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Antibacterial activity of vegetal extracts against serovars of Salmonella/ Atividade antibacteriana de extratos vegetais sobre sorovares de Salmonella.

INTRODUCTION

The last century was marked by efforts to search for compounds with therapeutic properties, giving the scientific community numerous substances that showed antimicrobial activity (EMEA 1999). The specific and rapid action of such antibiotics has promoted considerable progress, since they surpassed previously known drugs. However, the majority of antibiotics act as bacteria-selective agents, which increases bacterial resistance through genetic mutation.

Currently, there is concern about bacterial resistance to antibiotics. This concern is based on the gradual reduction of the number of efficient antibiotics, and on the toxic effects of the antibiotic's residues in animal products (CHAGAS, 2004; TRABULSI & ALTHERTHUM, 2005). In this context, there has been increased interest in studies searching for vegetal compounds that present antibacterial activity.

Among the numerous pathogenic bacteria with an antimicrobial resistant profile, Salmonella are important agents that cause foodborne diseases worldwide. Currently, there are 2,501 known serovars of Salmonella, some more restricted and adapted to a unique host, and others capable of infecting several species (FRANCO et al., 2005; TRABULSI & ALTHERTHUM, 2005).

The large numbers of serovars, the adaptation to several hosts, and the ability to acquire and transmit alleles of resistance to antimicrobials are some of the factors that contribute to the pathogenicity of Salmonella (TRABULSI & ALTHERTHUM, 2005). This picture requires control of the use of antimicrobials and research into new antimicrobials, with focus on human health and to reduce losses in animal production. Some studies (SOUZA et al., 2000; AVANCINI et al., 2000; CIRAJ et al., 2001; LOGUERCIO et al., 2005) have demonstrated the potential use of plant extracts with bactericidal or bacteriostatic for Salmonella. In the search for alternatives to conventional antibacterials, new plant species should be tested in order to identify which are more efficient as antimicrobial agents. The use of vegetal extracts represents a possibility which seems to be economically viable and ecologically safe for Salmonella control. The objective of this study was to evaluate in vitro the antimicrobial activity of some vegetal extracts against Salmonella serovars.

MATERIAL AND METHODS

Material sampling and preparation of vegetal extracts

The vegetal species used (Table 1) were collected in Concordia--Santa Catarina State, Brazil, except Caryophyllus aromaticus, which was acquired in a commercial establishment. Sampling procedure was performed in the morning between 7 and 8h, during March and May of 2007. All the sampled plants were located away from any chemical contaminants. Voucher specimens were prepared and kept in the Herbarium of the Universidade do Contestado-UnC, Concordia-Santa Catarina. The identification of the plants was carried out from the analysis of morphological characters and identification keys (BREMER et al., 2000; LORENZI & MATOS, 2002; THE ANGIOSPERM PHYLOGENY GROUP, 2003; SOUZA& LORENZI, 2005).

Sampled fresh vegetal portions were cleaned with a distilled-water wet paper towel and submitted to mechanical grinding. In order to obtain hydroethanolic extracts, a one-week extraction was performed using 1g of plant per 4mL of ethanol (80%). The solution was submitted to centrifugation (5 minutes at 540g), in order to remove suspended particles, then further incubated at 50[degrees]C for the evaporation of ethanol. The residual material was re-suspended in ethanol (80%) in a way that each mL contained the extract equivalent of 5g of the plant. This concentrate was centrifuged at 13000g and kept under refrigeration (VIEIRA et al., 2005; COELHO et al., 2003).

In vitro antibacterial activity evaluation.

Twenty serovars of Salmonella from the Animal Health Laboratory of Embrapa Swine & Poultry in Concordia, Santa Catarina State, Brazil were used (Table 2). The selecting tests for the extracts were performed by well diffusion method on plates (GROOVE & RANDALL, 1995). Aliquots of 0.1mL containing approximately [10.sup.6] colony-forming units (CFU) [mL.sup.-1] were spread with sterile swabs on the surface of plates with 10cm diameter containing nutrient agar. On each plate, six wells of 6mm diameter were prepared. Each well received 40 [micro]L of extract, diluted in a 1:5 ratio in 80% ethanol. This amount of extract corresponds to the extract obtained from 40mg of plant in its natural form. All tests were performed in duplicate. Nalidixic acid and 80% ethanol were used for positive and negative controls, respectively. The plates were kept in the refrigerator for one hour for diffusion of the extracts, and incubated for 18 to 24h at 37[degrees]C. Antibacterial activity was evaluated through reading of the growth inhibition zone.

The six extracts that showed activity in at least 70% of the serovars in the well diffusion method were submitted to the dilution technique for determining quantitatively the Minimum Inhibitory Concentration (MIC). Based on the results obtained in this study with the Myrtaceae family, the extract of Eucalyptus sp. was also included in the determination of MIC.

Determination of the Minimum Inhibitory Concentration (MIC) and the Minimum Bactericidal Concentration (MBC)

The tests were based on the technique of broth microdilution (ELOFF, 1998). Bacterial inoculation were standardized on 0.5 MacFarland's scale tube and diluted to 1:100. Aliquots (10mL) of the dilution were distributed in 96 wells microtiter plates containing 100mL of nutrient broth, obtaining approximately [10.sup.5] CFU [mL.sup.-1], with posterior addition of the extracts. The extracts were diluted in concentrations between 10 and 320mg [mL.sup.-1]. The plates were incubated at 37[degrees]C for a period of 18 to 24h. In order to evaluate the antibacterial activity, each well received 20 [micro]L of 0.5% triphenyl tetrazolium chloride, with reading being performed after one hour. MIC was identified visually and considered as the lowest concentration of the extract capable of inhibiting bacterial growth (SARTORATTO et al., 2004).

Determination of MBC was performed by inoculating 25 [micro]L of each dilution, with no apparent growth in MIC, in Brilliant Green Agar, with incubation (37[degrees]C) for a period of 18 to 24h. The presence of colonies was considered a evidence of bacteriostatic action, while the absence of colonies indicated bactericidal activity. MBC was considered on the plate which presented no bacterial growth (BARBOSA & TORRES, 1998). All tests were performed in duplicates.

RESULTS AND DISCUSSION

In vitro antibacterial activity evaluation

In the tested concentration, 85.7% of the extracts presented inhibitory activity against some serovar of Salmonella (Table 1). All serovars were susceptible to a minimum of five (25%) and maximum of 11 extracts tested (55%) (Figure 1).The six extracts that presented action against most of the serovars were the following ones: Punica granatum (Lythraceae), Achyrocline satureioides (Compositae), Eugenia jambolana, Eugenia uniflora, Caryophyllus aromaticus and Psidium araca (Myrtaceae) (Table 1). The extracts of Myrtaceae are among the five most active ones. The species of Myrtaceae and Lythraceae, belonging to the order Myrtales (BREMER et al., 2000; THE ANGIOSPERM PHYLOGENY GROUP, 2003) are genetically closely related, which could justify the similar behavior concerning inhibitory capacity.

[FIGURE 1 OMITTED]

Determination of Minimum Inhibitory Concentration (MIC) and Minimum Bactericidal Concentration (MBC)

The seven extracts submitted to MIC and MBC presented bacteriostatic activity and six of them showed bactericidal activity. Due to technical problems some extracts were not tested (NT) against all serovars, as shown in table 2. The extract of Caryophyllus aromaticus presented higher antimicrobial activity for MIC and MBC (Table 2, Figure 2). NASCIMENTO et al. (2000) also confirmed the inhibitory activity of this species against 64.2% of the evaluated bacteria, including S. Choleraesuis. Phytochemical composition performed by the authors detected the presence of eugenol, tannins and flavonoids, and tests with eugenol showed an inhibitory effect against S. Choleraesuis.

The antibacterial activity of Punica granatum was significant considering the bacteriostatic effect against all serovars (Table 2, Figure 2). Similar results with this species were obtained by MICHELIN et al. (2005) against several organisms. The antimicrobial potential of Punica granatum has been verified against several bacteria species (HOLETZ et al., 2002; MACHADO et al., 2002; MICHELIN et al., 2005; NASCIMENTO et al., 2000; VORAVUTHIKUNCHAI et al., 2005), however, no data have shown such activity against Salmonella. MACHADO et al. (2002) attributed the antimicrobial activity to the presence of punicalagin.

[FIGURE 2 OMITTED]

The extract of Eucalyptus sp. presented inhibition against 100% of the serovars tested, showing bactericidal effect on 42.1% of them. FRANCO et al. (2005) reported antimicrobial activity of Eucalyptus cinerea against five distinct bacteria and attributed such activity to the presence of 1-8 cineol or eucalyptol in its essential oil. Psidium araca presented bacteriostatic activity against all serovars and bactericidal activity to S. Derby, S. Enteritidis and S. Manhatan. No similar report has been found, indicating the need for more studies with this extract.

Eugenia jambolana demonstrated bacteriostatic activity against all serovars and bactericidal activity only against S. Pullorum. MICHELIN et al. (2005) described similar values for MIC, although against other bacterial species. LOGUERCIO et al. (2005) verified antimicrobial activity of E. jambolana against 17 bacterial isolates, including S. Typhi. NASCIMENTO et al. (2000) confirmed the inhibitory activity against 57% of 14 microorganisms tested, but not against S. Choleraesuis. Such variation in the activity of the plant extracts might be related to factors such as age, physiological state, part of the plant used, and season, which affects both the concentration and the metabolite groups present in the extracts (POSER & MENTZ, 2004; RAVEN et al., 2007).

The extract of Eugenia uniflora was bacteriostatic against 89.47% of the serovars (Table 2). Substances such as flavonoids, sesquiterpenes, tannins, antocianic pigments, and saponins were identified in its composition (LORENZI & MATOS, 2002). Tannins and saponins presented antimicrobial properties (LOGUERCIO et al., 2005; RAVEN et al., 2007; SANTOS & MELLO, 2003; VORAVUTHIKUNCHAI, 2005). Achyrocline satureioides presents bacteriostatic activity against 61.1% of the serovars (Table 2). POLYDORO et al. (2004) assessed the inflorescences of this species and confirmed that the hydroethanolic extracts presented high levels of flavonoids, whose effect, however, only retarded the bacterial multiplication.

The efficacy of each extract varied for different serovars. While S. London presented resistance to all extracts in MBC, S. Pullorum was the most susceptible serovar (Table 2). This serovar is present only in avian species, while the others are adapted to several different hosts. Different susceptibility of the serovars is probably related to defense mechanisms, since it is well known that bacteria can develop protection mechanisms such as changes in the permeability and structure of the cell wall, production of inhibitory enzymes, and alteration of the molecules attacked by the antibacterial (TRABULSI & ALTHERTHUM, 2005).

Some results obtained in the present tests to determine MIC and diffusion in agar doesn't have relation among each other does not present relationships with one another. Regarding the first, the best results were obtained with the extract of P. granatum, which inhibited all serovars. However, this result was not associated with the lowest MIC, which was obtained from the extract of C. aromaticus.

Similarly, some extracts, which were inactive in the agar diffusion test, presented activity in broth microdilution technique. This result is justified by the physical-chemical properties of the components of each extract, which could influence the diffusion of its components in the culture medium. Thus, in the case of plant extracts, the soleus diffusion in agar for assessing antimicrobial activity is not recommended. On the contrary, it can be used as orientation for selecting species with antimicrobial properties to determine the MIC and MBC, or even, to assess the results obtained in this study with the same sample.

CONCLUSION

The results obtained indicated that the vegetal extracts tested present potential antimicrobial activity with efficient properties in the inhibition of Salmonella, especially those from the Myrtaceae family. Such properties may be the object of further and specific studies for the identification and isolation of the active compounds or the assessment of their usefulness as therapeutic agents.

ACKNOWLEDGEMENTS

The authors want to thank for Fundo de Apoio a Pesquisa--FAP da Universidade do Contestado--UnC, Concordia, SC, for granting a scholarship to the first author. Laurimar Fiorentin (in memorian).

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VORAVUTHIKUNCHAI, S.P et al. Inhibitory effects of active compounds from Punica granatum pericarp on verocytotoxin production by enterohemorrhagic Escherichia coli O157: H7. J Health Sci, v.51, n.5, p.590-596, 2005. Available from: <http://jhs.pharm.or.jp/51(5)/51_590.pdf>. Accessed: Set. 23, 2006.

Daiane Voss-Rech (I, II) * Catia Silene Klein (I) Vania Helena Techio (III) Gerson Neudi Scheuermann (I) Gilberto Rech (II) Laurimar Fiorentin (I, IV)

(I) Empresa Brasileira de Pesquisa Agropecuaria (Embrapa) Suinos e Aves, Br 153, Km 110, Vila Tamandua, 89700-000, Concordia, SC, Brasil. E-mail: daiane@cnpsa.embrapa.br. * Autor para correspondencia.

(II) Universidade do Contestado (UnC), Concordia, SC, Brasil.

(III) Departamento de Biologia, Universidade Federal de Lavras (UFLA), Lavras, MG, Brasil.

(IV) In memorian.

Received 07.12.10 Approved 11.27.10 Returned by the author 01.19.11 Cr-3831
Table 1--Frequency of Salmonella serovars inhibited by plants extracts.

Vegetal species                          Common Names

Punica granatum L.                       Pomegranate
Eugenia jambolana Lam.                   Rose apple
Eugenia uniflora L.                      Surinam cherry
Caryophyllus aromaticus L.               Clove
Psidium araca Raddi                      Araca
Achyrocline satureioides (Lam.)          Macela
Rosmarinus officinalis L.                Rosemary
Cynara scolymus L.                       Artichoke
Salvia officinalis L.                    Common sage
Laurus nobilis L.                        Sweet bay
Bidens pilosa L.                         Hairy beggarticks
Baccharis trimera (Less.) DC             Carqueja
Plectranthus barbatus Andrews            Forskohlii
Sonchus oleraceus L.                     Annual sowthistle
Mikania glomerata Spreng.                Guaco
Taraxacum officinale F.H. Wigg.          Common dandelion
Emilia sonchifolia (L.) DC               Cupid's shaving-brush
Plantago australis Lam.                  Mexican plantain
Maytenus ilicifolia (Schrad.) Planch.    Holy-thorn
Aloe arbores cens Mill.                  Candelabra aloe
Malva sylvestris L.                      Common mallow

Vegetal species                          Family

Punica granatum L.                       Lythraceae
Eugenia jambolana Lam.                   Myrtaceae
Eugenia uniflora L.                      Myrtaceae
Caryophyllus aromaticus L.               Myrtaceae
Psidium araca Raddi                      Myrtaceae
Achyrocline satureioides (Lam.)          Asteraceae
Rosmarinus officinalis L.                Lamiaceae
Cynara scolymus L.                       Asteraceae
Salvia officinalis L.                    Lamiacae
Laurus nobilis L.                        Lauraceae
Bidens pilosa L.                         Asteraceae
Baccharis trimera (Less.) DC             Asteraceae
Plectranthus barbatus Andrews            Asteraceae
Sonchus oleraceus L.                     Lamiacae
Mikania glomerata Spreng.                Asteraceae
Taraxacum officinale F.H. Wigg.          Asteraceae
Emilia sonchifolia (L.) DC               Asteraceae
Plantago australis Lam.                  Plantaginaceae
Maytenus ilicifolia (Schrad.) Planch.    Celastraceae
Aloe arbores cens Mill.                  Liliaceae
Malva sylvestris L.                      Malvaceae

Vegetal species                          Used portion

Punica granatum L.                       Fruit
Eugenia jambolana Lam.                   Leaf
Eugenia uniflora L.                      Leaf
Caryophyllus aromaticus L.               Package content
Psidium araca Raddi                      Leaf
Achyrocline satureioides (Lam.)          Flowered aerial portion
Rosmarinus officinalis L.                Leaf
Cynara scolymus L.                       Leaf
Salvia officinalis L.                    Leaf
Laurus nobilis L.                        Leaf
Bidens pilosa L.                         Flowered aerial portion
Baccharis trimera (Less.) DC             Aerial portion
Plectranthus barbatus Andrews            Leaf
Sonchus oleraceus L.                     Flowered aerial portion
Mikania glomerata Spreng.                Leaf
Taraxacum officinale F.H. Wigg.          Flowered aerial portion
Emilia sonchifolia (L.) DC               Flowered aerial portion
Plantago australis Lam.                  Leaf
Maytenus ilicifolia (Schrad.) Planch.    Leaf
Aloe arbores cens Mill.                  Leaf
Malva sylvestris L.                      Leaf

                                          Inhibited
Vegetal species                          serovars (%)

Punica granatum L.                           100
Eugenia jambolana Lam.                       90
Eugenia uniflora L.                          90
Caryophyllus aromaticus L.                   75
Psidium araca Raddi                          75
Achyrocline satureioides (Lam.)              70
Rosmarinus officinalis L.                    62.5
Cynara scolymus L.                           55
Salvia officinalis L.                        45
Laurus nobilis L.                            44.4
Bidens pilosa L.                             42.1
Baccharis trimera (Less.) DC                 30
Plectranthus barbatus Andrews                15.8
Sonchus oleraceus L.                         10
Mikania glomerata Spreng.                    10
Taraxacum officinale F.H. Wigg.              5
Emilia sonchifolia (L.) DC                   5
Plantago australis Lam.                      5
Maytenus ilicifolia (Schrad.) Planch.        0
Aloe arbores cens Mill.                      0
Malva sylvestris L.                          0

Table 2--Minimum Inhibitory Concentration (MIC) and Minimum
Bactericidal Concentration (MBC) of vegetal extracts against serovars
of Salmonella

                                      Species

                      Achyrocline    Caryophyllus   Eucaliptus
Salmonella Serovars   satureioides    aromaticus       sp.

                              MIC/MBC (mg [mL.sup.-1])

S. Agona                240/>LD        40/160        120/>LD
S. Anatum               >LD/>LD        40/120        80/320
S. Cerro                >LD/>LD        40/120        80/320
S. Choleraesuis         NP/>LD         30/120        80/>LD
S. Cubana               160/>LD        20/60         60/>LD
S. Derby                320/>LD        60/80         60/320
S. Enteritidis          240/>LD        40/>LD        80/>LD
S. Give                 320/>LD        30/60         40/160
S. Heidelberg           240/>LD        30/40-60      160/>LD
S. Infantis             >LD/>LD        40/40-60      120/>LD
S. London               320/>LD        40/>LD        120/>LD
S. Manhattan            >LD/>LD        40/60         60/160
S. Meleagridis          320/>LD        30/>LD        80/320
S. Montevideo           >LD/>LD        40/60         80/>LD
S. Newport              320/>LD        40/320        40/>LD
S. Oranienburg          >LD/>LD        60/120        160>LD
S. Panama               160/>LD        30/120        60/320
S. Pullorum             320/>LD        10/80         40/320
S. Typhimurium          >LD/>LD        60/80         160/>LD

                                       Species

                       Eugenia    Eugenia    Psidium    Punica
Salmonella Serovars   jambolana   uniflora    araca    granatum

                              MIC/MBC (mg [mL.sup.-1])

S. Agona               160/>LD    240/>LD    80/NP     40/>LD
S. Anatum              160/>LD    160/>LD    80/>LD    80/>LD
S. Cerro               80/>LD     240/>LD    80/>LD    80/>LD
S. Choleraesuis        120/>LD    160/>LD    30/>LD    NP/>LD
S. Cubana              80/>LD     120/>LD    40/>LD    20/160
S. Derby               160/>LD    80/>LD     80/320    80/>LD
S. Enteritidis         120/>LD    160/>LD    80/320    80/>LD
S. Give                40/>LD     120/>LD    60/>LD    80/>LD
S. Heidelberg          80/>LD     120/>LD    60/>LD    80/>LD
S. Infantis            160/>LD    240/>LD    80/NP     240/>LD
S. London              160/>LD    >LD/>LD    80/>LD    120/>LD
S. Manhattan           160/>LD    160/>LD    80/320    80/>LD
S. Meleagridis         160/>LD    240/>LD    80/>LD    60/>LD
S. Montevideo          160/>LD    320/>LD    80/>LD    120/>LD
S. Newport             160/>LD    160/>LD    40/>LD    80/>LD
S. Oranienburg         160/>LD    160/>LD    160/>LD   80/>LD
S. Panama              160/>LD    160/>LD    80/>LD    40/>LD
S. Pullorum            40/240     120/240    80/>LD    40/60
S. Typhimurium         320/>LD    >LD/>LD    80/>LD    320/>LD

LD: Limit of detection (320mg [mL.sup.-1]); NP: Not performed.
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Author:Voss-Rech, Daiane; Klein, Catia Silene; Techio, Vania Helena; Scheuermann, Gerson Neudi; Rech, Gilbe
Publication:Ciencia Rural
Date:Feb 1, 2011
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