Original Article

High Blood Alcohol Levels in Women — The Role of Decreased Gastric Alcohol Dehydrogenase Activity and First-Pass Metabolism

Mario Frezza, M.D., Carlo di Padova, M.D., Gabriele Pozzato, M.D., Maddalena Terpin, M.D., Enrique Baraona, M.D., and Charles S. Lieber, M.D.

N Engl J Med 1990; 322:95-99January 11, 1990

Abstract

Abstract

After consuming comparable amounts of ethanol, women have higher blood ethanol concentrations than men, even with allowance for differences in size, and are more susceptible to alcoholic liver disease. Recently, we documented significant "first-pass metabolism" of ethanol due to its oxidation by gastric tissue. We report a study of the possible contribution of this metabolism to the sex-related difference in blood alcohol concentrations in 20 men and 23 women. Six in each group were alcoholics.

The first-pass metabolism was determined on the basis of the difference in areas under the curves of blood alcohol concentrations after intravenous and oral administration of ethanol (0.3 g per kilogram of body weight). Alcohol dehydrogenase activity was also measured in endoscopic gastric biopsies. In nonalcoholic subjects, the first-pass metabolism and gastric alcohol dehydrogenase activity of the women were 23 and 59 percent, respectively, of those in the men, and there was a significant correlation (r_s = 0.659) between first-pass metabolism and gastric mucosal alcohol dehydrogenase activity. In the alcoholic men, the first-pass metabolism and gastric alcohol dehydrogenase activity were about half those in the nonalcoholic men; in the alcoholic women, the gastric mucosal alcohol dehydrogenase activity was even lower than in the alcoholic men, and first-pass metabolism was virtually abolished.

We conclude that the increased bioavailability of ethanol resulting from decreased gastric oxidation of ethanol may contribute to the enhanced vulnerability of women to acute and chronic complications of alcoholism. (N Engl J Med 1990; 322:95–9.)

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Media in This Article

Figure 1Effects of Sex and Chronic Alcohol Abuse on Blood Ethanol Concentrations.

Figure 2Correlation between the Magnitude of the First-Pass Metabolism of Ethanol and the Activity of Gastric Alcohol Dehydrogenase.

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Article

THE liver is the chief site of ethanol metabolism, but other tissues may contribute to ethanol metabolism as well. In particular, local metabolism of ethanol in gastrointestinal tissue has been reported,1 , 2 but its extent was believed to be negligible.3 , 4 Recently, however, Julkunen et al.5 found that in rats a substantial fraction of orally administered ethanol did not enter the systemic circulation but was oxidized mainly by the gastric mucosa, which contains alcohol dehydrogenase. This "first-pass metabolism" of ethanol has also been found to be substantial in men and to decrease with long-term ethanol consumption.6 Furthermore, recent studies of the intraduodenal administration of ethanol or of patients who have undergone gastrectomy7 have indicated that the first-pass metabolism in human subjects is also due to the gastric oxidation of ethanol. Thus, variations in the capacity of the gastric mucosa to metabolize ethanol could be a determinant of its bioavailability and toxicity.8

Alcoholic liver disease develops more readily in women than in men.9 10 11 12 13 Women also have higher blood ethanol concentrations than men after an equivalent oral dose.14 This difference has been attributed to a smaller volume of distribution of ethanol because of a lower water content in the body in women than in men,15 although after intravenous administration blood ethanol concentrations in women and men are similar.16 An alternative explanation for the sex-related differences in blood concentrations of ethanol after its ingestion could be differences in the capacity of the stomach to oxidize ethanol. We undertook this study to investigate possible sex-related differences in the gastric oxidation of ethanol and to determine how such oxidation might be affected by long-term consumption of ethanol.

Methods

Subjects

Seventeen nonalcoholic women 22 to 48 years old, 14 nonalcoholic men 26 to 53 years old, 6 alcoholic women 17 to 52 years old, and 6 alcoholic men 45 to 61 years old gave informed consent for this investigation, which was approved by the ethics committees of the University of Trieste and the Bronx Veterans Affairs Medical Center. The numbers of subjects participating in the two parts of the study are shown in Table 1Table 1Distribution of the Study Subjects According to the Type of Study Performed.. All the subjects were Italians.

Although the pharmacokinetics of ethanol are similar throughout the menstrual cycle,15 all premenopausal women were studied in the second half of the menstrual cycle. To avoid any hormonal interference with the metabolism of ethanol, none took birth-control pills during the preceding three months.17 The alcoholic subjects had no signs of overt malnutrition, ascites, esophageal varices, or hepatic encephalopathy. Liver biopsies performed in two men and one woman revealed fatty liver tissue in all three subjects and some fibrosis in the woman. After the study, the alcoholic subjects entered an alcoholism-rehabilitation program.

Pharmacokinetic Studies

On consecutive days the subjects received doses of ethanol (0.3 g per kilogram of body weight) orally and intravenously, in a randomized sequence. In the subjects who had gastric biopsies, the pharmacokinetic studies were performed 48 hours or more afterward. Ethanol was given in an isotonic solution of dextrose (5 g per deciliter) one hour after a standard breakfast — two eggs, two slices of bacon, two pieces of buttered toast, two cups of coffee, and 120 ml of orange juice — to exclude the effects of fasting on the first-pass metabolism of ethanol.6 The subjects were asked to drink the ethanol within 10 minutes. The intravenous infusions of ethanol lasted 20 minutes, a time that was chosen so that peak blood alcohol concentrations would be attained in both groups at approximately the same time after the start of the administration of ethanol.6

Before ethanol administration and at various times afterward (Fig. 1Figure 1Effects of Sex and Chronic Alcohol Abuse on Blood Ethanol Concentrations.), heparin-treated blood samples were collected through an indwelling venous catheter for the measurement of ethanol concentrations as reported elsewhere.6 The area under the curve (AUC) of the blood ethanol concentration was calculated by the trapezoidal method of integration from the start of ethanol administration to the time at which alcohol was no longer detectable in the blood.18 The magnitude of first-pass metabolism was calculated as the difference between the AUC after intravenous administration and that after oral intake.6 The rate of elimination of ethanol and the volume of distribution were calculated from the blood ethanol concentrations after intravenous administration. The rate of elimination of ethanol was calculated by dividing the dose by the time needed for elimination, as defined by extrapolation of the linear part of the decreasing curve to the abscissa. The volume of distribution was calculated by dividing the dose by the concentration at zero time; the latter was calculated by extrapolation of the linear part of the decreasing curve to the ordinate.

Gastric Alcohol Dehydrogenase

The kinetics of gastric alcohol dehydrogenase activity was determined first in specimens of gastric antral mucosa obtained from two men (47 and 53 years old) at the time of surgery for peptic ulcer disease. The mucosal specimens were weighed and homogenized in 1.15 percent potassium chloride (10 ml per gram of tissue). After centrifugation at 10,000 ×g, the supernatants were centrifuged at 100,000 ×g at 4°C for 60 minutes to obtain the cytosol. Cytosolic alcohol dehydrogenase activity was determined by measuring the reduction of 2.4 mmol of NAD per liter19 to NADH at 22°C in 0.1 M phosphate or glycine buffer, to achieve a pH between 7.0 and 10.6. Concentrations of 30, 200, 500, and 1000 mmol of ethanol per liter were used with and without 0.1 to 20 mmol of pyrazole per liter, an inhibitor of hepatic alcohol dehydrogenase. Values for K_m and K_i (Michaelis constant and inhibition constant) were determined by Lineweaver—Burk and Dixon plots, respectively,20 with a computerized data-analysis program.21

Biopsy specimens (mean weight, 6.1 mg; range, 4 to 10) were taken by endoscopy from apparently normal areas of the gastric antrum. The endoscopy was carried out with an Olympus panendoscope after premedication with diazepam and atropine. The medical indications for the biopsies were dyspeptic symptoms, and the procedure was carried out in all but three women and three men. Gastric alcohol dehydrogenase activity was measured in duplicate specimens at pH 9.6, with use of 500 mmol of ethanol and 2.4 mmol of NAD per liter as substrates. The activity was expressed as micromoles of reduced NAD per minute per gram of tissue or as nanomoles of NADH per minute per milligram of cytosolic protein.22

Statistical Analysis

The statistical significance of the differences in alcohol dehydrogenase activity and first-pass metabolism was assessed by computer-assisted23 two-way analysis of variance for unequal replications, with alcohol consumption and sex as the two factors. The correlation between these two factors was analyzed by the Spearman nonparametric method. Comparisons between individual groups were assessed by the Newman—Keuls test. Differences between the effects of the route of alcohol administration in the same subjects were assessed by a two-tailed, paired Student's t-test.24 P values under 0.05 were considered to indicate statistical significance.

Results

Subject Distribution and Alcohol Consumption

Most of the subjects entered the study after undergoing medically indicated endoscopic biopsies, none of which showed any lesions. In a majority of the subjects, both gastric alcohol dehydrogenase activity and first-pass metabolism of ethanol were measured (Table 1). A few did not volunteer for the pharmacokinetic studies, and therefore additional subjects were recruited.

The nonalcoholic subjects reported only occasional consumption of alcohol — less than 70 g per week —in the four weeks before the pharmacokinetic studies, and the rate of consumption was similar in both men and women. The alcoholic subjects reported heavy drinking — more than 120 g per day of ethanol in the men and more than 100 g per day in the women — for at least six months, until two days before the endoscopy and four days before the pharmacokinetic studies. Most of the alcoholic subjects had abnormal results on biochemical and hematologic tests indicative of chronic alcohol consumption, such as assays of serum gamma-glutamyltransferase and aspartate aminotransferase levels as well as of mean corpuscular volume (Table 2Table 2Clinical Laboratory Data on the Study Subjects.*).

First-Pass Metabolism of Ethanol

In both the nonalcoholic and the alcoholic groups, women had higher blood ethanol concentrations than men after ingesting an equivalent dose of ethanol (Fig. 1). By contrast, no significant sex-related differences were found when ethanol was administered intravenously.

In the nonalcoholic subjects (Table 3Table 3Comparison of the Areas under the Curve of Blood Ethanol Concentration after Oral (AUC_po) or Intravenous (AUC_iv) Administration of Ethanol, According to Sex and Chronic Alcohol Abuse.*), the mean AUC of the blood ethanol concentrations after oral ingestion was significantly larger in the women than in the men (P<0.01). By contrast, the mean AUC values after intravenous administration were similar in the two nonalcoholic groups. In the women, the mean difference between the intravenous and the oral AUC values (first-pass metabolism) was not significant (1.2 mmol per liter · hour), whereas in the men it was 5.2 mmol per liter · hour (P<0.01). The difference in first-pass metabolism between the sexes was also significant (P<0.01). In the alcoholic subjects, the mean AUC value in the men was significantly larger after intravenous than after oral administration (P<0.05), but the first-pass metabolism was half that in the nonalcoholic men. In the alcoholic women, the mean AUC values after intravenous and oral administration of ethanol were almost identical. Thus, first-pass metabolism in the alcoholic women was significantly lower than that in the alcoholic men (P<0.01), which in turn was significantly lower than that in the nonalcoholic men. Thus, both factors, sex and alcoholism, had significant effects on the first-pass metabolism of ethanol.

In the nonalcoholic subjects, the mean (±SE) rates of ethanol elimination were similar in the men (2.04±0.11 mmol [93.7±5.0 mg] per kilogram per hour) and women (1.98±0.13 mmol [90.9±6 mg] per kilogram per hour). The apparent volume of distribution, calculated from the intravenous curves, was 12 percent larger in the men than in the women (767±4 ml per kilogram in the men and 686±6 in the women; P<0.05). This sex-related difference in the volume of distribution for ethanol tended to persist in the alcoholic subjects (717±48 ml per kilogram in the men vs. 653±59 in the women), but the difference was not significant. As expected, the rates of elimination of ethanol were higher in the alcoholic subjects, but there were no differences between men (2.76±0.07 mmol [126.9±3.4 mg] per kilogram per hour) and women (2.62±0.36 mmol [120.4±16.9 mg] per kilogram per hour).

Gastric Alcohol Dehydrogenase Activity

In the two surgical antral-biopsy specimens, alcohol dehydrogenase activity was optimal, at pH 9.6. It continued to increase at ethanol concentrations above 500 mmol per liter, with apparent K_m values for ethanol of 662 and 374 mmol per liter and K_i values for pyrazole of 1.7 and 5 mmol per liter, respectively, in the two biopsies.

When 500 mmol of ethanol per liter was used (a concentration likely to occur in the stomach during drinking), both sex and alcoholism had significant effects on the alcohol dehydrogenase activity of the endoscopic-biopsy samples from the gastric antrum of the study subjects (Table 4Table 4Effect of Sex and Chronic Alcohol Abuse on the Alcohol Dehydrogenase Activity of the Gastric Antral Mucosa.*). Gastric alcohol dehydrogenase activities were 70 to 80 percent higher in the nonalcoholic men than in the nonalcoholic women. As compared with the values in the nonalcoholic men and women, respectively, chronic alcohol abuse was associated with a reduction of 37 to 46 percent in gastric alcohol dehydrogenase activity in men and a decrease of 11 to 20 percent in women. The results were similar whether the activity was expressed in grams of tissue or milligrams of cytosolic proteins.

Gastric alcohol dehydrogenase activities correlated significantly with the magnitude of the first-pass metabolism (Fig. 2Figure 2Correlation between the Magnitude of the First-Pass Metabolism of Ethanol and the Activity of Gastric Alcohol Dehydrogenase.).

Discussion

These results indicate that the bioavailability of ethanol is much greater in women than in men, because women have less gastric first-pass metabolism of ethanol. This was associated with less gastric alcohol dehydrogenase activity in the women. Moreover, alcoholism was associated with a further decrease in gastric alcohol dehydrogenase activity; the first-pass metabolism was virtually abolished in the alcoholic women.

These observations on the influence of the route of alcohol administration clarify many of the contradictions between previous studies of sex-related differences in blood ethanol concentrations.14 15 16 17 Differences in volume of distribution were previously invoked to explain the sex-related differences. However, neither we nor Arthur et al.16 found significant differences in blood levels, AUC values, or rates of elimination of ethanol between men and women after the intravenous administration of ethanol, even though we confirmed that the volume of ethanol distribution is lower in women. Thus, an additional mechanism must explain the large sex-related differences in blood ethanol concentrations after oral administration. Indeed, when we gave ethanol orally, our results were consistent with those of Marshall et al.15: the AUC values were greater in the women than in the men, and the volume of distribution was markedly decreased in the women when this value was calculated with the assumption that the entire dose of ethanol reached the systemic circulation. However, the volume of distribution for ethanol should be independent of the route of administration. Since we found a much smaller sex-related difference in the volume of distribution after intravenous than after oral administration, a more likely explanation for these results is that the differences in volume of distribution were overestimated, because only a fraction of the dose of ethanol ingested reaches the systemic circulation; we found that this fraction was higher in the women.

In men, the difference in AUC values after the intravenous and oral administration of ethanol was not due to the retention of ethanol in the stomach7 but to first-pass metabolism, as suggested by the earlier appearance of ethanol metabolites after oral than after intravenous ethanol administration.6 This first-pass metabolism did not occur after the intraduodenal administration of ethanol or in patients who had undergone gastrectomy,7 indicating that in humans, as in rats,8 gastric rather than hepatic oxidation of ethanol is the primary mechanism for this apparent first-pass effect. The extent of first-pass metabolism may be determined in part by variations in the rate of gastric emptying, thereby varying the time of exposure of ethanol to gastric oxidative activity. The sex-related differences in first-pass metabolism were clearly associated with differences in the ethanol-oxidizing activity of the gastric mucosa. In fact, a significant correlation was found between the magnitude of the first-pass metabolism and gastric alcohol dehydrogenase activity (Fig. 2).

Gastric alcohol dehydrogenase activity was measured in endoscopic gastric biopsy specimens at 500 mmol of ethanol per liter (2.3 g per deciliter), a concentration in the range of that reported to occur in the stomach after drinking.25 Although a gastric alcohol dehydrogenase isoenzyme with a high K_m for ethanol and a high K_i for pyrazole has been well documented in rats26 , 27 and baboons,28 it has not been found in humans at autopsy.29 However, in two surgical biopsies of the gastric antrum, we found one or more alcohol dehydrogenase isoenzymes with a high K_m for ethanol, as judged by the progressive increase in activity with increasing concentrations of ethanol, to levels much higher than those known to saturate alcohol dehydrogenase isoenzymes with a low K_m; there was also a high K_i for pyrazole, reminiscent of the alcohol dehydrogenase isoenzymes with a high K_m.27 The high K_m for ethanol and the high K_i for pyrazole of the human gastric mucosa are intermediate between those reported for the Class II (or pi) and Class III (or chi) liver alcohol dehydrogenase isoenzymes. This activity may contribute significantly to the overall metabolism of ethanol. Although in vitro findings should be extrapolated with caution to in vivo events, the mean level of activity found in nonalcoholic men at 500 mmol of ethanol per liter (2.64 μmol per minute per gram of mucosa) could account for the oxidation of at least 20 percent of the administered dose by 200 g of mucosa in three hours. Further evidence for the participation of this activity in the human first-pass effect has recently been obtained by Caballería et al.,30 who found that cimetidine — a noncompetitive inhibitor of the gastric alcohol dehydrogenase activity — decreases the first-pass metabolism of ethanol in both men and rats.

The oxidation of ethanol in the stomach decreases its systemic bioavailability, and sex-related differences in this process explain at least partly the sex-related differences in blood levels achieved after the ingestion of ethanol. These differences should be considered in the definition of safe levels of drinking for men and women driving motor vehicles or engaging in other activities requiring a high degree of attention or coordination.31 Moreover, the ingestion of equivalent doses of ethanol per kilogram of body weight can be expected to result in higher levels of ethanol in women than in men, not only in the systemic but especially in the portal circulation. Thus, in addition to the smaller volume of ethanol distribution, the decrease in first-pass metabolism and gastric oxidation of ethanol may contribute to the higher vulnerability to hepatic injury of women as compared with men who consume similar amounts of ethanol.9 10 11 12 13 Furthermore, one might expect that the greater bioavailability of ethanol in women would be exaggerated by other factors known to decrease the rate of gastric oxidation of ethanol, such as fasting or prolonged alcohol abuse.6

Supported by a grant (AA 03508) from the Department of Health and Human Services and the Department of Veterans Affairs.

Source Information

From the Institute of Medical Pathology, University School of Medicine, Trieste, Italy (M.F., G.P., M.T.); and the Alcohol Research and Treatment Center, Veterans Affairs Medical Center, Bronx, N.Y., and the Mount Sinai School of Medicine, New York (C.d.P., E.B., C.S.L.). Address reprint requests to Dr. Lieber at the Alcohol Research and Treatment Center, Veterans Affairs Medical Center, 130 W. Kingsbridge Rd., Bronx, NY 10468.

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