Vol. 89, Issue 3, 877-883, September 2000
Postprandial increases in serum antioxidant capacity in older
women
Guohua
Cao and
Ronald L.
Prior
Jean Mayer Human Nutrition Research Center on Aging at Tufts
University, Agriculture Research Service, United States Department
of Agriculture, Boston, Massachusetts 02111
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ABSTRACT |
Eight women were recruited for studying the effects of a meal
on overall antioxidant status. Subjects resided in a metabolic research unit for two 36-h periods. During period A,
subjects fasted overnight (12 h) and were then given a breakfast, a
lunch, a snack, and a dinner. During period B, subjects
fasted for 23 h and were then given a dinner. These meals were
designed to contain negligible antioxidants. Blood samples were
collected for analyzing total antioxidant capacity (TAC) and individual
antioxidants. The results showed that serum TAC significantly increased
by up to 23% after the consumption of the lunch and dinner during
period A. Serum TAC did not increase until after the
consumption of the dinner during period B. Among the
antioxidants (vitamin C, 
-tocopherol, bilirubin, and uric acid)
examined, serum uric acid was the only one that showed a significant
postprandial increase, which was also parallel to the postprandial
response in serum TAC. These results indicate that food intake, even if
low in antioxidants, can increase the serum total antioxidant activity.
meal; reactive oxygen species; free radical; oxygen radical
absorbance capacity
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INTRODUCTION |
THE OCCURRENCE OF
REACTIVE oxygen (ROS) and nitrogen species (RNS) is an attribute
of normal aerobic metabolic processes. Among the most significant
biological sources of ROS are those that lead to O2-derived
superoxide radicals from electron transport associated with
mitochondrial membranes. It is well documented that, under normal
physiological conditions, an estimated 1-3% of respired oxygen is
converted to superoxide radicals. Other ROS include hydroxyl, peroxyl
radicals, and H2O2. RNS include nitric oxide
(NO·) and nitrogen dioxide (NO2·). NO· is formed from
the amino acid L-arginine. NO2· is made when
NO· reacts with O2. There is a considerable body of
biological evidence that ROS and RNS can be damaging to cells and thus
might contribute to cellular dysfunction and diseases. The existence
and development of cells in an oxygen-containing environment would not
be possible without the presence of a complicated defense system that
includes enzymatic and nonenzymatic antioxidant components. Therefore, a healthy aerobic life is characterized by a steady formation of
ROS and RNS balanced by a similar rate of their consumption by an
antioxidant system.
The nonenzymatic antioxidants, most of which have low molecular weights
and are able to directly and efficiently quench ROS and RNS, constitute
an important aspect of the body's antioxidant system. Measurement of
total antioxidant capacity (TAC) from all of these nonenzymatic
antioxidants becomes necessary and more important in many conditions
because of the difficulty in measuring all of them individually. Our
oxygen radical absorbance capacity (ORAC) assay (5,
12) is one of the tests recently developed to measure the
TAC of biological samples. The main advantage of the ORAC assay over
other similar methods is its use of a biologically and pathologically
important ROS and its application of an area-under-curve technique in
the quantitation process (6, 22). The
area-under-curve technique considers both inhibition time and
inhibition percentage of free radical action by an analyzed antioxidant
sample. The ORAC assay has been used by different laboratories
(1, 13, 17, 20,
21, 23, 26) and has provided
significant information regarding the antioxidant capacity of various
biological samples from pure compounds, such as melatonin, dopamine,
and flavonoids, to complex matrices, such as tea, fruits, vegetables,
herbs, and animal tissues (1, 4,
5, 9-11, 13,
17, 20, 21, 23,
24, 26). In this human study, we
found a significant postprandial increase in serum TAC by using the
ORAC assay and two other TAC assays. The results not only have their
own physiological implications but also help design a better controlled
animal or human study that measures serum or plasma antioxidant status.
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SUBJECTS AND METHODS |
Subjects and diets.
Eight healthy female subjects [age 66.9 ± 0.6 (SE) yr, body mass
index 26.1 ± 0.7 kg/m2] were recruited to
participate in this study. All study participants were in good health
as determined by a medical history questionnaire, physical examination,
and normal results from clinical laboratory tests. All of the subjects
fulfilled the following eligibility criteria: 1) no history
of cardiovascular, hepatic, gastrointestinal, or renal disease;
2) no alcoholism; 3) no antibiotic or
supplemental vitamin and/or mineral use for >4 wk before the start of
the study; and 4) no smoking. The study protocol was
approved by the Human Investigation Review Committee of Tufts
University and the New England Medical Center, and written informed
consent was obtained from each study participant.
Subjects were required to reside in the Metabolic Research Unit at the
Jean Mayer US Department of Agriculture Human Nutrition Research Center
on Aging at Tufts University for two 36-h periods (periods A
and B). During period A, eight subjects were
asked to come to the Metabolic Research Unit in the evening and fast overnight. In the morning, an intravenous catheter was inserted into
one forearm. A 10-ml fasting blood sample (the baseline zero time
sample) was obtained at about 8 AM, after which the subject was given a
breakfast drink (1,004 kJ; Table 1).
Blood samples (10 ml) were collected again at 0.25, 0.5, 1, 2, and
4 h after consumption of the breakfast drink. A lunch meal was
given (2,385 kJ; Table 1) immediately after the blood sampling at
4 h. Additional blood samples were obtained at 7, 9, 11, 13, 15, and 24 h after the initial blood sampling. A snack (1,063 kJ;
Table 1) was given immediately after the 7-h blood sampling. A dinner
(2,621 kJ; Table 1) was given immediately after the 11-h blood
sampling. The breakfast, lunch, snack, and dinner were designed to
contain as little as possible of known antioxidants (no significant
amounts of vitamin C, -tocopherol, carotenoids, and flavonoids) but
provide the recommended daily allowance for protein and energy (Table 1). Blood samples were collected more frequently after breakfast compared with after lunch or dinner because of the tests needed for
other treatments, which have been published (8). During period B, we were able to retest five of the eight subjects
to confirm that the postprandial change in serum TAC that we observed during period A was due to meals and not the
endocrinological or any other physiological factors exercised around a
meal time. Therefore, during period B, subjects were given a
dinner, but not a breakfast, lunch, or snack. The blood sampling
procedure and schedule were the same as those used in period
A.
Serum TAC analyses.
Three different methods were used for the serum TAC analyses. They were
the 1) ORAC assay, 2) trolox equivalent
antioxidant capacity (TEAC) assay, and 3) ferric reducing
ability/power (FRAP) assay.
Serum ORAC was determined by the automated method of Cao and co-workers
(5, 12) using serum deproteinized with 0.5 mol HClO4/l (1:1 vol/vol). Briefly, in the final assay
mixture (0.4 ml total volume), R-phycoerythrin (16.7 nM) was
used as a target of free radical attack, with
2,2'-azobis(2-amidinopropane) dihydrochloride (4 mM) as a peroxyl
radical generator. Trolox was used as a control standard. Final results
were calculated by using the differences of areas under the
R-phycoerythrin decay curves between the blank and a sample and are
expressed as micromoles of Trolox equivalents per liter.
Serum TEAC was measured by using the method of Miller and co-workers
(19) with commercially available kits (Total Antioxidant Status, lot 21440, Randox Laboratories, Lakewood, CA). This method for
measuring antioxidant activity is based on the inhibition by
antioxidants of the absorbance of the radical cations of
2,2'-azinobis(3-ethylbenzothiazoline 6-sulfonate) (ABTS) at 600 nm.
ABTS radical cations are formed by incubation of ABTS with metmyoglobin
and H2O2. The final results are expressed as
micromoles of Trolox equivalents per liter.
Serum FRAP was determined by the method of Benzie and Strain
(3). The FRAP assay measures the ferric-reducing ability
of plasma or serum. At low pH, when a ferric
(Fe3+)-tripyridyltriazine complex is reduced by
antioxidants to the ferrous (Fe2+) form, an intense blue
color with an absorption maximum at 593 nm develops. In the FRAP assay,
Fe2+ was used as a standard. The final results were
converted to micromoles of Trolox equivalents per liter. The relative
activity of Trolox in the FRAP assay was 2.0; i.e., the direct reaction
of Fe2+ gave a change in absorbance of one-half that of an
equivalent molar concentration for Trolox (3).
Determination of protein, uric acid, bilirubin, -tocopherol,
and vitamin C.
Protein, uric acid, and bilirubin were measured in serum by using a
Cobas Mira spectrophotometric centrifugal analyzer with reagent kits
purchased from Roche Diagnostic Systems (Branchburg, NJ).
-Tocopherol in serum was analyzed by reverse-phase HPLC (18) coupled to an ESA coulometric detection system (ESA,
Chelmsford, MA). Vitamin C was determined by HPLC analysis of plasma
deproteinized immediately after separation with 0.5 mol
HClO4/l (2).
Statistical analyses.
Postprandial responses in serum TAC, uric acid, -tocopherol,
bilirubin, and plasma vitamin C were evaluated by using a paired t-test (Systat). Linear regression analyses of the change in
serum TAC vs. the change in serum uric acid were computed by using MGLH in Systat for Windows. A linear fit adequately described the data as
assessed by the correlation coefficient.
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RESULTS |
Postprandial responses in serum TAC.
Fasting serum TAC before the consumption of breakfast during
period A and before breakfast time (no breakfast) during
period B are shown in Table 2.
The fasting ORAC and FRAP were significantly different between
period A and period B, indicating effects of season or daily life (diet, exercise) on the serum TAC. Besides being
expressed in micromoles per liter, serum TAC was also expressed in
nanomoles per milligram protein to correct for any possible effects
resulting from blood dilution. These subjects received normal saline
continuously through an intravenous catheter maintained in one forearm
for blood sampling. Also, the water intake was not restricted for these
subjects during both periods. The responses in serum ORAC, FRAP, and
TEAC after the initial blood sampling are shown in Figs.
1 and 2 for
both periods.
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Fig. 1.
Postprandial changes (means ± SE) in serum total
antioxidant capacity (TAC) measured as oxygen radical absorbance
capacity (ORAC), ferric reducing ability/power (FRAP), and Trolox
equivalent antioxidant capacity (TEAC) expressed in nanomoles per
milligram protein. PCA, serum treated with perchloric acid. Baseline
ORAC, FRAP, and TEAC data are presented in Table 2. During period
A, a breakfast drink was given at time 0 followed by
lunch, snack, and dinner at 4, 7, and 11 h, respectively. During
period B, only the dinner was given. Data are expressed in
nanomoles per milligram protein to correct for any possible effect
resulting from blood dilution. These subjects received normal saline
continuously through an intravenous catheter maintained in 1 forearm
for blood sampling. Also, water intake was not restricted for these
subjects during both periods. Significantly different
(P < 0.05) from time 0 for
* period A and # period B. Down
arrows indicate meal time (no breakfast and lunch were given during
period B).
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Fig. 2.
Postprandial changes in serum TAC measured as ORAC, FRAP,
and TEAC and expressed as micromoles per liter. Baseline ORAC, FRAP,
and TEAC data are presented in Table 2. * Significantly different
(P < 0.05) from time 0. See Fig. 1 legend
for additional details about the experiments.
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Apparently there were three peaks in the response of serum ORAC during
period A, one after breakfast, one after lunch (at 4 h), and one after dinner (at 11 h), although the increase in serum
ORAC after the breakfast meal was not statistically significant. The
increase in serum ORAC after the consumption of the lunch meal was
significant, and the increase lasted for 11 h during the period.
When expressed in nanomoles per milligram protein, serum ORAC (Fig. 1)
at 7, 9, 11, 13, or 15 h was significantly higher than that at
0 h; the percent increases were 19, 21, 13, 20, and 23%,
respectively. When expressed in micromoles per liter (Fig. 2), serum
ORAC at 9, 13, or 15 h was also significantly higher than that at
0 h; these percent increases were 17, 16, and 15%, respectively.
However, during period B, when no breakfast, lunch or snack
was given, serum ORAC did not increase significantly until after the
consumption of a dinner meal, which was given at 11 h. Serum ORAC,
expressed in nanomoles per milligram protein, was significantly higher
at 13 or 15 h than at 0 or 11 h during the period. When
expressed in micromoles per liter, serum ORAC showed a trend of
increasing after the dinner, but the increase was not statistically
significant due to the effect of blood dilution, which resulted from
normal saline infusion during the fasting period.
As seen with serum ORAC, there were also three peaks in the response of
serum FRAP during period A: one after breakfast, one after
lunch, and one after dinner. Serum FRAP increased significantly during
period A after the consumption of the lunch meal, and the increase lasted for 11 h. When expressed in nanomoles per
milligram protein (Fig. 1), serum FRAP at 7, 9, 11, 13, or 15 h
was significantly higher than that at 0 h, with percent increases
at 21, 12, 13, 18, and 21%, respectively. When expressed in micromoles
per liter (Fig. 2), serum FRAP at 7 and 13 h was significantly
higher than at 0 h, with percent increases at 12 and 12%,
respectively. During period B, in the absence of breakfast
and lunch, serum FRAP did not increase significantly until after the
consumption of the dinner meal. Serum FRAP, expressed in nanomoles per
milligram protein, was significantly higher at 13 or 15 h than at
0 h during the period.
Serum TEAC showed a similar postprandial response pattern as serum ORAC
and FRAP during both period A and period B when
it was expressed in nanomoles per milligram protein (Fig. 1). However, when expressed as micromoles per liter, serum TEAC showed no
significant postprandial response during either periods (Fig. 2).
Postprandial responses in blood individual antioxidants.
Fasting concentrations of serum uric acid, -tocopherol,
bilirubin, and plasma vitamin C before the consumption of the breakfast during period A and before the breakfast time (no breakfast)
during period B are shown in Table 2. There were no
significant differences in these parameters between period A
and period B (-tocopherol was not measured in
period B).
Responses in serum uric acid, bilirubin, -tocopherol, and plasma
vitamin C levels after the consumption of the breakfast (period
A) or breakfast time (period B) are shown in Figs.
3 and 4.
Among these blood antioxidants, only serum uric acid showed a
postprandial response, which was parallel to serum TAC measured as ORAC
or FRAP. There were two peaks in the response of serum uric acid during
period A, one after lunch and another after dinner, whether
it was expressed as micromoles per liter or nanomoles per milligram
protein. During period B, when no breakfast, lunch, or snack
was given, serum uric acid did not increase significantly until after
the consumption of the dinner meal. The postprandial change in serum
uric acid was linearly correlated with the change in serum ORAC or FRAP
(P < 0.001) (Fig. 5);
however, the correlation coefficients were relatively low.
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Fig. 3.
Postprandial changes in serum uric acid, plasma vitamin
C, -tocopherol, and bilirubin concentrations (nmol/mg protein).
Baseline uric acid, -tocopherol, bilirubin, and plasma vitamin C
concentrations are presented in Table 2. Significantly different
(P < 0.05) from time 0 for
* period A and # period B. See
Fig. 1 for additional details about the experiments.
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Fig. 4.
Postprandial changes in serum uric acid, plasma vitamin
C, -tocopherol, and bilirubin concentrations (µmol/l). Baseline
uric acid, -tocopherol, bilirubin, and plasma vitamin C
concentrations are presented in Table 2. Significantly different
(P < 0.05) from time 0 for
* period A and # period B. See
Fig. 1 for additional details about the experiments.
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Fig. 5.
Postprandial change in serum TAC (Y) as
measured by ORAC and FRAP as a function of postprandial changes in
serum uric acid concentration (X). Thick line, line of best
fit.
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During period A, serum bilirubin concentrations, when
expressed in nanomoles per milligram protein, decreased significantly after the lunch but not after the breakfast or dinner (Fig. 3). Serum
bilirubin also showed a continuous decrease after the initial sampling
when it was expressed in micromoles per liter during the period (Fig.
4). However, during period B, when no breakfast and lunch
were given, serum bilirubin showed a continuous increase until after
the consumption of the dinner meal (Figs. 3 and 4).
There were no significant changes in plasma vitamin C and serum
-tocopherol concentrations during period A. However,
during period B, plasma vitamin C showed a significant
increase after the dinner was consumed.
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DISCUSSION |
The present study showed a clear postprandial response in serum
TAC in older women. Serum TAC, which was measured by using different
analytic techniques (ORAC, FRAP, and TEAC), increased significantly
after the consumption of meals that were designed to contain
negligible antioxidants. The postprandial responses in serum ORAC,
FRAP, and TEAC were parallel to each other and gave two significant
peaks during period A: one seen 3-4 h after the lunch
and one seen 4 h after the dinner. It appeared that there was also
a peak after the breakfast, but the change was not statistically
significant. Serum TAC during period A remained elevated
above the basal level between the lunch and dinner. This could be a
result of the extended effect of the lunch but is more likely an effect
of the snack that was given between the lunch and dinner during
period A.
The postprandial increase in serum TAC observed in the human subjects
in this study was clearly a food-related observation. When the subjects
fasted for 23 h before a dinner was given during period
B, their serum TAC did not increase until after consumption of the
dinner. This postprandial increase in serum TAC indicates the
importance of controlling diets in clinical studies that involve the
measurement of antioxidant status. A measured increase in serum or
plasma antioxidant capacity after the consumption of a diet containing
antioxidants could be a general effect of food intake, not a specific
effect from the antioxidants contained in the diet. The increase in
serum antioxidant capacity after a meal could result from an increased
production of antioxidant amino acids from proteins contained in the
meal and/or from an increased internal antioxidant release into the
blood during the process of absorbing, storing, or metabolizing the
ingested nutrients. The FRAP assay used in this study does not measure
sulfhydryl-containing amino acids or peptides (3), but
serum FRAP showed a significant postprandial increase parallel to serum
ORAC, indicating that increased amino acid production after a meal was
not a primary mechanism underlying the postprandial increase in serum
antioxidant capacity.
Interestingly, the time course of the response in serum TAC was similar
to that of "the thermic effect of food," a well-known phenomenon
referring to the increase in oxygen consumption or energy expenditure
after the consumption of a meal. When one meal was fed to four male and
four female volunteers, LeBlanc and Soucy (15) observed a
gradual increase in oxygen consumption for up to 80 min; the value for
the increased oxygen consumption was still higher than 50% of the peak
value for increased oxygen consumption by 140 min. The thermic effect
of food (kJ/min) in young women after ingestion of meals was
energy-content dependent; the total food-induced thermogenesis values
were significantly higher in subjects with higher energy intakes
(25). The postprandial response in serum TAC appeared to
be also energy-content dependent. The response in serum TAC in the
older women during period A after breakfast (1,004 kJ) was
much weaker than that after lunch (2,385 kJ) or dinner (2,621 kJ). For
example, the maximum increase in serum ORAC (nmol/mg protein) during
period A after breakfast (1,004 kJ) was 6%, whereas those
after lunch and dinner were 21 and 23%, respectively.
Because oxygen consumption or energy expenditure increases after a meal
(the thermic effect of food), it would be reasonable to postulate a
food-induced increase in free radical (ROS and/or RNS) production from
the increased oxygen metabolism and thus a food-induced decrease in
serum antioxidant capacity (TAC). The amount of oxygen radicals derived
from oxygen is dependent on the amount of oxygen consumed. The more
oxygen consumed, the more oxygen radicals formed. Apparently, the human
body is protected against the potential damaging effects of the
postprandial increase in oxygen consumption or free radical production.
What we observed in this study is actually a postprandial or
"food-induced" increase in serum antioxidant capacity. This
food-induced increase in serum antioxidant capacity can be viewed as an
adaptive response to the food-induced oxidative stress. The adaptive
response in the antioxidant defense system to free radical production
in vivo has been demonstrated in calorie-restricted animals. Chronic
caloric restriction without essential nutrient deficiency is recognized as the most effective manipulation to extend the life span and retard
the aging process in laboratory rodents and other short-lived species.
Calorie restriction reduces both free radical production (16) and serum antioxidant capacity measured as ORAC
(7). The thermic effect of food, basal metabolic rate, and
total heat production of calorie-restricted animals were also
significantly lower than those for ad libitum-fed controls
(14).
In this study, uric acid was the only individual antioxidant found to
be responsible for part of the increased serum antioxidant capacity
after a meal. This postprandial increase in serum uric acid might have
critical physiological implications. Two evolutionary alterations have
led to high tissue concentrations of urate in humans: loss of
peroxisomal urate oxidase and active reabsorption of urate from the
kidneys. However, other physiological processes are also responsible
for the postprandial increase in serum TAC, because the contribution of
the increased serum uric acid to the increased serum ORAC (0-15 h)
was only ~29%.
The plasma vitamin C, when expressed in nanomoles per milligram
protein, increased significantly after the consumption of the dinner
given during period B. We do not have a clear explanation for it, because all the meals were designed to contain negligible antioxidants, which include vitamin C, although the consumption of a
vitamin C-containing beverage along with the dinner or after the dinner
by these fasted subjects cannot be excluded during the period. However,
the increased vitamin C level (after the dinner) could not fully
account for the increased serum TAC (after dinner) during period
B. During period A, plasma vitamin C remained unchanged, whereas postprandial increases in serum antioxidant capacity
were observed.
In conclusion, we observed in older healthy women a significant
postprandial increase in serum antioxidant capacity, which was partly
due to the food-related increase in serum uric acid concentration. This
postprandial increase in serum antioxidant capacity indicates an
adaptive physiological response in antioxidant defense systems.
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ACKNOWLEDGEMENTS |
Appreciation is expressed to Dr. R. Russell for serving as study
physician for this experiment; to Neil Lischner, John McEwen, and
Christine M. O'Brien for technical assistance; to Gayle Perrone and
the staff of the Nutrition Evaluation Laboratory for expertise in
performing many of the laboratory analyses; to Helen Rasmussen for
assistance in the formulation of the diets; and to the nursing staff of
the Metabolic Research Unit at the Human Nutrition Research Center for
assistance in the care of the subjects.
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FOOTNOTES |
Mention of a trade name, proprietary product, or specific equipment
does not constitute a guarantee by the US Department of Agriculture and
does not imply its approval to the exclusion of other products that may
be suitable.
Address for reprint requests and other correspondence: G. Cao,
USDA HNRCA at Tufts Univ., Rm. 712, 711 Washington St., Boston, MA
02111 (E-mail: gcao{at}hnrc.tufts.edu).
The costs of publication of this
article were defrayed in part by the
payment of page charges. The article
must therefore be hereby marked
"advertisement"
in accordance with 18 U.S.C. §1734 solely to indicate this fact.
Received 21 December 1999; accepted in final form 29 March 2000.
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J APPL PHYSIOL 89(3):877-883
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ABSTRACT
INTRODUCTION
