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An Antioxidative Nutrient-Rich Enteral Diet Attenuates Lethal Activity and Oxidative Stress Induced by Lipopolysaccharide in Mice
Shizuko Abe, MSc*,
Yoshiaki Tanaka, MD, PhD ,
Nobuaki Fujise, DVM*,
Tsuyoshi Nakamura, PhD*,
Hiroaki Masunaga, DVM, PhD*,
Takashi Nagasawa, PhD and
Minoru Yagi, MD, PhD
From the * Technical Research Laboratories, EN
Otsuka Pharmaceutical Co, Ltd, Hanamaki, Japan;
Department of Pediatric Surgery, Kurume
University School of Medicine, Kurume, Japan; and
Food and Health Science, Faculty of
Agriculture, Iwate University, Morioka, Japan
Correspondence: Shizuko Abe, MSc, Technical Research Laboratories, EN Otsuka
Pharmaceutical Co, Ltd, 4–3-5 Nimaibashi, Hanamaki, Iwate, Japan
025-0312. Electronic mail may be sent to
abes{at}enotsuka.co.jp.
Background: Oxidative stress is related to various diseases, such
as diabetes, cancer, inflammatory disease, and arteriosclerosis. The aim of
this study is to evaluate enhancement effect in serum antioxidant capacity
obtained from an antioxidative nutrient-rich enteral diet (AO diet). We also
investigated the ability of the AO diet to attenuate lethality, the production
of oxidized products, the production of inflammatory cytokines, and liver
injury using lipopolysaccharide (LPS)-injected mice. LPS mice were used as a
model to represent critically ill patients that have experienced a septicemia.
Methods: The AO diet contained polyphenol and enhanced vitamin C,
vitamin E, and trace elements. Total antioxidant activities of the control
enteral diet (Control diet) and the AO diet were measured by
1,1-diphenyl-2-picrylhydrazyl (DPPH) and
2,2'-azinobis-(3-ethylbenzthiazoline sulphonic acid; ABTS)
radical-scavenging activities. Male BALB/c mice were fed either of these diets
for 7 days and were injected with 5 mg/kg LPS. The survival of mice was
monitored from day 0 to day 8. To evaluate oxidative stress, inflammation, and
liver injury, blood and liver samples were collected, and tumor necrosis
factor- (TNF-), interleukin-6, thiobarbituric acid-reactive
substances (TBARS), protein carbonyl contents, aspartate aminotransferase,
alanine aminotransferase, and radical-scavenging activities were measured.
Results: The survival rate of mice receiving the AO diet or the
Control diet was 73.9% and 33.3%. In the AO diet group, levels of serum
TNF-, serum protein carbonyl contents, plasma, and liver TBARS were
significantly lower than in the Control diet group. DPPH and ABTS
radical-scavenging activities of the AO diet itself were significantly higher
than that of the Control diet, and serum activities in the AO diet group were
also higher. Conclusions: The antioxidative nutrient supplementation
of an enteral diet may be useful and offer relief from septic symptoms.
Bacterial lipopolysaccharide (LPS) is a major factor in the pathogenesis of
Gram-negative septic
shock,1 and this
shock causes a poor prognosis associated with organ dysfunction,
hypoperfusion, or
hypotension.2 In an
animal's body, LPS interacts with macrophages to produce reactive oxygen
species (ROS) such as hydroxyl radical (·OH), superoxide (O
–2) and hydrogen peroxide
(H2O2)3.
Additionally, proinflammatory cytokines, tumor necrosis factor-
(TNF-) and interleukin-6 (IL-6) are overproduced in response to
LPS-macrophage
interactions.4
LPS-induced stress leads to oxidative and inflammatory injuries in many
tissues, which may lead to organ
failure.5
Under physiologic conditions, there is a well-managed balance between the
formation and the scavenging of ROS by various
antioxidants.6
Systems including antioxidative enzymes, low-molecular-weight compounds such
as vitamin E (-tocopherol), vitamin C (ascorbic acid), and reduced
glutathione are involved in the aforementioned
equilibrium.6 The
balance of antioxidant compounds and ROS is maintained under noninvasive
conditions; however, excessive oxidative stress breaks the balance of this
system, and oxidative damage may lead to
disease.7 Therefore,
the effects obtained from the administration of various antioxidants on
oxidative stress have been studied in clinical trials and in experimental
animal models.
Enteral diets have only been used for nutrition support under conditions of
insufficient oral ingestion. Nowadays, several enteral diets that have special
functions that regulate body defense responses have been developed; for
example, immunopotentiator rich-enteral diets. In this study, we developed an
antioxidative nutrient-rich enteral diet (AO diet) and clarified the effect of
this diet on improving symptoms from diseases related to ROS. An AO diet was
supplemented with a potent antioxidant, polyphenol (a mixture of catechin and
proanthocyanidin), and high amounts of vitamin C, vitamin E and trace
elements. We examined the antioxidant capacity of the AO diet and serum
antioxidant capacity of mice fed on this diet. We also investigated AO dietary
intake effects on lethality, the production of peroxide compounds, the
production of inflammatory cytokines, and liver injury using an LPS-injected
mouse model for patients with septicemia.
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MATERIALS AND METHODS
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Animals and Diets
The experiments reported herein conform to guidelines for the care and use
of laboratory animals established by the Animal Use and Care Committee of EN
Otsuka Pharmaceutical Co, Ltd. Six-week-old male BALB/c mice were obtained
from CLEA Japan, Inc (Tokyo, Japan). Mice were individually housed in cages
under controlled conditions for temperature and humidity, with an alternating
12-hour light-dark cycle. Mice were fed commercial mouse chow with water
ad libitum for 7 days before further experimentation.
We produced the following experimental diets: a control enteral diet
(Control diet) and an AO diet (EN Otsuka Pharmaceutical Co, Ltd, Hanamaki,
Japan). The composition of the diets is shown in
Table I. The Control diet was
similar in composition to general enteral diets. The AO diet was supplemented
with polyphenol (a mixture of catechin and proanthocyanidin) and higher
amounts of vitamin C, vitamin E, and trace elements (zinc, copper, selenium,
and chromium). In the Control diet, trace elements were obtained from raw
material. On the other hand, we considered replenishing trace elements in the
AO diet.
Seven-week-old mice were divided into 2 groups fed either the AO diet or
the Control diet using supply nozzles for 7 days. The daily energy
administration volume was increased gradually to reduce differences in the
amount of individual feeding. Therefore, the administration volume of the
diets per day was 13 kcal on day 1, 15 kcal on day 2, 17 kcal on day 3, and 20
kcal on days 4–7. Water was given ad libitum. After the 7-day
prefeeding period, mice were injected intravenously with LPS (Escherichia
coli, serotype 011:B4; Sigma Chemical, St. Louis, MO) at a dose of 5
mg/kg. LPS was dissolved in saline, and the total injection volume was 10
mL/kg. The survival of mice was monitored for 8 days (n = 23–24), and
during this term, diets were given in 20 kcal, and water was available ad
libitum. Serum, plasma, and liver samples were obtained before the diet
prefeeding period and at times after the prefeeding period (ie, before and
after the LPS injection; n = 6). Blood samples were obtained by caudal vena
cava under ether anesthesia.
Measurement of 1,1-Diphenyl-2-Picrylhydrazyl (DPPH) and 2,2'-Azinobis-(3-Ethylbenzthiazoline Sulfate; ABTS) Radical-Scavenging Activities
Total antioxidant capacities of the Control diet and the AO diet were
measured by DPPH8
(1,1-diphenyl-2-picrylhydrazyl) and ABTS
(2,2'-azinobis-[3-ethylbenzthiazoline sulfate]) radical-scavenging assay
methods. The aforementioned assays rely on the ability of antioxidants in the
sample to eliminate DPPH radicals or ABTS radicals added to the reactive
solution. Under radical-scavenging assay conditions, antioxidants cause a
suppression in absorbance to a degree that is proportional to their
concentration.
The DPPH scavenging assay was measured according to Yamaguchi et
al.8 Briefly, diet
samples, 0.04-M sodium phosphate buffer (pH 7.4), and 0.25-M DPPH ethanol were
incubated for 20 minutes in the dark at room temperature. After the
incubation, reaction solution was added to the ethanol to precipitate the
protein in the samples, and samples were subsequently centrifuged at 3000 rpm
for 10 minutes. Supernatants were added to designated wells on a microplate,
and absorbance was determined at 520 nm using an absorption spectrometer.
The ABTS radical-scavenging assay was performed with the Cayman Chemical
Antioxidant Assay Kit (Cayman Chemical Company, Ann Arbor, MI), according to
the manufacturer's instructions. In this assay, 0.15 mL of chromogen solution
containing ABTS and 0.01 mL of metmyoglobin was added to 0.01 mL of serum
samples in designated wells on a microplate. Subsequently, 0.04 mL of hydrogen
peroxide working solution was added into the wells, and the microplate was
incubated for 5 minutes at room temperature. Following the incubation,
absorbance was measured at 750 nm using an absorption spectrometer.
DPPH and ABTS radical-scavenging activities were calculated using the
equation obtained from linear regression of the Trolox standard curve by
substituting values for each sample into the equation.
Total Antioxidant Capacity in the Serum of Mice Fed an AO or Control Diet
Total antioxidant capacity is a parameter that is sensitive enough to
detect circadian changes in the capacity of blood
plasma9,10
and thus effects of consuming green
tea11 or
wine,12 etc. To
confirm the change in antioxidant capacity associated with the consumption of
an AO diet, the serum antioxidant capacity of mice was also measured by DPPH
and ABTS radical-scavenging assays. The DPPH scavenging activity assay was
measured according to Janaszewska and
Bartosz.10 Briefly,
serum samples plus 4.7 mmol/L sodium phosphate buffer (pH 7.4) and a 5 mmol/L
DPPH ethanol solution were incubated in the dark at room temperature. After
the incubation, reaction solution was added to the ethanol to precipitate the
protein in the serum, and samples were centrifuged at 3000 rpm for 10 minutes.
The absorbance of the supernatant was determined at 520 nm.
The ABTS radical-scavenging activity assay was performed using the Cayman
Chemical Antioxidant Assay Kit as outlined above.
Measurement of Lipid Peroxide Thiobarbituric Acid-Reactive Substances (TBARS)
Lipid peroxidation in plasma and liver was determined from
TBARS.13 Liver
samples were homogenized in 4 volumes of 1.15% KCl buffer. Tissue homogenates
and plasma were added to 8.1% sodium dodecyl sulfate, 20% acetic acid, 0.8%
thiobarbituric acid, and distilled water. The reaction mixture was placed in a
waterbath for 1 hour, and distilled water plus a mixture of butanol/pyridine
was added to it. After centrifugation, the supernatant was added to designated
wells on a microplate, and absorbance was determined at 520 nm. TBARS
concentrations were calculated using 1,1,5,5-teraethoxypropane as a
standard.
Measurement of TNF-, IL-6, Aspartate Aminotransferase (AST), Alanine Aminotransferase (ALT)
Serum samples were obtained from 0 to 24 hours after an LPS injection.
Concentrations of circulating TNF- and IL-6 in serum were determined
by enzyme-linked immunosorbent assay (ELISA; BioSource International, Inc,
Camarillo, CA), according to the manufacturer's instructions. Briefly, samples
and incubation buffer were added into wells of a microplate coated by
polyclonal antibodies specific for mouse TNF- or IL-6, respectively.
After biotinylated monoclonal secondary antibodies were added,
streptavidin-peroxidase and a substrate to produce color were added to the
wells of the microplate. The intensity of the colored products was measured at
450 nm.
The activities of AST and ALT in serum were determined using a biochemical
automated analyzer (Fuji Drichem; Fujifilm Medical Co, Ltd, Tokyo, Japan). AST
and ALT activities were expressed in international units (U/L).
Protein Carbonyl Content Measurements
The oxidative modification of proteins can be evaluated by the amount of
protein carbonyl groups. The carbonyl group in the protein generates a
hydrazone compound by reacting with 2,4-dinitrophenylhydrazine (DNPH). In this
study, the level of protein carbonyl contents in liver tissues was determined
with the Cayman Chemical Protein Carbonyl Assay Kit (Cayman Chemical Company),
according to the manufacturer's instructions. Briefly, liver samples were
homogenized in 4 volumes of phosphate buffer (pH 6.7, containing 1 mmol/L
EDTA), and nucleic acids were removed with a 10% streptomycin sulfate stock
solution. Tissue homogenates and DNPH were mixed and incubated for 1 hour.
DNPH reacted with protein carbonyls and produced a corresponding hydrazine,
which was measured at 360 nm.
Statistical Analyses
Differences in TNF-, TBARS, DPPH, and ABTS radical-scavenging
activities and protein carbonyl contents between mice fed an AO or a Control
diet were determined with Student's t-tests. Differences in survival
rates of LPS-treated mice were determined by survival analyses, and p
values were determined by log-rank tests. Values are presented as mean
± SE. Significant differences were assumed when p < .5. All
calculations were performed with the computer program JMP V 5.1 (SAS Institute
Japan Ltd, Tokyo, Japan).
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RESULTS
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The Total Antioxidant Capacity of Experimental Diets
DPPH and ABTS radical-scavenging activities of the AO diet were 3 times
higher than those of the Control diet
(Table II).
AO Dietary Effect on the Survival Rate of Mice Treated With LPS
During the 7-day prefeeding period, mice were feeding almost all diets, and
at the end of the prefeeding, there was no significant difference in body
weight between mice fed the Control diet (24.9 ± 1.74 g, n = 24) and
the AO diet (25.4 ± 1.50 g, n = 23). Only 33.3% of mice that had
ingested the Control diet survived the LPS injection within 1–8 days. On
the other hand, 73.9% of mice that had ingested the AO diet survived
(Figure 1).
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FIGURE 1. AO dietary effects on the survival of LPS-treated mice. Mice were fed the
control enteral diet (Control diet) or the antioxidative nutrient-rich enteral
diet (AO diet) for 1 week and challenged with an IV-injection LPS at a dose of
5 mg/kg. The survival of mice was monitored for 8 days. •: Control diet
group (n = 24),  : AO diet group (n = 23). The overall difference in
survival rate between the AO diet group and the Control diet group is
significant (p = .0029). LPS, lipopolysaccaride.
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AO Dietary Effect on the Antioxidant Capacity of Mice
Before the experimental diet was ingested, serum DPPH and ABTS
radical-scavenging activities in mice (n = 6) were 0.56 ± 0.02 and 0.98
± 0.07 mmol/L (Trolox equivalent), respectively
(Table III). However, the
activities markedly increased to 0.81 ± 0.07 mmol/L (DPPH) and 1.93
± 0.27 mmol/L (ABTS) after a 7-day AO dietary feeding period, whereas
the activities of the Control diet group did not increase. The antioxidant
activities in the AO diet group remained high after the LPS injection, but the
Control diet group had lower antioxidant levels.
AO Dietary Effect on Lipid Peroxide in Mice Treated With LPS
The level of plasma TBARS in mice (n = 6) fed the Control diet increased
and almost doubled 24 hours after the LPS injection
(Figure 2). On the other hand,
the level did not change in mice fed the AO diet. The level of TBARS in the AO
diet group was significantly lower than that in the Control diet group. The
level of liver TBARS (n = 6) also continually increased in mice fed the
Control diet (Figure 3) but did
not change in mice fed the AO diet. Ten hours after the LPS injection, the
level of TBARS in the AO diet group was significantly lower than that in the
Control diet group.
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FIGURE 2. AO dietary effects on LPS-induced increases in serum levels of TBARS in
mice. Samples were obtained before (0 hours) and after the IV LPS injection (2
hours, 10 hours, and 24 hours). The degree of lipid peroxidation in plasma was
determined by measuring the absorbance of thiobarbituric acid-reactive
substances (TBARS) at 520 nm. TBARS concentrations were calculated using
1,1,5,5-teraethoxypropane as a standard. Values represent mean ± SE, n
= 6. *p < .05, **p < .01 compared with controls from t-tests. •:
control enteral diet (Control diet) group, : antioxidative nutrient-rich
enteral diet (AO diet) group. LPS, lipopolysaccaride.
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FIGURE 3. AO dietary effects on LPS-induced increases in liver levels of TBARS in
mice. Liver samples were collected before LPS injection (0 hours) and after
the injection (2 hours, 10 hours, and 24 hours), and were homogenized in 4
volumes of 1.15% KCl buffer. The degree of lipid peroxidation in the liver
sample was determined by measuring the absorbance of TBARS at 520 nm. Values
are mean ± SE, n = 6. **p < .01 compared with controls from t-tests.
•: control enteral diet (Control diet) group, : antioxidative
nutrient-rich enteral diet (AO diet) group.
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AO Dietary Effect on Protein Carbonylation in Mice Treated With LPS
The protein carbonyl content in livers obtained from mice (n = 6) fed the
Control diet increased until 10 hours after the LPS injection, and
subsequently decreased to baseline (Table
IV). Before the LPS injection (0 hours), there was no difference
between the Control diet group and the AO diet group; however, 10 hours after
the LPS injection, the level in the AO diet group was lower than that in the
Control diet group.
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Table IV Antioxidative dietary effects on LPS-induced increases in liver levels
of protein carbonyl contents in mice
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AO Dietary Effect on Inflammatory Cytokines in Mice Treated With LPS
Both TNF- and IL-6 were barely detectable before the LPS injection
(n = 6). The cytokines increased significantly after the LPS injection, peaked
at 2 hours, and dropped to near baseline after 24 hours
(Figure 4 and
Figure 5). At 2 hours, the
activity of TNF- in mice fed the AO diet was significantly lower than
that in mice fed the Control diet. On the other hand, the activities of IL-6
did not differ significantly between the 2 groups of mice.
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FIGURE 5. AO dietary effects on LPS-induced increases in serum levels of IL-6 in
mice. Samples were obtained before (0 hours) and after the IV LPS injection (2
hours, 10 hours, and 24 hours). The concentration of IL-6 circulating in the
serum was determined by an enzyme-linked immunosorbent assay (ELISA) kit.
Values represent mean ± SE, n = 6. •: control enteral diet
(Control diet) group, : antioxidative nutrient-rich enteral diet (AO
diet) group.
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AO Dietary Effect on Liver Injuries in Mice Treated With LPS
Serum AST and ALT activities increased enormously after the LPS injection
(n = 6; Table V). Both
parameters for liver injury did not differ significantly between the 2 groups
of mice.
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DISCUSSION
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The present study clearly shows that the AO diet, which is supplemented
with catechin, proanthocyanidin, vitamin C and vitamin E, and trace elements
(zinc, copper, selenium, and chromium), had a higher antioxidant activity
compared with the Control diet, increased the survival rate, and decreased
oxidative stress and inflammation in mice injected with LPS.
Catechin and proanthocyanidin are polyphenols. They are abundantly
contained in green
tea14 and red
wine,15
respectively, and our food has them in abundance. Hydroxyl groups in these
polyphenols have high reactivities toward
ROS16 and reduce
peroxides. Polyphenol has also been shown to suppress lipid
peroxidation17 and
DNA oxidation18;
moreover, polyphenol could protect against various diseases related to ROS;
for example, cardiovascular disturbances in
humans,19 ischemia
reperfusion injuries in rabbit
hearts,20 and
atherosclerosis in
mice.21
Vitamin C and vitamin E have also been studied for their role in
suppressing diseases related to ROS. Paolisso et
al22 reported that
vitamin C increased plasma vitamin levels in diabetic patients and inhibited
the nonenzymatic metabolism of glucose. Riordan et
al23 suggested the
systematic use of vitamin C as an adjuvant to cancer therapy. Additionally,
some reports show the attenuating effect of vitamin C on ischemia reperfusion
injury24 and
cardiovascular
disturbances.25
Vitamin E is a potent peroxy-radical scavenger. In cell membranes, vitamin E
inhibits ROS chain
reactions26 and
lipid peroxides. Additionally, vitamin E also functions with vitamin C
synergistically.27
Vitamin E is transformed into vitamin E radicals when there is a reduction in
lipid peroxide. However, vitamin C reduces the oxidized form of vitamin E
radicals to regenerate its antioxidant
function.28 Thus,
vitamin E and vitamin C may have synergistic effects. Nathens et
al28 reported that
the early administration of vitamin C and E to severe ICU patients reduces
organ damage and shortens the duration of hospital stays.
Trace elements, including selenium, zinc, chromium, and copper, offer
various protective effects against the metabolism of ROS. Trace elements
maintain or enhance the activity of antioxidant enzymes, attenuate oxidative
stress, and offer relief for various diseases such as
diabetes,29–31
ischemia reperfusion
injury,32 and
cancer.33 In
critical ICU patients, the administration of selenium, zinc, and vitamin E
suppressed a decrease of several antioxidant enzymes and activated glutathione
peroxidases
(GSHPx).34
According to the aforementioned reports concerning polyphenols, vitamin C,
vitamin E, and trace elements, we developed an AO diet. A 7-day prefeeding
period with the AO diet increased serum antioxidative activities as evaluated
by DPPH and ABTS radical-scavenging activities. After an LPS injection, the
serum antioxidative activities in mice fed the AO diet were maintained at
higher levels than mice fed a Control diet. The aforementioned results can be
attributed to the total activity of all the antioxidants, polyphenols, vitamin
C, vitamin E, trace elements, and possibly other endogenous components,
including antioxidative vitamins, enzymes, and sulfur-containing compounds
such as glutathione (GSH) and cysteine. Taken altogether, the results
presented herein suggest that the ingested antioxidants were enterally
absorbed, thereby increasing individual antioxidant levels in blood and
tissues, and enhanced the total antioxidant capacity of the living body.
Actually, the levels of TBARS and protein carbonyl contents were attenuated
in the AO-diet-fed mice. TBARS and protein carbonyl contents are commonly used
as oxidative stress markers (a lipid peroxidation marker and a protein
peroxidation marker, respectively). The production of lipid peroxidation is
thought to gradually injure cell
membranes,35 and
the levels of TBARS in blood and tissue of septic patients are higher than
those in healthy
individuals.36
Similarly, protein oxidation leads to protein damage and to losses in cellular
function,6 and the
level of protein carbonyl contents in septic patients is higher than in
healthy
individuals.36
Additionally, there is a strong correlation between TBARS and protein carbonyl
contents.36 Thus,
the suppression of TBARS and protein carbonyl contents levels in this study
suggests that the AO diet possibly attenuates oxidative stress in septic
patients. Although AST and ALT levels did not differ significantly between the
2 groups of mice in this study, the liver injury induced by LPS is thought to
not have been improved directly by the AO diet.
The TNF- concentration was also attenuated in the AO-diet-fed mice.
TNF- is known to play a pivotal role in lethal mice
endotoxemia.4,5
The serum concentration of TNF- dramatically increases in experimental
models, and this cytokine induces an overreaction in inflammation and lethal
shock.4,5
Generally, neutrophils and macrophages are activated, and inflammatory
cytokines are produced, with the overproduction of ROS in critical illnesses,
including septic disease. In this manner, inflammatory and oxidative stresses
are closely related, and they aggravate symptoms in sepsis. Therefore, our
results including the direct suppression of TNF- in serum suggest that
the AO diet possibly attenuated not only oxidative stress but also
overinflammatory reactions in septic shock.
In conclusion, the present study revealed that an enteral diet containing
abundant antioxidant substances had high antioxidant activities in
vitro. The oral intake of this diet enhanced the antioxidant capacity of
the living body and protected against LPS-induced lethal shock via
counteracting inflammatory and oxidative stress. Considering these results and
the clinical studies cited in the Discussion section above, supplementation of
antioxidants in enteral diets is expected to offer relief from septic symptoms
that are critical in illnesses related to oxidative stress and
inflammation.
Received for publication August 30, 2006.
Accepted for publication December 27, 2006.
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Journal of Parenteral and Enteral Nutrition, Vol. 31, No. 3,
181-187 (2007)
DOI: 10.1177/0148607107031003181
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MATERIALS AND METHODS
RESULTS