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Parasitol Res (2011) 108:14111416 DOI 10.



In vitro antiplasmodial activity of ethanolic extracts of seaweed macroalgae against Plasmodium falciparum
Sundaram Ravikumar & Samuel Jacob Inbaneson & Palavesam Suganthi & Ramasamy Gokulakrishnan & Malaiyandi Venkatesan

Received: 9 November 2010 / Accepted: 19 November 2010 / Published online: 1 December 2010 # Springer-Verlag 2010

Abstract Malaria is a major health problem in many developing countries. The drugs resistant Plasmodium falciparum causes the most virulent form of malaria in humans and it is described as a public health disaster causing increased morbidity and mortality. Thirteen seaweeds species which belong to four different families (Rhodomelaceae, Cladophoraceae, Ulvaceae, and Caulerpaceae) were collected from Mandapam coastal area and the seaweeds extracts were tested for in vitro antiplasmodial activity against P. falciparum. Among them, Caulerpa toxifolia (IC50 5.06 gml1) showed potential antiplasmodial activity than other seaweeds extracts and it can be comparable with the positive control artemether (IC50 4.09 gml1). Caulerpa peltata (IC50 16.69 gml1) also exhibited good antiplasmodial activity and the IC50 value is lesser than the positive control chloroquine (IC50 19.59 gml1). Statistical analysis reveals that significant in vitro antiplasmodial activity (P <0.05) was observed between the concentrations and time of exposure. The chemical injury to erythrocytes was also carried out and it shows that no morphological changes in erythrocytes by the ethanolic extract of seaweeds extracts after 48 h of incubation. The in vitro antiplasmodial activity might be due to the presence of sugars, proteins, and phenols in the ethanolic extracts of seaweeds. It is concluded from the present study that, the ethanolic extracts of seaweeds of C.

toxifolia and C. peltata possesses lead compounds for development of antiplasmodial drugs.

Introduction Malaria is still the most important parasitic disease in the world and caused by the protozoans belonging to the genus Plasmodium. The Plasmodium falciparum causes severe malaria, and the protozoan comes in contact with humans by the bites of female Anopheles mosquitoes. Nearly 1 million deaths, mostly of children under the age of 5 years were caused by malaria. There are currently 109 malarious countries and territories, of which 45 are within the World Health Organization African region (WHO 2008). Although a number of advances have been made towards the understanding of the disease, relatively few antimalarial drugs have been developed in the last 30 years (Ridley 2002). Antimalarial drug resistance has spread and intensified over the years leading to a dramatic decline in the efficacies of the antimalarial drugs (Marsh 1998; Bloland and Ettling 1999). The majority of antimalarial drugs have been derived from plants such as quinoline-based antimalarials, artemisinin, and its derivatives. Several other pharmacologically active antimalarial compounds have been isolated from plants and are at different stages of development (Brandao et al. 1997; Valentin et al. 1997; Ogwal-Okeng 1998; Waako et al. 2005a, b, 2007; Sebisubi 2007). India boasts remarkable biodiversity and rich cultural traditions of plant use. Several seaweeds have shown a wide range of bioactive properties (Ravikumar et al. 2002, 2005, 2009, 2010a; Suresh Kumar et al. 2002; Jothibai Margret et al. 2009; Barbosa et al. 2007; Sultana et al. 2005; Ponce et al. 2003; Bazes et al. 2009) and in the present study we determined the antiplasmodial efficacy of

S. Ravikumar (*) : S. Jacob Inbaneson : P. Suganthi : R. Gokulakrishnan : M. Venkatesan School of Marine Sciences, Department of Oceanography and Coastal Area Studies, Alagappa University, Thondi Campus, Thondi623 409, Ramanathapuram District, Tamil Nadu, India e-mail:


Parasitol Res (2011) 108:14111416

ethanolic extracts of seaweeds against P. falciparum in an in vitro experimental system.

Material and methods Fresh samples of Laurencia papillosa, Laurencia curciata, Acanthophora specifera, Chaetomorpha antennina, Chaetomorpha torta, Chaetomorpha crassa, Ulva reticulata, Enteromorpha intestinalis, Ulva lactuca, Caulerpa racemosa, Caulerpa peltata, Caulerpa scalpelliformis, and Caulerpa toxifolia were collected from Mandapam (Lat. 9 45 N and Lon. 79 13 E) of South East coast of India and were botanically authenticated by Dr. K. Eswaran, Scientist, Central Salt and Marine Chemical Research Institute (CSMCRI), Mandapam Camp, Ramanathapuram District, Tamil Nadu, India. The family names and the percentage extracts and yields were described in Table 1. A sample voucher specimen was deposited in the herbarium facility (Sponsored by Indian Council of Medical Research, New Delhi) maintained in the Department of Oceanography and Coastal Area Studies, Alagappa University, Thondi Campus, Thondi, Ramanathapuram District, Tamil Nadu, India. All the collected samples were washed thrice with tap water and twice with distilled water to remove the adhering salts and other associated animals.

extraction was calculated by using the following formula: percentage of extraction=weight of the extract (gram)/ weight of the plant material (gram)100. The extracts of seaweeds were screened for the presence of phytochemical constituents by following the method of Sofowora (1982) and Kepam (1986). The seaweeds extracts were dissolved in dimethyl sulphoxide (HiMedia Laboratories Private Limited, Mumbai, India) and filtered through Millipore sterile filters (mesh 0.20 m, Sartorious Stedim Biotech GmbH, Germany). The filtrates were used for testing at different concentrations of 100, 50, 25, 12.5, 6.25, and 3.125 gml1 (Ouattara et al. 2006).

Parasite cultivation The antiplasmodial activity of plant extracts was assessed against P. falciparum obtained from the Jawaharlal Nehru Centre for Advanced Scientific Research, Indian Institute of Science, Bangalore, India. P. falciparum are cultivated in human 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 Laboratories Private Limited, Mumbai, India) and 40 gml1 of gentamycin sulfate (HiMedia Laboratories Private Limited, Mumbai, India). Hematocrits were adjusted at 5% and parasite cultures were used when they exhibited 2% parasitemia (Trager 1987).

Extract preparation Shade-dried seaweeds were subjected for percolation by soaking in ethanol and water mixture (3:1). After 21 days of dark incubation, the filtrate was concentrated separately by rotary vacuum evaporation (>45C) and then freeze dried (80C) to obtain solid residue. The percentage of
Table 1 Percentage of ethanolic extracts from seaweed species

In vitro antiplasmodial assay Filter-sterilized seaweeds extracts (100, 50, 25, 12.5, 6.25, and 3.125 gml1) were incorporated in 96-well tissue

Botanical name


Weight of plant (g)

Yield of extract (g) % 1.34 1.68 1.51 4.71 2.12 1.92 5.01 2.06 5.32 1.64 6.27 2.06 0.66

Laurencia papillosa Laurencia curciata Acanthophora specifera Chaetomorpha antennina Chaetomorpha torta Chaetomorpha crassa Ulva reticulata Enteromorpha intestinalis Ulva lactuca Caulerpa racemosa Caulerpa peltata Caulerpa scalpelliformis Caulerpa toxifolia

Rhodomelaceae Rhodomelaceae Rhodomelaceae Cladophoraceae Cladophoraceae Cladophoraceae Ulvaceae Ulvaceae Ulvaceae Caulerpaceae Caulerpaceae Caulerpaceae Caulerpaceae

36 41 62 39 34 36 134 20 31 80 39 43 62

0.48 0.69 0.94 1.84 0.72 0.69 6.71 0.41 1.65 1.31 2.44 0.89 0.41

Parasitol Res (2011) 108:14111416


culture plate containing 200 l of P. falciparum culture with fresh red blood cells diluted to 2% hematocrit. Negative control was maintained with fresh red blood cells and 2% parasitized P. falciparum diluted to 2% hematocrit, positive control was maintained with parasitized blood cells culture treated with chloroquine and artemether (Azas et al. 2002). Parasitemia was evaluated after 48 h by Giemsa stain and the average percentage suppression of parasitemia was calculated by the following formula: average% suppression of parasitemia=average% parasitemia in control average% parasitemia in test/average% parasitemia in control100.

Antiplasmodial activity calculation and analysis The antiplasmodial activity of seaweeds extracts was expressed by the inhibitory concentrations 50 (IC50), representing the concentration of drug that induced a 50% parasitemia decrease compared to the positive control culture referred as 100% parasitemia. The IC50 values were calculated (concentration of extract in X-axis and percentage of inhibition in Y-axis) using Office XP (SDAS) software with linear regression equation. This activity was analyzed in accordance with the norm of plants antiplasmodial activity of Rasoanaivo et al. (1992). According to this norm, an extract is very active if IC50 <5 gml1, active 5 gml1 <IC50 < 50 gml1, weakly active 50 gml1 <IC50 <100 gml1 and inactive IC50 >100 gml1.

Table 2. The extract of C. toxifolia (5.06 gml1) showed minimum level of IC50 value and followed by extract of C. peltata (16.69 gml1). The IC50 value of C. toxifolia extract is comparable to the positive control artemether (4.09 gml1) and C. peltata extract IC50 is less than the positive control chloroquine (19.59 gml1). Moreover, the extracts of L. curciata, C. torta, C. crassa, U. reticulata, and C. racemosa showed IC50 value of more than 100 gml1 (Table 2). The microscopic observation of uninfected erythrocytes added with the ethanolic extract of seaweeds and uninfected erythrocytes from the blank column of the 96-well plate showed no morphological differences after 48 h of incubation. The preliminary phytochemical study reveals that, the extracts from seaweeds have variety of phytochemical constituents, namely carboxylic acid, phenols, protein, and sugars (Table 3).

Discussion and conclusion Seaweeds provide a rich source of structurally diverse secondary metabolites. Several studies have demonstrated that seaweeds are an excellent source of components such as polysaccharides, tannins, flavonoids, phenolic acids, bromophenols, and carotenoids has exhibited different biological activities (Rodriguez-Bernaldo de Quiros et al. 2010). Seaweed extracts showed various bio potential activities such as antibacterial (Ravikumar et al. 2002, 2005, 2009; Suresh Kumar et al. 2002; Shehnaz 2003), antifungal (Ravikumar et al. 2009; Rao and Shelat 1982;

Chemical injury to erythrocytes To assess any chemical injury to erythrocytes that might be attributed to the extract, 200 l of erythrocytes were incubated with 200 gml1 of the extract at a dose equal to the highest used in the antiplasmodial assay. The conditions of the experiment were maintained as in the case of antiplasmodial assay. After 48 h of incubation, thin blood smears were stained with Giemsa stain and observed for morphological changes under high-power light microscopy. The morphological findings were compared with those in erythrocytes that were uninfected and not exposed to extract (Waako et al. 2007).
Table 2 IC50 value of seaweed extracts against P. falciparum Botanical name Laurencia papillosa Laurencia curciata Acanthophora specifera Chaetomorpha antennina Chaetomorpha torta Chaetomorpha crassa Ulva reticulata Enteromorpha intestinalis Ulva lactuca Caulerpa racemosa Caulerpa peltata Caulerpa scalpelliformis Caulerpa toxifolia Positive control Chloroquine Artemether IC50 (g ml1) 69.97 >100 39.94 51.08 >100 >100 >100 81.11 24.44 >100 16.69 27.34 5.06 19.59 4.09

Results The percentage yields of extracts were showed a range from 0.66 to 6.27% and were represented in Table 1. It reveals that, C. peltata (6.27%) showed maximum yield and followed by U. lactuca (5.32%). The IC50 values of the seaweeds extracts against P. falciparum strains are listed in

Sugars + + + + + + + + + + + + +

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Table 3 Phytochemical constituents in seaweed species

Phytochemical constituents

Carboxylic acid

Vidhyavathi and Sridhar 1991), antiviral (Ponce et al. 2003; Zhu et al. 2003), anti-inflammatory (Tan et al. 2000; Jothibai Margret et al. 2009), cytotoxic (Manilal et al. 2009; Shehnaz 2003), nematicidal (Manilal et al. 2009; Baqar Naqvi et al. 1992), antifeedant (Manilal et al. 2009), larvicidal (Manilal et al. 2009), phytotoxic (Shehnaz 2003), anticoagulant (Anand Ganesh et al. 2009), and spermicidal activities (Prakash 2004). Studies on antiplasmodial activities with seaweed extracts are too limited; in this connection, the present study was investigated with chosen seaweed extracts. Among the seaweeds, C. peltata and C. toxifolia were showed minimum IC50 values when compared with positive control chloroquine and artemether compounds respectively, this may be due to the presence of polysaccharides (Andrews et al. 2005; Clark et al. 1997; Xiao et al. 1996; Kisilevsky et al. 2002). The mechanism of action may be due to the inhibition of P. falciparum merzoites invasion into the erythrocytes (Adams et al. 2005) or disruption of P. falciparum rosettes (Carlson et al. 1992; Rowe et al. 1994). Ravikumar et al. (2010a) reported that, the seaweed Aegiceras corniculatum showed excellent in vitro and in vivo antiplasmodial activity. Ravikumar et al. (2010b) also reported that, the marine plants exhibited in vitro antiplasmodial activity. According to Rasoanaivo et al. (1992), these two seaweeds are having very active ingredients. Similar reports were identified by several authors (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. 2010a, b; Chenniappan and Kadarkarai 2010; Ramazani et al. 2010). These findings could encourage the carbohydrate-based drug development against antiplasmodial agents. It is concluded from the present study that the seaweeds which collected from South East coast of India showed enormous source for the identification of new drugs for the antiplasmodial activities. Investigations are in progress to identify the active antiplasmodial compounds of seaweeds extracts by bioassayguided fractionation.
Acknowledgments The authors are thankful to the authorities of Alagappa University for providing required facilities and also to Indian Council of Medical Research, New Delhi for financial assistance.

Tannins Steroids Resins Protein Xanthoproteins Saponins Phenols Quinones Flavonoids Coumarins Alkaloids

+ + + + + +

Laurencia papillosa Laurencia curciata Acanthophora specifera Chaetomorpha antennina Chaetomorpha torta Chaetomorpha crassa Ulva reticulata Enteromorpha intestinalis Ulva lactuca Caulerpa racemosa Caulerpa peltata Caulerpa scalpelliformis Caulerpa toxifolia

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