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ANIMAL NUTRITION |
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* Division of Animal Resources Science,
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School of Veterinary Medicine,
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Dept. of Animal Product and Food Science,
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School of Biotechnology,
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# Kangwon National University, Chuncheon,
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|| Potato Valley Co., Ltd. Hongcheon-Gun, and
¶ Research Centre for Proteineous Materials, Chosun University, Kwangju, Republic of Korea
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Abstract |
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 Top Abstract INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: antimicrobial activity • growth performance • intestinal morphology • nutrient digestibility • potato protein • weanling pig
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INTRODUCTION |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The regulatory pressure and public perception for the need to remove antibiotics from animal feeds has made it necessary to identify alternatives to replace antibiotics so as to maintain growth performance benefits (Bae et al., 1999).
Recently, antimicrobial peptides (AMP) have been isolated and characterized from tissues and organisms representing virtually every kingdom and phylum. Plants and animals are in close contact with diverse bacteria and fungi, but only in rare cases does this association result in the development of disease, mostly because of the existence of antimicrobial defense systems (Park and Hahm, 2005). These AMP are small gene-encoded peptides that show a broad range of activity against gram-negative and gram-positive bacteria, fungi, and myco-bacteria (Zasloff, 2002).
Potatoes (Solanum tuberosum) are commonly cultivated for human consumption worldwide and known to have antimicrobial (Han et al., 1996), and antifungal (Do et al., 2004) properties. A new potato variety developed by traditional crossing called Gogu valley (Solanum tuberosum L. cv. Gogu valley) is known for its resistance to diseases and rotting during storage. In a study on healthy humans, administration of juice from Gogu valley potato increased the growth responses of Bifidobacterium and Lactobacillus and decreased growth of Clostridium perfringens and Escherichia coli (Lee, 2005). Potamin-1, a protein of 5.6 kDa present in the potato tubers of Gogu valley, was shown to have antimicrobial activity (Kim et al., 2005).
Hence, in this study, the potato tubers of Gogu valley were selected and used with the objective of evaluating the potato protein (PP) obtained from these tubers for their antimicrobial activities as replacements for antibiotics in the diet of weanling pigs.
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MATERIALS AND METHODS |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Potato tubers (S. tuberosum L. cv. Gogu valley) were obtained from the Potato Valley Co., Ltd (Sammachiri 681–1, Hongcheon-Eup, Gangwon-Do, South Korea) and were stored at 4°C in the dark at a relative humidity of 95 to 100% for up to 6 mo. These tubers were soaked in distilled water for 2 h and then ground, following which a protein extraction buffer (50 mM Tris-HCl, pH 7.5, 10 mM EDTA, 150 mM NaCl, 1% dimethyl sulfoxide, and 0.1% β-mercaptoethanol) was added to the mash. This was followed by mixing the extraction buffer with potato mash for 15 min, for the extraction of proteins in extraction buffer, followed by centrifugation at 1,260 x g for 15 min. The supernatant obtained after centrifugation was freeze-dried to form potato protein powder.
The freeze-dried potato protein powder extracted from the potato tubers was dissolved in sterile, deionized distilled water to make a 10,000 µg/mL stock solution for microdilution assays to establish the minimal inhibition concentration (MIC) values. Four microbial strains, E. coli (K88), Staphylococcus aureus (ATCC 29213), Salmonella Choleraesuis (ATCC 13312), and Salmonella Gallinarum (ATCC 9184), selected for MIC test were provided by the National Veterinary Research Quarantine Service (Anyang, Korea). Mueller-Hinton broth (Difco Laboratories, Detroit, MI) was used for adjustment of the organism suspension to a density of 0.5 McFarland standards (1.5 x 108 cfu/mL; Andrews, 2001). Each suspension was diluted with Mueller-Hinton broth (1:300, vol/vol) to obtain 5 x 105 cfu/mL. A 1-mL aliquot of the test organism and 1 mL of the prepared stock solution of potato protein powder were added and mixed in a 15-mL glass tube. After shaking, the glass tubes were incubated at 35°C for 16 to 20 h. The MIC endpoint was read as the lowest concentration of potato protein at which there was no visible growth of selected microorganisms.
Animals and Diets
The project was approved by the Animal Care and Use Committee of Kangwon National University.
In this experiment, 280 weanling pigs (Landrace x Yorkshire x Duroc; average BW of 6.42 ± 0.74 kg; 23 ± 3 d of age) from the same ancestry but mixed sex were allotted to 5 treatments, each composed of 4 pens, with 14 pigs in each pen. The pigs were housed in partially slotted and concrete floor pens, with a pen size of 1.90 x 2.54 m, with a self-feeder and nipple waterer to allow ad libitum access to feed and water. The main objective of this experiment was to compare the effect of a basal diet with antibiotics (positive control, PC) compared with the basal diet containing PP, and to study the effect of increasing level of PP in the basal diet. Dietary treatments were PC (basal diet with 150 mg/kg apramycin and 10 mg/kg colistin sulfate added), and the basal diet devoid of antibiotics with 0, 0.25, 0.50, or 0.75% PP.
The experimental diets were fed in 2 phases (phase I, d 0 to 14 and phase II, d 14 to 28 postweaning). Diets for phase I (Table 1) were formulated to contain 3,400 kcal/kg of ME and 1.65% Lys, as fed. Diets for phase II (Table 2) were formulated to contain 3,350 kcal/kg of ME and 1.43% Lys, as fed. All diets met or exceeded the nutrient requirements, as suggested by the NRC (1998).
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Individual weanling pig BW and feed disappearance from each pen were recorded at the end of every phase to calculate ADG, ADFI, and G:F. Chromium oxide (0.25%) was used as an indigestible marker in the diets for both phases to calculate digestibility coefficients, as described previously by Hahn et al. (2006). All pigs in all pens were fed diets mixed with chromic oxide on d 8 to 14 (phase I) and d 22 to 28 (phase II), with fecal grab samples collected from each pen on the last 3 d of each phase to determine the digestibility of DM and CP. The feces collected over a 3-d period were pooled to represent 1 pen. Feces were dried in a forced-air drying oven at 60°C for 3 d and ground to pass through a 1-mm screen using a hammer mill (Buhler, Switzerland) for chemical analysis.
To study the effect of the diets on apparent ileal amino acid digestibility, small intestinal morphology, and microflora of large intestinal digesta, representative pigs from each group (2 per pen), reflecting the average BW of the pen, were selected and slaughtered by electrocution at d 28. The digesta from the terminal ileum was collected and stored in specimen cups on ice, after which it was freeze-dried for amino acid analysis. The contents from the large intestine (cecum, colon, and rectum) were also collected in a sterile plastic bottle for microbial analysis. At regular intervals (d 0, 7, 14, 21, and 28) fresh fecal samples were collected from 2 pigs in each pen and utilized for measuring fecal bacterial counts. The samples collected for microbial analysis were immediately placed on ice until the analyses were conducted later on the corresponding day. The average of these 2 values was considered to represent 1 pen.
The samples of the intestinal segment from the regions of the duodenum, jejunum, and ileum after removal of their contents were flushed with physiological saline and submerged in a fixative solution (0.1 M collidine buffer, pH 7.3) containing 3% glutaraldehyde, 2% paraformaldehyde, and 1.5% acrolein and then brought to laboratory to study the morphological changes.
Chemical and Microbial Analyses
Analysis of the experimental diets and excreta was done according to the methods of the AOAC (1990). Chromium was measured with an automated spectrophotometer according to the procedure of Fenton and Fenton (1979). Amino acid analysis was performed by HPLC after acid hydrolysis (Knabe et al., 1989). Methionine and cystine were determined after oxidation with performic acid (Moore, 1963).
The microbiological assay of fecal samples and large intestinal digesta was carried out by the procedure suggested by Torrallardona et al. (2003). The microbial groups enumerated were total bacteria (plate count agar, Difco Laboratories, Detroit, MI), coliforms (violet red bile agar, Difco Laboratories) and Staphylococcus spp., (Baird-Parker agar, Merck, Darmstadt, Germany; supplemented with egg yolk tellurite emulsion (Oxoid, Hampshire, UK).
Histomorphometry
Three cross sections for each intestinal sample were prepared after staining with azure A and eosin using standard paraffin embedding procedures (Uni et al., 1998). A total of 10 intact, well-oriented, crypt-villus units were selected in triplicate for each intestinal cross section. Villus height was measured from the tip of the villus to the villus crypt junction, crypt depth was defined as the depth of the invagination between adjacent villi, and villus width was measured at the mid villus. All morphological measurements (villus height, crypt depth, and villus width) were made in 10-µm increments by using an image processing and analysis system (Optimus version 6.5 software, Media Cybernetics, North Reading, MA).
Immunity Test
To evaluate the humoral immune response, 2 pigs from each pen were injected i.m. with 2.5 mL of a suspension of 20% sheep red blood cells (SRBC) in PBS (pH 7.4) on d 14. Blood samples were taken by venipuncture at d 7 and 14 postinjection. Blood was centrifuged at 1,260 x g for 15 min; serum from each sample was collected, heat inactivated at 56°C for 30 min, and stored at –20°C until further analysis. Antibody titers to SRBC were determined using the microtiter hemagglutination assay, as described by Wegmann and Smithies (1966). Briefly, 50 µL of serum was added in an equal amount of PBS in the first column of a 96-well, V-shaped bottom plate and serially diluted (1:2, vol/vol). Then, 50 µL of the 2% SRBC suspension was added to each well. The serum and SRBC mixture was incubated for 30 min at 37°C. Antibody titers were expressed as log2 of the reciprocal of the greatest dilution showing agglutination of SRBC.
At d 28, 2 pigs per pen (8 per treatment) were randomly selected to perform the cutaneous basophil hypersensitivity (CBH) assay by using phytohaemagglutin-P (PHA-P; Sigma Chemical Co., St. Louis, MO), as described by Corrier and Deloach (1990). All pigs were intradermally injected at 5 cm from the midline on the right and left side and 5 cm caudal to the last teat. The right side was injected with 150 µg of PHA-P in 0.1 mL of PBS solution and the left side was injected with 0.1 mL of PBS to serve as the control. The thickness of the injected region was then measured with a vernier caliper after 18 and 42 h. The evaluation of the CBH response was determined by measuring the thickness of the injected region using 2 methods; CBH1 measured the difference in thickness of the skin before and after (i.e., at 18 and 42 h after) the PHA-P/PBS solution injection; CBH2 measured the difference between the PHA-P/PBS postinjection skin thickness and the PBS postinjection skin thickness.
Statistical Analyses
The data generated were analyzed as a randomized complete block design using the GLM procedure (SAS Inst. Inc., Cary, NC). An independent-sample t-test was used for comparing the PC to the 0.25, 0.5, and 0.75% PP. The linear and quadratic trends were tested for comparing the effects of increasing dietary PP levels (0 to 0.75%). Pens were the experimental unit for all analyses. For ileal amino acid digestibility, fecal and intestinal microflora, and the immunity studies, the values of each pen represented the average of 2 replicates. The bacterial concentrations and antibody titers against SRBC were log-transformed before statistical analysis. Comparisons with P < 0.05 were considered significant, and those with P < 0.10 are presented as trends.
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RESULTS |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The MIC of PP against different types of bacteria is demonstrated in Table 3. At the level 300 µg/mL, there was no visible growth of Salmonella Gallinarum, whereas 400 µg/mL inhibited the growth of E. coli and Salmonella Choleraesuis. The greater concentration of 500 µg/mL inhibited the growth of Staphylococcus aureus. Based on the results of MIC, PP obtained from the tubers of Gogu valley potato having antimicrobial activity was added in the diet at 0.25, 0.50 or 0.75% of the diet.
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Growth performance of pigs is presented in Table 4. In phase I, there were no differences in ADG and ADFI among PC and PP treatments. However, in comparison with PP, the pigs fed PC diets had improved G:F (P < 0.05). Also during phase I, linear improvements in ADG (P = 0.055) and ADFI (P = 0.086) with increasing dietary PP levels were noted. In phase II, no differences in ADG, ADFI, and G:F were observed when compared among PP and PC; however, ADG was greater (linear, P < 0.05) and there was a trend toward improved ADFI (linear, P = 0.073) and G:F (linear, P = 0.071) with the increase in the dietary PP levels. During the overall experimental period, PC had greater (P < 0.05) overall ADG and improved G:F (P = 0.090) than PP, whereas pigs fed PP had linearly greater overall ADG (P < 0.05), ADFI (P = 0.052), and improved G:F (P = 0.098).
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The digestibility of DM and CP is presented in Table 5. In phase I, PC treatment had greater DM digestibility (P < 0.01) and CP digestibility (P = 0.068) compared with PP, whereas feeding of PP had no linear or quadratic effect on DM and CP digestibility. In phase II the digestibility of DM and CP were greater (P < 0.01) in pigs fed PC diets than those fed PP diets, and feeding of PP diets linearly improved the DM digestibility (P < 0.05).
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The effect of PP on bacterial populations in feces is presented in the Table 7. The fecal populations of total bacteria at d 14 and coliform bacteria at d 14 and 28 were decreased (P < 0.05) in PC compared with PP; however, no differences were observed in the fecal populations of total bacteria, coliforms, and Staphylococcus spp. at d 0, 7, and 21 when compared among PC and PP. Feeding of PP was effective in decreasing the fecal populations of total bacteria, coliform bacteria and Staphylococcus spp. on d 28 (linear, P < 0.05) and d 14 (linear, P < 0.001), with a quadratic effect for Staphylococcus spp. (P < 0.05) and also a tendency to reduce the population of coliforms (quadratic, P = 0.058) in feces. On d 21, PP was effective in reducing fecal Staphylococcus spp. (linear, P < 0.05) and also showed a tendency toward decreasing the fecal populations of total bacteria (linear, P = 0.062) and coliform bacteria (linear, P = 0.071). At d 7, PP diets showed a tendency toward lowering the fecal populations of total bacteria (linear, P = 0.059) and Staphylococcus spp. (linear, P = 0.063).
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. In comparison with PP, the total bacteria and Staphylococcus spp. in cecal contents (P < 0.05), total bacteria in colon contents (P < 0.01) and coliforms in the content of the rectum (P < 0.01) were decreased in pigs fed with PC diets. Feeding of PP diets reduced the population of total bacteria (linear, P < 0.01), Staphylococcus spp. (linear, P < 0.05) and tended to decrease the coliforms (linear, P = 0.089) count in the contents of cecum. Similarly, increasing PP showed decreased populations of total bacteria and Staphylococcus spp. in the contents of colon (linear, P < 0.05) and decreased total bacteria, coliform bacteria, and Staphylococcus spp. (linear, P < 0.05) in the contents of the rectum.
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The cutaneous basophilic hypersensitivity (CBH) and the humoral immune response (HA titer) in pigs fed PC and PP diets is presented in Table 9. Both PC and PP had no effect on the CBH response. However, feeding of PP showed linear improvements in the CBH1 (linear, P = 0.081) at 18 h, CBH2 at 18 h (linear, P = 0.057) and 48 h (linear, P = 0.090). The response to SRBC was greater in PC (P = 0.054), whereas PP had a quadratic influence on the HA titer (P = 0.070).
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Dietary treatments had no effect on the villus height, crypt depth, villus height:crypt depth ratio and villus width of the duodenum, jejunum, and ileum of pigs (Table 10); however, in comparison with PP, the PC diets tended to decrease the crypt depth (P = 0.068) and increase the villus height:crypt depth ratio (P = 0.082) of the ileum, whereas PP diets linearly decreased the villus width of the duodenum (P = 0.087).
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DISCUSSION |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The MIC of 30 mg/kg for apramycin (Kang et al., 2003) and 2 mg/kg for colistin (Andrews, 2001) were considered, and their inclusion level as feed additive was 5 times their MIC. Similarly, for PP at the concentration of 500 mg/kg there was no visible growth of the bacterial spp. (Staphylococcus aureus, Salmonella Choleraesuis, Salmonella Gallinarum, and E. coli) and hence PP levels 5 times the MIC values (2,500 mg/kg) were used in this experiment.
In this experiment, as in others (Hathaway et al., 1996; Kendall et al., 2000; Weber et al., 2001), weanling pigs fed diets containing antibiotics had greater overall ADG. Feeding of potato proteins was also effective in linearly improving the overall ADG and ADFI. Borggreve and Cornelissen (1983) and Smits et al. (1991) reported improved gains in pigs fed potato protein as compared with those fed control diets. But the potato protein used in the present study was different from that used by previous researchers because it was obtained from a functional breed of potato (Gogu valley) that is known to possess antimicrobial activity (Kim et al., 2005) and was processed using protein extraction buffer so as to retain the protein having antimicrobial activity. Greiner et al. (2004) had reported that feeding of different AMP (lactoferrin, lactoferricin, lysozyme, neutrophil peptides, and purothionin) to rats had no effect on their performance in terms of BW gain, feed intake, and G:F in comparison with control diets. However, in their study Greiner et al. (2004) had fed these antimicrobials only for 3 d, which may not be sufficient for the antimicrobials to elicit growth response. The improved gain observed on feeding of antimicrobials in our study may be associated with increased feed intake and improved feed efficiency, as is also evident by a greater DM and CP digestibility and also nonsignificant, but numerically greater apparent ileal digestibility of both essential and nonessential amino acids in pigs fed PC and with increasing dietary PP levels.
In general, the bacterial populations in feces of weanling pigs at weekly intervals were comparable among PC and PP treatments, except for the populations of total bacteria at d 14 and coliforms at d 7 and 14. However, at d 14 and 28, PP treatments had linearly reduced fecal bacterial populations. On d 28, the efficiency of PP in reducing the coliforms in cecum and colon was comparable with PC, but antibiotics were more efficient in lowering the population of total bacteria in cecum and colon, and coliforms in rectum. Similarly, PP treatments had linear lower populations of total bacteria and Staphylococcus spp. in cecum and colon, and a linear decrease in total bacteria, coliforms, and Staphylococcus spp. in the rectum. These results suggest that PP significantly reduced the pathogenic bacteria, thereby confirming that the potato proteins of Gogu valley had antimicrobial activity.
It has been estimated that as much as 6% of the energy in a pig’s diet may be lost due to microbial fermentation in the stomach and intestine (Doyle, 2001). Antimicrobials added to feed alter activities of microbial populations by inhibiting the pathogenic bacteria and may thereby prevent loss of energy due to microbial fermentation (Francosis, 1962). Intestinal bacteria also inactivate pancreatic digestive enzymes and metabolize dietary protein with the production of ammonia and biogenic amines. At weaning, the pig faces several stressors, which may reflect in reduced feed intake and growth rate. Moreover, at weaning greater fluctuations in intestinal populations occur, which provide an opportunity for pathogenic coliforms and other bacteria for invasion and contributing to gastric disorders and hence reduced performance (Mathew et al., 1996). Antimicrobials added to feed may inhibit these activities and hence contribute to improved performance.
The antibacterial properties of antibiotics are well documented. Colistin is a decapeptide with a narrow spectrum of antibacterial activity mainly against gram-negative microorganisms and is also able to inactivate bacterial toxins in vitro; hence, it is commonly used for treatment of diseases caused by gram-negative bacteria. Andreotis et al. (1980) reported that apramycin, which is from the aminoglycoside class, was effective as a feed additive to control colibacillosis in postweaning pigs. In an experiment using weaned pigs, supplementation of antimicrobials (antibiotic and lactoferrin) were effective in significantly reducing the total viable counts of E. coli and Salmonella in the intestine (Wang et al., 2007).
The gut mucosal barrier is very important to growth and immunity in weanling pigs (Bosi et al., 2003). The structure of the intestinal mucosa can reveal information on gut health. Changes in the intestinal morphology such as shorter villus and deeper crypts have been associated with the presence of toxins (Xu et al., 2003). After weaning, the height of villus is generally reduced and crypt depth is increased (Nabuurs, 1993; Pluske et al., 1996), these morphological changes are primarily related to the low feed intake immediately after weaning (Kelly et al., 1991). The thinning effect of antibiotics on the gastrointestinal tract and an overall decrease in total gut mass has been known for many years (Braude et al., 1955; Taylor and Harrington, 1955; Yen et al., 1985). It has also been reported that pigs supplemented with antibiotics and lactoferrin had greater villus height and lower crypt depth at the small intestinal mucosa, which may contribute to improved growth performance (Wang et al., 2006). Contrary to the above findings, in the present study we did not find any morphological changes in the small intestine; however, there was a trend toward a decrease in crypt depth of the ileum due to antibiotics, and a similar trend toward a decrease in villus width due to PP. This suggests that in our study the improved performance of pigs fed diets containing antibiotics and PP are mainly due to the reduction of pathogenic bacteria.
The antimicrobial activity exhibited by potato proteins is likely due to the presence of several proteins such as the proteinase inhibitors that mediate defense against pathogens and invading organisms (Plate et al., 1993), which represents about 20 to 50% of the water soluble proteins in potato tuber (Pouvreau et al., 2001). These inhibitors accumulate in the potato tubers and leaves in response to mechanical wounding (Valueva et al., 2001), UV-radiation (Conconi et al., 1996), and lesions by insects (Bergey et al., 1996) or phytopathogenic microorganisms (Valueva et al., 2003). Peptides like snakin-1 (Segura et al., 1999) and snakin-2 (Berrocal-Lobo et al., 2002) purified from potato tubers were shown to be effective against fungal and bacterial plant pathogens. An antifungal protein purified from tubers of potato (Solanum tuberosum L. cv. Jopung) inhibited yeast fungal strains, including Candida albicans and Trichosporon beigelii (Park et al., 2005).
A potato protein, potamin-1 (PT-1) isolated from the tuber of potato (Solanum tuberosum L. cv. Gogu valley) by the extraction of water-soluble fraction had protease inhibitor and antimicrobial activity (Kim et al., 2005). This PT-1 is a 5.6 kDa trypsin-chymotrypsin protease inhibitor having 62% homology with serine protease inhibitor. Potamin-1 had the ability to inhibit trypsin, chymotrypsin, and papain, but had no hemolytic activity. These serine proteinase inhibitors may also have a role in regulation of inflammation, tissue repair and host defense (Hiemstra, 2002). The ethanol-water extract of the Gogu valley potato inhibited growth of C. perfringes and E. coli but had no effect on the growth of Bifidobacterium bifidum, B. breve, B. longum, and Lactobacillus casei when tested in vitro (Lim et al., 2004), whereas supplementation with antibiotic not only reduced the pathogenic bacteria but also reduced the beneficial bacteria (Blake et al., 2003). In contrast, administration of juice obtained from Gogu valley potato to human subjects increased the growth responses of Bifidobacterium and Lactobacillus and decreased growth of C. perfringes and E. coli (Lee, 2005).
The amino acid sequence of PT-1 revealed that it was made up of 6 Cys residues, thereby forming 3 disulfide bridges. On treatment of PT-1 with a reducing agent, dithiothreitol, the reduced PT-1 did not exhibit protease inhibitory activity, thus indicating that the disulfide bonds in PT-1 are essential for protease inhibition (Kim et al., 2005). A class of AMP named as defensins are polycationic peptides characterized by the presence of 6 conserved Cys residues forming 3 intramolecular disul-fide bridges and show a broad-spectrum activity against various bacteria, fungi, and enveloped viruses (Zhang et al., 2000). These defensins are produced by myeloid-derived cells and epithelial cells lining the gastrointestinal tract (Fellermann and Stange, 2001) and are chemo-tactic for monocytes, T lymphocytes, and dendritic cells (Yang et al., 2002). Defensins produced by cells in the course of innate host defense serve as signals which initiate, mobilize, and amplify adaptive immune host defenses. Administration of defensins with antigens to mice was shown to enhances cellular (Th1-dependent) and humoral (Th2-dependent) cytokine production and immune responses (Oppenheim et al., 2003). The exact mechanism by which potato proteins exhibit antimicrobial activities is not clear; however, mechanisms like pore formation and membrane depolarization, disruption of bacterial energy metabolism, and interference with biosynthetic pathways are suggested for the antimicrobial activity of various antimicrobial peptides containing disulfide bridges.
The results of this study demonstrate that feeding of potato protein obtained from a new potato variety with red skin, Gogu valley, to weanling pigs is an effective means of improving growth performance and reducing pathogenic bacteria; hence, it can be one of the novel alternatives to medicated food with antibiotics. However, further work is needed to identify the different peptides present in potato tuber and the mechanism by which they exhibit antimicrobial activity.
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Footnotes |
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2 Corresponding author: bjchae{at}kangwon.ac.kr
Received for publication July 10, 2007. Accepted for publication March 3, 2008.
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LITERATURE CITED |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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