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Efectos Beneficiosos de La Suplementación Con Pleurotus Albidus
Efectos Beneficiosos de La Suplementación Con Pleurotus Albidus
1. Introduction species of mushrooms in nature, those that are easier to cultivate and,
1. Introduction largely,
species of themushrooms
edible onesinhave been
nature, usedthat
those in are
kitchens,
easier laboratories and
to cultivate and,
Functional foods have been used for centuries, since they present industries [3].
largely, the edible ones have been used in kitchens, laboratories and
promising health-giving
Functional properties,
foods have been used forsuch as: to since
centuries, promote
they satiety,
present The mushrooms
industries [3]. of the genus Pleurotus attract particular attention
to reduce weight
promising gain andproperties,
health-giving to improvesuch insulin
as: sensitivity
to promoteviasatiety,
many owing The mushrooms of content,
to their nutrient the genusbeing the most
Pleurotus popular
attract and cultivated
particular attention
mechanisms
to [1]. In
reduce weight this
gain sense,
and the number
to improve of sensitivity
insulin studies focusing on
via many worldwide
owing to their nutrient content, being the most popular andpreviously
[2,3]. This characteristic, added to their cultivated
functional products
mechanisms andsense,
[1]. In this their derived
the number compounds
of studiesasfocusing
sources onof described
worldwidemedicinal
[2,3]. Thisproperties, have motivated
characteristic, added studies
to theirinvestigating
previously
medicine inproducts
functional preventinganddiseases like hypertension,
their derived compounds as diabetes,
sourcesandof this mushroom genus in the treatment
described medicinal properties, have motivated studiesof several disorders [4,5].
investigating
cancer haveinbeen
medicine increasing
preventing recentlylike
diseases [2].hypertension, diabetes, and In fact, many reports showed that Pleurotus mushrooms
this mushroom genus in the treatment of several disorders [4,5]. exhibit
Among
cancer others,
have been mushrooms
increasing recentlystand
[2]. out not only for having antihypercholesterolemic,
In fact, many reports showed antihypertensive,
that Pleurotus antidiabetic,
mushrooms antiobesity,
exhibit
a remarkable nutritional
Among others, value,stand
mushrooms but also for exhibiting
out not anti-
only for having anti-aging, antimicrobial and antioxidant attributes, besides
antihypercholesterolemic, antihypertensive, antidiabetic, antiobesity, presenting
ainflammatory,
remarkable antimicrobial, hypolipidemic,
nutritional value, but also for anti-hyperglycemic,
exhibiting anti- aanti-aging,
hepatoprotective action and
antimicrobial [6,7].
antioxidant attributes, besides presenting
and antioxidant antimicrobial,
inflammatory, therapeutic properties [3]. Although
hypolipidemic, there are many
anti-hyperglycemic, a hepatoprotective action [6,7].work showed evidence that the water
Sheng et al. [8] in their
and antioxidant therapeutic properties [3]. Although there are many extract
Shengof another
et al. [8]species Pleurotus
in theirofwork showed evidencecitrinopileatus)
(Pleurotus that the water
*
had potential in the prevention of
extract of another species of Pleurotus (Pleurotus obesity and citrinopileatus)
prediabetes in
Corresponding author at: Department of Physiology and Pharmacology, Universidade Federal
de Pelotas, Campus Capão do Leão 96900-010 Pelotas, Brazil.
mice. In another
had potential in study, Balaji et al.of[9]
the prevention revealed
obesity andthat an extract of
prediabetes in
*
Corresponding author at: Department of Physiology and Pharmacology, Universidade Federal
E-mail address: schenkel.paulo@ufpel.edu.br (P.C. Schenkel) P. pulmonarius
mice. In another study, Balaji et al. [9] revealed that an extractand
has antihyperglycaemic, antihyperlipidemic, of
de Pelotas, Campus Capão do Leão 96900-010 Pelotas, Brazil.
Peer review under responsibility of KeAi Communications Co., Ltd.
E-mail address: schenkel.paulo@ufpel.edu.br (P.C. Schenkel)
defensive effectshas
P. pulmonarius in diabetic rats by reducing
antihyperglycaemic, blood glucose levels,
antihyperlipidemic, and
Peer review under responsibility of KeAi Communications Co., Ltd. lipid
defensive effects in diabetic rats by reducing blood and
profiles, enhancing the status of antioxidants decreasing
glucose levels,
lipid profiles, enhancing the status of antioxidants and decreasing
Publishing services by Elsevier
Publishing services by Elsevier
http://doi.org/10.1016/j.jfutfo.2021.08.002
2272-5669/© 2021 Beijing Academy of Food Sciences. Publishing services by Elsevier B.V. on behalf of KeAi Communications Co., Ltd. This is an open access article under the CC
http://doi.org/10.1016/j.jfutfo.2021.08.002
BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
2272-5669/© 2021 Beijing Academy of Food Sciences. Publishing services by Elsevier B.V. on behalf of KeAi Communications Co., Ltd. This is an open access article under the CC
10.1016/j.jfutfo.2021.08.002
BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
2772-5669 © 2021 Beijing Academy of Food Sciences. Publishing services by Elsevier B.V. on behalf of KeAi Communications Co., Ltd. This is an open access article under the
CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Paola Quevedo da Costa et al. / Journal of Future Foods 1-1 (2021) 98–103 99
injuries in the pancreas, liver, and kidney. Several other works have Petri dishes, and then stored in a temperature-controlled place
shown that edible mushrooms and their compounds, especially the (28 ºC). When total colonization of the culture medium and presence
mushrooms of the genus Pleurotus, have effects on the prevention of basidioma primordia were observed, the bags were drilled with a
of body weight gain, hyperlipidemia, hyperglycemia, and insulin scalpel and brought to the greenhouse at room temperature (between
sensitivity [10-17] 20 and 30 ºC) and relative humidity between 70% and 90% [18].
In vitro studies with P. albidus species, a mushroom native of Subsequently, the mushrooms were dried in a dehydrator
South America, revealed it as an important source of protein and fiber, (Funkitchen®, Britania Eletrodoméstico S.A, Pirabeiraba, Brazil) for
presenting low-fat levels, in line with other Pleurotus species [18]. 8 h at 50 °C, crushed in a grinder (Cadence®, Balneário Piçaras, Brazil)
Additionally, P. albidus has mitigated obesity, hyperglycemia, and stored at 4 °C. After that, 200 g of dried mushroom powder and
foam cell formation, and inflammation in vitro [5,19]. Furthermore, 2 000 mL of 70% ethanol were placed in a reflux system at 100 °C
it showed a significant in vitro antioxidant activity in hepatocytes for 30 min. Then the mixture was vacuum filtered and the ethanol-
and endothelial cells [18,20]. Besides that, Gambato et al. [4] soluble fraction was evaporated on a rotary evaporator. The ethanol-
investigated the main chemical compounds of P. albidus extract insoluble residue was re-extracted with 2 000 mL of water for an
and found these results: phenolics, (18.57 ± 0.26) mg of gallic acid additional hour. The extracts were aggregated and lyophilized until
equivalents/g PleExt; flavonoids, (4.71 ± 0.12) mg of quercetin the dried extract was obtained [4]. The yield of the extraction process
equivalents/g PleExt and ergothioneine, (2.13 ± 0.01) mg/g PleExt. was 20.65%.
One important factor in hyperlipidemia and hyperglycemia is
oxidative stress, which is a process associated with many diseases, since 2.3 Inhibition of lipase activity
elevated levels of reactive oxygen species induce membranes harm by
lipids oxidation, changes in protein structure and function, and structural In order to test the inhibition of lipase activity, a pancreatic
injury to deoxyribonucleic acid [21]. As a counter-regulatory strategy, lipase type II (Sigma; 0.2 mg/mL) inhibition assay was performed
antioxidant systems are stimulated in order to stabilize the reactive using a colorimetric method with 1-2-O-dilauryl-rac-glycero-3-
oxygen species and avoid/mitigate cell damage [22]. glutaric acid (6-methylresorufin)-ester (DGGR) as a substrate of
In this regard, previous in vitro findings incited our group to the enzymatic reaction [23]. The reaction medium was divided into
investigate P. albidus as a dietary supplementation to prevent and three groups: 25 mg/mL of extract, 50 mg/mL of extract and blank.
treat several disorders. Therefore, the objective of the present study The lipase inhibition was obtained by the difference of the readings
was to evaluate for the first time the influence of P. albidus extract in at two reaction times, at 90 and 180 s, as follows: Pancreatic lipase
vivo administration in healthy C57BL/6 mice. inhibition (%) = [(ΔAec - ΔAs)/ΔAec] × 100%, where ΔAec and ΔAs
are defined as the absorbance difference for the enzyme control and
2. Methods samples, at 570 nm [24].
2.1 Animals
2.4 In vivo tests
All animal protocols were in accordance with and approved by
the Guidelines for Ethical Care of Experimental Animals from the Lyophilized P. albidus extract was diluted in 0.9% sodium
Universidade Federal de Pelotas (#28614-2019). chloride and administered once daily (between 4:00 p.m‒5:00 p.m)
Fourteen male C57BL/6 mice (60 days, ± 23 g) were obtained by gavage (500 mg/kg body weight) [25]. This dosage was based on
from the Center for Reproduction and Experimentation of Laboratory the work of Xiong et al. [25], since P. albidus did not have any papers
Animals of the Universidade Federal de Pelotas, Brazil, and they were published in vivo. The animals from the control group underwent the
divided into two groups (n = 7 animals/group): (1) Control (mice that same procedure, except by receiving only 0.9% sodium chloride in
received 0.9% sodium chloride); (2) P. albidus (mice that received the same volume. The supplementation lasted 20 days [26].
P. albidus hydroalcoholic extract). All animals were maintained
under standard laboratory conditions (temperature: 22‒24 °C; relative 2.4.1 Insulin tolerance test (ITT)
humidity: 40%‒60%; light/dark cycle: 12 h) and received water and
standard laboratory feed (Nuvilab®, Colombo, Brazil) ad libitum. The ITT was performed 24 h after the last gavage. In this procedure,
food intake was measured once a week by the difference between the after 2 h of fasting, insulin was administrated in mice (1 IU/kg
food weight before and after 24 h. body weight, intraperitoneally). Whole blood samples were
collected from animals’ tails at 0, 5, 20, 35, 60 and 120 min after
insulin administration. The glucose meter AccuChek Active, Roche
2.2 Cultivation of P. albidus and extract preparation ®
Diagnostics , USA was used to measure the glucose levels.
P. albidus mushrooms (82F.7-MIUCS 1580) from the Laboratory
of Enzymes and Biomasses of the Caxias do Sul University, Brazil, 2.4.2 Lipid tests
were employed. Basidiomas were grown in polypropylene bags
containing 1.5 kg of medium (50% Vitis labrusca grape marc; 44% Following the ITT test, animals were anesthetized with isoflurane
Pinus sp. Sawdust; 5% wheat bran; 1.0% CaCO 3, and distilled and euthanized by exsanguination followed by cervical dislocation.
water to obtain 66% humidity). Primarily, the sacs were inoculated Blood samples were centrifuged for 10 min at 3 000 × g and the
with all the contents of previously grown fungus mycelium serum was stored at -20 ºC for the evaluation of triglycerides (TG),
100 Paola Quevedo da Costa et al. / Journal of Future Foods 1-1 (2021) 98–103
20
2.4.3 Hydroxyl radical generation system *
*cd
10
The livers were rapidly withdrawn and homogenated with
0
1.15% KCl (5 mL/g) in the presence of 100 mmol/L phenyl methyl 0 1 2 3
sulfonyl fluoride (PMSF). After that, samples were centrifuged for Weeks
20 min at 10 000 × g at 4 ºC and the supernatant was incubated with Fig. 2 Effect of P. albidus on food intake in healthy C57BL/6 mice. Data are
FeCl2, H2O2 and ascorbic acid to induce oxidative stress (hydroxyl given as mean ± SD. *P < 0.05 vs control group, a P < 0.000 1 vs. basal food
radical generation system) for 30 min at 37 °C [27]. Then, the intake of the control group, b P < 0.000 1 vs. food intake on the 2nd week of
the control group, c P < 0.000 1 vs. basal food intake of the P. albidus group,
samples were used to analyze the oxidative stress under previous d
P < 0.000 1 vs. food intake on the 2nd week of the P. albidus group.
studies: thiobarbituric acid reactive substances (TBARS) [28];
superoxide dismutase (SOD) [29]; catalase (CAT) [30]; glutathione
peroxidase (GPx) [31]. 250
200 2
0 0
Control P. albidus Control P. albidus
Group Group
60 C 8 D
6
40 *
4
20
2
0 0
Control P. albidus Control P. albidus
Group Group
Fig. 4 Effect of P. albidus on the TBARS levels and SOD, CAT and GPx activities in liver of healthy C57BL/6 mice. Data are given as mean ± SD.
*
P < 0.05 vs. control group.
100 A 100 B
80 80
TG (mg/dL)
TC (mg/dL)
60 60
40 40
20 20
0 0
Control P. albidus Control P. albidus
Group Group
60 C 80 D
HDL-c (mg/dL)
60
Urea (mg/dL)
40
40
20
20
0 0
Control P. albidus Control P. albidus
Group Group
Fig. 5 Effect of P. albidus on the serum TG, TC, urea, and HDL-c in healthy C57BL/6 mice. Data are given as mean ± SD.
administration for 21 days, which has high nutritional value and in this group. Sheng et al. [8] showed that the oral administration
pharmacological properties, reduced body weight in diabetics (400 mg/kg or 800 mg/kg weight/day) for 12 weeks of an aqueous
rats. Using mushroom ethanolic extracts of the same genus extract of P. citrinopileatus mushroom, an edible mushroom that has
(P. citrinopileatus – 500 mg/kg), Chi et al. [32] also verified a abundant bioactive molecules, promotes a significant decrease in food
reduction in the body weight in C57BL/6 mice after 12 weeks of intake, weight gain, and fat accumulation in obese mice. To confirm
supplementation. The Pleurotus eryngii var. tuolensis (500 mg/kg) these findings, an investigation with obese-hyperglycemic ob/ob
treatment for 40 days used by Ren et al. [33] similarly showed a mice, which has a physiologic leptin deficiency, is encouraged.
significant decrease in body weight. Although elevated, the initial whole blood glucose levels
In the current work, we showed a food intake reduction in the observed in our study are in agreement with the baseline mean
P. albidus group after the first and third weeks. Plausibly, at the glucose values previously described for healthy C57BL/6 mice [34].
beginning of the administration, mice were unfamiliar with P. albidus Nevertheless, it should be noted that all animals were subjected to
extract and to the gavage procedure, although we do not rule out the same experimental procedures, thus eliminating any discrepancy
animals satisfied hunger momentarily, reducing the food intake. Taken between the groups. Regarding the glycemic curve from the ITT, we
together with the decrease in body weight promoted by P. albidus did not detect differences in the whole blood glucose levels between
extract administration it is feasible to consider that its particular anti- the experimental groups. Similarly, Ng et al. [35] did not observe
obesity potential may also be related to the attenuation of appetite a significant change in the serum glucose levels in diabetic rats
102 Paola Quevedo da Costa et al. / Journal of Future Foods 1-1 (2021) 98–103
treated with the same dose of P. sajor-caju aqueous extract either. hepatocytes from both our groups when these cells were challenged
Despite these results, the in vivo hypoglycemic and lipid-lowering with a free radicals generation system [27].
activities of the mushrooms has been widely reported [26,36,34]. On the other hand, GPx, an enzyme that uses reduced glutathione
In this sense, Guo et al. [34] identified that the novel Grifola (GSH) as a substrate to exert its antioxidant role, showed decreased
frondosa polysaccharide-chromium is effective in preventing activity in P. albidus group compared to control. This result may be
the hyperglycemia in diabetic mice induced by a high-fat diet related to lower GSH levels in livers from P. albidus group, since
and streptozotocin. Likewise, the treatment of diabetics rats with GSH is depleted in xenobiotics detoxification during the first pass
P. ostreatus polysaccharides (100, 200, and 400 mg/kg) for effect after intestinal absorption. As a consequence, GPx activity
4 weeks decreased significantly the hyperglycemia, improved insulin would be reduced.
resistance and increased glycogen storage [35].
Considering serum lipid levels, our data disagrees with other 5. Conclusion
descriptive studies investigating other types of mushrooms [34,35].
We observed that TG, TC and HDL-c levels showed a tendency to Our study showed for the first time the influence of P. albidus
decrease in P. albidus group compared to the control group, but not hidroalcoholic extract supplementation. P. albidus seems to own
significantly. Conversely, P. eryngii var. tuoliensis administration the ability to decrease body weight and food intake, even though no
for 40 consecutive days in mice, led to a significant increment changes in glycemic, lipidic and oxidative stress parameters were
in HDL-c and a decrease in TG and TC [36]. Furthermore, an detected in our study conditions. The results presented here lead the
antihyperlipidemic effect was observed in another study in which way as basic references for future researches regarding P. albidus
G. frondosa polysaccharide-chromium complex was administered mushroom impact in vivo. Additional analyses exploring distinctive
in streptozotocin-induced diabetic mice [37]. As mentioned before, administration routes and inspecting higher doses of P. albidus extract
the G. frondosa polysaccharide-chromium complex also appears to are required to enrich the understanding of the mechanisms involved
be beneficial in diabetes by promoting a reduction in blood glucose in the results obtained in the present study.
levels [38]. Jo et al. [38], using the aqueous extract of P. eryngii var.
ferulae, observed an improvement in serum lipid profile, glucose Declaration of conflicting interest
tolerance, and insulin sensitivity in C57BL/6 mice after 12 weeks.
No conflict to declare.
These authors also verified a decline in body weight, white adipose
tissue weight and pancreatic lipase activity [38]. In the present study,
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