Screening of Five Brazilian Plants for Anti-inflammatory

and Antimicrobial Activities

Maria da Conceicao Torrado Truiti1, Ciomar Aparecida Bersani-Amado1, Benedito Prado Dias Filho2, Maria HelenaSarragiotto3, and Maria Conceicao de Souza4

1Departamento de Farm�aacia e Farmacologia; 2Departamento de An�aalises Clınicas; 3Departamento de Quımica;4Departamento de Biologia, Universidade Estadual de Maring�aa, Maring�aa, Brazil

Abstract

Ethanol extracts from the leaves of Cayaponia podanthaCogn. (Cucurbitaceae), Nectandra falcifolia (Nees) Casti-glioni (Lauraceae), and Paullinia elegans Cambess.(Sapindaceae), as well as from the aerial parts of Helic-teres gardneriana St. Hil. & Naud. (Sterculiaceae) andMelochia arenosa Benth. (Sterculiaceae), all naturallyoccurring species in the Brazilian part of the UpperParan�aa River and all belonging to genera used in folkmedicine, were screened for anti-inflammatory activityusing the carrageenan-induced pleurisy model in rats,and for antimicrobial activity using a broth microdilu-tion assay against Staphylococcus aureus, Bacillus subti-lis, Escherichia coli, Pseudomonas aeruginosa, Candidaalbicans, C. krusei, C. parapsilosis, and C. tropicalis. Inthe analysis of anti-inflammatory activity, a 500 mg=kgbody weight dose of the extracts of C. podantha, N. falci-folia, P. elegans, and H. gardneriana, administered orally(by gavage), reduced the volume of the inflammatoryexudates in rats induced by intrapleural injection.H. gardneriana also inhibited migration of leukocytesto the lesion site. Crude extract of M. arenosa was inef-fective on the intensity of the inflammatory response.Regarding antimicrobial activity, the best results wereobtained with N. falcifolia and M. arenosa against theGram-positive bacteria tested. N. falcifolia was activeagainst B. subtilis with a minimum inhibitory concen-tration (MIC) of 39 mg=ml and a minimum bactericidalconcentration (MBC) of 75 mg=ml and M. arenosa withMIC of 625 mg=ml against B. subtilis and MIC andMBC of 625 mg=ml against S. aureus. The resultsobtained demonstrate the importance of pharmacologi-cal studies with neotropical plants, and further research

into the specific components responsible for the observedbioactivities is under way.

Keywords: Anti-inflammatory activity, antimicrobialactivity, Cayaponia podantha, Helicteres gardneriana,Melochia arenosa, Nectandra falcifolia, Paullinia elegans.

Introduction

In terms of biodiversity, Brazil is one of the richest coun-tries on the planet, with more than 20% of the world bio-diversity located in its forests. It accounts for more than55,000 classified vegetable species; however, relativelyfew of these plants have been submitted to biologicalor pharmacological tests (Embrapa, 1996; Suffrediniet al., 2004; Wilson, 1988).

In the general floristic research carried out by Souzaet al. (2004) on the phytodiversity of the Upper Paran�aaRiver floodplain (Porto Rico, Paran�aa State, Brazil),specifically that carried out on the vascular plants of thatarea, 117 families and 652 species were registered. Manyof these plants are used in folk medicine, but few of themhave been studied scientifically.

Plants produce bioactive molecules that allow them tointeract with other organisms in their environment.Many of these substances are important in their defenseagainst herbivores and contribute to their resistance todiseases. Plants, therefore, can be promising sources ofantimicrobial agents.

Several vegetable species have been used popularlyfor the treatment of different types of infections and

Accepted: June 15, 2006

Address correspondence to: Maria da Conceicao Torrado Truiti, Departamento de Farm�aacia e Farmacologia, Universidade Estadualde Maring�aa, Av. Colombo, 5790, 87020-900 Maring�aa, PR, Brazil. Tel.: þ 55-32614301; Fax: þ 55-32634596. E-mail: mcttruiti@uem.br

DOI: 10.1080/13880200600879005 # 2006 Informa Healthcare

Pharmaceutical Biology2006, Vol. 44, No. 7, pp. 516–521

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inflammatory processes. Besides research on antimicro-bial substances, there has also been a significant search,by the pharmaceutical industry and research institutesfrom around the world, for anti-inflammatory agentsthat, besides being effective, present low toxicity andreduced adverse effects. Research with plants used in tra-ditional medicine, or plants related to them, can lead toan increase in the diversity of therapeutic agents.

Therefore, considering the importance of studies ontropical species, assays were performed, for the verifi-cation of the anti-inflammatory and antimicrobial activi-ties, with the ethanol extracts of five naturally occurringspecies of the area: Cayaponia podantha Cogn. (Cucurbi-taceae), popularly known as ‘‘taiui�aa,’’ Helicteres gard-neriana St. Hil. & Naud. (Sterculiaceae), ‘‘sacarrolha,’’Melochia arenosa Benth. (Sterculiaceae), ‘‘malva,’’ Nec-tandra falcifolia (Nees) Castiglioni (Lauraceae), ‘‘cane-linha,’’ and Paullinia elegans Cambess. (Sapindaceae),‘‘cip�oo-timb�oo.’’

Materials and Methods

Plant material

Plant material of the five species was collected in March2000 from different areas of the Upper Paran�aa Riverfloodplain: C. podantha (leaves) and H. gardneriana(aerial parts) from the Ivinhema River, municipal districtof Jatei (MS, Brazil), M. arenosa (aerial parts) from Gar-cas’ Lake, municipal district of Bataipora (MS, Brazil),N. falcifolia (leaves) from the Baıa River, municipal dis-trict of Taquarucu (MS, Brazil), and P. elegans (leaves)from Figueira’s Pond, municipal district of Porto Rico(PR, Brazil). Voucher specimens of each species havebeen deposited in the collection of the HNUP Herbarium(Nupelia, Universidade Estadual de Maring�aa, PR, Brazil;register numbers 1281; 2844; 1834; 1421, and 463,respectively).

Plant extraction

Plant material from each species was dried by airflow at40�C and powdered in a knife mill: C. podantha 200 g;H. gardneriana 450 g; M. arenosa 600 g; N. falcifolia580 g; and P. elegans 395 g. Crude extracts were preparedby percolation with ethanol at room temperature andwere dried under reduced pressure, obtaining 15.8, 32.7,71.0, 64.0, and 55.8 g of ethanol extracts, respectively.

Anti-inflammatory activity

Animals

Male Wistar rats weighting 180–200 g were used.The ani-mals were fasted for a period of 14 h before the singleadministration, orally (by gavage), of the extract

solutions (500 mg=kg of corporal weight). Simul-taneously, groups of control animals, treated withdimethylsulfoxide (DMSO; used in the dissolution ofthe extracts) and with indomethacin [the reference non-steroidal anti-inflammatory drug, which was adminis-tered orally (by gavage) in the dose of 5 mg=kg] wereevaluated.

Carrageenan-induced pleurisy

Pleurisy was induced by intrapleural injection of carra-geenan (200 mg), on the right side of the mediastinumbetween the third and fourth ribs, according to themethod of Vinegar et al. (1973). The carrageenan wasused in suspension form at 0.2% in sterile apyrogenic sol-ution of NaCl at 0.9%. Four hours after induction, therats were sacrificed and the skin and pectoral muscleretracted, leaving the rib cage exposed. A longitudinalincision was made between the third and fifth ribs oneach side of the mediastinum. The chest was openedand exudate was collected by aspiration and transferredto a conical centrifuge tube. The total volume of exudatewas determined and a 50-ml aliquot used to determine thetotal leukocyte count in a Neubauer chamber. Fordifferential cell counts, red blood cells were lysed bythe addition of Turk’s solution (Costacurta, 1969), andthe remaining fluid was centrifuged at 1500 rpm for10 min and cells resuspended in 0.1 ml of rat plasma.Exudate smears were prepared, air-dried, and fixed withRosenfeld stain (Rosenfeld, 1947).

Statistical analysis

The statistical analysis was carried out using the programGraphPad Prism, applying the Student’s t-test. Statisticalsignificance was set at p < 0.05.

Antimicrobial activity

Microorganisms and growth conditions

The following bacteria were used: Staphylococcus aureusATCC 25923, Bacillus subtilis ATCC 6623, Escherichiacoli ATCC 25922, and Pseudomonas aeruginosa ATCC15442. Cultures of these microorganisms were grown innutrient broth (Difco Laboratories, Detroit, MI, USA)at 37�C and maintained on nutrient agar slants at 4�C.The following yeasts, obtained from clinical material,were used: Candida albicans, C. krusei, C. parapsilosis,and C. tropicalis.

Reference antibiotics and antifungals

The following reference antibiotics and antifungals wereused: chloramphenicol, vancomycin, tetracycline, penicil-lin, and nystatin (Sigma Chemical Co., St. Louis, MO,USA).

Anti-inflammatory and antimicrobial activities of plants 517

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Susceptibility testing

The antimicrobial properties of the ethanol extracts wereevaluated by the broth microdilution procedure(NCCLS, 2000, 2002). The extracts were diluted inDMSO and Mueller-Hinton broth (1:9). Stock solutionsof the extracts and of the reference antibiotics were seri-ally diluted in Mueller-Hinton broth (Merck S.A., SaoPaulo, SP, Brazil). A volume of 100 ml of each dilutionwas added to the wells of a 96-well plate containing100 ml of the same medium. Each inoculum was preparedin phosphate saline 0.01 M, pH 7.2, at a density adjustedto a 0.5 McFarland turbid standard [108 colony-formingunits (CFU)=ml] and diluted 1:100 for the procedure.Next, 5 ml of the standardized microorganism suspen-sions were added in each well and the plates incubatedto 37�C for 24–48 h. Growth inhibition was evidencedby the absence of microbial growth in the medium,enabling determination of the minimal inhibitory concen-trations (MICs), that is, the lowest concentration of thesample capable of inhibiting in vitro microbial growth.Sample controls (Mueller-Hinton brothþmicrobialsample) and solvent controls (Mueller-Hinton brothþsolventþmicrobial sample) were carried out in parallel.Minimal bactericidal concentrations (MBCs) weredetermined by subculturing 10 ml of the content of thewell with the lowest concentration at which growth wasnot observed in Mueller-Hinton agar. After incubationat 37�C for 24–48 h, inhibition was evaluated. For theevaluation of antifungal activity, Sabouraud broth wasused as culture medium containing 104 to 106 CFU=mlof inoculum. After incubation to 37�C for 48 h, inhibitionwas evaluated.

Results

Anti-inflammatory activity

In the evaluation of anti-inflammatory activity of the fivespecies, the ethanol extract of M. arenosa, administeredorally (by gavage), in a daily dose of 500 mg=kg ofbody weight, did not provoke an effect on the intensity

of the inflammatory response induced by the intrapleuralinjection of carrageenan in rats. The results are presentedin Figure 1. On the other hand, treatment of the animalswith the ethanol extracts of H. gardneriana, C. podantha,P. elegans, and N. falcifolia, in the dose of 500 mg=kg, byoral route, reduced the volume of inflammatory exudatessignificantly, compared with the control animals. Thereductions were of 36.5%, 34.0%, 30.0%, and 25.0%,respectively. Indomethacin (5 mg=kg), used as the refer-ence drug, caused a reduction of 60% in the volume ofinflammatory exudate.

As observed, the ethanol extract of H. gardneriana,under the conditions used, not only reduced the volumeof inflammatory exudates but also inhibited themigration leukocytes to the location of the lesion, asevidenced by the reduction of cells present in the exudate(Table 1).

Figure 1. Effect of the ethanol extracts of Cayaponia podantha(Cp), Helicteres gardneriana (Hg), Melochia arenosa (Ma), Nectan-dra falcifolia (Nf), and Paullinia elegans (Pe), administered by oralroute (gavage) in the dose of 500 mg=kg of body weight, and ofindomethacin (Indo), in the dose of 5 mg=kg, on the volume ofexudate obtained in rats after carrageenan injection into thepleural cavity. �p < 0.05 compared with control groups (C) and��p < 0.05 compared with the indomethacin group (Student’st-test).

Table 1. Effect of the ethanol extracts of Cayaponia podantha (Cp), Helicteres gardneriana (Hg), Melochia arenosa (Ma), Nectandrafalcifolia (Nf), and Paullinia elegans (Pe), administered by oral route (gavage), in the dose of 500 mg=kg of body weight, and ofindomethacin, in the dose of 5 mg=kg, on the total and differential leukocytes counts.

Animal groups n Total leukocytes Mononuclear leukocytes Polymorphonuclear leukocytes

Control 16 61,040� 3918 13,340� 1352 47,700� 3456Indomethacin 8 64,630� 6522 9700� 1336 54,930� 5439Cp 15 55,860� 3980 11,190� 951,1 44,650� 4202Hg 5 41,500� 3694� 12,720� 1649 28,780� 2573�

Ma 20 63,310� 3205 13,350� 1156 49,960� 2862Nf 13 55,750� 2795 8292� 730,7 47,458� 2781Pe 5 53,900� 3616 10,110� 1425 43,790� 3725

n, number of test animals; �p < 0.05 compared with control groups (Student’s t-test).

518 M. da Conceicao Torrado Truiti et al.

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Antimicrobial activity

In relation to antimicrobial activity, the best results wereobtained for N. falcifolia and M. arenosa against theGram-positive bacteria tested (Table 2). The ethanolextract of N. falcifolia was active against B. subtilis, withMIC of 39 mg=ml and MBC of 78 mg=ml. The extract ofM. arenosa presented a MIC of 625 mg=ml against B. sub-tilis and MIC and MBC of 625 mg=ml against S. aureus.

The extracts showed no antifungal activity against theyeasts tested, under the conditions used.

Discussion

Medicinal plants and phytopreparations play an impor-tant role in the treatment and prevention of varioushuman diseases, mainly in the developing countries,where modern health services are limited (Lovkovaet al., 2001; Katewa et al., 2004). Research with plantsused in folk medicine, or related to them, has increasedall over the world, especially in developing countries, asan alternative form of health care.

In this paper, five naturally occurring Brazilian spe-cies, all belonging to genera with several species used intraditional medicine, were studied.

Among the species of the genus Cayaponia used in folkmedicine, C. espelina Cogn. and C. tayuya (Vell.) Cogn.(antisyphilitic, anti–snake venom, tonic, diuretic, anti-asth-matic, purgative, and depurative effects and to combatdiarrhea, bronchitis, pain, and epilepsy), C. pilosa Cogn.(antisyphilitic, emmenagogue, and purgative effects), andC. cabocla M. (as a purgative, depurative in cutaneous dis-eases, and emmenagogue) are noteworthy. Pharmacologi-cal studies have demonstrated the anti-inflammatoryactivity of C. tayuya (Correa, 1984; Rodrigues & Carvalho,2001; Lorenzi, 2002; Recio et al., 2004) and recently, in theassays performed by Truiti et al. (2005), the trypanocidalactivity of C. podantha has been verified.

Examples of popularly used species of the genusHelicteres are H. angustifolia (analgesic, anti-inflamma-

tory, and antibacterial effects), H. sacarolha Juss.(depurative and in syphilitic inflammations), H. isoraL. (as an expectorant, demulcent, astringent, antigalacta-gogue, anthelmintic, for the relief of the flu, in treatmentof chronic nephritis, dysentery, gastrospasm, empyema,stomach affections, and diabetes), and H. ovata Lam.(depurative, emollient, and antisyphilitic). Pharmaco-logical studies have demonstrated the hypoglycemicand hypolipidemic activities of H. isora L. (Correa,1984; Chang et al., 2001; Kamiya et al., 2001; Chakra-barti et al., 2002; Venkatesh et al., 2003, 2004; Katewaet al., 2004).

Some species of the genus Melochia that have beenused in traditional medicine are M. corchorifolia L. (dys-entery, abdominal swellings, and water-snake bites), M.umbellata (Houtt.) Stapf (deobstruent), and M. pyrami-data L. (bronchitis and cough) (Correa, 1984; Bhakuniet al., 1987; Lorenzi, 1991). In the research carried outby Truiti et al. (2005), M. arenosa presented trypanocidaland molluscicidal activities.

Species of the genus Nectandra have been used in folkmedicine for the relief of pain, arthritis, rheumatism, anddiarrhea and also as antifungals, and pharmacologicalstudies have demonstrated the antimalarial activity ofN. cuspidata Nees, vascular and antimalarial activitiesof N. salicifolia Nees, antitumoral activity of N. rigidaNees, analgesic and trypanocidal activities of N. megapo-tamica (Spreng) Chodat et Hassler (Le Quesne et al.,1980; Correa, 1984; Bohlke et al., 1996; Slish et al.,1999; Mu~nnoz et al., 2000; Silva Filho et al., 2004a,b),and antileishmanial activity of N. falcifolia, verified byTruiti et al. (2005).

Paullinia cupana H.B.K. and P. yoco Schultes & Killipare traditionally used to prepare stimulating beveragesand P. pinnata L. for the treatment of human malaria.Many other qualities are attributed to the famous Brazi-lian guaran�aa, P. cupana, such as, aphrodisiac, tonic, anti-diarrheic, and diuretic. Tests in animals have shown anantifatigue effect and improvement of mental perform-ance from this plant, and an antioxidant effect in vitrohas also been verified (Mattei et al., 1998; Abourashedet al., 1999; Carlini, 2003; Weckerle et al., 2003).

In this study, compared with the controls, oral admin-istration of ethanol extracts of H. gardneriana,C. podantha, P. elegans, and N. falcifolia inhibited devel-opment of the inflammatory response induced by pleuralinjection of carrageenan.

The ethanol extract of H. gardneriana also inhibitedleukocyte migration to the location of the lesion. Inter-estingly, this reduction was due to the decrease in thenumber of polymorphonuclear cells. On the other hand,no significant reduction in the number of leukocytes wasobserved for the other extracts or for indomethacin (ref-erence drug).

Steroidal and nonsteroidal drugs are commonly usedin the treatment of inflammatory diseases. Despite their

Table 2. Minimal inhibitory concentration (MIC) and mini-mal bactericidal concentration (MBC) of the ethanol extractsof Cayaponia podantha (Cp), Helicteres gardneriana (Hg),Melochia arenosa (Ma), Nectandra falcifolia (Nf), and Paulliniaelegans (Pe).

MIC (MBC) mg=ml

Plants S. aureus B. subtillis E. coli P. aeruginosa

Cp >1250 >1250 >1250 >1250Hg >1250 >1250 >1250 >1250Ma 625(625) 625(1250) >1250 >1250Nf 1250 39(78) >1250 >1250Pe >1250 >1250 >1250 >1250

Anti-inflammatory and antimicrobial activities of plants 519

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widespread use, nonsteroidal drugs are frequently asso-ciated with adverse effects; the most common being gas-trointestinal bleeding (Gepdiremen et al., 2004). Plantswith anti-inflammatory activity could increase thera-peutic agent diversity and effectiveness while givingreduced adverse effects.

The data of this study demonstrate that the extracts ofH. gardneriana, C. podantha, P. elegans, and N. falcifoliapresented important anti-inflammatory activity, whichcan be researched further in the future.

In the analysis of antimicrobial activity, the bestresults were obtained with the extract of the leaves ofN. falcifolia, which demonstrated activity against B. sub-tilis in concentrations below 100 mg=ml, presenting MICof 39 mg=ml and MBC of 75 mg=ml. The concentrationof 100 mg=ml is currently considered the appropriate con-centration for an antimicrobial extract (Suffredini et al.,2004). The extract of the aerial parts of M. arenosashowed moderate activity against S. aureus, presentingMIC and MBC of 625 mg=ml, and against B. subtilis, pre-senting MIC of 625 mg=ml. These results justify furtherresearch into these plants.

The incidence of severe nosocomial infections causedby Gram-positive bacteria has increased in the past dec-ades. This increase has been accompanied by theincreased resistance of these microorganisms to variousantimicrobials. The recent emergence of bacterial infec-tions and resistant strains has stimulated the investi-gation of plants as a source of new anti-infective agents(Truiti et al., 2003).

A large number of new antibiotics introduced on themarket have been obtained from natural or semisyntheticresources (Suffredini et al., 2004). It is also important tonote that besides the direct use of vegetable extracts, orsubstances isolated from them, there is also the possi-bility of their association with antibiotics in such a wayas to obtain a synergic effect, leading to new optionsfor the treatment of infectious processes.

The relevance of studies on tropical vegetable speciesis based on the countless results that have so far beenobtained. In addition to the increase in therapeuticoptions, the isolation of biologically active substancesis also worthy of note. The five species studied here havepreviously been evaluated regarding antiprotozoal andmolluscicidal activities (Truiti et al., 2005), and this studycomplements the research on the biological properties ofthese plants. Based on the results obtained, furtherresearch into the specific components responsible forthe observed bioactivities is already under way.

Acknowledgments

The authors are grateful to Dr. Carmen L. Crist�oobal andDr. Maria Silvia Feruci, Instituto de Botanica del Nor-deste, Corrientes, Argentina, and to Dr. Joao Batista

Baitelo, Instituto Florestal, Sao Paulo, SP, Brazil, foridentifying the plants.

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