Potential Beneficial Effects of Chenopodium quinoa and Salvia hispanica L. in Glucose Homeostasis in Hyperglycemic Mice Model ^†

Abstract

Impaired glucose homeostasis is associated with an increased risk of developing metabolic alterations. In this study, a model in which mice treated with streptozotocin were fed a high-fat diet was used to mimic early stages of the onset of metabolic disorders, and different bread formulations were administrated to evaluate the effect of replacing wheat flour with Chenopodium quinoa (Q) (25%) and Salvia hispanica L. (Sh) (20%). Plasmatic glucose and insulin concentrations were quantified and the homeostasis model assessment (HOMAir) was calculated. Q and Sh showed a lower tendency to hyperglycemia compared to wheat bread (WB). Besides, these low glucose levels were accompanied by three-fold lower values of HOMAir respect to WB, suggesting an improved insulin sensitivity. Thus, inclusion of C. quinoa and S. hispanica into bread formulations could improve the control of glucose homeostasis, which could help to prevent/ameliorate metabolic glucose alterations.

1. Introduction

A good control in glucose homeostasis has shown to be determinant in the prevention and improvement of metabolic disorders, such as insulin resistance, obesity, or type 2 diabetes (T2D) [1]. In recent years, Latin-American crops have become a focus of study because of their beneficial nutritional properties [2]. Chenopodium quinoa and Salvia hispanica L. in bread formulations [3] have shown an enhanced insulin signaling modulating peroxisome proliferator-activated receptor (PPAR)-γ activation, which has been related to a marked improvement of whole-body insulin sensitivity in T2D patients [2,4].

Thus, the objective of the present investigation was to evaluate the inclusion of flour from C. quinoa and S. hispanica as a substitute to wheat flour in bread formulations in the control of glucose homeostasis in a hyperglycemic-mouse model.

2. Materials and Methods

2.1. Sample Breads

White quinoa seeds (Organic quinoa Real©) from ANAPQUI, La Paz, Bolivia, were purchased from Ekologikoak (Bizkaia, Spain). Chia flour was purchased from the Primaria Premium Raw Materials Company (Valencia, Spain). Wheat flour was provided from a local market. Three bread formulations were prepared: white quinoa (Q) at 25% and chia (Sh) at 20% and were compared to wheat bread (WB), as a control [3].

2.2. Experiment Design

Female C57BL/6 mice were obtained from Centro de Investigaciones Biológicas (CIB-CSIC) in Madrid, Spain. All animals were injected intraperitoneally with 2 low doses of streptozotocin (25 mg/kg) and they received a high-fat diet for 3 weeks. Animals were distributed into groups depending on the administered bread, and they received 3 doses (14 mg/day/animal) per week during all the treatment.

2.3. Glucose and Insulin Concentration

Insulin and glucose concentrations were determined in plasma samples. Insulin was measured by ELISA kit (RAB0817-1KT, Sigma-Aldrich, Darmstadt, Germany) and glucose (MAK263-1KT, Sigma-Aldrich, Darmstadt, Germany).

2.4. Homeostatic Model Assessment of Insulin Resistance (HOMAir)

Insulin resistance (IR) was defined as the HOMAir value and was calculated according to the following formula: [insulin (μU/mL) × glycaemia (mg/dL)]/405 [5].

2.5. Statistical Analysis

Multiple ANOVA and Fisher’s least significant differences (LSD) were applied to establish statistically significant differences. Statistical analyses were performed with the software Statgraphics Centurion XVI and the significance level was established at p < 0.05.

3. Results and Discussion

This study showed that metabolic alterations occurring at early stages, onset, and disease progression derived from impairment of glucose homeostasis, improved with the inclusion of flours obtained from C. quinoa and S. hispanica into bread formulations. Hyperglycemia is a hallmark of a profoundly altered metabolism, which is associated with stress oxidative and inflammatory response in the liver [1]. In this study, glucose blood concentrations decreased, following this order: WB > Q > Sh (Figure 1), displaying a positive effect in Q and Sh and suggesting a more controlled glucose homeostasis, which could have important consequences limiting the hepatic endogenous glucose output and liver metabolic stress [6]. The glycemic index is used to determinate the total rise in blood glucose level; however, it could not reflect the real absorption and modulation in glucose homeostasis. The latter is supported by the lack of differences in the glycemic index reported between C. quinoa and WB and the higher transcript levels of PPAR-γ in C. quinoa [2]. These observations are concordant with the low HOMAir value reported in animals fed C. quinoa (Figure 1).

HOMAir is considered an index of insulin resistance, which is a risk factor of the progression of type 2 diabetes. Animals administered with WB showed values above 3.8, which is indicative of insulin resistance, meanwhile Q and Sh were below. In line with the glucose levels, Sh obtained 1.5-fold lower HOMAir than Q. The effect of S. hispanica seeds in a state of insulin resistance has shown an improved sensitivity associated with increased expression levels of the peroxisome proliferator-activated receptor-γ coactivator-1α (PGC-1α) and promoting the absorption of glucose by muscle in obese rats [7]. In line with these positive effects of flour from S. hispanica, it was demonstrated that long-term supplementation with S. hispanica attenuates cardiovascular risk factors with the reduction of systolic blood pressure and serum C-reactive protein concentration in diabetic patients [8].

4. Conclusions

Replacing flour wheat with S. hispanica and C. quinoa flour could exert beneficial effects, improving insulin resistance and control of glucose homeostasis and, thus, promoting a better metabolic modulation that could prevent the onset or progress of early metabolic alterations.