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Title: High intake of phytochemical-rich foods is related to pre-diabetes: a case-control study
Maryam Abshirini, MSPH student, Department of Community Nutrition, School of Nutritional Sciences and Dietetics, Tehran University of Medical Sciences, Tehran, Iran
Fariba Bagheri, MSPH, Department of Community Nutrition, School of Nutritional Sciences and Dietetics, Tehran University of Medical Sciences, Tehran, Iran
Fereydoun Siassi, Ph.D, Professor, Department of Community Nutrition, School of Nutritional Sciences and Dietetics, Tehran University of Medical Sciences, Tehran, Iran
Fariba Koohdani, Ph.D, Professor, Department of Cellular, Molecular Nutrition, School of Nutritional Sciences and Dietetics, Tehran University of Medical Sciences, Tehran, Iran.
Gity Sotoudeh, Ph.D, Professor, Department of Community Nutrition, School of Nutritional Sciences and Dietetics, Tehran University of Medical Sciences, Tehran, Iran

Corresponding author: 
Gity Sotoudeh, Department of Community Nutrition, School of Nutritional Sciences and Dietetics, Tehran University of Medical Sciences, Hojatdost street, Naderi street, Keshavarz Blv., Tehran, Iran.
Email: HYPERLINK "mailto:gsotodeh@tums.ac.ir"gsotodeh@tums.ac.ir, Tel: 09123906617, Fax: +98-21-88974462


Abstract
Obejective: Phytochemical-rich foods contain natural bioactive compounds with protective effects on chronic diseases. For the first time, this case-control study was conducted to investigate the relationship between dietary phytochemical index (DPI) and the risk of pre-diabetes.
 Methods: Three hundred participants were assigned into 150 pre-diabetic (cases) and 150 healthy (controls) groups. Anthropometric values, fasting blood glucose (FBG) and 2-hour oral glucose tolerance test (OGTT) were measured. The DPI was calculated based on data collected from 168-item validated food frequency questionnaire.
Results: The sex-specific energy-adjusted DPI was inversely related to FBS and OGTT (p <0.001). The odds ratio (OR) of pre-diabetes was assessed across sex-specific energy-adjusted DPI quartiles. After adjusting for BMI, physical activity, education, dietary intake of energy, fiber, carbohydrate (% of energy), fat (% of energy) and protein (% of energy), the OR of pre-diabetes across the sex-specific energy-adjusted DPI quartiles decreased significantly (p-trend <0.001).
 Conclusion: We found that more intakes of phytochemical-rich foods may have protective properties against pre-diabetes.

Keywords:  Dietary phytochemical index, fasting blood glucose, insulin resistance, pre-diabetes, Fruit, Vegetables, Phytochemical intake.  







Introduction
Pre-diabetes has been defined as a progression from normal range of glucose tolerance to clinical diabetes mellitus (T2DM). It represents a stage of impaired glucose tolerance (IGT, 2-h oral glucose tolerance test (OGTT) 140�199 mg/dl) and impaired fasting glucose (IFG, 110�125 mg/dl) [1]. Five to ten percent of people with pre-diabetes will progress to T2DM per year [2]. The prevalence of pre-diabetes has increased worldwide during the past decades [3]. National survey of Tehran Lipid and Glucose Study reported that from each thousand  men and women, 46 men and 38 women became pre-diabetic after 9 years follow up [4].
Previous studies linked diet rich in fresh fruits and vegetables, whole grains, nuts, legumes and plant-based foods, which are high in phytochemicals, fibre, and antioxidants with chronic diseases risk reduction [5,6]. Current data on relating diet with insulin and glucose homeostasis are insufficient. Three year follow-up in Tehran adults, showed higher intake of phytochemical-rich foods was negatively associated with occurrence of hyperinsulinemia and insulin resistance [7]. Data from other prospective and meta-analysis studies have shown an inverse relationship between consumption of fruits and vegetables and the risk of obesity and abdominal obesity as main predictors of glucose intolerance and pre-diabetes [8, 9].
Chemical compounds found abundantly in plant foods including polyphenols, phytoestrogenes and organosulfur and plant sterols by acting as antioxidant and balancing the inflammation, provide protection against development of insulin resistance, abnormal glucose and lipid disturbances [10-12]. 
For the first time, health promotional effects of phytochemicals proposed by McCarty as the phytochemical index (PI), which defined as the percent of dietary calories derived from foods rich in phytochemicals. PI could be an alternative for quantifying the phytochemicals in consumed foods for improvement in dietary intake during a dietary modification program [13]. This index is a simple method for assessment of phytochemical intake and despite its limitations, could provide important background for diet quality and may have high practical and clinical use for food selection improvement [14].
Few studies have been conducted to investigate the association between DPI and the risk of chronic diseases. Several prospective studies investigated the relation of DPI with cardio metabolic risk factors, lipid profile changes, and visceral obesity in healthy subjects [15-17]. A study in overweight young adult showed inverse association between DPI with weight gain and blood biomarkers of oxidative stress [14]. However, association of DPI and risk of per-diabetes has not been determined yet. In this study we aimed to investigate the relationship between DPI and pre-diabetes morbidity in a case�control study.

 Materials and Methods  
300 men and women including 150 healthy and 150 pre-diabetic subjects from diabetes screening center in Shahreza, Iran were invited for this study. The methods of study were described previously [18], and are briefly described here. All the participants had the age above 30 and met one of the criteria including body mass index (BMI) e"25 kg/m2, having a family history of diabetes or reporting of at least two symptoms of diabetes prior to enrollment to the study. Subjects were not enrolled into the study if they were using alcohol, drug and any tobacco products, having BMI e" 40 kg/m2. In addition, pregnant or lactation women, subjects with special diet during last year, subjects with history of  heart disease, diabetes, hypertension, dyslipidaemia, renal or hepatic failure and multiple sclerosis were not included in the study. Pre-diabetic subjects had fasting blood glucose (FBG) within 100 to 125 mg/dl or 2-h OGTT 140-199 mg/dl, diagnosed less than three months before enrollment to the study. Controls subjects had FBG <100 mg/dl or OGTT <140 mg/dl during screening. We used the frequency matching method and matched the two groups by age and sex. The age-frame for matching was 35�44, 45�54 and 55�65 years. This study was approved by the Ethics Committee of Tehran University of Medical Sciences. All participants read and signed a written informed consent prior to participation. 
Height was measured to the nearest 0.1 cm while standing barefoot using the Seca 216 stadiometer. Body weight was determined while participants wore undergarments, using a Seca scale to the nearest 0.1 kg. WC was measured using tape at the midpoint between the lowest rib and the iliac crest. Waist circumference (WC) e" 94 for men and e" 80 for women were considered as the cut- points for central obesity [19]. Physical activity was assessed with the short form of the International Physical Activity Questionnaire (IPAQ) [20]. This measure was selected to assess the physical activity during the previous week by multiplying the duration and frequency of activity days to the metabolic equivalent task (MET) value of the activity. The total of the scores was considered as the total physical activity per week.
Blood samples were taken after at least 8 hours fasting for FBG measurement. Moreover, the subjects underwent a 2-h OGTT. The plasma glucose level was measured at 546 nm using the photometric method (glucose oxidase method).
Dietary data were collected using a validated semi-quantitative FFQ with 168 food items [21]. Trained dietitian asked participants to report their consumption frequency for each food items consumed during the previous year on a daily, weekly, or monthly basis. Portion sizes of foods were reported in household measures then converted to grams. The Excel program analysed the nutrients of each food item. Food items were analysed for energy content using Nutritionist 4 software (First Databank Inc., Hearst Corp, San Bruno, CA) modified for Iranian foods.

The DPI was calculated based on the assessment method proposed by McCarty [13] as the percent of dietary calorie derived from foods rich in phytochemicals; [PI=(daily energy derived from phytochemical-rich foods (kcal)/ total daily energy derived from food intake (kcal)�100]. Fruits and vegetable )except potatoes(, legumes, whole grains, nuts, seeds, olive and olive oil were considered as the photochemical-rich foods categories.
The Kolmogorov�Smirnov test was used to evaluate the normality of the data. Energy-adjusted DPI were determined using the residual method [22]. The energy-adjusted DPI was categorized based on sex-specific quartiles. The mean value of quantitative variables were compared across the sex-specific energy-adjusted DPI quartiles categories using the ANOVA and Kruskal-Wallis test for normal and non-normal distribution, respectively. To assess the overall trends of odd ratio (OR) across the sex-specific energy-adjusted DPI quartiles categories the simple logistic regression models was used: Model 1= crude. Model 2= adjusted for BMI, physical activity, education, dietary intake of energy, fiber, carbohydrate (% of energy), fat (% of energy) and protein (% of energy). All statistical analysis were conducted using SPSS version 16.0 and p- values < 0.05 were considered significant.

Result
Table 1 presents characteristics of participants across sex-specific quartiles of energy-adjusted DPI. Participants in the upper quartiles had lower FBS, OGTT (p -trend <0.001), and higher physical activity level (p-trend=0.04). The mean energy-adjusted DPI score of pre-diabetic participants was significantly lower than the control group (28.6 �13.4 vs. 40.6�23.3, respectively).
The relative contributions of different phytocemical-rich food groups to DPI were relatively similar in men and women as shown in Table 2. Our participants consumed a higher percentage of calories from fruits, legumes, vegetables, nut and seeds, olive, olive oil and whole grains, respectively.  

The DPI score was inversely related with pre-diabetes. Compared with participants in the lowest quartile of DPI, those in the highest quartile had significantly lower OR for pre-diabetes (model 1: OR 0.1, 95% CI 0.04-0.21), which remained significant after further adjustment for BMI, physical activity, education, dietary intake of energy, fiber, carbohydrate (% of energy), fat (% of energy) and protein (% of energy), (model 2: OR 0.09, 95% CI 0.03-0.25) (p-trend <0.001) (Table 3).

Discussion
In this case-control study we determined the association of DPI with chance of pre-diabetes. Our results showed that compared to the control group, pre-diabetic subjects had lower DPI score. After adjustment for BMI, physical activity, education, intake of energy, fiber, carbohydrate (% of energy), fat (% of energy) and protein (% of energy), subjects with higher sex-specific energy-adjusted DPI had significantly lower OR of pre-diabetes. In the present study, mean score of DPI for the control and pre-diabetic groups were 28.6�13.4 and 40.6�23.3, respectively. Our findings also showed that pre-diabetic subjects consumed fewer calorie from fruits, vegetables, nuts, legumes, olive and olive oil. 
The association and potential effects of dietary phytochemicals on prevention of T2DM and hyperinsulinemia have been confirmed in previous studies [23, 24]. However, the relationship of DPI and pre-diabetes morbidity has not been determined yet. To our knowledge, the present study is the first study reporting relationship between DPI and pre-diabetes with considering the FBG and OGTT in a case-control study.  
Dietary phytochemicals have been shown to lower postprandial glycaemia and development of glucose intolerance [25]. Prior studies have confirmed intake of plant-based foods, rich in phytochemicals, were associated with improvement in glucose tolerance and insulin sensitivity in overweight subjects [25, 26]. Data from Tehran Lipid and Glucose Study found higher DPI was associated with lower FBG in healthy subjects. However, this study had lack of data on the postprandial glucose level [7].
In the present study, the result showed a decreasing trend of OR of pre-diabetes across the increasing quartiles of DPI. This result is supported by the report from a controlled cross-over study which showed consuming whole grains, fruits and vegetables had beneficial effects on FBG and insulin resistance in obese subjects with elevated FBG [27]. However, DPI did not show significant association with HbA1c in another study in normal and overweight participants [14]. 
We previously on the present study population reported that participants who had the higher adherence to the fruits, vegetables and legumes dietary pattern had lower FBG and OGTT [18]. Regarding the sources of DPI, fruits (approximately 46%) were the main contributor to DPI, followed by the legumes, vegetables, nuts and seeds, olive ,olive oil and whole grains. Therefore, increased consumption of these high-nutrient, lower energy foods could be a beneficial dietary target for prevention of IGT as well as attenuating the development of chronic diseases. 
 A prospective study in healthy women demonstrated that higher intake of green leafy vegetables and whole fruits was associated with a lower risk of T2DM, whereas increase in fruit juice intake did not appear to be beneficial for reducing the risk [28]. Polyphenols, found abundantly in berry, apple and cherry, are among the main phytochemicals compounds with anti-hyperglycemic properties [25]. Evidence from large prospective cohort studies supported  this fact that high consumption of whole fruits specially blueberries, grapes, and apples, is strongly related to a reduced risk of  developing T2DM [29]. There are several mechanisms through which the dietary phytochemicals could improve postprandial glucose as well as long term glucose metabolism [11]. Phytochemicals derived from plant foods has shown to possess beneficial effects including improvement of pancreatic �-cell function by boosting antioxidant system, increasing insulin sensitivity and enhancing uptake of  insulin-dependent glucose transporter 4 (GLUT4) [30, 31].
Our results was in conflict with previous studies, not showed decreasing trend in BMI, WC and energy intake with increasing sex-specific energy-adjusted DPI quartiles. A cross-sectional study reported that DPI score was strongly and negatively associated with BMI, WC, waist-to-hip ratio and body fat in overweight adults. Furthermore, this study  showed a significant inverse association between DPI and weight gain over the previous year of study [14]. Data from a large longitudinal study on healthy adults revealed DPI assessed at baseline of study was inversely associated with body weight and WC and 3 years weight gain. Therefore, high DPI and consumption of phytochemical-rich foods could be beneficial for prevention of obesity and maintenance of body weight which are linked to imbalance glucose homeostasis and T2DM. However,  in this study DPI was not adjusted for energy [32].
Plant based foods and vegetarian diet are high in many dietary phytochemicals which appear to be related to the lower body weight and risk of metabolic disorders [33-35]. Phytochemical-rich foods have lower calorie and glycemic index which explain the reduced risk of obesity [36, 37]. Moreover, plant phytochemical have strong anti-obesity effects by targeting adipocyte lifecycle in different ways, including inhibiting proliferation and increasing apoptosis in adipocytes [34]. 
Our study has some limitations including the case-control nature of the study does not allow cause and effect conclusions. On the other hand, the assessing dietary intake using a food frequency questionnaire may have measurement error. Not considering the non-calorie phytochemical-rich foods such as green and black tea, spices, type and source of phytochmical and food processing are among the other limitations of our study. Despite these limitations, this is the first study to examine the relationship of DPI and pre-diabetes prevalence in a case-control design. Our study supported this fact that higher intake of dietary phytochemicals may be beneficial for pre-diabetes prevention. Nevertheless, it would be important to investigate these findings in other groups and prospective studies as well.

Acknowledgment
This research project was supported by Tehran University of Medical Sciences (TUMS) (grant no. 93-454-76).































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Table 1. Characteristics of participants across the sex-specific quartiles of energy-adjusted phytochemical index

VariablesQ1
(n74)
(<16.47)Q2
(n75)
(16.47-28.13)Q3
(n77)
(28.14-52.45)Q4
(n74)
(>52.45)
P- trend
Mean � SEM (Sex n(%)
Male
Female

Age (years)
Education (years)

Dietary supplement 
Intake n (%)
Yes 
No

BMI(a) (kg/m2)
		
25 (8.3)
49 (16.3)
47.9�0.9
8.4�0.5


17 (5.7)
57 (19)

27.6�0.4

26 (8.7) 
49 (16.3)
47.7�0.8
6.9�0.4


8 (2.7)
67 (22.3)

27.9�0.5
26 (17)
51 (8.7)
46.9�0.8
8.5�0.5


12 (4)
65 (21.7)

28.8�0.4
		
25 (8.3)
49 (16.3)
47.6�0.8
7.7�0.4


13 (4.3)
61 (20.3)

28.5�0.4
0.9**

0.7*
0.7*



0.2**

0.1*WC (a) (cm)
91�1.391.7�1.392.3�1.190.7�1.30.8*FBS(a) (mg/dl)
102.9�1.594.3�1.895.2�1.790.3�1.5<0.001*OGTT (a) (mg/dl)

137.3�2.2131.4�2.2132.2�2.2127 �1.7
0.001*PA(a) (MET/h/week)
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2236.4�23.42358.9�32.52411.3�34.32319�46.90.01*(a) BMI: body mass index; WC: waist circumference; FBS: fasting blood glucose; OGTT: oral�glucose tolerance test; PA: physical activity
* P-value is for ANOVA test 
**P-value is for Chi square test 

Table 2. Contribution of food groups to energy-adjusted dietary phytochemical index (%)  
Food groupsFruitVegetablesLegumesNuts and seedsOlive, Olive oilWhole grainsMale48.613.7
14.1203.20.2Female44.212.216.812.93.90.3Total45.712.715.915.33.70.3
























Table 3. Odds ratio (OR) and 95% confidence intervals (95% CIs) for pre-diabetes across sex-specific quartiles of energy-adjusted dietary phytochemical index 
Phytochemical indexQ1
(n74)
(<16.47)Q2
(n75)
(16.47-28.13)Q3
(n77)
(28.14-52.45)Q4
(n74)
(>52.45)P-trendModel 1OR
95%CI1.000.25
(0.12-0.52)0.24
(0.11-0.49)0.10
(0.04-0.21)<0.001P-value<0.001<0.001<0.001Model 2OR
95%CI1.000.41
(0.16-1.01)0.2
(0.11-0.75)0.09
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