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Article

A High Oat-Bran Intake Does Not Impair Zinc Absorption in Humans When Added to a Low-Fiber Animal Protein-Based Diet¹

Brittmarie Sandström^*2, Susanne Bügel^*, Brian A. McGaw, John Price^** and Martin D. Reid^**

^* Research Department of Human Nutrition, The Royal Veterinary and Agricultural University, Rolighedsvej 30, DK-1958 Frederiksberg C, Denmark; School of Applied Sciences, The Robert Gordon University, St. Andrew St., Aberdeen, AB25 1HG, Scotland, United Kingdom; and ^** The Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen, AB2 9SB Scotland, United Kingdom.

²To whom correspondence should be addressed.

	ABSTRACT

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Oat bran has a high phytate content and a low or inactivated phytase activity. A high intake of oat bran could therefore result in an impaired absorption of trace elements. The effect of a mean daily intake of 142 g of oat bran (102 g/10 MJ) on absorption of zinc was evaluated by the use of stable isotopes and fecal monitoring in 12 healthy subjects (6 males and 6 females). Each subject participated in two separate diet periods each of 21 d with identical low-fiber diets and with oat bran added in one of the periods. The oat bran was incorporated into bread and served at three daily main meals. The intake of zinc and phytate per 10 MJ was 138 µmol (9.0 mg) and 0.5 mmol, respectively, in the low-fiber period and 225 µmol (14.7 mg) and 4.0 mmol, respectively, in the oat bran period. Stable isotopes of zinc (⁷⁰Zn) were added to the diets at d 7 of each period. The fractional absorptions (means ± SD) of zinc from the low-fiber and oat bran diets were 0.48 ± 0.11 and 0.40 ± 0.15 (P = 0.07), respectively. The higher zinc content in the oat bran period resulted in a greater amount of zinc absorbed (64 ± 19 µmol and 99 ± 51 µmol, respectively, P = 0.009). Balance data suggest that the higher absorbed amount of zinc resulted in correspondingly higher intestinal endogenous excretion of zinc. In conclusion, the absorption of zinc was high and not affected by addition of oat bran.

KEY WORDS: • oat bran • zinc • phytate • stable isotopes • humans

	INTRODUCTION

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A high daily intake of oat bran and other food sources rich in soluble fiber has been shown to result in a small but significant lowering of plasma total cholesterol and LDL cholesterol concentrations (Brown et al. 1999 ). In contrast to soluble fiber sources such as pectin and guar gum, oat bran has a high phytate (myo- inositol hexa phosphate) content. Phytate impairs absorption of zinc and iron and presumably also other trace elements by forming poorly soluble complexes. Activation of endogenous phytases in cereals by soaking or fermentation improves absorption of iron and zinc (Nävert et al. 1985 , Sandberg and Svanberg 1991 ). Oat products are considered to have a low endogenous phytase activity, which is further reduced by heat treatment of all commercial oat products. A low zinc and iron absorption has been demonstrated from breakfast meals containing oat porridge and oat bran bread (Rossander-Hulthén et al. 1990 , Sandström et al. 1987 ). These effects are probably not attributable to the oat fiber per se as malting of oats under optimal conditions for activation of phytase has been shown to reduce phytate content and significantly improve iron and zinc absorption (Larsson et al. 1996 ).

The above-quoted oat product absorption studies are single meal studies where the oat products have been the major source of minerals in the meal. To achieve clinically important effects on blood lipids, intake of oat bran in the order of > 80 g/d is needed (Brown et al. 1999 ) by necessity divided over several daily servings. Consequently the phytate in oat bran could interact with a number of other dietary components, and the net effect on availability of minerals would be dependent on the composition of each of the individual meals. The results from single meal studies are therefore not necessarily valid for the impact of oat bran on the total dietary content of minerals. The effect of oat bran on mineral availability from a total diet has only been addressed in one earlier study in humans. Spencer et al. (1991) evaluated the effect of a daily intake of oat bran muffins for 32 d on calcium absorption (evaluated by ⁴⁷Ca) and zinc and magnesium balances. Calcium absorption seemed not to be affected, while urinary calcium excretion was reduced, and the endogenous fecal excretion of calcium was increased. Apparent balances of zinc and magnesium were not different in the oat bran period compared to a control period.

The aim of this study was to determine the effect of a high daily intake of oat bran added to a low-fiber diet on zinc absorption in young healthy subjects using fecal monitoring of stable isotopes. In addition the apparent balance of zinc was measured, and the endogenous intestinal excretion was estimated by combining the stable isotope absorption and chemical balance data.

	MATERIALS AND METHODS

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Subjects.

Six males and 6 nonpregnant females, 22–30 y, volunteered for the study. They were all apparently healthy and nonsmokers. One of the women used oral contraceptives, while none of the subjects used other medication, or vitamin and mineral supplements. They were allowed to use painkillers if necessary but were then asked to deliver a duplicate for mineral analysis. The subjects were all given oral and written information about aims and procedure of the study. The project was approved by the local Ethical Committee of Frederiksberg and Copenhagen [(KF)V.V.200.2016/90].

Study design.

The study was designed as a cross-over study with 2 x 3 wk dietary periods separated by a wash-out period of 4 wk. The diets were based on natural food items. In one dietary period, the volunteers were given a low-fiber diet, and in the other period they were given an identical low-fiber diet but with addition of 102 g of oat bran/10 MJ. Stable isotopes of zinc were given orally on d 7, and complete collection of feces was made from d 5 to d 13 and from d 17 to d 20. The fecal excretion of stable isotopes was monitored using radio-opaque pellets (60/d) in different shapes (Cummings et al. 1976 ) administered in gelatin capsules with the three daily main meals; 24-h urine was collected from d 6 to d 12 and d 16 to d 19. Para-aminobenzoic acid (PABA)³ (3 x 80 mg/d) was administered to validate the completeness of the urine collection (Bingham and Cummings 1983 ). During the study, body weights were determined three times a week.

Diets.

The dietary intake in the study periods was planned to have a fat content of 35% of total energy, i.e., corresponding to habitual intake of this age group. The fatty acid content of the oat bran was matched by addition of vegetable oil to the diet in the low-fiber period. The oat bran (Kungsörnen AB, Järna, Sweden) was incorporated into bread and served at three main meals. Seven different menus were prepared with virtually identical trace element and protein content (Table 1 ). All foods were prepared in advance in the metabolic kitchen. Precautions were taken to avoid any contamination. Individual portions of the meals were weighed according to estimated energy requirements. In order to match the zinc content of the added isotopes, zinc (as ZnCl₂), corresponding to 1.0 mg/10 MJ, was added to the low-fiber diet and 1.5 mg/10 MJ was added to the oat bran diet (0.5 mg/10 MJ was added to the daily hot dish, and the rest was added to the bread dough of the bread made for the study). Separate portions were prepared for consumption on the day for ⁷⁰Zn administration with no additional zinc. The individual meals were stored at -20°C after cooking and were thawed and heated on the day of consumption.

Preparation and administration of stable isotopes.

The stable zinc isotope [⁷⁰ZnO (⁷⁰Zn: 71.6%) MEDGENIX Group, Düsseldorf, Germany] was administered d 7. The zinc isotopes were dissolved in a few drops of 12 mol/L HCl (analytical grade; Merck, Darmstadt, Germany) and then diluted with deionized H₂O (resistance 18 M cm, Millipore MilliQ water purification system (Millipore Corporation, Bedford, MA). The isotopes were added to the three main meals of the day according to the native zinc content of the respective meal. The solution of the stable isotopes was dripped onto the bread and added to the hot dish the day before it was served, and the meals were kept refrigerated. The intention was to add 1.0 mg/10 MJ and 1.5 mg/10 MJ of stable isotopes in the low-fiber and the oat bran diet, respectively, to match the amount added to the prepared food and to achieve approximately the same relation between the added and native zinc isotopes in the two diets. By mistake, this was not done for the first six subjects entering the study, and due to limited availability of isotopes, adjustments had to be made for the subjects entering later. The amount of stable isotopes administered to each of the subjects is given in Table 2 .

Duplicate portions of the diet were collected and prepared for analysis as described by Knudsen et al. (1996) . Nitrogen content of the food was determined by the Dumas technique (Automatic Nitrogen Analyzer, NA 1500; Carlo Erba Instrumentazione, Milano, Italy) (Kirsten and Hesselius 1983 ). Protein was calculated from the nitrogen content by multiplication by 6.25. Total fat, carbohydrate, and soluble and nonsoluble nonstarch polysaccharides were analyzed as described by Sandström et al. (1994) . Phytic acid was determined by a modification (Sandberg et al. 1982 ) of the iron-precipitation method of Ellis et al. (1977) . All glassware was washed in HCl and rinsed in deionized water before use. Portions of freeze-dried food were analyzed for sodium, potassium and phosphorus after wet ashing (290–300°C, 15 min). Phosphorus was determined according to the method of Fiske and Subbarow (1925) . Sodium and potassium were determined by flame emission (Corning 410; Corning Science Products, Essex, England), total diet reference material for sodium and potassium [ARC/CL HDP reference material; Agricultural Research Center of Finland, Jokionen, Finland (Kumpulainen and Tahvonen 1990 )] were analyzed simultaneously. The analyzed sodium and potassium concentrations were 7.73 ± 0.24 mg/g and 9.29 ± 0.29 mg/g compared with certified values of 7.87 ± 0.57 mg/g and 9.42 ± 0.30 mg/g, respectively.

Zinc, copper, magnesium and calcium content was measured by atomic absorption spectrometry (GBC-932 AA, Victoria, 3175, Australia) after acid decomposition in sealed vessels under elevated pressure using microwave energy (Knudsen et al. 1995 ). Calibration of measurements was performed using commercial standards (Tritisol, Merck). The relative standard deviations for the determination of zinc, copper, magnesium and calcium were 6.4, 3.7, 8.0 and 1.6%, respectively. All measurements were carried out with standard flame operating conditions as recommended by the manufacturer. Reference standard materials for zinc, copper, magnesium and calcium (ARC/CL HDP reference material, Agricultural Research Center of Finland) were analyzed simultaneously. The analyzed zinc, copper, magnesium and calcium concentrations were 40.1 µmol/100 g, 6.2 µmol/100 g, 3.3 mmol/100 g and 8.3 mmol/100 g compared with certified values of 44.2 ± 2.0 µmol/100 g, 5.0 ± 0.3 µmol/100 g, 3.2 ± 0.1 mmol/100 g and 7.15 ± 0.3 mmol/100 g, respectively.

Blood sampling and analysis.

Blood was drawn with minimal stasis from an antecubital vein in trace element free tubes (Vacutainer 606526; Becton Dickinson, Meylan-Cedex, France). Samples were collected in the morning (0700–0900 h) from resting individuals (15–20 min of recumbent rest) with 20 G needles and evacuated tubes. The volunteers were fasted (>12 h) and had abstained from severe physical activity and any kinds of drugs for 48 h and from alcohol for 24 h. Blood was collected. After centrifugation, samples were stored at -20°C. Duplicate serum samples were analyzed for zinc by flame atomic absorption spectrometry (Perkin Elmer Model 5000; Perkin Elmer, Norwalk, CT) with standard flame operating conditions as recommended by the manufacturer. Standard reference materials (Seronorm Trace Element; Nycomed Pharma AS, Oslo, Norway) were analyzed along with the samples. The analyzed zinc concentration of the standard material (n = 3) was 25.1 ± 0.59 µmol/L compared with a certified value of 26.0 µmol/L.

Fecal and urinary collection and analysis.

Feces were collected in acid-washed plastic containers from d 5 to 13 and from d 17 to 20. Fecal samples were weighed, freeze-dried, lyophilized, crushed to powder, carefully mixed and stored in a dry place. Radio-opaque markers (Marker Capsules; Dunn Nutrition Center, Cambridge, England), 60/d, in four different shapes were consumed three times per day from the beginning to the end of the experiment. One shape of fecal marker was consumed in the days before isotope administration (d 5 and 6); another shape of fecal markers was used on the day of isotope administration (d 7); and a third shape was used for the following days. After X-raying and counting the fecal markers, the feces samples were pooled according to the shape of fecal markers. For each subject four pools were made: i) the fecal samples collected before appearance of the first isotope day, ii) samples containing markers from the day of isotope administration marker, iii) the subsequent fecal samples collected up to d 13 and iv) the samples collected from d 17 to d 20. Urine (24-h) was collected from d 6 to 12 and from d 16 to 19 in acid-washed plastic bottles containing 10 mL of 1 mol/L HNO₃. Portions of urine were analyzed in duplicate for their contents of nitrogen, sodium, potassium and zinc. All glassware was washed in HCl and rinsed in deionized water before use. Feces were analyzed for sodium and potassium after wet ashing (290–300°C, 15 min) of 0.1 g freeze-dried samples in 1 mL of concentrated H₂SO₄ with addition of 3 mL of H₂O₂ (8.8 mol/L). Sodium and potassium in feces and urine were determined by flame emission (Corning 410; Corning Science Products, Essex, United Kingdom). Reference standard materials (ARC/CL HDP reference material, Agricultural Research Center of Finland) were analyzed along with the feces samples (see above). Reference standard materials (Lyphocheck Biorad Ecs Division, Anaheim, CA) were analyzed along with the urine samples. The analyzed sodium, potassium and zinc concentrations of the standard material (n = 11) were 62.36 ± 0.92 mmol/L, 21.73 ± 0.65 mmol/L and 3.3 ± 0.08 µmol/L compared to certified values of 60 (48–72) mmol/L, 22 (18–26) mmol/L and 3.7 (3.0–4.5) µmol/L, respectively.

Analysis of stable isotopes.

The fecal pools were analyzed for enrichment of zinc isotopes. Acid microwave digestion was performed in Savillex (Savillex Inc., Minneapolis, MN) digestion vessels with concentrated (Primar/Aristar grade) HNO₃ and H₂O₂ (Model Proline Micro Chef ST44). HNO₃ (1.8 mL) and H₂O₂ (0.2 mL) were added to 500 mg of freeze-dried fecal sample. After digestion, 1 mL of the digest solution was diluted with 9.0 mL of 18 H₂O. The remaining sample was dried on a hot plate in a fume hood. The sample was resolved in 5 mL of 1 mol/L of ammonium acetate and centrifuged. The supernatant was placed on a Chelex 100 resin column, and 20 mL of 1 mol/L of ammonium acetate was added. The final fraction containing copper and zinc was eluted with 20 mL of 2.5 mol/L HNO₃. Isotope ratios were measured by inductively coupled plasma mass spectrometry using a VG PQ2 + inductively coupled plasma mass spectrometer (VG Elemental, Winsford, United Kingdom) equipped with a quartz torch, a Meinhard nebulizer (TR-30-a3) and a Scott-type water-cooled double-pass spray chamber cooled to 4°C. Typical operating conditions were as follows: R.F power = 1350W, nebulizer argon flow rate = 0.75 L/min, cool argon flow rate = 14 L/min and auxiliary argon flow rate = 0.7 L/min. Samples were introduced by a peristaltic pump (Gilson miniplus 3; Gilson Medical Electronics, Middleton, WI) with the flow rate set at 0.8 mL/min, a sample uptake time of 2 min and a wash time of 3 min. Blank values (for background subtraction) were acquired once, whereas samples and standards were acquired five times. The mass range, m/z 62–71, was scanned with 1600 sweeps, a dwell time of 80 µs and 512 channels. Aldrich (Milwaukee, WI) atomic absorption standards were used to correct for instrument mass bias. The determination of stable isotopes in the fecal samples was made using ⁷⁰Zn/⁶⁸Zn ratios. The relative standard deviation for these isotope ratio measurements was < 1.5%. Prior to the analysis of the samples, a blank was run followed by a zinc standard (500 µg/L) of natural abundance, which was used to correct for instrument mass bias. This was then followed by another blank (to check for absence of carry-over) and then by four samples. After every fourth sample, another standard was analyzed to correct for any drift in the instrument mass bias.

Calculations and statistics.

The determination of the stable isotopes in the fecal samples was based on the ratios ⁷⁰Zn/⁶⁸Zn and the amount of total zinc in each enriched fecal sample. The equations used for calculation of the amounts of stable isotope in the fecal samples was according to Ehrenkranz et al. (1989) , and the native isotope distribution used for calculation was according to DeLaeter et al. (1991) . The isotopic enrichment of stable isotopes in fecal samples was expressed as a percentage of administered dose. The amounts of stable isotope in excess of natural abundance were added to obtain the amount per subjects of each fecal-eliminated label. Only fecal samples containing radio-opaque markers originating from the day of isotope administration were included in the estimates of the "true" absorption of the elements. Chemical balances were calculated based on all days of fecal and urinary collections. The total zinc content of the fecal samples was calculated, and excretion of fecal radio-opaque markers was used to calculate average daily excretion. Apparent absorption was calculated as the difference between dietary intake and fecal excretion of the minerals. Zinc balances were calculated from the difference between dietary intake and the sum of fecal and urinary excretions during the intervention period. Endogenous fecal loss was calculated as the difference between the total fecal content of zinc and the fecal content of unabsorbed dietary zinc estimated from the fecal content of the eliminated stable zinc isotope.

Calculation of the tracer recovered in each sample was made using the equation of Ehrenkranz et al. (1989) :

where

70Zn^*_f = amount of ⁷⁰Zn originating from the in vivo label recovered in the fecal sample

R_70/68 = mass isotope ratio (on atom basis) for ⁷⁰Zn/⁶⁸Zn determined in the fecal sample

R_70/68⁰ = the native isotope ratio (on atom basis) for ⁷⁰Zn/⁶⁸Zn

K_A = 100/(atom% of ⁷⁰Zn in zinc)

Zn_f = total amount of zinc determined in the fecal sample

The data were compared by Student’s t test for paired data using the Statistical Package for the Social Sciences (SPSS/PC + 8.0; SPSS, Chicago, IL). The differences were considered significant if P < 0.05.

	RESULTS

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The body weights of the subjects at the start and on d 21 of the two study periods were 70.2 ± 9.7 kg and 70.5 ± 9.2 kg, respectively, with the low-fiber diet, and 71.6 ± 9.8 kg and 70.7 ± 9.4 kg, respectively, with the oat bran diet. The mean weight changes were 0.55 ± 0.35 kg or 0.78% of body weight when subjects consumed the low-fiber diet and 0.55 ± 0.26 kg or 0.77% of body weight when they ate the oat bran diet. Serum zinc concentration was 13.2 ± 1.6 µmol/L at end of the low-fiber diet period and 12.7 ± 1.4 µmol/L at end of the oat bran period (P = 0.3). Recovery of urinary PABA showed complete urinary collection. The completeness of fecal collections estimated from recovery of radioopaque pellets originating from the day of isotope administration was 95% ± 9.

The content of energy, zinc phytate, fiber and selected nutrients of the two experimental diets per 10/MJ is given in Table 3 . Addition of oat bran to the low-fiber diet increased the content of phytate (from 0.5 to 4.0 mmol) and zinc (from 115 to 202 µmol), as well as the content of protein, phosphorus, copper, magnesium and iron.

	DISCUSSION

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The results from this study suggest that when oat bran is added to an animal protein-based diet, zinc absorption is not impaired. The study was designed to evaluate the effect on zinc absorption from the total diet. Therefore the addition of the stable isotopes was done in accordance with the native zinc content of the meals, and the zinc content was adjusted on the remaining days in order to as far as possible keep the zinc intake constant in each period. The small differences in the total zinc intake on the days of isotope administration are taken into account in the calculation of the apparent balances and are not very likely to have affected the overall results.

The zinc intake in the low-fiber period was rather low (151 µmol/10 MJ) and a high fractional zinc absorption was consequently expected (Sandström 1992 ). The observed zinc absorption (47%) is comparable to zinc absorption (53%) determined from a low-zinc (84 µmol/d) diet based on animal and vegetable sources of zinc supplemented with an energy formula (Wada et al. 1985 ). From a low-fiber (3 g/d) high-zinc (200–230 µmol/d) formula diet, 39% absorption has been reported (August et al. 1989 ), illustrating the effect of total zinc content on fractional absorption. The virtually similar and high fractional zinc absorption in the oat bran period was unexpected considering the high phytate content of oat bran as well as the higher zinc content. It has been suggested that the phytic acid to zinc molar ratio could be used as an index of zinc availability. In the present study the molar ratios of phytate to zinc were 4 (low-fiber) and 18 (oat bran). Studies with infant formula indicate that a negative effect on zinc absorption is observed at a ratio above 6 (Lönnerdal et al. 1988 ). From an oatmeal porridge with a molar ratio of 15, only 8% was absorbed (Sandström et al. 1987 ). In a similar total diet stable isotope study with an intake of 140 µmol zinc/10 MJ and 1 mmol phytic acid, mainly derived from rye and wholewheat bread, i.e., a ratio of 7, zinc absorption was 29% (Knudsen et al. 1996 ). A similar level of zinc absorption (25%) was also observed in a study using blended food items of animal origin (Zn intake of 250 µmol/d) and an isotope ratio of 6 (Swanson et al. 1983 ). Addition of pure phytate (2.34 g/d or 3.6 mmol/d) to a semipurified liquid high-zinc diet (15 mg (229 µmol) (molar ratio 0 and 15) for 15 d decreased the zinc absorption from 34 to 17.5% (Turnlund et al. 1984 ). Thus if zinc and phytate content had been the only determinants for zinc absorption, a fractional absorption of < 20% was expected. Animal protein has in single meal studies been shown to overcome the zinc absorption impairing effect of phytate (Sandström and Cederblad 1980 , Sandström et al. 1980 ). This may have contributed to the lack of effect of oat bran observed in this study but cannot fully explain the differences in results compared to the study by Knudsen et al. (1996) .

A possible, although not very likely, explanation to the high fractional absorption from the oat bran diet would be a poor isotopic exchange between the zinc present in the oat bran and the added stable isotope. The rationale for the isotope techniques is the assumption of complete isotopic exchange so that the disappearance or appearance of the added tracer mirrors the fate of the total native element in question (Sandström et al. 1993 ). Similar zinc absorptions from extrinsically and intrinsically foods have been demonstrated (Egan et al. 1991 , Gallaher et al. 1988 , Serfass et al. 1989 ). Whether this is also valid for oat bran is not known. A poor exchange would mean absorption from a smaller dietary pool of zinc and consequently a higher fractional absorption. The molar ratio phytate to zinc in the oat bran was ~40, and it is possible that insoluble zinc (and other mineral) complexes were formed already during the bread-making process. However, even with an incomplete isotopic exchange, the conclusions from this study would still be that oat bran does not impair absorption of zinc from the total diet.

The disappearance of stable isotopes was used to estimate the endogenous excretion of zinc. Turnlund et al. (1984) has suggested that phytate increases the endogenous excretion of zinc by reducing the intestinal reabsorption of endogenously excreted zinc. In this study the estimated endogenous excretion was significantly higher when adding oat bran to the low-fiber diet but appeared to be a reflection of the higher amount of zinc absorbed. Changes in endogenous excretion are quantitatively important in maintaining body zinc homeostasis (Wada et al. 1985 ). If isotope exchange had not taken place and the true amount of zinc absorbed from the oat bran diet was lower (i.e., the disappearance of the stable isotopes was only reflecting the fate of zinc originating from other foods), the endogenous excretion would be correspondingly lower. The results in the study suggest that this ability to adjust to different intakes of zinc was not impaired by intake of oat bran. To confirm the hypothesis of a poor availability and exchange of the oat bran zinc and for a direct measurement of the endogenous excretion of zinc, multi-isotope techniques and intrinsic labeling would be necessary.

The apparent absorption and the zinc balance were negative in both periods, especially if an allowance is made for integumental losses of zinc. This could be due to the relatively short intervention periods not reflecting true balances and an influence of preceding habitual diet with a higher content of available zinc. Schwartz et al. (1986) have suggested that an adaptation period of at least 4 wk with a constant intake of the element of interest is needed before reliable balances can be obtained.

In conclusion, a high intake of oat bran incorporated into bread and taken as a part of an animal protein-based diet did not impair fractional absorption of zinc. If isotope exchange is assumed to take place between added isotope and all zinc in the diet including oat bran zinc, a higher amount of zinc was absorbed from the oat bran diet, which in turn resulted in an increased intestinal endogenous excretion of zinc.

	FOOTNOTES

 
¹ Financial support from Ministry of Agriculture, Denmark, Grant LMF-KVL-8.

³ Abbreviation used: PABA, para-aminobenzoic acid.

Manuscript received August 23, 1999. Initial review completed September 29, 1999. Revision accepted November 29, 1999.

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