Dipteryx alata Vogel May Improve Lipid Profile and Atherogenic Indices in Wistar Rats Dipteryx alata and Atherogenic Indices

Abstract

Worldwide prevalence of noncommunicable chronic degenerative diseases is among the main causes of death worldwide. The consumption of some foods such as nuts and seeds may be beneficial in preventing these diseases. Dipteryx alata Vogel (DA), known popularly as Baru, belongs to the family Fabaceae and is a native fruit tree from the Brazilian savanna. The purpose of this study was to evaluate the use of seeds of DA on the metabolic and oxidative profile of Wistar rats. Animals were divided randomly into four groups (n = 10): G1 (control group), and G2 (treated with DA 20%), G3 (treated with DA 30%), and G4 (treated with DA 40%). After 40 days, animals were euthanized and metabolic and oxidative profiles were analyzed (glycemia, cholesterol, triglycerides [TGs], high-density lipoprotein-cholesterol [HDL-c], very low-density lipoprotein-cholesterol [VLDL-c], low-density lipoprotein-cholesterol [LDL-c], C reactive protein, aspartate aminotransferase, alanine aminotransferase, Lee index, weight, visceral fat, ferric reducing ability of plasma, and ferric–xylenol orange method. The use of the seeds was effective in reducing TGs, VLDL-c, LDL-c, and increasing HDL-c but did not interfere in the percentage of weight gain, visceral fat, levels of total cholesterol, and oxidative stress. Based on our results, it is possible to say that the use of DA may improve the lipid profile of Wistar rats and we may suggest that the consumption of DA almonds or products prepared with them may be an effective option for the intake of healthy products.

Introduction

Worldwide prevalence of noncommunicable chronic degenerative diseases is among the main causes of the burden on the healthcare system and death worldwide. Metabolic syndrome and cardiovascular complications consist in a collection of several conditions related to hereditary or environmental circumstances related to cardiovascular issues.^1
–3

The consumption of some foods such as nuts and seeds has been found beneficial in preventing these diseases mainly because of its composition in unsaturated fatty acids and many other bioactive compounds. The consumption of Dipteryx alata Vogel (DA) seeds is becoming very popular in Brazil because of the pleasant flavor and nutritional content.^4

–7

DA, popularly known as Baru, Cumaru, Cumbaru, Bugueiro, Barujo, and Cambaru, belongs to the family Fabaceae and is a native fruit tree from the Brazilian savanna. Brazilian savanna is also known as Cerrado and it is considered as the world's richest savanna in biodiversity. Among so many fruits in this biome, Baru is one that is less explored. Its elliptical dark brown almonds are protected by a thin brown shell and a sweet yellow pulp and possess a wide range of applications as substrate for the pharmaceutical industry. Popularly it is used as a vermifuge and to treat rheumatism and anemia.^8,9

There is a high content of protein in the Baru seeds (250–300 g/kg) with predominance of a fraction similar to legumin-type protein. It also contains fibers, lipids (especially unsaturated fatty acids such as oleic, erucic, and gadoleic acid), vitamins, and minerals such as calcium, iron, and zinc. It also contains phytate and tannins.^10

–14 Fernandes et al.¹⁵ showed that the lipid and protein contents present in almonds of DA are similar to those of true nuts.

Local people commonly use the roasted almonds as an ingredient in sweets and in gastronomy in the central western region of Brazil. One of the reasons of the increasing popularity of the DA almond is because of its flavor that is similar to peanut.^6,16

The use of plants for functional purposes in the production of processed products can be a viable and easy option for preventing diseases. Although some authors have shown that the almond of DA can be used as a complementary source of nutritional components, only a few studies about its effects are found in the literature. For this reason, the aim of this study was to evaluate the effects of consumption of DA almonds on the metabolic and oxidative profile of Wistar rats.

Materials and Methods

Ethical principles

This research was approved by the Animal Research Ethics Committee of the Faculty of Food Technology of Marília (FATEC), Marília,—SP, Brazil, under protocol number 001/2016. Animals were fed and watered ad libitum during the experimental period and were cared for according to the recommendations of the Canadian Council's “Guide for the care and use of experimental animals.”

Preparation of the supplemented rat feed

DA almonds were obtained from markets in the city of Unaí–Minas Gerais State, Brazil, and were toasted in an air circulating oven at 130°C for 30 min, immediately before the preparation of the three types of rat feed that were manufactured weekly in a proportion of, respectively, 20%, 30%, and 40% of toasted almonds and commercial feed. Almonds and rat feed were crushed, mixed and molded into pellets that were dried in an air circulating oven at 65°C for about 8 h, stored in polyethylene packaging, and refrigerated at 5°C until its utilization.

Analysis of the rat feed

The rat feed with DA almonds was analyzed to identify the moisture content by gravimetric method in an oven at 105°C for 16 h until it reached a constant weight. Lipids were evaluated by the Soxhlet extraction. Total nitrogen was analyzed by the Kjeldahl method. A muffle furnace at 550°C was used to study the ash content, carbohydrates by difference, as well as crude fiber.¹⁷ Analyses were performed in triplicate.

Determination of vitamin C, anthocyanin, carotenoids, and antioxidant activity

Vitamin C, anthocyanin, carotenoids, and antioxidant activity were determined, respectively, according to Terada et al. ¹⁸; Lees and Francis¹⁹; Higby²⁰; and Singleton et al.²¹ These determinations were performed at the Biochemistry and Nutrition Laboratory—FATEC (SP, Brazil).

Animal groups

Male Wistar rats (180–220 g) were maintained in the vivarium at the FATEC, SP, Brazil, and housed in collective cages under a dark/light cycle of 12 h, room temperature of 22°C ± 2°C, and relative air humidity of 60% ± 5%. After acclimation for 7 days to laboratory conditions, the animals were divided (n = 10) randomly into G1 that were fed water and rat food ad libitum, G2 that were fed water and rat food supplemented with DA 20% ad libitum, G3 that were fed water and rat food supplemented with DA 30% ad libitum, and G4 that were fed water and rat food supplemented with DA 40% ad libitum. Weight gain was evaluated every 3 days.

Blood collection and analysis

After 40 days of treatment, the animals suffered euthanasia with a lethal intraperitoneal injection of thiopental (200 mg/kg) until complete sedation. After death, blood samples were collected from the vena cava for biochemical profile evaluation of glucose, total cholesterol (TC), low-density lipoprotein-cholesterol (LDL-c), very low-density lipoprotein-cholesterol (VLDL-c), high-density lipoprotein-cholesterol (HDL-c), triglycerides (TGs), high-sensitivity-C reactive protein (hs-CRP), aspartate aminotransferase (AST), and alanine aminotransferase (ALT).

Atherogenic index (AI), atherogenic coefficient (AC), cardiac risk ratio 1 (CRR1), cardiac risk ratio 2 (CRR2), and non-HDL-c levels were calculated according to Erejuwa et al. ²² and Ahmadvand et al. ²³

Lipid peroxidation was estimated by the analysis of the ferric–xylenol orange (FOX) method, according to Jiang et al. ²⁴ and adapted for plasma and serum by Arab and Steghens.²⁵ This methodology is based on the oxidation of ferrous ion (Fe²⁺) to ferric ion (Fe³⁺) in the presence of lipidic hydroxyperoxides and formation of Fe³⁺ complexes with xylenol orange, which generates a characteristic color that can be measured by the spectrophotometer. Oxidative stress in plasma was evaluated using blood samples collected in heparinized syringes and subsequently centrifuged at 503 g for 5 min at 4°C. Then 20 μL of the collected plasma was added to 180 μL of a solution prepared with absolute methanol 81%, xylenol orange 100 μmol, sulfuric acid 25 mM, butylated hydroxy toluene 40 mM, and ferrous sulfate 250 μmol. Absorbance readings were taken at 560 nm (ΔA_560 nm) and the concentration of the solution was calculated for each sample and related to ΔA_560 nm of a hydrogen peroxide standard solution tested in parallel.

For the evaluation of the antioxidant capacity of plasma, the ferric reducing ability of plasma (FRAP) method was used. Three solutions were prepared: A (acetate buffer: 300 mM, pH 3.6, and hydrochloric acid 40 mM HCl), B (2,4,6-tri [2-pyridyl]-s-triazine 10 mM), and C (ferric chloride hexahydrate 20 mM). These solutions were mixed to obtain a ratio of 10:1:1 (A:B:C, v/v). Blood was collected in heparinized syringes and centrifuged at 349 g for 10 min at 4°C. Then, 0.8 mL of the obtained plasma was added to a mixture of deionized water (2.4 mL) with the solution already prepared (0.25 mL). Absorbance readings were taken at 593 nm (ΔA_593 nm) and the concentration of the solution was calculated for each sample and related to ΔA_593 nm of a ferrous sulfate standard solution tested in parallel.²⁶

Both FRAP and FOX were evaluated only in the control group and in G4 (group treated with the rat feed with 40% of Baru seeds).

Anthropometric parameters

After euthanasia, weight and length of the animal were evaluated to find the Lee index = cube root of body weight (g)/nose–anus length (cm), and the percentage of weight gain.²⁷

Statistical analysis

Analysis of variance supplemented with Tukey's test, and Student's test were used for statistical analysis, and the variables are presented as mean and standard error of mean, adopting a 5% level of significance.

Results

We did not find significant differences among raw and roasted seeds in the levels of vitamin C, anthocyanin, carotenoids, and antioxidant activity (Table 1).

Table 1.

Mean and Standard Deviation for the Results of Vitamin C, Anthocyanin, Carotenoid, and Antioxidant Activity in Raw and Roasted Seeds of Baru (Dipteryx alata)

Parameters	Raw Baru	Roasted Baru
Vitamin C (mg/100 g)	18.8 ± 0.16^a	18.5 ± 0.13^a
Anthocyanin (mg/100 g)	0.65 ± 0.07^a	0.55 ± 0.09^a
Carotenoid (mg/100 g)	0.66 ± 0.05^a	0.55 ± 0.83^a
Antioxidant activity (%)	99.49 ± 0.01^a	99.42 ± 0.02^a

Indicates a significant difference between the treatments at a level of 5%.

Table 2 shows that the use of DA almonds did not interfere in the weight gain, visceral fat, and Lee index, but significantly decreased levels of TGs, VLDL-c, LDL-c, and hs-CRP. It increased significantly levels of HDL-c.

Table 2.

Mean and Standard Deviation of the Anthropometric and Biochemical Parameters in the Control Group (G1) and Groups Treated with Dipteryx alata Vogel (G2–G4)

Parameters	G1	G2	G3	G4
Weight gain (g)	140.22 ± 17.65^a	120.26 ± 16.90^a	130.26 ± 22.03^a	139.12 ± 18.00^a
Lee index (g/cm)	2.72 ± 0.11^a	3.09 ± 0.16^a	3.01 ± 0.09^a	2.98 ± 0.10^a
Glucose (mg/dL)	140.63 ± 19.84^a	132.13 ± 6.98^a	129.25 ± 9.16^a	133.88 ± 10.22^a
TC (mg/dL)	67.75 ± 8.21^a	69.75 ± 7.91^a	63.50 ± 7.84^a	69.88 ± 10.26^a
TG (mg/dL)	141.13 ± 47.6^b	61.38 ± 18.8^a	55.88 ± 17.4^a	65.00 ± 21.38^a
VLDL-c (mg/dL)	12.13 ± 3.04^b	8.38 ± 1.77^a	8.75 ± 1.49^a	10.38 ± 0.13^a
LDL-c (mg/dL)	16.50 ± 4.04^b	11.63 ± 2.07^a	12.00 ± 1.20^a	13.08 ± 0.92^a
HDL-c (mg/dL)	52.38 ± 4.50^a	59.88 ± 5.49^b	56.75 ± 5.37^b	59.88 ± 6.71^b
hs-CRP (mg/dL)	0.42 ± 0.01^b	0.03 ± 0.01^a	0.03 ± 0.02^a	0.03 ± 0.01^a
AST (U/L)	50.50 ± 8.77^ab	43.75 ± 4.8^a	44.75 ± 5.7^a	50.63 ± 4.17^b
ALT (U/L)	140.57 ± 24.57^b	105.25 ± 16.25^a	100.25 ± 18.1^a	136.50 ± 16.53^b

Different superscript letters indicate a significant difference between the treatments at a level of 5%.

G1, control group; G2, group treated with DA 20%; G3, group treated with DA 30%; G4, group treated with DA 40%.

ALT, alanine aminotransferase; AST, aspartate aminotransferase; DA, Dipteryx alata Vogel; HDL-c, high-density lipoprotein-cholesterol; hs-CRP, high-sensitivity C reactive protein; LDL-c, low-density lipoprotein-cholesterol; TC, total cholesterol; TGs, triglycerides; VLDL-c, very low-density lipoprotein-cholesterol.

DA improved AI, AC, CRR1 and CRR2, and non-HDL-c levels (Table 3).

Table 3.

Mean and Standard Deviation of Cardiovascular Indices of the Control Group (G1) and Groups Treated with Dipteryx alata Vogel (G2–G4)

Parameters	G1	G2	G3	G4
AI	0.41 ± 0.14^b	−0.01 ± 0.20^a	0.00 ± 0.12^a	0.01 ± 0.16^a
AC	0.29 ± 0.10^b	0.14 ± 0.08^a	0.15 ± 0.07^a	0.13 ± 0.09^a
CRR1	1.39 ± 0.10^b	1.17 ± 0.11^a	1.18 ± 0.10^a	1.17 ± 0.14^a
CCR2	0.31 ± 0.07^b	0.20 ± 0.04^a	0.22 ± 0.03^a	0.22 ± 0.03^a
Non-HDL-c	15.08 ± 0.12^b	10.15 ± 0.17^a	9.2 ± 0.05^a	10.34 ± 0.26^a

Different superscript letters indicate a significant difference between the treatments at a level of 5%.

G1, control Group; G2, group treated with DA 20%; G3, group treated with DA 30%; G4, group treated with DA 40%.

AC, atherogenic coefficient; AI, atherogenic index, CRR, cardiac risk ratio; DA, Dipteryx alata.

We did not observe modifications in FRAP and FOX evaluation in G1 and G4 as shown in Table 4.

Table 4.

Mean and Standard Deviation for the Results for Ferric Reducing Ability of Plasma and Ferric–Xylenol Orange Method in G1 (Control Group) and G4 (Treated with Dipteryx alata Vogel 40%)

Parameter	G1	G4
FRAP	2.098 ± 0.319^a	2.273 ± 0.432^a
FOX	154.664 ± 16.748^a	145.414 ± 6.871^a

Same superscript letters indicate that there is no significant difference between the treatments at a level of 5%.

FOX, ferric–xylenol orange; FRAP, ferric reducing ability of plasma.

The composition of the rat feed (moisture, lipids, total nitrogen, ashes, carbohydrates, and crude fiber) did not significantly differ from that prepared with 20%, 30%, and 40% of seeds of DA (data not shown).

Discussion

The demand for natural products has been growing rapidly worldwide mainly because of the presence of phytochemicals. Many studies point to the use of plants as a rich source of natural antioxidant compounds and active agents for the pharmaceutical and cosmetic industry.²⁸

Our results show important reduction in TG, LDL-c, and in the AIs after treating the animals with DA seed. Bento et al. ⁷ studied the effects of DA almonds in the lipid profile in 25 mildly hypercholesterolemic subjects supplemented with 20 g/day of Baru almonds or placebo and found that, comparing with placebo, supplementation with the seeds decreased TC, LDL-c, and non-HDL-c. They did not find significant modifications in anthropometric parameters such as body weight, fat, and body mass index. Authors did not find significant modifications in the body weight and body fat.

Fernandes¹⁶ studied the effects of consumption of Baru almond in the lipid profile and peroxidation of Wistar rats fed a high-fat diet and observed reduction in the levels of TC and TG, and improvement of the HDL-c levels. In our work, we did not observe reduction in cholesterol levels.

A plethora of studies have demonstrated that the evaluation of TG, LDL-c, HDL-c, and non-HDL-c may be helpful in cardiovascular disease risk evaluation. Apolipoprotein B is important for the binding of LDL-c particles, and consequent absorption of cholesterol by the cell. In excess, this apolipoprotein may positively correlate with non-HDL-c levels, which is an important trigger to the atherogenic process. Increased values of non-HDL-c associated with hypertriglyceridemia and in presence of abnormal glycemia increase the risk for cardiovascular diseases. In our study, all the groups treated with DA almonds presented lower LDL-c and TG levels and higher values of HDL-c than the control group. This indicates that this plant may help prevent degenerative chronic diseases.^22,29,30

Increase in the levels of AST and ALT may indicate the destruction of liver cells.³¹ We did not observe increase in the level of these enzymes after animals consumed DA almonds, which may indicate that it is safe for consumption. No studies were found for comparison of the effects of consumption of the DA almonds in the levels of AST and ALT.

The AIs are also strongly linked to the development and progression of cardiovascular disease.^23,32,33 In our study, the use of DA almond promoted significantly the reduction in CRR, AI, AC, and non-HDL-c, showing that this seed may help in the prevention of cardiovascular disease. Bento et al. ⁷ did not find changes in the ratios CCR1 and CCR2 after treatment with Baru, unlike our results.

Studies have shown that medicinal plants can also control oxidative damage and help maintenance of health and prevent chronic diseases by reducing oxidative stress, which is defined as the presence of active oxygen species exceeding the available antioxidant buffering capacity. These products may damage proteins, carbohydrates, lipids, and DNA, by changing structure and functions of the cell. This condition is well known to be involved in the pathogenesis of lifestyle-related diseases, including hypertension, diabetes mellitus, cardiovascular diseases, cancer, and several others.^34,35 Our results did not show statistical differences in FRAP and FOX in animals treated with DA. In contrast, Siqueira et al. ³⁶ showed that the consumption of aqueous extracts of the Baru almond by rats may provide tissue protection against iron-induced oxidative stress, possibly because of the presence of phenolic compounds. They observed reduction in the carbonyl levels in heart, liver, and spleen of rats supplemented with iron and reduction in the iron-induced lipid oxidation in the liver and spleen. With these results, authors have concluded that the consumption of Baru seeds may protect tissues against iron-induced oxidative stress possibly because of the presence of phytic acid and other phenolic compounds.

Our results showed the presence of vitamin C, carotenoids, anthocyanins, and antioxidant activity in the crude and roasted seeds of DA. Authors have shown that these seeds also present lupane triterpenoids as lupeol, lupenone, betulin, and 28-OH-lupenone. These compounds may be related to the effects on the lipid profile and AIs. Furthermore, some of the observed effects of DA almonds may be associated with the content of vitamin C, vitamin E, n-3-polyunsaturated fatty acids, selenium, and fibers. Some authors have shown that these compounds are associated with reduction of risk factors for obesity, diabetes, metabolic syndrome, and cardiovascular diseases because of their capacity of acting as antioxidants. Thus they are able to reduce the effects of free radicals and inflammation processes in the organism.^{6,7,11,37

–40} The reduction in inflammation may be corroborated by the levels of hs-CRP observed in the treated groups. This protein is known as an inflammatory biomarker commonly regulated by cytokines as interleukin-1 (IL-1), IL-6, and tumor necrosis factor α that can be associated with low-grade inflammation processes.⁴¹ It is interesting to say that the raw and roasted seeds did not show significant differences regarding the content of carotenoids, vitamin C, anthocyanins, and antioxidant activity, indicating that the thermal processing characteristic of food preparation does not interfere with these beneficial properties.

In conclusion, our study showed that the use of DA seeds may improve lipid profile and indices for cardiovascular disease in Wistar rats. Based on these findings, we may suggest that the consumption of these seeds or products prepared with them may be an effective option for prevention of the occurrence of cardiovascular risk factors and other pathologies associated with increased levels of TGs, LDL-c, hs-CRP, and decreased levels of HDL-c.

Footnotes

Author Disclosure Statement

No competing financial interests exist.

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