ORIGINAL PAPER

In vitro antiplasmodial activity of ethanolic extractsof mangrove plants from South East coast of Indiaagainst chloroquine-sensitive Plasmodium falciparum

Sundaram Ravikumar & Samuel Jacob Inbaneson &

Palavesam Suganthi & Murugesan Gnanadesigan

Received: 27 September 2010 /Accepted: 12 October 2010# Springer-Verlag 2010

Abstract Malaria is one of the most prevalent infectiousdiseases in the world. Treatment for malaria is commonlyinadequate due to the lack of quality assured effectivedrugs. The effectiveness of these drugs is declining at anever accelerating rate, with consequent increase in malariarelated morbidity and mortality. The newest antiplasmodialdrug from plants is needed to overcome this problem.Numerous mangroves and mangal associates are used asfolklore medicine to treat various human diseases. Themangrove plant species are a good source of potentialbioactive entities which exhibits many therapeutic proper-ties. The present study was carried out to test theantiplasmodial activity of five mangrove plant speciesdistributed along the South East coast of India. Bruguieracylindrica, Ceriops decandra, Lumnitzera racemosa,Rhizophora apiculata, and Rhizophora mucronata man-grove plant extracts exhibited in vitro antiplasmodialactivity against chloroquine-sensitive Plasmodium falcipa-rum. Of which, the ethanolic bark extract of R. mucronataexhibited high antiplasmodial activity (IC50=62.18 μg.ml−1).Statistical analysis reveals that, significant antiplasmodialactivity (P<0.05) was observed between the concentrationsand time of exposure. The chemical injury to erythrocyteswas also carried out and it shows that no morphologicaldifferences in erythrocytes by the ethanolic extract ofmangrove plants after 48 h of incubation. The screening forphytochemical constituents in the mangrove plants werecarried out and it reveals that, the presence of alkaloids,

triterpenes, flavonoids, tannins, catachin, anthroquinone,phenols, sugars, and proteins. This study shows that themangrove plants had a source of lead compounds for thedevelopment of new drugs for the treatment of malaria.

Introduction

Malaria is a curable and preventable disease, its prevalenceincreased in the 1980s and 1990s as the parasites developedresistance to the most frequently used antimalarial drugs(Le Bras and Durand 2003; Basco et al. 1995; Durand et al.1997; Parzy et al. 1997) and the vectors became resistant toinsecticides. Therefore, new drugs are urgently requiredto overcome malaria (Omulokoli et al. 1997; Rasoanaivoet al. 1992). Mangrove plants are specially adopted woodyplants found interface between land and sea (Kathiresanand Bingham 2001) possess several biological activitiessuch as antibacterial (Ravi Kumar et al. 2009; Raja 2009;Sivaperumal 2009; Muthuraja 2009), antifungal (RaviKumar et al. 2009), antiviral (Padmakumar and Ayyakkannu1997; Premanathan et al. 1996), antioxidant (Larson 1988;Masuda et al. 1999), antitumor (Hirazumi and Furusawa1999), and anticancer (Jongsuvat 1981). The present studyevaluated the antiplasmodial activity of five mangrove plantsagainst the chloroquine-sensitive Plasmodium falciparumstrain.

Materials and methods

Collection of plant materials

Fresh samples of different plant parts from Bruguieracylindrica, Ceriops decandra, Lumnitzera racemosa, Rhi-

S. Ravikumar (*) : S. Jacob Inbaneson : P. Suganthi :M. GnanadesiganSchool of Marine Sciences, Department of Oceanographyand Coastal Area Studies, Alagappa University,Thondi Campus, Thondi,623 409 Ramanathapuram District, Tamil Nadu, Indiae-mail: ravibiotech201321@gmail.com

Parasitol ResDOI 10.1007/s00436-010-2128-z

zophora apiculata, and Rhizophora mucronata were col-lected from Pichavaram mangrove forest (latitude 11° 27′ Nand longitude 79° 47′ E) and Karangkadu mangrove forest(latitude 9° 38′N and longitude 78° 57′ E) of South East coastof India. All the five mangrove plant samples were depositedin the Department of Oceanography and Coastal Area Studies,Alagappa University and voucher specimens are also main-tained. All the collected samples were washed thrice with tapwater and twice with distilled water to remove the adheringsalts and other associated animals. The authentication of theplant species were done by Prof. K. Kathiresan, Centre ofAdvanced Study in Marine Biology, Annamalai University,Porto Novo, Tamil Nadu, India.

Extract preparation

Shade-dried mangrove plants samples were subjected forpercolation by soaking in ethanol and water mixture (3:1).After complete extraction, the filtrates were concentratedseparately by rotary vacuum evaporation (>45°C) and thenfreeze dried (−80°C) to obtain solid residue. The percentageof extraction was calculated by using the following formula:percentage of extraction=weight of the extract (g)/weight ofthe plant material (g) ×100. The extracts of mangroves werescreened for the presence of phytochemical constituents byfollowing the method of Sofowora (1982) and Kepam (1986).The plant extracts were dissolved in dimethyl sulphoxide(HiMedia Laboratories Private Limited, Mumbai, India) andfiltered through Millipore sterile filters (mesh 0.20 μm,Sartorious Stedim Biotech GmbH, Germany). The filatratewas used for testing at different concentrations of 200, 100,50, 25, 12.5, 6.25, and 3.125 μg.ml−1 (Ouattara et al. 2006).

Parasite cultivation

The antiplasmodial activity of plant extracts was assessedagainst chloroquine-sensitive P. falciparum obtained fromthe Jawaharlal Nehru Centre for Advanced Scientific

Research, Bangalore, India. P. falciparum are cultivated inhuman O Rh+ red blood cells using RPMI 1640 medium(HiMedia Laboratories Private Limited, Mumbai, India)(Moore et al. 1967) supplemented with O Rh+ serum(10%), 5% sodium bicarbonate (HiMedia LaboratoriesPrivate Limited, Mumbai, India) and 40 μg.ml−1 ofgentamycin sulfate (HiMedia Laboratories Private Limited,Mumbai, India). Hematocrits were adjusted at 5% andparasite cultures were used when they exhibited 2%parasitemia (Trager 1987).

In vitro antiplasmodial assay

Filter sterilized extracts (200, 100, 50, 25, 12.5, 6.25, and3.125 μg·ml−1) were incorporated in 96-well tissue cultureplate containing 200 μl of P. falciparum culture withfresh red blood cells diluted to 2% hematocrit. Negativecontrol was maintained with fresh red blood cells and 2%parasitized P. falciparum diluted to 2% hematocrit,positive control was maintained with parasitized bloodcells culture treated with chloroquine (Azas et al. 2002).Parasitemia was evaluated after 48 h by Giemsa stain andthe average percentage suppression of parasitemia wascalculated by the following formula: average percentagesuppression of parasitemia=average percentage parasitemiain control−average percentage parasitemia in test/averagepercentage parasitemia in control×100. The IC50 valueswere calculated (concentration of extract in X-axis andpercentage of inhibition in Y-axis) using Office XP (SDAS)software with linear regression equation.

Chemical injury to erythrocytes

To assess any chemical injury to erythrocytes that might beattributed to the extract, 200 μl of erythrocytes wereincubated with 200 μg.ml−1 of the extract at a dose equalto the highest used in the antiplasmodial assay. Theconditions of the experiment were maintained as in the

Mangrove species Plant part Percentage of extraction IC50 μg.ml−1

Lumnitzera racemosa Leaf 12.35 110.93

Bruguiera cylindrica Leaf 15.84 173.75

Ceriops decandra Leaf 17.72 150.31

Rhizophora apiculata Bark 7.86 ≥200Rhizophora mucronata Bark 12.86 62.18

Ceriops decandra Collar 7.48 ≥200Rhizophora mucronata Collar 9.55 132.50

Rhizophora mucronata Stilt roots 11.91 119.37

Ceriops decandra Hypocotyl 6.49 123.25

Lumnitzera racemosa Stem 9.15 ≥200Chloroquine Control – 12.96

Table 1 Screening of mangroveextracts against Plasmodiumfalciparum

Values are found significantbetween concentrations and timeof exposure (P<0.05)

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case of antiplasmodial assay. After 48 h of incubation, thinblood smears were stained with Giemsa stain and observedfor morphological changes under high-power light micros-copy. The morphological findings were compared withthose in erythrocytes that were uninfected and not exposedto extract (Waako et al. 2007).

Results

The IC50 values of the mangrove extracts showed a rangeof inhibitory concentrations. The bark extract of R.mucronata (62.18 μg.ml−1) and leaf extract of L. racemosa(110.93 μg.ml−1) showed minimum level of IC50 values atsignificant (P<0.05) levels. Moreover, the bark extract ofR. apiculata, collar extract of C. decandra and stemextract of L. racemosa showed IC50 values greater than200 μg.ml−1 (Table 1).

The microscopic observation of uninfected erythrocytesincubated with the ethanolic extract of mangrove plants anduninfected erythrocytes from the blank column of the 96-well plate showed no morphological differences after 48 hof incubation. The phytochemical studies reveals that theextracts of mangrove plants have variety of phytochemicalconstituents, namely, alkaloids, triterpenes, flavonoids,tannins, catachin, anthroquinone, phenols, sugars, andproteins (Table 2), whereas some of the phytochemicalconstituents are restricted to certain mangrove plant speciesexcept the steroids which was not reported in all themangrove plant species.

Discussion and conclusion

The present study was undertaken to evaluate the in vitroantiplasmodial activity of five mangrove plants. The extractfrom bark of R. mucronata was shown to have maximum invitro antiplasmodial activity against chloroquine-sensitiveP. falciparum strains. The antiplasmodial activity exhibitedby the bark extract of R. mucronata was due to thesynergistic activity of one or more phytochemical constituents(Table 2). Clarkson et al. (2004) reported that the leaves andtwigs extracts of R. mucronata were showed antiplasmodialactivity against P. falciparum strain D10. In the presentstudy, the leaf extract of L. racemosa, leaf and hypocotylextracts of C. decandra, collar and stilt root extracts of R.mucronata and leaf extract of B. cylindrica were showed invitro antiplasmodial activity. Moreover, the IC50 values ofthe abovementioned extracts were showed greater than100 μg.ml−1 concentration; according to Rasoanaivo et al.(1992) the plant extract which shows in vitro activity morethan 100 μg.ml−1 is inactive. From the IC50 values, the barkextract of R. mucronata was showed IC50 value less than T

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Ceriops

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++

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−+

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++

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Rhizoph

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++

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Ceriops

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++

++

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+,present;−,absent

Parasitol Res

100 μg.ml−1 hence this can be used as an active antiplasmo-dial drug. Previously it has been reported that several plantsincluding polyherbal extracts has exhibited antiplasmodialactivities (Azas et al. 2002; Sanon et al. 2003; Son et al.2007; Moon 2007; Chung et al. 2008; Lee et al. 2009;Gansane et al. 2010; Ravikumar et al. 2010; Chenniappanand Kadarkarai 2010; Ramazani et al. 2010)

The mangrove plants are well known in the scientificliterature for its other biological activities. Ravi Kumar etal. (2009) reported that the leaf, bark, seedling, and flowerextracts from R. mucronata showed higher inhibitoryactivity against bacterial and fungal pathogens. Akalankaet al. (2002), Chou et al. (1977), and Padmakumar (1988)also reported that the leaf and bark extracts of R. mucronatashowed antibacterial compounds against human bacterialpathogens. The R. mucronata extract showed antiviralactivity against Semliki Forest virus (Premanathan et al.1995), Newcastle disease virus (Premanathan et al. 1993),Encephalomyocarditis virus (Premanathan et al. 1994),human immunodeficiency virus (Premanathan et al.1996, 1999a, b), and vaccinia virus (Premanathan et al.1999a). The extracts from R. mucronata of various partsshowed larvicidal activity against Culex quinquefasciatus(Subramonia Thangam and Kathiresan 1997) and Anophelesstephensi (Subramonia Thangam and Kathiresan 1988).

Alstonia macrophylla is a mangrove-associated plantspecies, exhibiting antiplasmodial activity due to an arrayof alkaloids present in the plant (Keawpradub et al. 1999).Over 100 alkaloids from higher plants were reported tohave significant antimalarial activity in studies publishedfrom 1990 to 2000 and some of which are more potent thanchloroquine (Saxena et al. 2003). Basak et al. (1996)reported that the extract from R. mucronata containsalkaloids, phenols, polysaccharides, and flavanoids whichmight be exerted the antiplasmodial activity againstchloroquine-sensitive P. falciparum. Many of the polyphe-nols are well documented to treat chronic diseases such ascardiovascular disease, cancer, diabetes, bacterial, andparasitic infections (Murakami et al. 1994; Sherman andBilling 1999; Scalbert 1991; Cowan 1999). Otoguro et al.(2004) reported that, polysaccharides, polyketides, andpolysaccharide derivatives (Prumycin) are having potentialantiplasmodial activity. The polysaccharides of higherplants possess immunostimulatory, anti-complementary,anti-inflammatory, hypoglycemic, and antiviral activities(Bandaranayake 2002).

Several classes of flavonoids play a significant role inmany physiological processes and show antioxidant andfungicidal activity (Larson 1988). The phytochemicalconstituents present in the bark extract of R. mucronata,especially alkaloids, terpenoids, polysaccharides, flavo-noids, and phenols might be responsible for the antiplas-modial activity. According to Hoet et al. (2004), the

presence of alkaloids and terpenoids might be responsi-ble for the antimalarial activity exhibited by Artemisiamaciverae and Artemisia maritima. The crude extractsisolated from mangrove plants exhibited potent in vitroantiplasmodial activity represent potential sources of newantiplasmodial drugs. The new tools for the treatment ofmalaria are badly needed considering the deterioratingglobal malarial situation and the continuing spread of drugresistance. This study indicates that, mangrove plants havea high potential for the production of lead compounds forthe development of antimalarials. It is concluded by thepresent study that, the ethanolic bark extract of R.mucronata possess significant suppressive effects on invitro cultures of chloroquine-sensitive P. falciparum.Further study is in progress to study the active principlesresponsible for this antiplasmodial activity.

Acknowledgments The authors are thankful to the authorities ofAlagappa University for providing required facilities and also toIndian Council of Medical Research, New Delhi for financialassistance.

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