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Centre de Recherche en Nutrition Humaine d’Auvergne, Laboratoire Maladies Métaboliques et Micronutriments, INRA de Clermont-Ferrand/Theix, 63122 Saint Genès Champanelle, France * Laboratoire díhydrologie, Institut Louise Blanquet, Faculté de Pharmacie, BP 38, Clermont-Ferrand, France
2To whom correspondence and reprint requests should be addressed.
 |
ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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KEY WORDS: • red wine • ethanol • intestinal absorption • zinc • copper • stable isotopes • rats
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). Moreover, red wine
is rich in some essential minerals, in particular Fe (5–100 mg/L), Zn
and Cu. Several studies have clearly shown that red wine or other
polyphenol-rich products decrease Fe absorption substantially
(Brune et al. 1989
, Cook et al. 1995
,
Hurrell 1990
), whereas ethanol alone increases Fe
absorption and its concentration in liver (Fairweather-Tait et al.1988
). This inhibitory effect of PP seems to be due
to the chelation capacity of these compounds to metal ions
(Spencer et al. 1988
). The effect of red wine on Zn and
Cu absorption has received little attention, although the available
information suggests that PP can chelate these elements and may affect
their availability for absorption (Coudray et al. 1998
).
The stable isotope approach is now recognized to be an excellent tool
for mineral bioavailability studies (Aggett 1997
,
Coudray et al. 1997
, Sandstroem et al. 1993
, Turnlund 1989
). Our study was conducted to
assess the short- and long-term effects of red wine and ethanol
intake on intestinal absorption and status of Zn and Cu in rats, using
Zn and Cu stable isotopes. |
MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The red wine used in this work was Cabernet-Sauvignon, Arzens
origin, 1996, obtained from the Station expérimentale de pech
rouge, in the Institut National de la Recherche Agronomique (INRA) in
Montpellier, France. It is also largely marketed to and consumed by the
population. The alcohol concentration of this wine was 12.45%, total
acids were 3.7 g/L, sugars 1.7 g/L and pH 3.63. The total polyphenol
concentration measured by the Folin-Ciocalteu test was 2.1 g/L
(Scalbert et al. 1989
). Mineral levels determined in
this red wine were (mg/L) Ca, 59; Mg, 86; Zn, 1.10; Fe, 4.45; Cu, 0.30;
and Mn, 0.82.
Reagents and materials.
Enriched 67Zn (94.6%) and 65Cu (99.6%) isotopes, in the oxide form, were obtained from Euriso-top, (Saint Aubin, France). Ethanol 95%, suprapure HNO3, suprapure H2O2 and standard solutions (1 g/L) of Zn and Cu were obtained from Merck (Darmstadt, Germany). All other chemicals were of the highest quality available, and demineralized water was used throughout.
The isotope-ratio measurements were performed using an inductively coupled plasma/mass spectrometry (ICP/MS) instrument (a Plasmaquad II system from Fisons Instruments, Manchester, UK), equipped with a Meinhard nebulizer. Within- and between-run percentage residual SD were 0.65 and 1.11% for 67Zn and 66Zn, respectively, and 0.56 and 0.89% for 65Cu and 63Cu, respectively, on fecal mineralisate solutions. An atomic absorption spectrometer (Perkin Elmer, St-Quentin en Yvelines, France) was used for total Zn and Cu measurements. Urinary Cu was determined by electrothermal atomic absorption using a Hitachi 8270 spectrometer (Tokyo, Japan).
Stable isotope preparation.
The enriched zinc used in this study was 94.60% 67Zn. Enriched Zn (20 mg; 24.9 mg of ZnO) was moistened with 1 mL of demineralized water, and 1 mL of 12 mol/L HCl (suprapure) was added to transform the oxide into the soluble chloride of Zn. The solution was then diluted with 7.5 mL of demineralized water to give a concentration of 2 g 67Zn/L. The enriched copper used in the study was 99.61% 65Cu. Enriched Cu (70 mg; 88 mg of CuO) was moistened with 1 mL of demineralized water; 1 mL of 12 mol/L HCl was added and heated at 80°C for 2 h to transform the oxide into the soluble chloride of Cu. The solution was then diluted with 8 mL of demineralized water to give a concentration of 7 g 65Cu/L. The target isotope doses were 60 µg (923 nmol) of 65Cu and 130 µg (1940 nmol) of 67Zn for each rat. On the prepared isotope solution, we checked the concentration of total Zn and Cu by atomic absorption spectrometry and determined the actual isotope concentration by ICP/MS to calculate the actual dose of isotopes. The actual doses of 65Cu and 67Zn isotopes were 902 nmol 65Cu and 2027 nmol 67Zn.
Animals and diet.
Male Wistar rats weighing ~200 g were used. They were obtained from
the colony of laboratory animals of the Institut National de la
Recherche Agronomique (INRA of Clermont-Ferrand/Theix, France). The
rats were housed under conditions of constant temperature (20–22°C),
humidity (45–50%) and a standard dark cycle (2000–0800 h). The rats
received humane care in compliance with the guidelines formulated by
the European Community for the use of experimental animals
(L358–86/609/EEC). Rats initially underwent an adaptation period of
8 d with free access to a semipurified diet and demineralized
water. The diet used was that recommended by AIN (Reeves 1997
). Its composition is shown in Table 1
. Zinc and Cu levels were 44 and 6.6 mg/kg dry diet (672 and 101
µmol/kg) respectively. Semipurified powdered diet (100
g) was mixed with 100 mL of demineralized water to form a semiliquid
food prepared on site and offered daily at 1600 h.
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After an 8-d adaptation period to the semipurified diet and demineralized water, rats were assigned randomly to three groups (n = 16). They received the same diet and either demineralized water (control group), ethanol 6% (ethanol group) or red wine diluted by half in demineralized water (red wine group) as fluid. Thus, the alcohol concentration was similar in the ethanol and red wine beverages offered to rats. The rats consumed the semipurified diet and these beverages ad libitum for 3 d before isotope testing. One day before isotope administration, the rats were placed into individual metabolism cages, and 24-h fecal samples (nonlabeled samples) were collected from each animal. At 0800 h, the stable isotopes were diluted in 2 mL of the corresponding beverages and given by gastric gavage. The rats continued to consume their diet and respective beverages for three additional days. Feces and urine were then collected quantitatively for the 3 d after isotope administration and pooled for analysis by atomic absorption and mass spectrometry.
Long-term study.
In the long-term study, the above experimental protocol was repeated, except that the rats were fed their diets and respective beverages for 4 wk before the stable isotope test. Furthermore, in this long-term study, blood, liver and tibia were sampled to assess Zn and Cu status.
Sample treatment and analysis.
Individual feces collected before and after isotope administration were freeze-dried, powdered and subsamples (0.25 g) were ashed at 500°C for 10 h. The ashes were dissolved in 0.2 mL of 14 mol/L HNO3 and heated for 2 h at 100°C on a hot plate, diluted adequately with 0.14 mol/L HNO3 and analyzed for Zn and Cu isotope ratios by ICP/MS, using Zn and Cu solutions as external standards and indium as internal standard. The concentration of Cu and Zn in final solutions of feces mineralisates for ICP/MS measurements was ~200 and 40 µg/L, respectively. Total Zn and Cu were determined by flame atomic absorption spectrometry (Perkin Elmer 560, Saint Quentin en Yvelines, France), at 213.8 and 324.7 nm, respectively.
The mass spectrometer settings and plasma conditions for the ICP/MS instrument were optimized with a solution of 10 µg/L indium. The instrument operating conditions were as follows: radio frequency generator, 27.12 MHz; forward RF power, 1350 W; reflected RF power, <3 W; outer argon flow rate, 14 L/min; intermediate argon flow rate, 0.7 L/min; nebulizer argon flow rate, 0.76 L/min; mass resolution, 0.9 amu at 10% of peak height. Sample uptake rate was 0.6 mL/min.
Plasma Zn and Cu levels were determined by flame atomic absorption spectrometry (Perkin Elmer 560) after adequate dilution. Urinary Zn was determined by flame atomic absorption spectrometry after a 20% dilution in 0.1 mol/L HCl. Urinary Cu was determined by electrothermal atomic absorption without dilution.
Zn and Cu levels were also determined in liver and tibia after dry-ashing followed by wet ashing. The mineralisate was then adjusted to 5 mL with HNO3 (0.14 mol/L) and diluted adequately for atomic absorption spectrometry measurement. Seronorm trace element serum and urine (Oslo, Norway) were used as precision and accuracy internal quality controls.
Erythrocyte superoxide dismutase, as a Cu biomarker, was measured
according to Marklund’s technique (Marklund and Marklund 1974
). Alkaline phosphatase, as a Zn biomarker, was measured by
a commercial kit (Bohringer, Meylan, France) on an Hitachi
automate analyzer.
Calculations.
Isotopic percentage of enrichment for 67Zn or 65Cu in feces was obtained from the following equation: enrichment = 100 x [(measured IR - baseline IR)/(baseline IR)], given that baseline isotopic ratios (IR) are obtained by the instrument for samples before isotope administration.
Total fecal unabsorbed isotopes were then determined as previously
described (Coudray et al. 1998
): total 67Zn*
or 65Cu* coming from only the administered isotope = [total fecal mineral x (M IR - B IR)]/[Y
+ (M IR - B IR)], where M IR is measured isotope ratio and B IR
is baseline isotope ratio. IR is 67Zn/66Zn for
Zn and 65Cu/63Cu for Cu. Y is
3.584 for Zn, the reciprocal of 0.279 to convert 66Zn
quantity to total Zn, and Y is 1.4451 for Cu, the
reciprocal of 0.692 to convert 63Cu quantity to total Cu.
Total fecal Zn or Cu (mmol) is determined by atomic absorption
spectrometry. 67Zn or 65Cu apparent absorption
was calculated from the following formula: absorption = 100
x [(administered isotope - isotope excreted in the
feces)/(administered isotope)]. Endogenous excretion of Zn and Cu was
calculated as follows: endogenous excretion (µg/d)
= mineral excretion in the feces (µg/d) - nonabsorbed mineral (µg/d).
Statistical analysis.
Standard procedures were used to calculate means and (SEM). Results from experimental groups were compared by ANOVA using Instat software (GraphPad Software, San Diego, CA). ANOVA was followed by the Student-Newman-Keuls-test. Differences between groups were considered significant when P < 0.05.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Analysis of the 3-d fecal pools showed an isotopic enrichment of 170%
for 67Zn and 66% for 65Cu
in the control group. Such large isotopic enrichments guarantee highly
reliable isotope ratio measurements by the ICP/MS instrument used in
this study. Intestinal absorption of 67Zn and
65Cu in the short-term study, calculated on
the basis of the 3-d fecal pool, is shown in Table 2
. The short-term intake of either red wine or ethanol did not affect
67Zn or 65Cu absorption in
rats in this study. Moreover, urinary excretion of Zn and Cu did not
differ among the three experimental groups. Because of the short period
of red wine and ethanol intake in this study, blood and tissue
concentrations of Zn and Cu were not determined.
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Food intake was significantly less in the experimental groups (red wine
and ethanol) compared with the control group (Table 3
). Moreover, the consumption of red wine was significantly less than
that of other beverages. The red wine contained Zn and Cu, but its
contribution to the Zn and Cu intakes was negligible (~5%). Body
weight gain was not affected by red wine or ethanol consumption (Table 3)
. Intestinal absorption of 67Zn and
65Cu, calculated on the basis of the 3-d fecal
pool, is shown in Table 4
. Long-term consumption of red wine did not modify intestinal
absorption of Zn or Cu in rats. Long-term ethanol intake increased
significantly 67Zn and 65Cu
apparent absorption in rats in this study. However, endogenous
excretion of both Zn and Cu did not differ significantly in the three
groups. Zn and Cu urinary excretions also did not differ (Table 4)
.
Blood and tissue Zn and Cu concentrations and indices (plasma Zn,
plasma alkaline phosphatase, red blood cell Zn, liver Zn and tibia Zn,
plasma Cu, red blood cell Cu, red blood cell superoxide dismutase,
liver Cu and tibia Cu) were not significantly altered by red wine or
ethanol intake (data not shown).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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) and humans
(Bezwoda et al. 1985
, Cook et al. 1995
,
Duane et al. 1992
, Hurrell 1990
,
Tuntawiroon et al. 1991
) and of other
polyphenol-rich products on Fe absorption and status in animals
(Brown et al. 1990
, Garcia-Lopez et al. 1990
, Greger and Lyle 1988
, Morck et al. 1983
, Record et al. 1996
, Rossowska et al. 1997
). However, only few studies examined the effects of
either red wine or ethanol (Dinsmore et al. 1985a
and
1985b
, Fairweather-Tait et al. 1988
,
McDonald and Margen 1980
), or other polyphenol-rich
products (Ganji and Kies 1994
, Greger and Lyle 1988
, Record et al. 1996
, Rossowska and Nakamoto 1990
, Rossowska et al. 1997
) on Zn or
Cu absorption and status in animals and humans. The goal of this work
was to provide information on the short- and long-term effects of
both red wine and ethanol on Zn and Cu absorption and status in rats
using stable isotopes of Zn and Cu.
Our findings from the short-term study show clearly that neither
red wine nor ethanol consumption affected Zn or Cu intestinal
absorption in rats. The results of the long-term study show that
the consumption of red wine for 4 wk did not affect intestinal
absorption of Zn and Cu compared with the control group. Moreover, the
endogenous excretion of Zn and Cu and their blood status were not
altered by consumption of red wine. However, long-term consumption
of ethanol was accompanied by a significant increase in both Zn and Cu
absorption. Endogenous excretion of Zn and Cu was not significantly
different among the experimental groups although it tended to be
greater (P = 0.0925 and 0.0531, respectively)
in the ethanol group. An enhancing effect of ethanol on Zn and Cu
absorption may be explained in the following ways: 1)
ethanol may damage the intestinal cells and increase the space between
the cells where paracellular passive absorption may increase
(Crissinger et al. 1990
, Persson et al. 1990
); 2) ethanol affects Zn metabolism and
conservation by increasing its urinary excretion, which may be
responsible for a Zn depletion, which in turn may increase intestinal
absorption of Zn (McDonald and Margen 1980
,
Zarski et al. 1985
); 3) ethanol affects Cu
metabolism and conservation by increasing its accumulation in the liver
(Fields et al. 1995
). In all of these cases, the effect
of ethanol on Zn or Cu is not a short-term but rather a
long-term effect.
The absence of an effect of red wine on Zn and Cu absorption may be due
to the antagonist actions of polyphenols and ethanol. Indeed, it is
possible that the increased intestinal absorption of Zn and Cu due to
ethanol was counterbalanced by an inhibitory action of polyphenols on
Zn and Cu absorption. Indeed, red wine polyphenols may protect the
intestinal mucosa from the effects of ethanol. Polyphenols may also
chelate Zn and Cu and reduce their passive transport across the altered
mucosa. In a previous study, we showed that phenolic acids may decrease
intestinal absorption of Zn without affecting that of Cu in rats
(Coudray et al. 1998
).
In the short-term study, neither beverage altered Zn or Cu urinary
excretion. Body Zn and Cu levels (mineral status) were not determined
because we did not expect significant modifications in mineral status
after such a short period of red wine or ethanol intake. In the
long-term study, 4 wk consumption of red wine or ethanol did not
significantly alter urinary excretion of Zn or Cu. Moreover, plasma,
red blood cell, liver and tibia levels of these minerals and their
biological biomarkers were unaffected. It may should not be surprising
that increased intestinal absorption of Zn or Cu in the ethanol group
was not accompanied by significant modification in their body levels.
Zn and Cu homeostasis is well controlled, and remains constant over a
wide range of dietary intakes for a limited interval
(Kirchgessner 1993
). In an unpublished study, we
observed that the tissue levels of these minerals did not differ
between rats fed a diet containing 33% Zn and Cu for 4 wk and a
control group. Indeed, the endogenous excretion of Zn or Cu in the
feces is highly regulated in relation to dietary intake. Only very low
or very high dietary intakes for long periods cause the regulatory
mechanisms to become overloaded, resulting either in a depletion or an
accumulation of the element in the body. Therefore, it would be
interesting to study the effects of red wine and ethanol on Zn and Cu
intestinal absorption and status over a longer time period.
Few data exist in the literature on the effect of red wine on Zn or Cu
absorption in rats or humans. McDonald and Margen (1980)
reported increased absorption and possibly decreased endogenous
secretion of Zn during wine or de-ethanolized wine consumption
compared with ethanol or demineralized water consumption in humans. To
our knowledge, our study is the only one to evaluate the effect of red
wine on Zn and Cu absorption in rats. Studies on the effects of ethanol
on Zn and Cu absorption are also very scarce. We were unable to find
any study on the effect of ethanol on Zn absorption in animals; a few
studies in humans exist, with discordant results. McDonald and Margen (1980)
reported a nonsignificant, decreased absorption
of Zn during an ethanol consumption period compared with demineralized
water in six healthy men. Dinsmore et al. (1985a)
, using
a dual isotope absorption technique, reported a lower absorption of Zn
(P < 0.001) in alcoholic patients than in a normal
control group. In another study, Dinsmore et al. (1985b)
, reported a lower postprandial serum Zn in alcoholics
compared with normal subjects. However, when Zn was given in a single
dose to normal subjects, ethanol increased the serum Zn and therefore
appeared to increase the intestinal absorption of Zn (Dinsmore et al. 1985c
). The findings of these studies are thus
discordant and the exact effect of ethanol on Zn absorption is not
clear.
One study exists on the effect of ethanol on Cu absorption in rats; in
that study, Klevay and Moore (1990)
observed that rats
drinking beer had higher Cu absorption and higher liver Cu than the
control rats. This result agrees with ours and is compatible with the
hypothesis that long-term consumption of ethanol may damage the
intestinal cells and increase the paracellular passive absorption of
minerals.
In this work, many precautions were taken to produce valid data.
First, it is known that previous meals and beverages may influence the
effect of the studied compound (diet or beverage) on mineral absorption
(Garcia-Lopez et al. 1990
). Therefore, in the
short-term study, experimental beverages were given to the rats for
3 d before stable isotope tests. Second, beverages with a higher
concentration of alcohol may not be readily consumed by the animals.
Therefore, the red wine was diluted by half in demineralized water to
reduce the alcohol concentration to a level acceptable for rats.
Finally, to produce conclusive results, we used a large number of rats
in each group (n = 16). Such a high number is necessary
to attenuate the interindividual variability in each group. Classical
experiments in the literature have been conducted on 6–10 animals per
group.
In conclusion, short-term intake of red wine or ethanol did not alter intestinal absorption or urinary excretion of Zn and Cu in rats. Long-term consumption of ethanol, but not of red wine, increased significantly the intestinal absorption of both Zn and Cu. The absence of an effect of red wine intake on Zn and Cu intestinal absorption may be due to possible antagonist actions of both components of red wine, i.e., polyphenols and ethanol. Further studies are necessary to understand the respective effects of red wine components on the absorption of Zn and Cu.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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3 Abbreviations used: ICP/MS, inductively coupled
plasma/mass spectrometry; IR, isotopic ratio; PP, polyphenols.
Manuscript received October 19, 1999. Initial review completed November 9, 1999. Revision accepted January 26, 2000.
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