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ANIMAL NUTRITION |
,2
* EVIALIS, 56250 Saint-Nolff, France;
and
Etablissement National d’Enseignement Supérieur Agronomique de Dijon, 21079 Dijon, France;
and
Université de Clermont-Ferrand, 63000 Clermont-Ferrand, France; and and
Texas A&M University, College Station 77843-4475
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Abstract |
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 Top Abstract INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: bacteria • digestion • equine • fermentation • microflora • stomach
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INTRODUCTION |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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).
Compared with the large intestine, little information is available on the postprandial characteristics of the gastric ecosystem. However, the activity of the gastric microflora cannot be ignored, because it could be involved in the digestion of dietary starch. Indeed, a large amount of starch, ranging from 41 to 76% (Varloud et al., 2004), has been shown to disappear from the stomach of the horse. Although the potential fermentation of the dietary starch may modify its energetic advantage, this early disappearance of starch has never been measured in live horses, and its relation to the gastric microbiota has not been clearly demonstrated.
This experiment was designed to determine the post-prandial dynamics of some bacterial populations, microbial metabolite concentrations, and physicochemical characteristics of the gastric contents in live and conscious horses after ingestion of a test meal. The second aim of this experiment was to evaluate the role of the microbial populations on dietary starch digestibility.
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MATERIALS AND METHODS |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The pelleted concentrate was fed twice daily and the hay was fed once daily (Table 2). To limit potential contamination by AIA, the hay was washed with water immediately before feeding. No refusal of concentrates or hay was observed during the experiment. Horses were adapted to the diet for 21 d before the first collection of gastric contents. No antibiotics were administered for at least 3 mo before the initiation of the experiment.
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. For each horse, sampling occurred 30 min before (T–30), and 60 (T60), 120 (T120), and 210 min (T210) after feeding the first concentrate meal of the day. Horses had no access to water during the hour preceding the meal and during the collection procedure. However, to mimic the voluntary postprandial water intake, which was previously observed with the same experimental horses, sterile water (200 mL/100 kg of BW) was introduced via an NG tube 45 min after feeding. At each collection time, the first aliquot of chyme was reserved for microbial analysis and immediately transported to the laboratory in a CO2-saturated flask maintained at 38°C. Temperature and pH were measured on the second aliquot of digesta with an electronic pH-meter (340i/SET, WTW Wissenschaftlich-Technische Werkstätten GmbH, Weilheim, Germany) immediately after the sample collection. Approximately 10 mL of the second aliquot of digesta was filtered through a 100-µm Blutex nylon screen (SAATI, Sailly-Saillisel, France). The filtered contents were divided into 3 subsamples and immediately frozen (–20°C) for later determination of NH3 (3 mL), D- and L-lactate (1 mL), and VFA [1 mL added to 0.1 mL of preservative solution (5 mL of H3PO4 and 1 g of HgCl2 in 100 mL of demineralized water); Sigma Aldrich, Saint-Quentin-Fallavier, France]. A third aliquot (about 30 mL) was immediately frozen at –25°C in hermetically sealed plastic boxes, freeze-dried (168 h), and ground with a ball mill (MM200, Retsch, Haan, Germany) at 30 oscillations/s for 2 min for D-glucose and starch determination. The remaining digesta were immediately weighed and frozen at –25°C for later determination of DM and AIA. The NG tube was disinfected with alcohol and rinsed with demineralized water after each collection.
Microbial Analyses
For inoculation on specific media, decimal dilution series of the gastric samples were prepared under O2-free CO2 in an anaerobic mineral solution (Bryant and Burkey, 1953). Total, viable anaerobic bacteria and lactic acid-utilizing bacteria counts were determined in roller tubes under CO2 gas phase on a nonselective medium (Leedle and Hespell, 1980) and a selective medium containing lactate as the sole energy source (Mackie and Heath, 1979), respectively. The number of viable bacteria was determined by using 4 replicate roll tubes prepared from dilutions representing 10–3 to 10–8 mL and 10–2 to 10–5 mL of chyme for total anaerobes and lactate-utilizing bacteria, respectively.
Streptococcus spp. were cultured on a bile-esculinazide agar medium (BK158HA, Biokar diagnostics, Beauvais, France). Lactobacillus spp. were cultured on Rogosa agar medium (BK033, Biokar Diagnostics). Three replicate Petri plates were inoculated from dilutions representing 10–1 to 10–6 mL of chyme. All counts were performed after 48 h of incubation at 38°C.
Biochemical Analyses
All samples were analyzed in duplicate. L-Lactate and D-lactate were assayed with an enzymatic reaction procedure (D-Lactic Acid/L-Lactic Acid Enzymatic Bio-Analysis/Food Analysis kit, Cat. No. 1002891, ENZY-TEC/SCIL Diagnostics GmbH, Martinsried, Germany), and quantified spectrophotometrically at 340 nm (MRX Revelation, Dynatech Laboratories, Guyancourt, France). Ammonia concentration was measured with an NH3 electrode (152303000, Crison, Barcelona, Spain) connected to an iono-meter (GLP 22, Crison). The VFA concentrations were assayed by GLC (gas chromatograph model 437 A, United Technologies Packard, Zurich, Switzerland; Jouany, 1982). After drying in a forced-air oven at 60°C to a constant weight for the determination of DM, the same digesta and feeds were ground through a 1-mm screen with a hammer mill. The NDF, ADF, and ADL contents were determined according to the method described by Van Soest et al. (1991), and OM and AIA contents were evaluated as described by the Ministry of Agriculture, Fisheries and Food (1986). The starch proportions were estimated through an enzymatic procedure (Kozlowski, 1995), which allowed the determination of the D-glucose concentration. The starch values refer to all 
-linked polymers of glucose and are expressed as glucose equivalents.
Data Calculations
The organic acids and NH3 concentrations were expressed in millimoles per liter. Starch disappearance, calculated for T60, T120, and T210, was expressed as percentage of the initial value and was transformed using the arcsine transformation before statistical analysis. Microbial counts were expressed as log10 of colony-forming units per milliliter.
Statistical Analyses
The data were analyzed by using the MIXED procedure of SAS (SAS Inst. Inc., Cary, NC). The effect of the horse and the linear and quadratic effects of the time of collection of the gastric content were evaluated. Least squares means are presented. The results were considered significant if P 
0.05.
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RESULTS |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). None of the different characteristics of the gastric content showed a quadratic pattern with the time of digesta collection. Gastric contents were observed using the video-endoscope, and it appeared that digesta were formed into a paste in the shape of a ball after the meal (Figure 1).
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). The density of the gastric contents was 1.16 ± 0.03 g/mL. In 1 horse, the density of the content (1.60 ± 0.30 g/mL) was greater than that in the other 2 horses (0.88 ± 0.08 and 0.93 ± 0.08 g/mL). The DM content of the samples was 499 ± 39 g/mL, whereas ash represented 229 ± 13 g/mL of the DM content. The temperature of the gastric content was 28.4 ± 0.4°C. The pH was 5.84 ± 0.17, ranging from 1.11 to 7.57; the greatest variation was among unfed horses
Microbial Counts
The concentration of the total anaerobic bacteria population in gastric contents increased linearly (P < 0.001) from 5.54 ± 0.30 to 6.98 ± 0.29 log10 cfu/mL between T–30 and T60, and 8.32 ± 0.35 log10 cfu/mL at T210. The concentration of lactate-utilizing bacteria was 4.30 ± 0.15 log10 cfu/mL. Differences among individuals were observed (5.13 ± 0.23, 4.48 ± 0.06, 4.34 ± 0.14, and 3.22 ± 0.04 log10 cfu/mL; P < 0.001). The concentrations of lactobacilli and streptococci were 5.52 ± 0.35 and 4.82 ± 0.55 log10 cfu/mL, respectively. The lactobacilli concentration increased linearly (P = 0.029). In some samples, these lactic acid bacteria concentrations were measured below the dilution limit (10 cfu/mL) and the bacteria concentration could not be quantified.
Substrate and Metabolites Concentrations
The D-glucose concentration in the gastric contents was 28.51 ± 16.33 mmol/L. The concentration at T–30 (14.35 ± 1.24 mmol/L) was lower than at T120 and T210 (43.36 ± 15.36 and 41.25 ± 11.80 mmol/L, respectively). The NH3 concentration in the gastric content was 2.48 ± 0.28 mmol/L. The NH3 concentration increased linearly (P = 0.023) during the sampling period.
The lactate concentration was 3.88 ± 0.76 mmol/L and it increased linearly (P = 0.013) during the sampling period. Before meal and until T120, the concentrations of L- and D- forms were similar, but the L-enantiomer predominated at T210. Consequently, the L-/D-lactate ratio increased from 0.9 to 3.2 between T120 and T210. At T210, L-lactate represented 70% of the total lactate concentration.
The total concentration of VFA in the gastric contents was 5.18 ± 0.79 mmol/L. It increased linearly (P = 0.002) during the postprandial period (Figure 2). Acetate was the major VFA (77.8 ± 1.6 mol/100 mol of total VFA) in gastric contents. The concentration of acetate in the gastric content was 4.14 ± 0.67 mmol/L and it increased linearly (P = 0.001) during the postprandial period. Pro-pionate was the second major VFA in the gastric content (5.9 ± 0.92 mol/100 mol of the total VFA); its proportion decreased (P < 0.05) from 10.42 ± 2.70 to 3.95 ± 0.60 mol/100 mol of total VFA before and after the meal, respectively (data not shown).
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). Starch digestibility coefficients differed widely among horses (66.5, 13.6, 6.8, and 7.9%; P = 0.005). |
DISCUSSION |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Physicochemical Conditions
The high DM content of the gastric chyme observed, especially after ingestion of a meal, was consistent with the endoscopic observations. In a postmortem experiment that used a similar diet, we reported that the DM content of gastric chyme 240 min after the meal was 20% (Varloud et al., 2004). In deeply anesthetized horses, sphincters were considered to be closed, and gastric secretions may have contributed to the decrease in the DM content of the gastric digesta. Nevertheless, at a daily secretory rate of 50 to 100 mL/kg of BW, gastric secretion alone could not fully explain the difference between the present and previous experiments. In the present experiment, horses were not anesthetized, and, unlike the animals used by de Fombelle et al. (2003), the gastric emptying was not stopped. It is well known that the liquid phase of the digesta would be emptied faster than the solid phase (Ringger et al., 1996). Thus, we can assume that the DM content of the gastric digesta observed in the present experiment would be realistic. The restriction of water intake may also have contributed to reduce the DM content of the gastric digesta.
Interestingly, regardless of the feeding status of horses, the average temperature of the gastric contents was about 10°C lower than normal body temperature. After the meal, water was provided at room temperature. In fed horses, it might have partially reduced the temperature of the gastric contents. However, this cannot explain the temperature observed in gastric contents from fasted horses. The collection procedure might have contributed to the reduction in the temperature because the temperature was measured after aspiration through a 2.8-m NG tube. No published data are available to evaluate the validity of our results. Because the temperature should have an impact on the development of bacteria within the stomach, further investigations are required for a better understanding of the dynamics of the gastric microbial population.
According to previous reports (Baker and Gerring, 1993a,b), the pH measured in unfed horses showed variation among individuals. However, the pH measured after feeding appeared to be neutral and less variable. This tendency for the pH to stabilize and then increase could be related to the buffering effect of salivary secretions, which accompany the mastication of feed. The results may also be partially explained by the feed itself, especially by the use of alfalfa, which was included in the concentrate (15% DM) as a raw material and is known to have a buffering effect (McDonald et al., 1991). These observations support the recommendation to maintain feed in the stomach in an effort to decrease the incidence of equine gastric ulcer syndrome (EGUS).
Microbial Population
Considering the abiotic characteristics of the ecosystem before feeding, the rather large microbial populations observed in the gastric contents before feeding were unexpected. For example, in the stomach of the horse with the lowest intragastric pH (1.11), the total anaerobes and lactate-utilizing populations were 4.8 and 3.2 log10 cfu/mL, respectively. In the same animal, the lactobacilli and streptococci populations, which are considered to be acid-tolerant, were not detected at the 10–2 dilution. To survive in this low pH environment, some bacteria may exhibit specific abilities such as preventing protons from entering the cell and pumping protons out of the cell. Some neutralophilic bacteria that can survive in the stomach have developed acute acid-resistance mechanisms (Valenzuela et al., 2003). To our knowledge, no previous work had quantified the microbial concentration in the gastric contents of unfed horses. Two lactobacilli species, Lactobacillus delbrueckii and Lactobacillus salivarius, have been identified in the gastric contents collected from dead horses that were previously fed a roughage-based diet and deprived of feed and water for 6 h before slaughter (Al Jassim et al., 2005).
The ecosystem of the horse stomach was modified during the first postprandial hour. The average post-prandial pH (6.04) became more compatible with microbial development while nutrients were available for the microorganisms. The total anaerobic bacteria population increased during the postprandial period. With an average increase of 1.9 log10 cfu/mL during the first hour after the meal (the lactobacilli appeared to be a more active population). Three hours and thirty minutes after the meal, the bacterial concentrations remained consistently lower than those reported from observations made with deeply anesthetized horses. We collected the gastric contents 210 min after the meal, whereas de Fombelle et al. (2003) collected at 270 min postprandial. In addition, in anesthetized horses, the gastric content was artificially retained in the stomach for 125 min (de Fombelle et al., 2003). In live and conscious horses under classical feeding practices, the stomach is emptying cyclically during the day and almost full during the hours after meal ingestion (Metayer et al., 2004). The favorable conditions needed for microbial growth and activity and ensured by the digesta are not stable during the day. Moreover, it could be expected that the microbial populations contained in the gastric content would flow with the digesta into the small intestine. Therefore, the origin of bacteria that colonize the digesta is of interest; some bacteria could originate from feedstuffs. Feeds indeed play a buffering and protective role against ingested bacteria (Drouault et al., 1999). Other bacteria that could be found in the mucosa may inoculate the ingesta and contribute to the initiation of microbial growth (Varloud et al., 2005). These observations are in agreement with previous reports with mice, rats, and swine (Dubos et al., 1965). In unfed and slaughtered horses, some lactobacilli strains, Lactobacillus salivarius, Lactobacillus reuteri, Lactobacillus agilis, and Lactobacillus crispatus, are indeed able to colonize the nonglandular area of the gastric mucosa (Yuki et al., 2000). Lactobacillus salivarius was one of the lactobacilli species previously identified in the gastric content of horses fed a hay-based diet (Al Jassim et al., 2005). These species could be expected to take advantage of their ability to colonize the gastric epithelium and survive during fasting periods. Moreover, as in murine species (Elliott et al., 1998), it could be expected that an induction of the colonization of the gastric mucosa by lactobacilli would accelerated EGUS healing. Further defining of the role of the gastric mucosal and luminal microflora in equine health and disease is needed.
Microbial Activity
As previously reported with unfed horses, the organic acid concentrations were low in the gastric contents of unfed horses and increased gradually after the meal. The concentrations of metabolites measured in the gastric pool were the result of their secretion, utilization by microorganisms in different metabolic pathways, absorption through the gastric mucosa, and emptying from the stomach. These fermentation products were mainly organic acids, lactate, and VFA.
The low lactate concentration measured before the meal (1.01 to 1.07 mmol/L) confirmed previous data collected in horses fitted with gastric cannulas (0.0 to 1.5 mmol/L; J. Nadeau, University of Connecticut, Storrs; personal communication) but was lower than the results obtained from slaughtered horses (0.4 to 4.0 mmol/L; Alexander and Davies, 1963). Similar concentrations were shown in rabbits fasted for 24 h and then slaughtered (0.87 ± 0.02 mmol/L; Alexander and Chowdhury, 1958).
As in rabbits (Alexander and Chowdhury, 1958), results from our study showed that lactate concentration increased greatly during the postprandial period. The lactate concentration increased slowly during the 2 first postprandial hours, and then increased rapidly between the 2 last sampling points, reaching 7.99 mmol/L 210 min after the meal. Based on our findings and published data, we would expect the peak lactate concentration in the gastric contents to occur between 235 and 360 min after the meal (Argenzio et al., 1974; Healy et al., 1995; Nadeau et al., 2000). Therefore, we would not expect the lactate concentration to rise substantially beyond the values we observed at 210 min after the meal, even if experimental sampling were extended to later time points.
The L-/D-lactate ratio exhibited a 3-fold increase during the postprandial time and reached a maximum (3.2) 210 min after the meal, which was consistent with previous data (de Fombelle et al., 2003). The L-/D-lactate ratio in the stomach of horses is pH dependent similar to that in the bovine rumen (Nocek, 1997). The pH was <5 in the unfed state and increased to 6 after feeding. Of the 3 lactobacilli strains isolated from the gastric content of horses, only Lactobacillus mucosae produced L-lactate under in vitro incubation, but all strains synthesized the D-isomer.
Even if the lacticolytic population of the gastric content contributed to moderate lactate accumulation within the stomach, some lactate would be flushed with the digesta into the small intestine, where it should be absorbed (Alexander and Davies, 1963; Wolter and Chaabouni, 1979). In previous studies, the greatest concentrations of lactate in the horse’s digestive tract were observed in the stomach (Alexander and Davies, 1963; Wolter and Chaabouni, 1979). Therefore, lactate, especially the L-enantiomer, is a potentially important nutrient absorbed from the small intestine.
Few data are available on the VFA concentration in the gastric content of fasted horses. In an experiment with slaughtered horses fed a grass- or hay-based diet, the concentration of VFA ranged from 6 to 56 mmol/L (Alexander and Davies, 1963), whereas we observed only 1.96 mmol of VFA/L in the gastric content. Our data are more consistent with the measurement made 11 h after feeding a pelleted high-cellulose diet (1.1 mmol/L; Argenzio et al., 1974).
In unfed horses, the combination of a potentially low pH (<4) in conjunction with the presence of VFA can be considered a threat to the integrity of the nonglandular mucosa of the stomach. Considering the lipid solubility of VFA at low pH, the aforementioned combination could be involved in EGUS pathogenesis (Nadeau et al., 2003a,b). In the present experiment, the total VFA concentration increased linearly to 8.17 mmol/L after feeding. In a previous study, conducted with conscious horses fitted with gastric cannulas, the total VFA concentration did not show the same pattern and decreased after reaching 20 mmol/L 1 h after the meal (Nadeau et al., 2000). The results of our experiment were more representative of what happened in the stomachs of slaughtered ponies, in which the VFA concentration increased to 37.1 mmol/L 4 h after the meal (Argenzio et al., 1974). Therefore, the VFA concentration in the gastric contents observed in the present experiment would not be expected to increase after the last sampling time.
According to some reports (Nadeau et al., 2000; Morris et al., 2002; de Fombelle et al., 2003), the increase in the VFA concentration is mainly due to the production of acetate. In the present experiment, acetate represented, on average, 80 mol/100 mol of the total VFA concentration and increased by 10% within the first postprandial hour to reach 83 mol/100 mol of total VFA 2 h after the meal. The acetate concentration only reached 10.40 mmol/L in the present experiment, whereas it has been reported to be greater than 14 mmol/L (Nadeau et al., 2000). As the proportion and concentration of acetate increased after the meal, propionate and butyrate proportions decreased from 10 to 4 and from 8 to 5 mol/100 mol of total VFA, respectively. In previous research (Nadeau et al., 2000; Morris et al., 2002; de Fombelle et al., 2003), a similar postprandial propionate concentration has been observed. The butyrate concentration observed in the present experiment was consistent with the results obtained by Nadeau et al. (2000) with horses fed alfalfa and grain (0.04 to 0.79 mmol/L). The VFA could be absorbed through the gastric wall or the wall between the stomach and the small intestine. These VFA could be an important energy source for the mucosal cells. Different areas within the stomach do not absorb VFA in the same manner. Unlike the nonglandular mucosa, the glandular and pyloric mucosa absorbed VFA at pH 7.4, which can be observed in a postprandial state. However, instead of being absorbed into the blood, as happens in the large intestine, VFA concentrate in the tissue (Argenzio et al., 1974). This has been shown to induce functional mucosal damages in the nonglandular mucosa of the horse’s stomach (Nadeau et al., 2003a,b). The postprandial increase in organic acid concentration did not contribute to an acidification of the gastric ecosystem, which was expected based on a previous report (Argenzio et al., 1974).
As an end-product of the microbial degradation of nitrogen-based compounds, NH3 was detected in the stomach. In unfed horses, we observed an NH3 concentration of 1.84 mmol/L (data not shown). In the empty stomachs of slaughtered horses, urea concentration was reported to be 5.41 mmol/L (Alexander and Davies, 1963). Urea is known to be rapidly hydrolyzed to NH3 by microbial enzymes (Jouany et al., 1995). Some bacteria, such as Streptococcus salivarius, produce urease, which plays a key role in acid tolerance because its activity contributes to the neutralization of acidic microenvironments by producing NH3 and CO2 (Valenzuela et al., 2003). Several other microbial species, such as some Lactobacilli spp., show urease activity (Laukova and Koniarova, 1995) with an optimum pH ranging from 3 (Moreau et al., 1976) to 4 (Suzuki et al., 1979). The concomitant concentration of urea and NH3 in the gastric contents of unfed horses may indicate that a similar acid-resistance mechanism can be exhibited by gastric bacteria. The postprandial NH3 concentration steadily increased to 3.5 mmol/L (data not shown). Protein degradation contributes to the production of the ionized form of NH3 (Jouany et al., 1995). In horses fed a pelleted or textured concentrate, the NH3 concentration in the gastric content can reach 23.5 mol/L. However, this concentration may have been overestimated and related to the 3-h interval between slaughter and the collection of digesta (Wolter and Chaabouni, 1979). In the filled stomachs of slaughtered horses, urea concentration averaged 6.30 mmol/L (ranging from 3.17 to 11.67 mmol/L; Alexander and Davies, 1963). In S. salivarius, urea is known to be transported into the cell by a mechanism that is active at any pH. It can increase the resistance of bacteria to low pH and provide urea as a source of N for bacteria (Chen et al., 2000). Some bacteria found in the stomachs of horses could produce urease, and may have appropriate membrane transport mechanisms. It is possible that gastric bacteria may utilize urea released by the gastric epithelium and starch in the feed, with ammonia as an end-product of this metabolism.
Two hours after the meal, D-glucose represented 1.25% of DM of gastric contents (i.e., more than 5-fold the initial fraction of the pelleted feed). This indicates a strong starch-degrading activity of the microbial population, and agrees with the result of Healy et al. (1995) who reported that the D-glucose and L-lactate concentrations increased simultaneously in the gastric fluid of ponies given a textured or pelleted feed. Gastric starch digestibility is the result of the amylolytic and fermentative activity of the microbial population of the stomach. In the present study, gastric starch digestibility was evaluated by measurement of the starch disappearance using AIA fraction as a marker. Interestingly, and unlike the other markers of microbial activity, starch digestibility did not increase during the postprandial period and large variations were recorded among horses, especially 1 h after the meal (data not shown). These results were not consistent with previous reports (Wolter and Chaabouni, 1979; Varloud et al., 2004) or the expected gastric physiology. A differential transit of the marker (AIA) and the dietary fraction could explain these unexpected results. Indeed, feed processing (especially heating concentrate at 80°C) may have increased the proportion of gelatinized starch in the feed. Gelatinized starch is more soluble than native starch (Hall, 2003) and could be concentrated in the liquid phase of the gastric content. Similar to chromic oxide in the pig stomach (Holmes et al., 1974), AIA could be retained with solid particles in the horse stomach. This could be verified by measuring the repartitioning of starch and AIA in the solid and liquid phases of the gastric content by the use of appropriate transit markers. To estimate the gastric digestibility of dietary starch in horses, an appropriate in vitro method should be developed.
Our experiment confirmed the abundant microbial colonization of the stomach of horses, and we observed noticeable differences in characteristics of the gastric content between pre- and postfeeding sampling times. Our experiment also highlighted some methodological difficulties, especially the assessment of the partial digestibility of starch in the stomach of the conscious horses. Having an appropriate in vitro method might be beneficial in evaluating the starch-degrading capacity of the gastric flora. Similar to other species, the horse may be susceptible to gastric ulcer syndrome. The implications of the gastric microbial populations on the nutrition and health of horses are currently under investigation in our laboratory.
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Footnotes |
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2 Corresponding author: mvarloud{at}evialis.evls.net
Received for publication March 25, 2006. Accepted for publication May 22, 2007.
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LITERATURE CITED |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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