake of coffee, caffeinated or decaffeinated, can reduce the risk of DM2, being moderate coffee intake (≥4 cups of coffee/d of 150 mL or ≥400 mg of caffeine/d) the disclosed benefic dose. It is noticeable that results of most studies suggest a dose-response relation, with greater reductions in DM2 risk in the higher levels of coffee intake, and that adjusting the associations for potential confounding normally strengthened this inverse association. Even though none of the studies found any negative effects of coffee over the risk of DM2, it is also important to highlight that habitual coffee/caffeine consumption have been related to deleterious effects such as bone loss in elderly postmenopausal women, increases in serum homocysteine and cholesterol and blood pressure, as well as risk of coronary heart disease.
Currently, several substances other than caffeine, e.g. chlorogenic acid and magnesium, have been suggested as responsible for the protective effect of coffee in the risk of DM2. However, since it is difficult to control all confounder's variables and consider individual's behaviors, the precise coffee constituent responsible for this association remains uncertain, as well as the mechanisms underlying the beneficial effects of coffee intake over glucose metabolism.
Although habitual moderate coffee intake seems to be safe and reduce the risk of DM2, referenced researchers  in the theme state that it is early to recommend an increase in coffee consumption as a public health strategy for preventing diseases.
World Health Organization (WHO): Diet, nutrition and the prevention of chronic diseases. 2003, Geneva: WHO/FAO. Expert Consultation on diet, nutrition and prevention of chronic diseases
McCarthy MI: Growing evidence for diabetes susceptibility genes from genome scan data. Curr Diab Rep. 2003, 3 (2): 159-167. 10.1007/s11892-003-0040-y.
Keijzers GB, De Galan BE, Tack CJ, Smits P: Caffeine can decrease insulin sensitivity in humans. Diabetes Care. 2002, 25 (2): 364-369. 10.2337/diacare.25.2.364.
Duffey KJ, Popkin BM: Shifts in patterns and consumption of beverages between 1965 and 2002. Obesity. 2007, 15 (11): 2739-2747. 10.1038/oby.2007.326.
Paynter NP, Yeh HC, Voutilainen S, Schmidt MI, Heiss G, Folsom AR, Brancati FL, Kao WH: Coffee and sweetened beverage consumption and the risk of type 2 diabetes mellitus. The atherosclerosis risk in communities study. Am J Epidemiol. 2006, 164 (11): 1075-1084. 10.1093/aje/kwj323.
Iso H, Date C, Wakal K, Fukui M, Tamakoshi A: The relationship between green tea and total caffeine intake and risk for self-reported type 2 diabetes among Japanese adults. Ann Intern Med. 2006, 144 (8): 554-562.
Van Dam RM, Feskens EJ: Coffee consumption and risk of type 2 diabetes mellitus. Lancet. 2002, 360 (9344): 1477-1478. 10.1016/S0140-6736(02)11436-X.
Salazar-Martinez E, Willet WC, Ascherio A, Manson JE, Leitzmann MF, Stampfer MJ, Hu FB: Coffee consumption and risk for type 2 diabetes mellitus. Ann Intern Med. 2004, 140 (1): 1-8.
Carlsson S, Hammar N, Grill V, Kaprio J: Coffee consumption and risk of type 2 diabetes in Finnish twins. Int J Epidemiol. 2004, 33 (3): 616-617. 10.1093/ije/dyh185.
Rosengren A, Dotevall A, Wilhelmsen L, Thelle D, Johansson S: Coffee and incidence of diabetes in Swedish women: a prospective 18-year follow-up study. J Intern Med. 2004, 255 (1): 89-95. 10.1046/j.1365-2796.2003.01260.x.
Tuomilehto J, Hu G, Bidel S, Lindström J, Jousilahti P: Coffee consumption and risk of type 2 diabetes mellitus among middle-aged Finnish men and women. JAMA. 2004, 291 (10): 1213-1219. 10.1001/jama.291.10.1213.
Department of Agriculture Agricultural Research Service: USDA National Nutrient Database for Standard Reference. 2007, 10.2337/diacare.29.02.06.dc05-1512.
Van Dam RM, Willett WC, Manson JE, Hu FB: Coffee, caffeine, and risk of type 2 diabetes: a prospective cohort study in younger and middle-aged U.S. women. Diabetes Care. 2006, 29 (2): 398-403. 10.1001/archinte.166.12.1311.
Pereira MA, Parker ED, Folsom AR: Coffee consumption and risk of type 2 diabetes mellitus: an 11-year prospective study of 28 812 postmenopausal women. Arch Intern Med. 2006, 166 (12): 1311-1316. 10.2337/diacare.28.6.1390.
Wu T, Willett WC, Hankinson SE, Giovannucci E: Caffeinated coffee, decaffeinated coffee, and caffeine in relation to plasma C-peptide levels, a marker of insulin secretion, in U.S. women. Diabetes Care. 2005, 28 (6): 1390-1396. 10.1016/0140-6736(90)91302-Q.
Zock PL, Katan MB, Merkus MP, van Dusseldorp M, Harryvan JL: Effect of a lipid-rich fraction from boiled coffee on serum cholesterol. Lancet. 1990, 335 (8700): 1235-1237. 10.1016/0140-6736(90)91302-Q.
Weusten-Van der Wouw MPME, Katan MB, Viani R, Huggett AC, Liardon R, Lund-Larsen PG, Thelle DS, Ahola I, Aro A, Meyboom S, Beynen AC: 3 Identity of the cholesterol-raising factor from boiled coffee and its effects on liver function enzymes. J Lipid Res. 1994, 35 (8): 721-733. 10.2337/dc06-1084.
Smith B, Wingard DL, Smith TC, Kritz-Silverstein D, Barret-Connor E: Does coffee consumption reduce the risk of type 2 diabetes in individuals with impaired glucose?. Diabetes Care. 2006, 29 (11): 2385-2390. 10.1016/S0140-6736(03)12583-4.
Reunanen A, Heliövaara M, Aho K: Coffee consumption and risk of type 2 diabetes mellitus. Lancet. 2003, 361 (9358): 702-703. 10.2337/diacare.26.7.2211.
Saremi A, Tulloch-Reid M, Knowler WC: Coffee consumption and the incidence of type 2 diabetes. Diabetes Care. 2003, 26 (7): 2211-2212. 10.1001/jama.294.1.97.
Van Dam RM, Hu FB: Coffee consumption and risk of type 2 diabetes: A systematic review. JAMA. 2005, 294 (1): 97-104. 10.1001/jama.294.1.97.
Graham DM: Caffeine: its identity, dietary sources, intake and biological effects. Nutr Rev. 1978, 36 (4): 97-102.
Sinclair CJD, Geiger JD: Caffeine use in sport: a pharmacological review. J Sports Med Phys Fitness. 2000, 40 (1): 71-79. 10.1007/BF00609587.
Newton R, Broughton LJ, Lind MJ, Morrison PJ, Rogers HJ, Bradbrook ID: Plasma and salivary pharmacokinetics of caffeine in man. Eur J Clin Pharmacol. 1981, 21 (1): 45-52. 10.2337/diacare.25.2.399.
Biaggioni I, Davis SN: Caffeine: A Cause of insulin resistance?. Diabetes Care. 2002, 25 (2): 399-400. 10.1056/NEJM199911253412210.
Eskenazi B: Caffeine: filtering the facts. N Engl J Med. 1999, 341 (22): 1688-1689. 10.1056/NEJM199911253412210.
Kalow W, Tang BK: The use of caffeine for enzymatic assays: A critical appraisal. Clin Pharmacol Ther. 1993, 53 (5): 503-514. 10.1007/BF01061844.
Blanchard J, Sawers SJ: Comparative pharmacokinetics of caffeine. J Pharmacokinet Biopharm. 1983, 11 (2): 109-126. 10.1016/0278-6915(95)00093-3.
Barone JJ, Roberts HR: Caffeine consumption. Food Chem Toxicol. 1996, 34 (1): 119-129. 10.1590/S0102-311X2005000600042.
Souza RAG, Sichieri R: Caffeine intake and food sources of caffeine and prematurity: a case-control study. Cad Saude Publica. 2005, 21 (6): 1919-1928. 10.1590/S0102-311X2005000600042. [Article in Portuguese]
Armstrong L: Caffeine, body fluid-electrolyte balance, and exercise performance. Int J Sports Nutr Exerc Metab. 2002, 12 (2): 189-206.
Armstrong L, Pumerantz AC, Roti MW, Judelson DA, Watson G, Dias JC, Sokmen B, Casa DJ, Maresh CM, Lieberman H, Kellogg M: Fluidelectrolyte and renal indices of hydration during eleven days of controlled caffeine consumption. Int J Sports Nutr Exerc Metab. 2005, 15 (3): 252-265. 10.1080/0265203021000007840.
Nawrot P, Jordan S, Eastwood J, Rotstein J, Hugenholtz A, Feeley M: Effects of caffeine on human health. Food Addit Contam. 2003, 20 (1): 1-30. 10.1080/0265203021000007840.
Canadian Clinical Practice Guidelines: Originating Associations. 2008
Greenberg JA, Boozer CN, Geliebter A: Coffee, diabetes, and weight control. Am J Clin Nutr. 2006, 84 (4): 682-93. 10.1017/S0007114508944135.
Hamer M, Witte DR, Mosdøl A, Marmot MG, Brunner EJ: Prospective study of coffee and tea consumption in relation to risk of type 2 diabetes mellitus among men and women: The Whitehall II study. Br J Nutr. 2008, 100 (5): 1046-1053. 10.1017/S0007114508944135.
Tagliabue A, Terracina D, Cena H, Turconi G, Lanzola E, Montomoli C: Coffee induced thermogenesis and skin temperature. Int J Obes Relat Metab Disord. 1994, 18 (8): 537-541.
Lopez-Garcia E, van Dam RM, Rajpathak S, Willett WC, Manson JE, Hu FB: Changes in caffeine intake and long-term weight change in men and women. Am J Clin Nutr. 2006, 83 (3): 674-680. 10.1038/oby.2005.142.
Westerterp-Plantenga MS, Lejeune MPGM, Kovacs EMR: Body weight loss and weight maintenance in relation to habitual caffeine intake and green tea supplementation. Obes Res. 2005, 13 (7): 1195-1204. 10.1079/BJN20041061.
Kovacs EMR, Lejeune MPGM, Nijs I, Westerterp-Plantenga MS: Effects of green tea on weight maintenance after body-weight loss. Br J Nutr. 2004, 91 (3): 431-437. 10.1172/JCI116186.
Nauck MA, Heimesaat MM, Orskov C, Holst JJ, Ebert R, Creutzfeldt W: Preserved incretin activity of glucagon-like peptide 1 [7-36 amide] but not of synthetic human gastric inhibitory polypeptide in patients with type-2 diabetes mellitus. J Clin Invest. 1993, 91 (1): 301-307. 10.2337/diabetes.50.11.2497.
Meier JJ, Hucking K, Holst JJ, Deacon CF, Schmiegel WH, Nauck MA: Reduced insulinotropic effect of gastric inhibitory polypeptide in first-degree relatives of patients with type 2 diabetes. Diabetes. 2001, 50 (11): 2497-2504. 10.2337/diabetes.50.11.2497.
Martins MN, Telles MM, Zemdegs JC, Andrade IS, Ribeiro EB, Miranda A: Evaluation of new leptin fragments on food intake and body weight of normal rats. Regul Pept. 2008, 153 (1-3): 77-82. 10.1515/BC.2003.016.
Carvalheira JB, Ribeiro EB, Folli F, Velloso LA, Saad MJ: Interaction between leptin and insulin signaling pathways differentially affects JAK-STAT and PI3-kinase-mediated signaling in rat liver. Biol Chem. 2003, 384 (1): 151-159. 10.1016/j.mehy.2004.03.037.
McCarty MF: A chlorogenic acid-induced increase in GLP-1 production may mediate the impact of heavy coffee consumption on diabetes risk. Med Hypotheses. 2005, 64 (4): 848-853. 10.1136/bmj.300.6725.642.
Tuomilehto J, Tuomilehto-Wolf E, Virtala E, LaPorte R: Coffee consumption as trigger for insulin dependent diabetes mellitus in childhood. Br Med J. 1990, 300 (6725): 642-643. 10.1002/(SICI)1097-0010(19990301)79:3<362::AID-JSFA256>3.0.CO;2-D.
Clifford MN: Chlorogenic acids an other cinnamates-nature, occurrence and dietary burden. J Sci Food Agric. 1999, 79 (3): 362-372. 10.1002/(SICI)1097-0010(19990301)79:3<362::AID-JSFA256>3.0.CO;2-D.
Johnston KL, Clifford MN, Morgan LM: Coffee acutely modifies gastrointestinal hormone secretion and glucose tolerance in humans: glycemic effects of chlorogenic acid and caffeine. Am J Clin Nutr. 2003, 78 (4): 728-733. 10.1021/jf001251u.
Matsui T, Ueda T, Oki T, Sugita K, Terahara N, Matsumoto K: alpha-Glucosidase inhibitory action of natural acylated anthocyanins. 1. Survey of natural pigments with potent inhibitory activity. J Agric Food Chem. 2001, 49 (4): 1948-1951. 10.1021/jf0006832.
Kobayashi Y, Suzuki M, Satsu H, Arai S, Hara Y, Suzuki K, Miyamoto Y, Shimizu M: Green tea polyphenols inhibit the sodium-dependent glucose transporter of intestinal epithelial cells by a competitive mechanism. J Agric Food Chem. 2000, 48 (11): 5618-5623. 10.2337/diabetes.33.2.192.
Newgard CB, Foster DW, McGarry JD: Evidence for suppression of hepatic glucose-6-phosphatase with carbohydrate feeding. Diabetes. 1984, 33 (2): 192-195. 10.2337/diabetes.33.2.192.
Youn JH, Youn MS, Bergman RN: Synergism of glucose and fructose in net glycogen synthesis in perfused rat livers. J Biol Chem. 1996, 261 (34): 15960-15969. 10.1006/abbi.1996.9874.
Arion WJ, Canfield WK, Ramos FC, Schindler PW, Burger HJ, Hemmerle H, Schubert G, Below P, Herling AW: Chlorogenic acid and hydroxynitrobenzaldehyde: new inhibitors of hepatic glucose 6-phosphatase. Arch Biochem Biophys. 1997, 339 (2): 315-322. 10.1016/S0378-8741(01)00335-X.
Andrade-Cetto A, Wiedenfeld H: Hypoglycemic effect of Cecropia obtusifolia on streptozotocin diabetic rats. J Ethnopharmacol. 2001, 78 (2-3): 145-149. 10.1001/archinte.167.2.204-b.
Mascitelli L, Pezzetta F, Sullivan JL: Inhibition of iron absorption by coffee and the reduced risk of type 2 diabetes mellitus. Arch Intern Med. 2007, 167 (2): 1311-1316. 10.1001/jama.291.6.711.
Jiang R, Manson JE, Meigs JB, Ma J, Rifai N, Hu FB: Body iron stores in relation to risk of type 2 diabetes in apparently healthy women. JAMA. 2004, 291 (6): 711-717. 10.1001/jama.291.6.711.
Facchini FS, Saylor KL: Effect of iron depletion on cardiovascular risk factors: studies in carbohydrate intolerant patients. Ann NY Acad Sci. 2002, 967 (1): 342-351. 10.1016/S0098-2997(02)00090-0.
Barbagallo M, Dominguez LJ, Galioto A, Ferlisi A, Cani C, Malfa L, Pineo A, Busardo' A, Paolisso G: Role of magnesium in insulin action, diabetes and cardio-metabolic syndrome X. Mol Aspects Med. 2003, 24 (1-3): 39-52. 10.1007/BF00404136.
Paolisso G, Scheen A, D'Onofrio F, Lefebvre P: Magnesium and glucose homeostasis. Diabetologia. 1990, 33 (9): 511-514. 10.1016/S0895-7061(96)00342-1.
Paolisso G, Barbagallo M: Hypertension, diabetes mellitus, and insulin resistance: the role of intracellular magnesium. Am J Hypertens. 1997, 10 (3): 346-355. 10.1016/S0895-7061(99)00041-2.
Humphries S, Kushner H, Falkner B: Low dietary magnesium is associated with insulin resistance in a sample of young, nondiabetic Black Americans. Am J Hypertens. 1999, 12 (8 Pt 1): 747-756. 10.1210/jc.80.4.1382.
Paolisso G, Ravussin E: Intracellular magnesium and insulin resistance: results in Pima Indians and Caucasians. J Clin Endocrinol Metab. 1995, 80 (4): 1382-1385. 10.1007/s00125-004-1573-6.
van Dam RM, Dekker JM, Nijpels G, Stehouwer CD, Bouter LM, Heine RJ: Coffee consumption and incidence of impaired fasting glucose, impaired glucose tolerance, and type 2 diabetes: the Hoorn Study. Diabetologia. 2004, 47 (12): 2152-2159. 10.2337/dc06-2089.
Schulze MB, Hoffmann K, Boeing H, Linseisen J, Rohrmann S, Möhlig M, Pfeiffer AF, Spranger J, Thamer C, Häring HU, Fritsche A, Joost HG: An accurate risk score based on anthropometric, dietary, and lifestyle factors to predict the development of type 2 diabetes. Diabetes Care. 2007, 30 (3): 510-515. 10.2337/dc06-2089.
Odegaard AO, Pereira MA, Koh WP, Arakawa K, Lee HP, Yu MC: Coffee, tea, and incident type 2 diabetes: the Singapore Chinese Health Study. Am J Clin Nutr. 2008, 88 (4): 979-985.
Pimentel GD and Zemdegs JCS are recipients from the National Council for Scientific and Technological (CNPq, Brazil).
The authors declare that they have no competing interests.
GDP made substantial contributions to conception and design, acquisition of data. He has also been involved in drafting the manuscript and revised it critically as corresponding author. GDP and JCSZ screened all titles and abstracts, assessed the full text papers and checked the extracted study data and participated in the critical revision of include articles and in the writing of the manuscript. JAT and JFM have been involved in developing the electronic-search strategy, contributed in the acquisition of data, and revised the manuscript critically. All authors have made substantial contributions to the analysis and interpretation of include articles. All authors have given final approval of the submitted version.