Content uploaded by Hamid Reza Roosta
Author content
All content in this area was uploaded by Hamid Reza Roosta on Nov 29, 2023
Content may be subject to copyright.
Available via license: CC BY 4.0
Content may be subject to copyright.
Functional Foods in Health and Disease 2023; 13(8): 398-408 FFHD Page 398 of 408
Research Article Open Access
Hypoglycemic and hypolipidemic activity of moringa grown in
hydroponics and soil in Ararat Valley
Anna Tadevosyan1, Anahit Hakobjanyan1, Anahit Tovmasyan1, Armenuhi Asatryan1, Hamid Reza Roosta2 and Mahsa
Daryadar1
1G.S. Davtyan Institute of Hydroponics Problems NAS RA, Republic of Armenia; 2Department of Horticultural Sciences,
Faculty of Agriculture and Natural Resources, Arak University, Arak, Iran
*Corresponding Author: Anahit Hakobjanyan.Ph.D., Senior Researcher, Department of Plant Nutrition and
Productivity, G.S. Davtyan Institute of Hydroponics Problems, National Academy of Sciences, Yerevan, Armenia
Submission Date: July 25th, 2023; Acceptance Date: August 29th, 2023; Publication Date: August 31st, 2023
Please cite this article as: Tadevosyan A., Hakobjanyan A., Tovmasyan A., Asatryan A., Roosta H. R., Daryadar M.
Hypoglycemic and Hypolipidemic Activity of Moringa Grown in Hydroponics and Soil in Ararat Valley. Functional Foods
in Health and Disease 2023; 13(8): 398-408. DOI: https://www.doi.org/10.31989/ffhd.v13i8.1158
Background: Moringa has a hypoglycemic and hypolipidemic influence, and the water extract of its leaves can
decrease the amount of glucose during Diabetes Mellitus. Moringa leaves in extract or powder form influenced
type I and type II diabetes by enhancing insulin secretion and improving glycogen synthesis and glucose uptake in
the liver and muscles. This occurred in the case of type I diabetes, as well as by inhibiting glucose uptake and
slowing gastric emptying in the case of type II diabetes.
Objective: In our study, we try to evaluate the hypoglycemic, hypolipidemic, and antistress activity of Moringa
grown for the first time in Armenia in hydroponic and soil conditions to find out the beneficial cultivation method
of Moringa from the point of view of these activities.
Materials and Methods: The study was done with the usage of a rabbit model, using water extract of Moringa
leaves made with a 150 mg count of leaves on 1 kg weight of the animal. Hyperglycemia in the rabbits was induced
by 21-day immobilization stress (3 hours a day). Rabbits were divided into 4 groups: the first group was treated
with the extract from the hydroponic Moringa in a dose of 2 ml/day, the second group received the extract from
the soil Moringa in a dose of 2 ml/day, the third group was the control—which did not receive any extract, but was
exposed to stress, like first and second groups— and the fourth group was the norm, which did not receive any
extract and was stress free. Each group included 3 animals as means of replication. The glycogen level was
measured in the livers, hearts, and muscles of rabbits. The level of glucose, total cholesterol, HDL, and LDL were
measured in the serum of animals.
Functional Foods in Health and Disease 2023; 13(8): 398-408 FFHD Page 399 of 408
Results: Our results showed that after a 21-day period of stress, the increased level of glucose stays at a high level
in control groups, while the use of a hydroponic Moringa extract developed stress tolerance in animals and in soil
Moringa extract stabilizes glucose levels in the blood. The cholesterol exceeded the norm 1.8 times in the control
group and was inferior in hydroponic and soil groups by 1.5 and 1.4 times, respectively. These changes reflect the
amount of HDL and LDL. Under stress conditions, the quantity of glycogen decreased from the norm in the liver,
muscles, and heart muscle in the control group (2.5; 2.4; and 2.4 times, respectively) and increased in hydroponic
(1.6; 1.5; and 2.1 times, respectively) and soil (1.6; 1.5; and 2.4 times, respectively) groups. This evidence shows
that under stress conditions the glucose level of blood is improved on the 21st day of stress in groups that received
the extract of moringa because of glucose exchange to glycogen with high efficiency in different organs.
Keywords: antistress activity, diabetes, HDL, glucose, Moringa oleifera, total cholesterol
©FFC 2023. This is an Open Access article distributed under the terms of the Creative Commons Attribution 4.0
License (http://creativecommons.org/licenses/by/4.0)
INTRODUCTION
Moringa oleifera (Moringa) is native to India and is
used in many areas of human life due to the macro
and microelements it contains [1-3]. It is known that
Moringa has a hypoglycemic influence [4] and the
water extract of its leaves may be used for Diabetes
mellitus to reduce the blood glucose level [5]. It was
shown that the extract of the Moringa leaves inhibits
intestinal α-glucosidase, pancreatic cholesterol
esterase, and pancreatic lipase activities, thus helping
in the treatment of diabetes mellitus [6]. The decrease
in theactivity of pancreatic cholesterol esterase
supports lowering the level of cholesterol in the
organism.
With Diabetes mellitus, lipid concentration is
increased in the blood, enhancing the risk of
premature atherosclerosis. Crude leaf extract of
Moringa along with a high-fat diet reduces the level of
cholesterol and triacylglycerol in serum. It was shown
that the use of Moringa extract decreased the lipid
profile of the liver, heart, and aorta [7]. The use of
powder of Moringa leaves decreased low-density
lipoproteins (LDL) levels, atherogenic risk, and
glycemia in HIV-negative children [8].
Moringa leaf extract had a hepatoprotective
action against acetaminophen-induced hepatotoxicity
in mice and rats in a dose-depended manner. It did so
Functional Foods in Health and Disease 2023; 13(8): 398-408 FFHD Page 400 of 408
by decreasing the levels of serum aspartate
aminotransferase (AST), alanine aminotransferase
(ALT), and increasing antioxidant enzymes in the liver
and glutathione level (GSH) [9]. The increases in the
AST/ALT level is conditioned by the increase in the
death level of cardiovascular patients [10] and the
increase of the cancer probability [11], which may be
formed because of stress. In mice fed with a high-fat
diet, the leaf extract of Moringa protects against liver
damage by decreasing levels of AST, alkaline
phosphatase (ALP), ALT, lipid peroxidation (LPO) and
increasing GSH [9]. Oral administration of Moringa
leaf extract caused a maximum reduction of 26.7% in
fasting blood glucose level (FBG), and a maximum
reduction of 30% in glucose tolerance after 3 hours of
glucose consumption in normal and streptozotocin
(STZ)-induced sub, mild, and severely diabetic albino
rats. After 21 days of intake, FBG and postprandial
blood glucose levels have a maximum reduction of
69.2% and 51.2%, respectively [11]. The use of
Moringa leaves extract or powder may positively
influence type I and type II diabetes by enhancing
insulin secretion and both improving glycogen
synthesis and glucose uptake in the liver and muscles.
This pertains to type I, and functions in the case of
type II by inhibiting glucose uptake and slowing gastric
emptying.[9].
Nowadays, stress is one of the causes of the high
number of diabetic patients, especially with type II
diabetes. It is mentioned that stress-induced
hyperglycemia may take place because of diseases
leading to insulin resistance and decreased insulin
secretion. This leads to an increase in blood glucose
level, and the use of external insulin because of the
lack of insulin in the organism [12]. It is shown that
chronic stress may increase the level of LDL, and
cholesterol, causing hyperlipidemia with subsequent
development of atherosclerosis [13], which is one of
the complications of diabetes [14]. High cholesterol
level in the blood plasma adversely influences the
progress of cardiovascular diseases and liver disorders
(non-alcoholic fatty liver disease, non-alcoholic
steatoses hepatitis) that is conditioned by the
activation of oxidative stress and endoplasmic
reticulum stress. Studies done on animal models and
humans have shown that high cholesterol level is
included in the development of many metabolic
diseases [15].
In our study, we tried to estimate the
hypoglycemic and hypolipidemic influences of the
water extract of Moringa leaves on the rabbit model
using leaves of Moringa grown in hydroponic and soil
conditions. Like this, we try to estimate the effectivity
of these two Moringa groups and understand which
growing method is more beneficial for the treatment
of stress-activated hyperglycemia.
MATERIAL AND METHODS
Study design and animal model: The hypoglycemic
activity of the extract was studied on male rabbits
with a body mass of 1800-2100g. The initial body mass
of the animals was recorded 1 day before the start of
the experiment. The animals were kept under
standard environmental conditions (22±2°C
temperature, light/dark 12-hour cycle). During the
experiment, rabbits had free access to eat and drink.
All studies were done according to the modern ethical
norms confirmed by the “International
Recommendation on Carrying out of Biomedical
research with Use of Animals” and the research plan
was validated by the Armenian National Center of
Bioethics.
The hyperglycemia in rabbits was induced by the
21-day-long immobilization stress (3 hours a day).
They were fixed on board [16]. The rabbits were
divided into four groups with 3 animals in each group.
The mentioned number of animals was chosen since it
provides reliable reproducible results. The first group
received 2 ml of water extract from the
hydroponically cultivated plant once a day. The
second group received 2 ml water extract of plant
grown in soil once a day. The control group was the
third one, which included healthy animals that did not
receive any plant extract. The fourth group was set as
the norm , which did not undergo stress and did not
Functional Foods in Health and Disease 2023; 13(8): 398-408 FFHD Page 401 of 408
receive any treatment. The amount of the given
extract was calculated at the rate of 150 mg per 1 kg
of body weight. The extract was given by mouth with
a syringe. All experiments were done based on the
current ethical norms stated by “International
Recommendation on Carrying out of Biomedical
Research with Use of Animals,” and have been
approved by the National Center of Bioethics
(Armenia).
Biochemical analyses: The blood glucose level,
lipid profile, and body mass of rabbits were measured
at the beginning of the study and the 1st, 7th, 14th, and
21st days of the oral injection experiment. Blood
samples were taken from the ear vein and were
collected in serum separation tubes (Huma Tube K3E,
Germany). A blood clot was removed by 10 min
centrifugation at 3000 g under 4 °C. The received
supernatant was the serum.
At the end of the study animals were
decapitated: the glycogen level in the liver and muscle
of animals was analyzed.
The levels of glucose, total cholesterol, high-
density lipoproteins (HDL), LDL, and triglycerides were
measured in the serum. All indicators were measured
using enzyme kits. Glucose level (mmol/L) in serum
was defined using a glucose test kit based on the
glucose oxidase method (Dialab Glucose, GOD-PAP,
Austria) [17]. Total cholesterol and triglycerides were
estimated by the method provided earlier [18]. HDL
and LDL were measured using the described method
[19]. Analytical tests were carried out using a UV-Vis
spectrophotometer (Genesys 10S, USA). The glycogen
content was determined by the described method
[20]. The creatinine level was estimated by the
modified Jaffe’s method, and the urea level was
measured using Berthelot reaction [19]. Protein
analyses were done based on biuret reaction [21].
Statistical analyses: Statistical analyses were done
with the help of GraphPadPrism 8 program and Excel.
p<0.05 was considered statistically significant.
RESULTS AND DISCUSSION
Glucose: In our study before the stress, the glucose
level was 5.8mmol/L in the rabbits of the control
group, 5.7mmol/L in the hydroponic group,
4.9mmol/L in the soil group, and 4.9 mmol/L in the
norm group. On the first day of the stress the highest
level of glucose was observed in the soil group,
followed by the control. On the 21st day, the lowest
level of glucose was in the soil group from the stress-
influenced ones, and the highest in the control. In the
soil and hydroponic groups, the level of glucose on the
21st day increased by 1.14 times compared with its
level before the experiment started, while it increased
in the control group by 1.5 times. In the control group,
the stress consequences existed after 21 days (Fig. 1).
Feeding animals with hydroponic Moringa generates
tolerance in animals and the use of the soil Moringa
extract stabilizes the glucose level in the blood after
stress.
Fig. 1. Glucose level (mmol/L) on the 1st, 7th, 14th, and 21st days after stress in norm, control, hydroponic, and soil
groups (stress was induced on the 1st day). * p<0.05, ** p<0.01, *** p<0.001 compared to norm group.
Functional Foods in Health and Disease 2023; 13(8): 398-408 FFHD Page 402 of 408
The glucose tolerance test shows that in groups with
soil and hydroponic Moringa extracts, the glucose
amount regulation was also observed within 120
minutes, while in the control group any regulation
was not observed and was significantly higher from
the norm group (Fig. 2). This shows that the tincture
of Moringa leaves has the ability to regulate glucose
amount.
Fig. 2. Glucose tolerance test (OGTT, mmol/L), done after stress during 120 min with 30 min intervals in control,
hydroponic, and soil groups compared with the norm. * p<0.01 compared to norm group.
Influence on ALS and AST: ALT and AST are the
assessment markers of liver function. During diabetes,
there can be disorders of the liver functioning. Many
studies showed that the AST and ALT values may be
used for the diagnosis of diabetes [22].
In our study, in the control group, the AST and
ALT values increased by 1.8-1.9 times on the 21st day
of the stress, compared with the start day of the
experiment, while in hydroponic and soil groups these
indicators were reduced 1.4 times. Despite these
existing differences, the values of the AST and ALT
stayed between the ranges of the norm values
reported for the rabbits in the literature (AST 35-130
IU/L and ALT 45-80 IU/L) [23], except for the 21st
day’s ALT value of the control.
According to the reports, there is a positive
correlation between the amount of AST, ALT, and
inulin and glucose [24]. In our study, in the animals
taking Moringa the amount of ALT and AST were
reduced (Fig. 3), consequently, the glucose amount
was also reduced.
The AST/ALT ratio of De Ritis is interconnected
with oxidative stress and systemic inflammation [25].
Normally, in humans, it should be in the range of 0.91-
1.75 (1.33±0.42) and values less than 1 provide
evidence for liver lesion [26]. The ratio of the AST and
ALT average values given in Mellilo’s article is 1.32,
which is near the AST/ALT ratio value for human
beings [24].
The AST/ALT ratio of less than 1 and the increase
in the ALT level are connected with insulin resistance
[27]. It has been shown that the development of type
2 diabetes is probable when AST/ALT values are less
than 0.882 [28]. According to other data, this
threshold is higher and the AST/ALT≤0.93 ratio
suffices for the development of type 2 diabetes [29].
Functional Foods in Health and Disease 2023; 13(8): 398-408 FFHD Page 403 of 408
Fig. 3. The levels of ALT and AST and their ratio before the experiment and on the 21st day of the experiment in
control, hydroponic, and soil groups and norm. * p<0.05, ** p<0.01.
In our study, in the control group on the 21st
day, the levels of glucose, AST, and ALT increased,
respectively, 1.5, 1.9, and 1.9 times (Fig. 3). It provides
evidence for the development of diabetes [30]. In the
hydroponic and soil groups on the 21st day of stress,
the AST/ALT value decreased.
Table 1. The amounts of the cholesterol and triglycerides, as well as total proteins, urea, creatinine, HDL, and LDL,
measured in control, hydroponic and soil groups of rabbits and in the norm.
Indices
mmol/L
Norm
Control
Hydroponic
Soil
Cholesterol
1.93 ± 0.08
3.53 ± 0.16
1.3 ± 0.05
1,4 ± 0,05
Triglycerides
0.89 ± 0.06
0.85 ± 0.06
1.32 ± 0.42
1.27 ± 0.36
HDL
1.33 ± 0.51
1.0 ± 0.15
1.32 ± 0.34
1.17 ± 0.43
LDL
1.04 ± 0.19
1.49 ± 0.08
0.95 ± 0.12
0.90 ± 0.22
Creatinine
197.0 ±1.81
149.0 ±1.21
113.0 ±1.29
114.0 ± 1.42
Urea
5.9 ± 0.46
8.9± 0.34
7.6 ± 0.62
6.5 ± 0.42
g/L
Total proteins
111.0 ±1.09
50.0 ± 0.65
97.0 ± 0.33
95.0 ± 0.51
Functional Foods in Health and Disease 2023; 13(8): 398-408 FFHD Page 404 of 408
Cholesterol: The increase of cholesterol in the
pancreatic β-cells leads to the decrease in insulin
exocytosis from these cells with further development
of type I diabetes mellitus and stimulation of
apoptosis of these cells. Because of this, diabetic
patients are often suggested to take cholesterol-
lowering drugs to protect β-cells [31, 32].
In our study, the cholesterol amount increased
by 1.83 times in the control group compared with the
norm and decreased by 1.5 and 1.4 times,
respectively, in groups that received hydroponic and
soil Moringa extracts (Table 1). This proves that under
stress, the cholesterol amount increases in the
organism, and the use of the Moringa extract forms
the stress-resistance in the organism, protecting it
from different diseases conditioned by stress, such as
cardiovascular diseases [33-35].
HDL and LDL and Moringa extract: The
change in the amount of cholesterol is reflected in the
amount of HDL and LDL. LDL is defined with a high
content of cholesterol, while HDL is not. In our study,
compared with the norm group data, the amount of
LDL increased in the control group, while the amount
of HDL is enhanced in the groups that received
Moringa extract, coinciding with our cholesterol
results. In the control group an increase in cholesterol
level is expressed by an increase in LDL. It is
mentioned in the literature that oxidation of LDL is
one of the main causes of inflammation and
atherogenesis, and plasmic HDL has antiatherogenic,
antioxidant, and anti-inflammatory influences. The
activity of some enzymes inhibiting LDL oxidation is
due to the presence of HDL [36]. LDL increase and HDL
decrease cause the development of cardiovascular
diseases, while LDL decrease and HDL increase
prevent it [37]. One of the main causes of death in
diabetic patients is cardiovascular disease [38]. Our
results of HDL and LDL (Table 1) evidence that the use
of Moringa extract will reduce the probability of
cardiovascular disease development in diabetic
patients and will reduce the risk of death. Note that
according to Kruit et al. HDL protects the β-cells from
the disorders induced by cholesterol, from apoptosis
generated by stress, and from the type 2 diabetes
pathogenesis of Langerhans islands, and the
therapeutic normalization of HDL quantity and quality
may be a new approach for the type 2 diabetes
prevention or treatment [39].
Triglycerides: Triglycerides are part of very low-
density lipoproteins (VLDL). The latter become
intermediate-density lipoproteins (IDL), later
transforming into LDLs [40]. It is proposed that
hypertriglyceridemia is an important trigger of β-cells
insulin excretion in young organisms during fast, as
well as during good nutrition, while excess production
of insulin and chronic hyperinsulinemia have a
pathogenic influence in the development of type 2
diabetes [41]. In our study, compared with the norm,
the level of triglycerides increased only in groups that
received Moringa extract (Table 1), which evidences
the increase of insulin production in these groups.
This by itself proves the fact that in these groups on
the 21st day of stress, the amount of glucose is near to
the norm. As in these groups, the amount of LDL is
less than the norm, which means that the
transformation of VLDL to LDL does not take place,
thus the diabetes development does not trigger.
Creatinine, urea, and protein: In our study,
compared with the norm, the level of creatinine
decreased in control (1.3 times), hydroponic (1.7
times), and soil (1.7) groups (Table 1). The literature
data is controversial. Harita and others mention that a
low level of creatinine in blood serum enhances the
probability of type 2 diabetes generation [42], which
was confirmed for male population by Song and
others [43]. According to Chutani and Pande, a
statistically significant increase of the urea and
Functional Foods in Health and Disease 2023; 13(8): 398-408 FFHD Page 405 of 408
creatinine in blood serum is detected in patients with
type 1 and type 2 diabetes, compared with the
healthy population [44]. The increase in the urea level
in patients with type 2 diabetes was detected also by
Azeez and others [45]. In our study, the level of urea
was also increased in the control (1.5 times),
hydroponic (1.3 times), and soil (1.1 times) groups,
compared with the norm. In groups with the use of
Moringa extract the increase was low.
The total proteins decreased strictly in the
control group compared with the norm (2.22 times).
In hydroponic and soil groups the decrease was less
(1.14 and 1.17 times, compared with the norm). As a
great portion of the HDL are proteins, the decrease of
the protein amount may be combined with the HDL.
The total protein/HDL ratio in the norm, control,
hydroponic and soil groups were 83.5, 50, 73.5, and
81.2, respectively.
Glycogen: In our study under stress conditions,
compared with the norm, the amount of glycogen in
the liver, skeletal muscles, and heart muscle was
reduced in the control group (2.5, 2.4, and 2.4 times,
respectively), increased in hydroponic (1.6, 1.5, and
2.1 times) and soil (1.6, 1.5, and 2.4 times) groups
(Table 2). This testifies that under stress conditions on
the 21st day, the blood glucose level is regulated in
the groups receiving an extract of Moringa, due to its
transformation to glycogen in different organs with
high efficiency. It was shown in the literature that the
strategy to increase the content of liver glucose in
mice leads to the long-term inhibition of the diabetes
phenotype expression regardless of the circulating
insulin amount [46]. It is also mentioned that in the
case of type 2 diabetes, the amount of glycogen
decreases in muscles [47].
Table 2. Glycogen amount in the liver, skeletal, and heart muscles of control, hydroponic, and soil groups’ rabbits and
norm.
Tissues
Glycogen concentration (mg/g tissue)
Norm
Control
Hydroponic
Soil
Liver
5,4 ± 0,44
2,2 ± 0,32
8,8 ± 0,24
8,9 ± 0,35
Skeletal muscle
3,1 ± 0,16
1,3 ± 0,42
4,8 ± 0,12
4,8 ± 0,14
Heart muscle
2,2 ± 0,15
0,9 ± 0,16
4,6 ± 0,12
5,2 ± 0,12
CONCLUSION: Generally, it may be assumed that
the use of Moringa extract decreases the undesirable
consequences of stress by regulating the glucose level
and decreasing the amount of LDL in the blood.
Hydroponic and soil grown Moringa are equivalent in
hypoglycemic and hypolipidemic activities.
Abbreviations: ALT - alanine aminotransferase; AST
- aspartate aminotransferase; HDL - high-density
lipoproteins; LDL - low-density lipoprotein
Authors Contribution: Each author contributed to
the planning of the experiment, its implementation,
processing the results and writing the article.
Competing Interests: There are no competing
interests.
Acknowledgment/Funding: The work was
supported by the Science Committee of RA, in the
frames of the research project 20TTWS-1F023.
Functional Foods in Health and Disease 2023; 13(8): 398-408 FFHD Page 406 of 408
REFERENCES
1. Peñalver, R., L. Martínez-Zamora, J.M. Lorenzo, G. Ros, and G.
Nieto: Nutritional and Antioxidant Properties of Moringa
oleifera Leaves in Functional Foods. Foods 2022, 11(8):1107.
DOI: https://doi.org/10.3390/foods11081107
2. Gopalakrishnan, L., K. Doriya, and D.S. Kumar: Moringa
oleifera: A review on nutritive importance and its medicinal
application. Food science and human wellness 2016, 5(2):49-
56. DOI: https://doi.org/10.1016/j.fshw.2016.04.001
3. Varkey, A.J.: Purification of river water using Moringa
Oleifera seed and copper for point-of-use household
application. Scientific African 2020, 8, e00364. DOI:
https://doi.org/10.1016/j.sciaf.2020.e00364
4. Vargas-Tineo, O.W., D.M. Segura-Muñoz, L.K. Becerra-
Gutiérrez, J.P. Amado-Tineo, and H. Silva-Díaz: Hypoglycemic
effect of Moringa oleifera (Moringa) compared with
Smallanthus sonchifolius (yacon) on Rattus norvegicus with
induced diabetes mellitus. Rev Peru Med Exp Salud Publica
2020, 37(3):478-484. DOI:
https://doi.org/10.17843/rpmesp.2020.373.5275
5. Pradana, D.L.C., E.P. Rahmi, and A.F. Muti: Hypoglycemic
Effect of Moringa oleifera Aqueous Extract in Diabetic Animal
Studies: A Mechanisms Review. In 4th International
Conference on Sustainable Innovation 2020–Health Science
and Nursing (ICoSIHSN 2020) 2021, Atlantis Press, (pp. 620-
624). DOI: https://doi.org/10.2991/ahsr.k.210115.117
6. Toma, A., E. Makonnen, Y. Mekonnen, A. Debella, and S.
Addisakwattana: Intestinal α-glucosidase and some
pancreatic enzymes inhibitory effect of hydroalcholic extract
of Moringa stenopetala leaves. BMC complementary and
alternative medicine 2014, 14(1):1-5.
DOI: https://doi.org/10.1186/1472-6882-14-180
7. Villarruel-López, A., D.A. López-de la Mora, O.D. Vázquez-
Paulino, A.G. Puebla-Mora, M.R. Torres-Vitela, L.A. Guerrero-
Quiroz, and K. Nuño, Effect of Moringa oleifera consumption
on diabetic rats. BMC complementary and alternative
medicine 2018, 18(1):1-10. DOI:
https://doi.org/10.1186/s12906-018-2180-2
8. Tété-Bénissan, A., M.A. Quashie, K. Lawson-Evi, K. Gnandi, K.
Kokou, and M. Gbeassor: Influence of Moringa oleifera leaves
on atherogenic lipids and glycaemia evolution in HIV-infected
and uninfected malnourished patients. Journal of Applied
Biosciences 2013, 62:4610-4619.
DOI: https://doi.org/10.4314/jab.v62i0.86072
9. Ma, Z.F., J. Ahmad, H. Zhang, I. Khan, and S. Muhammad:
Evaluation of phytochemical and medicinal properties of
Moringa (Moringa oleifera) as a potential functional
food. South African Journal of Botany 2020, 129:40-46. DOI:
https://doi.org/10.1016/j.sajb.2018.12.002
10. Jaiswal, D., P. Kumar Rai, A. Kumar, S. Mehta, and G. Watal:
Effect of Moringa oleifera Lam. leaves aqueous extract
therapy on hyperglycemic rats. J Ethnopharmacol 2009,
123(3):392-6. DOI: https://doi.org/10.1016/j.jep.2009.03.036
11. Liu, H., C. Ding, L. Hu, M. Li, W. Zhou, T. Wang, L. Zhu, H. Bao,
and X. Cheng: The association between AST/ALT ratio and all-
cause and cardiovascular mortality in patients with
hypertension. Medicine (Baltimore) 2021, 100(31): e26693.
DOI: https://doi.org/10.1097/MD.0000000000026693
12. Chen, W., W. Wang, L. Zhou, J. Zhou, L. He, J. Li, X. Xu, J.
Wang, and L. Wang: Elevated AST/ALT ratio is associated with
all-cause mortality and cancer incident. J Clin Lab Anal. 2022,
36(5): e24356. DOI: https://doi.org/10.1002/jcla.24356
13. Vedantam, D., D.S. Poman, L. Motwani, N. Asif, A. Patel, and
K.K. Anne: Stress-Induced Hyperglycemia: Consequences and
Management. Cureus. 2022, 14(7): e26714.
DOI: https://doi.org/10.7759/cureus.26714.
14. Devaki, M., R. Nirupama, and H.N. Yajurvedi: Chronic stress-
induced oxidative damage and hyperlipidemia are
accompanied by atherosclerotic development in rats. Stress.
2013, 16(2):233-43. DOI:
https://doi.org/10.3109/10253890.2012.719052.
15. Sozen, E. and N.K. Ozer: Impact of high cholesterol and
endoplasmic reticulum stress on metabolic diseases: An
updated mini review. Redox biology 2017, 12:456-461.
DOI: https://doi.org/10.1016/j.redox.2017.02.025
16. Lamharzi, N., C.B. Renard, F. Kramer, S. Pennathur, J.W.
Heinecke, A. Chait, and K.E. Bornfeldt: Hyperlipidemia in
concert with hyperglycemia stimulates the proliferation of
macrophages in atherosclerotic lesions: potential role of
glucose-oxidized LDL. Diabetes 2004, 53(12):3217-3225. DOI:
https://doi.org/10.2337/diabetes.53.12.3217
17. Aghajanyan, A. A. and Tadevosyan, A. H. Hypoglycemic
activity of $ origanum~ vulgare $ l. Aqueous extract in
hyperglycemia induced by immobilization stress in
rabbits. Proceedings of the YSU B: Chemical and Biological
Sciences. 2022. 56(2 (258)), 141-150. DOI:
https://doi.org/10.46991/PYSU:B/2022.56.2.141
18. Trinder, P.: Determination of blood glucose using an oxidase-
peroxidase system with a non-carcinogenic
chromogen. Journal of clinical pathology 1969, 22(2):158-161
DOI: https://doi.org/10.1136/jcp.22.2.158
19. Trinder, P.: Determination of glucose in blood using glucose
oxidase with an alternative oxygen acceptor. Annals of
clinical Biochemistry 1969, 6(1):24-27.
https://doi.org/10.1177/000456326900600108
Functional Foods in Health and Disease 2023; 13(8): 398-408 FFHD Page 407 of 408
20. Friedwald, W.T., R.I. Levy, and D.S. Fredrickson: Estimation of
the concentration of low-density lipoprotein cholesterol in
plasma, without use of the preparative ultracentrifuge. Clin
Chem. 1972, 18(6):499-502. https://iaimjournal.com/wp-
content/uploads/2016/02/iaim_2016_0302_02.pdf
21. Danchenko, E.O., and A.A. Chirkin: [A new approach to the
determination of glycogen concentration in various tissues
and comments on the interpretation of its results]. Sud Med
Ekspert. 2010; 53(3):25-8. Russian.
22. Burtis C.A., Ashwood E.R., ed. Tietz Textbook of clinical
chemistry and molecular diagnostics, 4th ed. 2006, WB
Saunders, 798-9, 801-3, 801
23. Xie, W., W. Yu, S. Chen, Z. Ma, T. Yang, and Z. Song: Low
aspartate aminotransferase/alanine aminotransferase
(DeRitis) ratio assists in predicting diabetes in Chinese
population. Frontiers in Public Health 2022, 10:1049804.
DOI: https://doi.org/10.3389/fpubh.2022.1049804
24. Melillo, A.: Rabbit Clinical Pathology. J Exot Pet Med. 2007,
16(3):135-145.
DOI: https://doi.org/10.1053/j.jepm.2007.06.002.
25. Hanley, A.J., K. Williams, A. Festa, L.E. Wagenknecht, R.B.
D’Agostino Jr, J. Kempf, B. Zinman, and S.M. Haffner:
Elevations in markers of liver injury and risk of type 2
diabetes: the insulin resistance atherosclerosis study.
Diabetes 2004, 53(10):2623-2632.
DOI: https://doi.org/10.2337/diabetes.53.10.2623.
26. Xu, J., X. Shi, and Y. Pan: The Association of Aspartate
Aminotransferase/Alanine Aminotransferase Ratio with
Diabetic Nephropathy in Patients with Type 2 Diabetes.
Diabetes Metab Syndr Obes. 2021, 14:3831-3837.
DOI: https://doi.org/10.2147/DMSO.S330741
27. Биохимия / Под ред. Е. С. Северина. 2003. С. 469. — 779 с.
— ISBN 5-9231-0254-4.
28. Simental-Mendía, L.E., M. Rodríguez-Morán, R. Gómez-Díaz,
N.H. Wacher, H. Rodríguez-Hernández, and F. Guerrero-
Romero: Insulin resistance is associated with elevated
transaminases and low aspartate aminotransferase/alanine
aminotransferase ratio in young adults with normal weight.
Eur J Gastroenterol Hepatol. 2017, 29(4):435-440.
DOI: https://doi.org/10.1097/MEG.0000000000000811
29. Chen, L., K. Zhang, X. Li, Y. Wu, Q. Liu, L. Xu, L. Li, and H. Hu:
Association Between Aspartate Aminotransferase to Alanine
Aminotransferase Ratio and Incidence of Type 2 Diabetes
Mellitus in the Japanese Population: A Secondary Analysis of
a Retrospective Cohort Study. Diabetes, Metabolic Syndrome
and Obesity: Targets and Therapy 2021, 14:4483. DOI:
https://doi.org/10.2147/DMSO.S337416
30. Niu, H., and Y. Zhou: Nonlinear Relationship Between AST-to-
ALT Ratio and the Incidence of Type 2 Diabetes Mellitus: A
Follow-Up Study. Int J Gen Med. 2021, 14:8373-8382. DOI:
https://doi.org/10.2147/IJGM.S341790
31. Noroozi Karimabad, M., Khalili, P., Ayoobi, F., Esmaeili-
Nadimi, A., & La Vecchia, C. Serum liver enzymes and
diabetes from the Rafsanjan cohort study. BMC Endocrine
Disorders. 2022, 22(1), 1-12. DOI:
https://doi.org/10.1186/s12902-022-01042-2
32. Duan, Y., K. Gong, S. Xu, F. Zhang, X. Meng, and J. Han:
Regulation of cholesterol homeostasis in health and diseases:
from mechanisms to targeted therapeutics. Signal Transduct
Target Ther. 2022, 7(1):265. DOI:
https://doi.org/10.1038/s41392-022-01125-5
33. Reddy, V., Urooj, A., Sairam, S., Ahmed, F., and Prasad, N. N.
Hypocholesterolemic effect of Moringa oleifera polyphenols
in rats fed high fat-cholesterol diet. Malaysian Journal of
Nutrition. 2017, 23(3), 473-478. DOI:
https://nutriweb.org.my/mjn/publication/23-3/o.pdf
34. Alia, F., Putri, M., Anggraeni, N., & Syamsunarno, M. R. A. The
potency of Moringa oleifera Lam. as protective agent in
cardiac damage and vascular dysfunction. Frontiers in
Pharmacology. 2022, 12, 724439. DOI:
https://doi.org/10.3389/fphar.2021.724439
35. Kivimäki, M., & Steptoe, A. Effects of stress on the
development and progression of cardiovascular disease.
Nature Reviews Cardiology. 2018, 15(4), 215-229. DOI:
https://www.nature.com/articles/nrcardio.2017.189
36. Kontush, A., S. Chantepie, and M.J. Chapman: Small, dense
HDL particles exert potent protection of atherogenic LDL
against oxidative stress. Arteriosclerosis, thrombosis, and
vascular biology 2003, 23(10):1881-1888.
https://doi.org/10.1161/01.ATV.0000091338.93223.E8
37. Kontush, A., E.C. de Faria, S. Chantepie, and M.J. Chapman: A
normotriglyceridemic, low HDL-cholesterol phenotype is
characterised by elevated oxidative stress and HDL particles
with attenuated antioxidative activity. Atherosclerosis
2005, 182(2):277-285.
DOI: 10.1016/j.atherosclerosis.2005.03.001
38. Leon, B.M., and T.M. Maddox: Diabetes and cardiovascular
disease: Epidemiology, biological mechanisms, treatment
recommendations and future research. World J Diabetes.
2015, 6(13):1246-58. DOI:
https://doi.org/10.4239/wjd.v6.i13.1246
39. Kruit, J.K., L.R. Brunham, C.B. Verchere, and M.R. Hayden,
HDL and LDL cholesterol significantly influence β-cell function
in type 2 diabetes mellitus. Current opinion in lipidology
2010, 21(3):178-185. DOI:
https://doi.org/10.1097/MOL.0b013e328339387b
40. Sandhofer, F.: Physiologie und Pathophysiologie des
Stoffwechsels der Lipoproteine [Physiology and
Functional Foods in Health and Disease 2023; 13(8): 398-408 FFHD Page 408 of 408
pathophysiology of the metabolism of lipoproteins]. Wien
Med Wochenschr. 1994, 144(12-13):286-90.
41. Tricò. D., A. Natali, A. Mari, E. Ferrannini, N. Santoro, and S.
Caprio: Triglyceride-rich very low-density lipoproteins (VLDL)
are independently associated with insulin secretion in a
multiethnic cohort of adolescents. Diabetes Obes Metab.
2018, 20(12):2905-2910.
DOI: https://doi.org/10.1111/dom.13467
42. Harita N, Hayashi T, Sato KK, Nakamura Y, Yoneda T, Endo G,
Kambe H. Lower serum creatinine is a new risk factor of type
2 diabetes: the Kansai healthcare study. Diabetes Care. 2009
Mar;32(3):424-6. https://doi.org/10.2337/dc08-1265
43. Song, D.K., Y.S. Hong, Y.A. Sung, and H. Lee: Association of
serum creatinine levels and risk of type 2 diabetes mellitus in
Korea: a case control study. BMC Endocrine Disorders 2022,
22(1):1-7. DOI: https://doi.org/10.1186/s12902-021-00915-2
44. Chutani, A. and S. Pande: Correlation of serum creatinine and
urea with glycemic index and duration of diabetes in Type 1
and Type 2 diabetes mellitus: A comparative study. National
Journal of Physiology, Pharmacy and Pharmacology 2017,
7(9):914-914. DOI:10.5455/njppp.2017.7.0515606052017
45. Azeez, F., S. Sultan, and L. Othman: Estimation of Urea and
Creatinine in Type 2 Diabetes Mellitus Patients. Proceedings
of the 1st International Multi-Disciplinary Conference Theme:
Sustainable Development and Smart Planning, IMDC-SDSP
2020, Cyperspace, 28-30 June 2020 DOI:
https://doi.org/10.4108/eai.28-6-2020.2298519
46. López-Soldado, I., J.J. Guinovart, and J. Duran, Increasing
hepatic glycogen moderates the diabetic phenotype in
insulin-deficient Akita mice. Journal of Biological Chemistry
2021, 296. DOI: https://doi.org/10.1016/j.jbc.2021.100498
47. He, J., and D.E. Kelley: Muscle glycogen content in type 2
diabetes mellitus. Am J Physiol Endocrinol Metab. 2004,
287(5):E1002-7. DOI:
https://doi.org/10.1152/ajpendo.00015.2004