BRAZILIAN TYPICAL FOOD WITH POTENTIAL TO IMPROVE LIPID PROFILE

Abstract

ABSTRACT
Tapioca is a food produced from the cassava roots and is commonly used in Brazil to prepare many products.
The aim of this study was to evaluate the effects of tapioca on the metabolic profile of Wistar rats. Twenty
female rats were divided in G1: control group (n=10) and G2: treated group (n=10). The treated group
received tapioca flour mixed to the rat food for 45 days, and the control group received commercial rat food.
Body weight was evaluatedthree times a week. Blood samples were collected to evaluate glycemia, total
cholesterol (TC), LDL-c, HDL-c, and triglycerides (TG). Anthropometric parameters were also evaluatedas
well as atherogenic indices. A significant reduction was observed in the levels of TC, LDL-c, and abdominal
circumference in the treated group although the food intake was significantly higher in this group. The intake
of tapioca positively interferes with the lipid levels.

Full text

ORIGINAL RESEARCH ARTICLE
BRAZILIAN TYPICAL FOOD WITH POTENTIAL TO IMPROVE LIPID PROFILE
1Patrícia Cincotto dos Santos Bueno, 1,2,*Sandra Maria Barbalho, 1Isabela Ramos Araújo de
Medeiros, 1Isabella Vasconcelos Zattiti, 1Claudemir Gregório Mendes, 1ElenLandgraf Guiguer,
1Maricelma Silva Soares De Souza, 1Adriano Cressoni de Araújo and 1Raul J. S. Girio
1School of Medicine, University of Marília (UNIMAR), Av. Higino Muzzi Filho 1001, Marília,
15525-902, São Paulo, Brazil
2Department of Biochemistry and Nutrition, Faculty of Food Technology of Marília (FATEC), São Paulo, Brazil
ARTICLE INFO ABSTRACT
Tapioca is a food produced from the cassava roots and is commonly used in Brazil to prepare many products.
The aim of this study was to evaluate the effects of tapioca on the metabolic profile of Wistar rats. Twenty
female rats were divided in G1: control group (n=10) and G2: treated group (n=10). The treated group
received tapioca flour mixed to the rat food for 45 days, and the control group received commercial rat food.
Body weight was evaluatedthree times a week. Blood samples were collected to evaluate glycemia, total
cholesterol (TC), LDL-c, HDL-c, and triglycerides (TG). Anthropometric parameters were also evaluatedas
well as atherogenic indices. A significant reduction was observed in the levels of TC, LDL-c, and abdominal
circumference in the treated group although the food intake was significantly higher in this group. The intake
of tapioca positively interferes with the lipid levels.
Copyright © 2018, Patrícia Cincotto dos Santos Bueno et al. This is an open access article distributed under the Creative Commons Attribution License, which
permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
INTRODUCTION
The ingestion of many different kinds of foods has been
postulated to improve risk factors of chronic degenerative
diseases such as diabetes, obesity, metabolic syndrome, and
hypertension, which are related to cardiovascular diseases,
cancer, and death. Many of these foods have shown effects
against insulin resistance, dyslipidemia, overweight and
obesity (Telle-Hansen et al., 2017;Santos et al., 2017; Noumiet
al., 2017; Costa et al., 2017; Seo, Kim, 2017; Castellano-
Castillo et al., 2017). Tapioca has been considered in popular
medicine as also having effects under these conditions.
However, few studies are observed in the literature. Tapioca is
an edible starch, produced from the roots of cassava
(Manihotesculenta Crantz), which is used in the preparation of
sweet and savory dishes.
*Corresponding author: Sandra Maria Barbalho,
1School of Medicine, University of Marília (UNIMAR), Av. Higino
Muzzi Filho 1001, Marília, 15525-902, São Paulo, Brazil.
2Department of Biochemistry and Nutrition, Faculty of Food
Technology of Marília (FATEC), São Paulo, Brazil.
It is a plant widely cultivated in several tropical countries and
often consumed as a staple food. The roots provide a cheap
source of carbohydrate and a low content of proteins
(Kanmaniet al., 2018; Silva et al., 2013; Wang et al., 2014;
Maier et al., 2017). The cassava belongs to the family
Euphorbiaceae and is produced in Brazil under the system of
subsistence agriculture. Nowadays tapioca can be considered
one of the most traditional symbols of the cuisine of the North
and Northeast of the country and is used in different dishes
appreciated by the populations of all the income ranges (Oso et
al., 2014; Queirozet al., 2009; Dias, Leonel, 2006). Tapioca is
a very common food for Brazilians, has low cost, and
popularly is associated with the reduction of some
cardiovascular risk factors. For these reasons,the aim of this
study was to evaluate its effects on the metabolic profile of
Wistar rats.
METHODS
Ethical Principle and Group of Animals: This study had the
approval by the Animal Research Ethics Committee of the
ISSN: 2230-9926
International Journal of Development Research
Vol. 08, Issue, 02, pp.18969-18972, February,
2018
Article History:
Received 14th November, 2017
Received in revised form
20th December, 2017
Accepted 23rd January, 2018
Published online 28th February, 2018
Available online at http://www.journalijdr.com
Key Words:
Manihotesculenta
Crantz, Cholesterol,
Glycaemia, Body Weight.
Citation: Patrícia Cincotto dos Santos Bueno, Sandra Maria Barbalho, Isabela Ramos Araújo de Medeiros, Isabella Vasconcelos Zattiti, Claudemir
Gregório Mendes, ElenLandgraf Guiguer, Maricelma Silva Soares De Souza, Adriano Cressoni de Araújo and Raul J. S. Girio, 2018. “Brazilian
typical food with potential to improve lipid profile”, International Journal of Development Research, 8, (02), 18969-18972.
ORIGINAL RESEARCH ARTICLE OPEN ACCESS

Medical School of Marilia (UNIMAR) – Marilia – São Paulo,
Brazil. Twenty female Wistar rats (Rattusnorvegicus),
weighing 180g to 200g, were obtained from the Animal
Experimentation Center - University of Marilia (UNIMAR),
Marilia – São Paulo, Brazil. Seven days before the beginning
of the experimental protocol the female were separated into 2
groups andwas acclimated to the laboratory conditions and
housed in plastic boxes at controlled room temperature (20°C
to 25°C) and light/dark cycle of 12 hours. After acclimation,
female rats were divided in G1: control group (n=10) and G2:
treated group (n=10). The treated group received tapioca flour
during 45 days, and the control group received commercial rat
food. Both groups received water and food ad libitum.
The treated group received the commercial rat food mixed
with the tapioca flour in a ratio of 80:20 (commercial rat
food:tapioca). This mixture was moistened, and the pellets
were reconstituted and dried for later use. Body weight was
evaluatedthree times a week. At the end of the experimental
protocol,the rats were anesthetized with thiopental
(200mg/kg). After death, blood samples were collected to
evaluate the biochemical profile: glycemia, total cholesterol
(TC), HDL-c, and triglycerides (TG). Anthropometric
parameters were also evaluated (Lee Index, body weight,
thoracic circumference; abdominal circumference and visceral
fat weight).
Atherogenic Index (AI), Atherogenic Coefficient (AC), and
Cardiac Risk Ratio 1 (CRR1) were evaluated after Ahmadvand
et al., 2016; Munshi, Joshi and Rane, 2015); Ikewuchi, 2012):
non-HDL-c = Total cholesterol – HDL-c; AI = log (TG/HDL-
c); AC = (TC – HDL-c)/HDL-c; CCR1 = TC/HDL-c, and
CCR2 = LDL-c/HDL-c.
Statistical analysis
All data were expressed as mean ± standard deviation. The
analysis was performed initially by the unpaired T-test for the
variables with distribution or the Man-Whitney test when they
did not present normality. The results were analyzed using the
software BioEstat5.3, and the level of significance was 5%.
RESULTS
In Table 1 it is observed that the animals of the two groups
started the experiment with similar mean body weight. At the
end of the study, no significant difference was observed in the
mean weight gain, Lee index, Body Mass Index, thoracic
circumference, and visceral fat. A significantincrease in food
intake was observed in the treated group but no modifications
were observed in body weight and a reduction was seen in the
abdominal circumference.
Table 1. Food and water intake, nthropometric and biochemical parameters for G1 and G2
Parameters (mg/dL) G1 G2 p-value*
Weight
1
137.8±20.68 148.5±30.52 p = 0.185
Weight
2
224.5±16.54 233.4±15.83 p =0.117
Food intake (g) 82.06±20.15 105.24±17.05 p < 0.000‡
Water intake (mL) 140.17±29.03 133.15±28.56 p = 0.148
Lee Index 296.67±7.52 294.98±8.46 p =0.321
Body mass index 0.54±0.035 0.52±0.038 p =0.492
Weight gain (%) 67.40±35.84 62.38±31.144 p =0.452
T. Circumference 9.25±1.11 8.75±0.35 p = 0.153
A. Circumference 10.6±0.61 10.2±0.35 p = 0.045‡
Visceral fat 1.318±0.42 1.236±0.36 p = 0.323
1Weight at the beginning of the experimental protocol; 2Weight at the end of the experimental
protocol;T. Circumference: Thoracic circumference; A. Circumference: Abdominal circumference;
‡ significant difference.
Table 2. Biochemical parameters of G1 and G2 after the treatment with tapioca
Parameters (mg/dL) G1 G2 p-value*
Glycaemia 155.7±22.52 165.8±20.88 p= 0.156
Triglycerides 129.3±19.00 118.75±24.42 p= 0.158
Cholesterol 164.75±5.59 158.7±5.23 p= 0.0151‡
HDL-c 52.0±5.361 50.4±5.361 p=0.495
LDL-c 98.1±24.735 82.4±4.850 p=0.032‡
‡Significant difference; HDL-c: High-Density Lipoprotein; LDL-c: Low-Density Lipoprotein
Table 3. Atherogenic indices in the experimental protocol for G1 and G2
Parameters (mg/dL) G1 G2 p-value*
Non-HDL-c 119.0±23,317 108.3±5.510 p=0.081
AC 1.23±0.630 1.57±0.413 p=0.095
AI 2.233±0.633 2.579±0.413 p=0.919
CCR1 3.17±0.439 3.170±0.230 p=0.490
CCR2 1.389±0.896 1.652±0.203 p=0.336
AC: Atherogenic Coefficient; AI: Atherogenic Index; CRR1: Cardiac Risk Ratio 1;
CRR2: Cardiac Risk Ratio 2.
18970 Patrícia Cincotto dos Santos Bueno et al. Brazilian typical food with potential to improve lipid profile

DISCUSSION
Tapioca is the starch product extracted from the cassava roots
that are peeled, crushed, disintegrated, concentrated,
dehydrated and dried. It is a natural polysaccharide, consisting
of linear chains (amylose) and branched chains (amylopectin)
and obtained through roots of manioc roots. The result is a
product with a high carbohydrate content, low in protein,
lipids, and minerals. The tapioca flour presents 6.14% of
resistant starch, which does not undergo enzymatic digestionin
humans (Queirozet al., 2009). In Brazil, thepopulationhas been
using tapioca as an alternative to reduce weight. Also, our
results show areduction in the abdominal circumference and in
the food intake, although we did not observe significant
differences in the body weight of the animals. Ble-Castilloet
al. (2017) evaluated the effects of banana starch on the
appetite and found no associated effect on the subjective
appetite ratings or gut hormones but helped to reduce meal
size. Resistant starch supplementation is also related to the
reduction of body weight by some authors (Si et al., 2017;
Barczynska et al., 2016). Diet may interfere in the composition
of the human microbiome that displays several systemic
actions. Resistant starch may exhibit a plethora of health
benefits, including the increase in the ratio of Firmicutes:
Bacteroidetes (Maier et al., 2017). Furthermore, the
fermentation of resistant starch in the colon leads to the
production of acids and derivatives of organic acids with short
chain as acetate, butyrate, and propionate.
These compounds act in the reduction of
hypercholesterolemia. Our results also showed areductionon
the cholesterol and LDL-c levels. By reducing serum
cholesterol levels, resistant starch acts in the prevention of
diseases such as constipation, type 2 diabetes, andcoronary
heart disease. Some studies report a decrease in postprandial
blood glucose or insulin levels associated with ingestion of
resistant starch compared to the consumption of digestible
starch. Similarly to our results, other researchers found no
modification in the glycaemia (Reshmi, Sudha and
Shashirekha, 2017; Koh and Rowling, 2017; Matsuda et al.,
2016).
Liu et al. (2006) studied the effects of retrograded tapioca
starch on the ovarian hormone deficiency-induced
hypercholesterolemia in rats and showed that tapioca leads to a
hypocholesterolemic effect in ovariectomized rats but not in
sham-operated animals. Okafor et al. (2016) studied the effects
of four different blends of cassava-wheat bread samples with
0, 10, 15, and 20% of cassava flour. These samples were
included individually to groups of healthy human volunteers
that were studied in the morning after a 10-12-hr overnight
fast. Glycaemia was evaluated after 30 minutesand after 2
hours and observed that the increase in cassava incorporation
resulted insignificantly less glycemic index. We did not find
studies that showed the effects of tapioca on the abdominal
circumference. Our animals showed areduction of this
parameter, but the visceral fat weight did not show asignificant
reduction. The flour of other plants may reduce visceral
weight, such as Morindaoleifera flour (Guigueret al., 2016)
and Pereskia aculeate flour (Barbalho et al.., 2016).Visceral
fat is known as an endocrine organ associated with the
maintenance of homeostasis. On the other hand, it plays an
important role in the development of several comorbidities
such as insulin resistance, diabetes, inflammation and
cardiovascular diseases.
This association is due to the release of pro-inflammatory
cytokines such as resistin, leptin, Tumor Necrosis Factor,
Interleukin 6, and many othersbiomarkers (Edrisi et al.., 2017;
Shirkawa et al., 2017). The evaluation of the atherogenic
indices is capable of indicating the increase of the risks for
development of cardiovascular diseases and may be considered
in the clinical practice as a potential way of stratification of
these diseases(Choi et al., 2017; Mopuriet al., 2017;Ikewuchi,
2012). The intake of tapioca did not interfere in these indices.
Tapioca may bring positive effects on the metabolic profile of
Wistarrats. Nevertheless, we suggest more studies using this
product to establish the amounts that should be usedin order to
improve cardiovascular risks.
Conflict of interests
Authors declare no conflict of interests.
REFERENCES
Ahmadvand, H., Bagheri, S., Tamjidi-Poor, A., Cheraghi, M.,
Azadpour, M., Ezatpour, B., Moghadam, S., Shahsavari,
G. and Jalalvand, M. 2016. Biochemical effects of
oleuropein in gentamicin-induced nephrotoxicity
in rats.ARYA Atheroscler., 12(2), 87-93.
Barbalho, S.M., Guiguer, E.L., Marinelli, P.S. and Bueno,
P.C.S. 2016. Pereskia aculeata Miller Flour: Metabolic
Effects and Composition. J Med Food. 19, 890-4. doi:
10.1089/jmf.2016.0052. Epub 2016 Sep 1.
Barczynska, R., Slizewska, K., Litwin M, Szalecki M,
Kapusniak J. 2016. Effects of dietary fiber preparations
made from maize starch on the growth and activity of
selected bacteria from the Firmicutes, Bacteroidetes, and
Actinobacteria phyla in fecal samples from obese
children. Acta Biochim Pol., 63(2):261-6. doi:
10.18388/abp.2015_1068.
Ble-Castillo JL, Juárez-Rojop IE, Tovilla-Zárate CA. 2017.
Acute Consumption of Resistant Starch Reduces Food
Intake but Has No Effect on Appetite Ratings in Healthy
Subjects. Nutrients. 9(7). pii: E696. doi: 10.3390/nu
9070696.
Castellano-Castillo, D., Moreno-Indias, I., Fernández-García,
J.C., Alcaide-Torres, J., Moreno-Santos, I., Ocaña, L.,
Gluckman, E., Tinahones, F., Queipo-Ortuño, M.I. and
Cardona F. 2017. Adipose Tissue LPL Methylation is
Associated with Triglyceride Concentrations in
the Metabolic Syndrome. Clin Chem. pii: clinchem.2017.
277921. doi: 10.1373/clinchem.2017.277921.
Choi, J.Y., Kim, Y.J., Cho, S.J., Kwon, E.Y., Ryu, R. and
Choi, M.S. 2017. Metabolic Effect of an Oriental Herbal
Medicine on Obesity and Its Comorbidities with
Transcriptional Responses in Diet-Induced Obese
Mice.Int J Mol Sci., 18(4). pii: E747. doi:
10.3390/ijms18040747.
Costa, C., Tsatsakis, A., Mamoulakis, C., Teodoro, M.,
Briguglio, G., Caruso, E., Tsoukalas, D., Margina, D.,
Dardiotis, E., Kouretas, D. and Fenga, C. 2017. Current
evidence on the effect of dietary polyphenols intake on
chronic diseases.Food ChemToxicol. pii: S0278-
6915(17)30621-X. doi: 10.1016/j.fct.2017.10.023
Dias, L,T. and Leonel, M. 2006. Caracterização físico-química
de farinhas de mandioca de diferentes localidades do
Brasil. Ciênc Agrotecnol.,30, 692-700.
Edrisi, F., Salehi, M., Ahmadi, A., Fararoei, M., Rusta, F. and
Mahmodianfard, S. 2017. Effects of supplementation
18971 International Journal of Development Research, Vol. 08, Issue, 02, pp.18969-18972, February, 2018

with rice husk powder and rice bran on inflammatory
factors in overweight and obese adults following an
energy-restricted diet: a randomized controlled trial.Eur J
Nutr.. doi: 10.1007/s00394-017-1555-3
Guiguer. E,L., Barbalho, S.M., Marinelli, P.S. and Bueno,
P.C.S. 2016. of Moringa oleifera flour and its effects on
the biochemical profile and intestinal motility in an
animal model. Int J Phytomed.,8, 427-434.
doi.org/10.5138/09750185.1845
Ikewuchi, JC. 2012. Alteration of plasma biochemical,
haematological and ocular oxidative indices of alloxan
induced diabetic rats by aqueous extract of
Tridaxprocumbens Linn (Asteraceae). Excli Journal. 11:
291–308.
Kanmani, N., Romano, N., Ebrahimi, M., Nurul, Amin, S.M.,
Kamarudin, M.S., Karami, A. and Kumar, V. 2018.
Improvement of feed pellet characteristics by dietary pre-
gelatinized starch and their subsequent effects on growth
and physiology in tilapia.Food Chem., 239:1037-1046.
doi: 10.1016/j.foodchem.2017.07.061. Epub 2017 Jul 13.
Koh, G.Y. and Rowling, M.J. 2017. Resistant starch as a novel
dietary strategy to maintain kidney health in diabetes
mellitus. Nutr Rev., 75(5), 350-360. doi:
10.1093/nutrit/nux006.
Liu, X., Sawauchi, H., Ogawa, H., Kishida, T. and Ebihara, K.
2006. Retrograded tapioca starch prevents ovarian
hormone deficiency-induced hypercholesterolemia.J Nutr
Sci Vitaminol (Tokyo)., 52(2), 134-41.
Maier, T.V., Lucio, M., Lee, L.H., VerBerkmoes, N.C. and
Brislawn, C.J. 2017. Impact of Dietary Resistant
Starch on the Human Gut Microbiome, Metaproteome,
and Metabolome. M Bio., 17;8(5). pii: e01343-17. doi:
10.1128/mBio.01343-17.
Matsuda, H., Kumazaki, K., Otokozawa, R., Tanaka, M.,
Udagawa, E. and Shirai, T. 2016. Resistant
starch suppresses postprandial hypertriglyceri demia in
rats. Food Res Int., 89, 838-842. doi:
10.1016/j.foodres.2016.10.022. Epub 2016 Oct 15.
Mopuri, R. and Islam MS. 2017. Medicinal plants and
phytochemicals with anti-obesogenic potentials: A
review. Biomed Pharmacother., 89,1442-1452. doi:
10.1016/j.biopha.2017.02.108.
Munshi, R.P., Joshi SG. and Rane, B.N. 2014. Development of
an experimental dietmodel in rats to study hyperlipidemia
andinsulin resistance, markers for coronary heart disease.
Indian J Pharmacol., 46(3), 270-276.
Noumi, Y., Kawamura, R., Tabara, Y., Maruyama, K., Takata,
Y., Nishida, W., Okamoto, A., Nishimiya, T., Onuma, H.,
Saito, I., Tanigawa, T. and Osawa, H. 2017. An inverse
association between serum resistin levels and n-3
polyunsaturated fatty acids intake was strongest in the
SNP-420 G/G genotype in the Japanese cohort: The Toon
Genome Study.Clin Endocrinol., (Oxf). doi: 10.1111/
cen.13500
Okafor, E.N., Erukainure, O.L., Ozumba, A.U., Adewale,
C.O., Kayode, F.O., Asieba, G.O., Adesegha, O.I. and
Elemo GN. 2017. Cassava Flour Substitution Modulates
Glycemic Responses and Glycemic Index of Wheat
Breads in Apparent Healthy Volunteers. J Diet Suppl.,
4;14, 446-452. doi: 10.1080/19390211.2016.1267061.
Oso, A.O., Akapo, O., Sanwo, K.A. and Bamgbose, A.M.
2014. Utilization of unpeeled cassava
(Manihot esculentaCrantz) root meal supplemented with
or without charcoal by broiler chickens.J Anim Physiol
Anim Nutr (Berl). 98(3), 431-8. doi: 10.1111/jpn.12088.
Epub 2013 May 31.
Queiroz, H.G.S., Sampaio, N.A.; Pinto, R.S.; Rodrigues,
M.C.P. and Costa, J.M.C. 2009. Evaluation of the
physical-chemical and microbiological quality of tapioca
ice cream. Rev Ciênc Agron., 40, 60-65.
Reshmi, S.K., Sudha, M.L.and Shashirekha, M.N. 2017.
Starch digestibility and predicted glycemic index in the
bread fortified with pomelo (Citrus maxima) fruit
segments.Food Chem., 237, 957-965. doi:
10.1016/j.foodchem.2017.05.138.
Santos, L., Davel, A,P., Almeida, T.I., Almeida, MR., Soares,
E.A., Fernandes, G.J., Magalhães, S.F., Barauna, V.G.
and Garcia, J.A. 2017. Soy milk versus simvastatin for
preventing atherosclerosis and left ventricle remodeling
in LDL receptor knockout mice.Braz J Med Biol Res.,
50(3):e5854. doi: 10.1590/1414-431X20165854.
Seo, J.Y. and Kim, J.H. 2017. Validation of surrogate markers
for metabolic syndrome and cardiometabolic risk factor
clustering in children and adolescents: A nationwide
population-based study. PLoSOne., Oct
19;12(10):e0186050. doi: 10.1371/journal.pone.0186050.
eCollection 2017
Shirakawa, K., Endo, J., Katsumata, Y., Yamamoto, T.,
Kataoka, M., Isobe, S., Yoshida, N., Fukuda, K. and
Sano, M. Negative legacy of obesity. PLoS
One.,26;12(10):e0186303. doi: 10.1371/
journal.pone.0186303. eCollection 2017
Si X, Strappe P, Blanchard C, Zhou Z. 2017. Enhanced anti-
obesity effects of complex of resistant starch and chitosan
in high fat diet fed rats.Carbohydr Polym. 157, 834-841.
doi: 10.1016/j.carbpol.2016.10.042.
Silva, P.A., Cunha, R.L., Lopes, A.S. and Pena, A.S. 2013.
Characterization of tapioca flour obtained in Pará state,
Brazil. Ciência Rural.,43: 185-191.
Telle-Hansen, V.H., Christensen, J.J., Ulven, S.M., Holven,
K.B. 2017. Does dietary fat affect inflammatory markers
in overweight and obese individuals?-a review of
randomized controlled trials from 2010 to 2016.Genes
Nutr., 4;12:26. doi: 10.1186/s12263-017-0580-4.
eCollection 2017.
Wang, L., Zheng, M., Wang, Y., Zhang, Y., Qian, H., Zhang,
H. and Qi, X. 2014. Anti-diabetic activity of cassava
cross-linked octenyl succinic maltodextrin in STZ-
induced diabetic mice.Int J Biol Macromol., 64:247-51.
doi: 10.1016/j.ijbiomac.2013.11.017
*******
18972 Patrícia Cincotto dos Santos Bueno et al. Brazilian typical food with potential to improve lipid profile