Original researchConsumption of citrus and cruciferous vegetables with incident type 2 diabetes mellitus based on a meta-analysis of prospective study☆
Introduction
Over the past two decades, the prevalence of type 2 diabetes mellitus (T2DM) has been elevated markedly worldwide [1]. Studies have shown that increased exercise, quit smoking, weight lost among obese individuals, adoption of a diet rich in fiber may reduce the incidence of T2DM [2], [3].
Dietary factors are potential risk factors, but the relationship between fruit and vegetable intake and incidence of T2DM is not fully understood. Although a meta-analysis published in 2010, which included six prospective cohort studies, reported that greater intake of fruits was not associated with risk of T2DM [Summary relative risk (SRR) = 0.93, 95% confidence interval (CI): 0.83 to 1.01] [4], the updated two meta-analyses, which included 10 prospective cohort studies, found a protective role for fruit intake [5], [6]. Furthermore, a significantly inverse association between citrus fruits consumption and risk of T2DM was observed among one cohort of Chinese women with intermediate levels of citrus consumption (10.0–25.2 g/day) as compared to low citrus consumption, but no significant association was found for a high intake (median, 44.4 g/day) [7]. Others, studies from USA and Europe found a non-significant association between citrus consumption and risk of T2DM [8], [9], [10]. Likewise, mixed results were reported for the association between CV consumption and T2DM [7], [8], [9], [10]. Like other fruits, both citrus fruits and CV contain many nutrients, such as carotenoids, polyphenols, flavonoids, limonoids, folic acid, and dietary fiber, which are believed to delay the digestion and absorption of carbohydrates and suppress postprandial glycemia, oxidative stress, and low-grade inflammation [10]. Importantly, CVs are unique in that they are rich sources of glucosinolates [11], [12], the precursors of isothiocyanates and indole-3-carbinol [13], [14]. Researches have observed a protective role of isothiocyanate in the development of DM via improved glucose tolerance and insulin signaling [15]. In addition, researches [16], [17] have indicated that extract of citrus fruits has hypoglycemic effects in the diabetic experimental models.
In this meta-analysis, we focused on only prospective cohort studies due to the following: (1) no systematic reviews and meta-analyses have looked at the effects of intake of citrus fruits and CV on the overall risk of T2DM. (2) Both case-control and cross-sectional designs are subjected to the selection and recall bias, and the prospective evidences on these associations have been reported with inconsistent results [7], [8], [9], [10], [18]. (3) Only several clinical trials investigate the effects of intakes of citrus [19] and CV [20], [21] on the development of complications in patients with T2DM, but not the development of T2DM. Therefore, to better characterize this issue, we conducted a meta-analysis of prospective cohort studies to evaluate such relationships following the meta-analysis of observational studies in epidemiology (MOOSE) [22].
Section snippets
Search strategy
For this meta-analysis, searches were performed electronically through the MEDLINE and EMBASE database for prospective cohort studies examining the association between citrus fruits and CV intake and risk of T2DM. We supplemented this search by hand-searching the reference lists of the retrieved articles. The search strategy used the following terms of Medical Subject Headings or keywords: (1) fruit OR citrus OR grapefruit OR orange OR tangerine OR lemon OR lime OR cruciferous vegetables OR
Search results
The search strategy generated 1439 citations (Fig. 1). We assessed titles and abstracts and 23 were considered of potential value and the full text was retrieved for detailed evaluation. Eighteen of these 23 articles were subsequently excluded from the meta-analysis for various reasons. No additional articles were included from reference review. So, a total of 5 publications with 7 prospective cohort studies were used in this meta-analysis [7], [8], [9], [10], [18]. Of these, the Nurses’ Health
Discussion
In this meta-analysis of prospective cohort studies, we investigated the association between citrus and CV consumption and T2DM incidence. We found that consumption of CV had a protective role in the T2DM incidence. This association was independent of the main risk factors for cardiovascular disease: smoking, alcohol use, BMI, and physical activity etc. Consumption of citrus fruits did not have a protective role in the T2DM development.
Several laboratory studies might explain an inverse
Conflict of interest
There are no conflicts of interest to declare.
References (48)
- et al.
Global estimates of the prevalence of diabetes for 2010 and 2030
Diabetes Res. Clin. Pract.
(2010) - et al.
Fruit and vegetable consumption and risk of type 2 diabetes mellitus: a dose-response meta-analysis of prospective cohort studies
Nutr. Metab. Cardiovasc. Dis.
(2015) - et al.
Vegetable but not fruit consumption reduces the risk of type 2 diabetes in Chinese women
J. Nutr.
(2008) - et al.
Intake of fruit, berries, and vegetables and risk of type 2 diabetes in Finnish men: the Kuopio Ischaemic Heart Disease Risk Factor Study
Am. J. Clin. Nutr.
(2014) - et al.
A review of mechanisms underlying anticarcinogenicity by brassica vegetables
Chem. Biol. Interact.
(1997) - et al.
Phenethyl isothiocyanate: a comprehensive review of anti-cancer mechanisms
Biochim. Biophys. Acta
(2014) - et al.
In vitro alpha-amylase inhibitory activity and in vivo hypoglycemic effect of methanol extract of Citrus macroptera Montr. fruit
Asian Pac. J. Trop. Biomed.
(2014) - et al.
Effects of red orange juice intake on endothelial function and inflammatory markers in adult subjects with increased cardiovascular risk
Am. J. Clin. Nutr.
(2012) - et al.
Broccoli sprouts powder could improve serum triglyceride and oxidized LDL/LDL-cholesterol ratio in type 2 diabetic patients: a randomized double-blind placebo-controlled clinical trial
Diabetes Res. Clin. Pract.
(2012) - et al.
Meta-analysis in clinical trials
Controlled Clin. Trials
(1986)
Dietary flavonoids intake and risk of type 2 diabetes: a meta-analysis of prospective cohort studies
Clin. Nutr.
Oleanolic acid improves hepatic insulin resistance via antioxidant, hypolipidemic and anti-inflammatory effects
Mol. Cell Endocrinol.
Greater whole-grain intake is associated with lower risk of type 2 diabetes, cardiovascular disease, and weight gain
J. Nutr.
Reproducibility and validity of food intake measurements from a semiquantitative food frequency questionnaire
J. Am. Diet. Assoc.
Reproducibility and validity of dietary patterns assessed with a food-frequency questionnaire
Am. J. Clin. Nutr.
Fruit and vegetable intake and risk of cancer: a prospective cohort study
Am. J. Clin. Nutr.
Fruit, vegetables, and colorectal cancer risk: the European prospective investigation into cancer and nutrition
Am. J. Clin. Nutr.
Meta-analysis of atherogenic index of plasma and other lipid parameters in relation to risk of type 2 diabetes mellitus
Prim. Care Diabetes.
Prevention of type 2 diabetes mellitus by changes in lifestyle among subjects with impaired glucose tolerance
N. Engl. J. Med.
Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin
N. Engl. J. Med.
Fruit and vegetable intake and incidence of type 2 diabetes mellitus: systematic review and meta-analysis
BMJ
Fruit and vegetable intake and risk of type 2 diabetes mellitus: meta-analysis of prospective cohort studies
BMJ Open
A prospective study of fruit and vegetable intake and the risk of type 2 diabetes in women
Diabetes Care
Fruit and vegetable intake and type 2 diabetes: EPIC-InterAct prospective study and meta-analysis
Eur. J. Clin. Nutr.
Cited by (36)
Aryl Hydrocarbon Receptor Activation Coordinates Mouse Small Intestinal Epithelial Cell Programming
2023, Laboratory InvestigationAmerican Association of Clinical Endocrinology Clinical Practice Guideline: Developing a Diabetes Mellitus Comprehensive Care Plan—2022 Update
2022, Endocrine PracticeCitation Excerpt :There is a large body of data indicating that isocaloric substitution of specific macronutrients can improve insulin sensitivity assessed by clamp studies and CVD risk factors.836 These data would generally support macronutrient intake as follows: (1) limitations on fat intake, (2) emphasis on poly/mono-unsaturated fats over saturated fats, (3) no trans fats,835 (4) complex over simple carbohydrates, (5) whole grains over refined grains934, (6) fruits and vegetables,837 (7) dietary fiber,838 and (8) reduced consumption of processed food.839 Dietary enrichment of these macronutrients can enhance insulin sensitivity,836 aligning with the Mediterranean diet and other meal patterns that are epidemiologically associated with reduced prevalence of T2D,839 and predictably would be beneficial based on the role of insulin resistance in the pathophysiology of CMD.
Effect of citrus fruit and juice consumption on risk of developing type 2 diabetes: Evidence on polyphenols from epidemiological and intervention studies
2021, Trends in Food Science and TechnologyCitation Excerpt :A study in postmenopausal women (Women's Health Initiative study) found no association between 100% citrus (orange and grapefruit) and other fruit juice intake and risk of type 2 diabetes, even at high levels of consumption (Auerbach et al., 2017). Similarly, no effect was reported in several other studies (Jia et al., 2016; Murphy, Barrett, Bresnahan, & Barraj, 2017; Palmer, 2008). In a cross-sectional study of females aged 18–76 years, higher intakes of both anthocyanins and flavones improved insulin resistance and lowered high-sensitivity C-reactive protein, while no association was found with flavanone, flavanol and flavan-3-ol intake (Jennings, Welch, Spector, Macgregor, & Cassidy, 2014).
Polyphenol exposure and risk of type 2 diabetes: Dose-response meta-analyses and systematic review of prospective cohort studies
2018, American Journal of Clinical Nutrition
- ☆
Funds of Scientific and Technological Development from Medicine and Healthcare in Shandong Province (2013BJYB05).