Abstract
Plants continue to be a major source for new chemical entities to develop novel therapeutic agents. Large number of plants has been shown to be active in vitro against a variety of human pathogenic viruses or their near congeners. In several cases the active compounds have been isolated and characterized. Very few of them, however, have been investigated in detail in vivo or taken to the clinic. Pure compounds like andrographolide, curcumin and glycyrrhizic acid as well as extracts of Azadirachta indica have shown activity against several viruses and should be investigated further for their therapeutic potential. An analysis of available data from several hundred species indicates that antiviral activity is more likely to be found in plants belonging to certain families. It is necessary to screen more plants of these families which are available in India to obtain further leads.
Similar content being viewed by others
Introduction
Natural products have been, and continue to be, a major source of new chemical entities (NCE) for development of better therapeutic agents against infective and non-infective disorders. The bio-molecules are more stable, clinically more specific and available from renewable source [1]. Plants of Indian origin have provided several novel leads in the past [2] and are likely to yield more NCE in future also.
The contribution of natural products to anti-viral chemotherapy, however, has been more modest. Several factors have contributed to this scenario. Viral infections like the common cold are self limited and require only symptomatic treatment. Public health measures like vector control have succeeded in controlling vector transmitted infections. Similarly, development of effective vaccines has played a major role in eliminating diseases like small pox, near eradication of poliomyelitis and treatment of rabies. A major reason for limited input from Indian plants has been the non-availability of strict containment facility needed for such work at most institutions in the country. A large number of plants found in India have, therefore been investigated and found active in Japan, South Korea, US, etc. Data on all such plants also has been included in the present review along with analysis of data generated within the country. Plants active in viruses closely related to human virus [e.g. feline Human Immunodeficiency Virus (HIV) or duck hepatitis] have also been included. Maximum plants have been screened against Ranikhet disease (RNA) virus (RDV) and vaccinia (DNA virus) followed by herpes, HIV and hepatitis. The data in following sections has been arranged in the same order.
Most of the studies have used in vitro test systems and crude extracts of various parts of the plants. Pure compounds have been tested in some cases and in vivo procedures have been used in very few cases. In limited number of cases clinical studies also have been done. In several cases the name of the plant or family has been changed now. The name given in the original publication has been retained in the present review to avoid confusion but the names of family have been revised.
Ranikhet Disease and Vaccinia Viruses
CSIR Central Drug Research Institute Lucknow (CDRI) has been the pioneer institute to undertake large scale screening of Indian plants for anti-microbial and other biological activities using about 80 in vitro and in vivo tests. The program has used 50% ethanolic extracts of botanically authenticated plant samples. The extracts have been screened in vitro against one RNA virus (Ranikhet disease virus) and one DNA virus (vaccinia virus). Some samples have also been screened against encephalomyocarditis (EMCV), Japanese Encephalitis B (JE) and Semiliki Forest (SFV) viruses. Extracts showing high degree of activity were fractionated according to a standardized protocol to localize activity in one or more fractions. The results of testing 3,789 samples from 3,482 plants belonging to 233 families have been reported in a series of publications [3–14]. In addition, 967 of these plants were also tested for interferon-like activity against RD and vaccinia viruses [15]. A mid-term review of the work has also been published [16]. Antiviral activity was observed in 242 samples belonging to 96 families. The results have been summarized in Table 1. The plants have been listed under the appropriate families which have been arranged alphabetically. It also indicates plants where activity has been confirmed further in fractions or those exhibiting anticancer activity also.
Some of the active plants have been followed up at CDRI for isolation and characterization of the active constituents. The antiviral activity of (+) odorinol isolated from Aglaia roxburghiana has been reported by Joshi et al. [17]. Subsequently two new triterpinoids also have been isolated and characterized [18]. Lupeol has been identified as the active moiety of hexane fraction of Vicoa indica. It was effective against EMCV, RDV and SFV. Lupeol isolated from same fraction was active against RDV only [19]. Furomolligin isolated from Rubia cardifolia was active against EMCV [20].
The interferon like activity of five plants (Acacia auriculiformis, Cassia fistula, Olex polyama, Senecio tenuifolius and Zingiber capitatum) has been investigated further. The classical fractionation failed to localize activity in a particular fraction. The activity could be localized in each case in non-dialyzable fraction. It was destroyed on treating the fraction with trypsin. These results suggest the presence of an interferon-like or interferon inducing substance in the non-dialyzable fraction [15].
CDRI has also tested plants used as hepato-protective agents in traditional systems of Indian medicine for their anti-hepatitis B virus surface antigen (HBsAg) activity in serum of patients or carriers. Promising results were obtained with Phyllanthus amarus [21] and Picrorhiza kurroa [22–26]. These have been reviewed in the section on hepatitis virus.
Herpes Virus
Activity against herpes virus has been reported in 49 Indian plants. These have been listed in Table 2. The activity is distributed widely and the plants belong to 34 families. Most of them have been reported active against herpes-1 virus though a few are active against both herpes-1 and 2. In 12 cases the strain used has not been mentioned. Only four publications have reported in vivo activity. Pure isolated compounds have been tested in 26 cases. Two of the compounds glycyrrhizin and lupeol are active against other human viruses also and this has been indicated at appropriate places in this review. Unfortunately none of them appear to have been followed up further. The results have been published in 43 papers and only 9 of them are from Indian laboratories. Table 2 includes only those plants from foreign publications which are found in India.
Human Immunodeficiency Virus
Large number of papers has been published in recent years reporting anti-HIV activity in numerous natural products, partly because of the large screening program of US National Cancer Institute. Activity has been reported only in 38 Indian plants in 32 papers. These have been shown in Table 3 and belong to 28 families. Data on 41 materials has been reported and 24 of them are pure compounds. Most investigators (26) have studied the activity on HIV-1 and in 10 cases the strain has not been mentioned. HIV-2 has been included in two studies only. Two of the reported plants have been found active against feline immunodeficiency virus (FIV), a close congener of HIV. Most of the publications in this case also are from foreign laboratories and there are only seven Indian publications. There have been claims of usefulness of Ayurvedic and Siddha formulations in treatment of AIDS but no reliable clinical data is available either with these formulations or with the plants listed in Table 3. Data with Curcuma longa has not been included in this table because curcumin isolated from this plant and its several semi-synthetic and synthetic analogues have been tested. The data has been included in concluding remarks.
Hepatitis Viruses
Large number of medicinal plants has been used for treatment of hepatic disorders in most traditional system of medicine. The parameters generally followed were clearance of jaundice and return of liver function tests to normalcy. Clearance of viraemia in infective hepatitis, the commonest hepatic disorder, became an important parameter after the demonstration of carrier stage and possible induction of malignancy in such persons. One of the earliest demonstrations of viral clearance was provided by the pioneering studies of Thyagarajan et al. [106] with Phyllanthus amarus. This led to screening of large number of plants for activity against the virus. The availability of the duck model for in vivo studies materially facilitated these studies. Protective effect has been reported with 17 Indian plants belonging to 14 families. These have been listed in Table 4. Most of the plants have been tested against hepatitis B virus by several in vitro procedures. The active compound has been isolated and characterised in nine of these plants.
Several hepatoprotective plants have been tested for anti-hepatitis B virus surface antigen (HBsAg) activity in vitro using serum from patients or asymptomatic carriers harbouring the infection. Neutralizing activity has been reported with extract of Phyllanthus amarus [21]. A purified standardized extract (Picroliv) and a pure compound catalpol isolated from Picrorhiza kurroa were also found active while andrographolide (active constituent of Andrographis paniculata) and silymarin were inactive [22].
Clinical studies have been undertaken with some of the active plants in patients of infective hepatitis. As already reported above [23] efficacy of Picroliv has been demonstrated in Phase III multicentric trials. Beneficial effects have been reported with Phyllanthus amarus and glycyrrhizin also. These and other studies have been reviewed by Handa in a comprehensive publication [114] on hepatoprotective activity of Indian medicinal plants.
Respiratory Viruses
Interest in respiratory virus has increased following the recent epidemics of SARS and H1N1 infection. Activity has been reported in 18 Indian plants belonging to 16 families. Pure compounds isolated from plants have been tested in nine cases. Activity has been reported against five respiratory viruses. Activity against influenza has been observed in seven samples and against H1N1 in four cases. One sample was active against SARS. The data about active plants has been summarized in Table 5.
Pox Viruses
Interest in this group of viruses has continued because of continued occurrence of chicken-pox and measles infection. Only 14 plants have been reported active against a variety of pox viruses. These plants belong to 13 families. Glycyrrhizin from Glycyrrhiza glabra is the only pure compound reported active. Extract from Hibiscus sabdariffa is the only product showing activity against measles. Most of the extracts have been found active against fowl pox. Details of activity have been shown in Table 6.
Other Viruses
Activity in several Indian plants has also been reported against a variety of other viruses causing human infection or their close congeners. Table 7 shows such plants belonging to 24 families. In 10 cases pure compounds isolated from plants have been found active. The list includes 12 viruses. The preparations showing activity against chikungunya, Japanese encephalitis and rotavirus are of particular interest due to wide occurrence of these infections in the country and need to be investigated on a priority basis.
Concluding Remarks
The broad based biological screening program of CDRI had included tests for several other activities also with the same standardized protocol. An analysis of the results has shown that each particular activity was preferentially observed in certain families. The top 11 families for anti-viral activity and three other major activities have been arranged in rank order in Table 8. It will be observed that rank order is different for different activities even though some families exhibit more than one type of activity. The top 11 families in each case contain 35–45% of the plants for the concerned activity. The 11 families identified for anti-viral activity contain about 41% of the 242 active plants from 96 families. About 27% plants reported active against other viruses and included in Tables 2, 3, 4, 5, 6 and 7 also belong to these 11 families. It should be useful to screen other plants of these families to obtain more active plants. It will be evident from data in Tables 1 and 8 that many plants and families have both anti-viral and anticancer properties. It may be mentioned also that several smaller countries like Egypt [39], Nepal [43], Sudan [54] and Togo [27] have undertaken systematic evaluation of their flora for anti-viral activity following the lead given by CDRI.
It is evident from the data reviewed above that little effort has been made to study the marine flora around the vast Indian coast line for antiviral compounds. Several Indian mangrove plants (Ceriops decandra, Excocaria agallocha and three species of Rhizophora i.e. lamarckii, mucoranata and spiculata) have been reported to exhibit potent anti-HIV activity [142] highlighting the need of further exploration of this valuable resource.
Most of the data reported in this review is from in vitro studies and the leads do not appear to have been followed up. This is partly because of lack of suitable animal models for several infections and partly due to lack of the requirement containment facility in majority of Indian institutions. It is suggested that multi-pronged strategy should be adopted to utilise these leads. There are certain viral infections like Japanese encephalitis, chikungunya or rotavirus which are major national concern. Only few leads are available against them and these need to be followed.
A number of pure compounds have demonstrated activity against several viral infections. These are compounds of varying chemical complexity ranging from simple compounds like curcumin to complicated structures like iridoids glycosides. Adequate attention has not been paid to use them as basic templates to optimise the activity in synthetic or semi-synthetic derivatives. Successful use of this strategy has been made in the case of andrographolide [143] and curcumin [136], for example.
Activity has also been reported in certain compounds which have undergone extensive clinical evaluation in non-viral diseases. Their available safety and dosage regimen data would help in initiating clinical evaluation in viral infection where in vitro or in vivo activity data is available. Andrographolide is a potent hepatoprotective agent [114] besides being active against herpes [30], influenza and H1N1 infections [116]. Dehydroandrographolide succinic acid monoester is active against HIV [143]. Another clinically authenticated hepatoprotective agent Picroliv [23] is also active against several viral infections including hepatitis B [24–26]. Curcumin has received the maximum attention after its activity against HIV was demonstrated. Large number of semi-synthetic or synthetic derivatives have been prepared and tested for anti-HIV activity. Its boron complexes; semi-synthetic reduced curcumin, allyl curcumin and tocopheryl-curcumin and synthetic analogues dicafferoyl methane and rosemarinic acid are highly active against HIV in a variety of in vitro protocols. Curcumin is active against herpes simplex 2 in a mouse model and Human papilloma and Epstein Barr viruses in vitro. These activities have been reviewed recently by Krishnaswamy [136]. Its in vitro activity against Friends leukaemia [25], Newcastle and Poliomyelitis viruses [120] has also been reported. Fiore et al. [41] in a recent review have provided reference for activity of glycyrrhizin and its analogues against herpes, hepatitis (including clinical trial), influenza, respiratory syncytial, SARS and vesicular stomatitis viruses. Other investigators have found it active against Japanese encephalitis [137], poliomyelitis [138], vaccinia and varicella [130]. It perhaps has the widest spectrum of antiviral activity among the natural products so far investigated. Adequate clinical evaluation is necessary to assess its role in treatment of viral disorders. Azadirachta indica also is a promising plant, even though most of the studies have used its extract. It has a variety of compounds and also has a long history of use in traditional medicine in many countries of the world. The viruses against which the extracts or some of the isolated compounds have shown activity include chikungunya, fowl pox, measles, vaccinia [128], buffalo pox [127], Coxsackie [134] and herpes [32]. Detailed studies against some of these viruses, specially herpes and chikungunya are strongly warranted. In conclusion it may be stated that the rich and valuable resource of Indian plants needs to be more extensively exploited to provide new drugs for the treatment of viral disorders.
References
Dhawan BN (2005) Biodiversity as a source of new chemical entities. In: Tandon P, Sharma M, Swaroop R (eds) Biodiversity status and prospects. Narosa Publishing House, New Delhi, pp 25–34
Mukherjee PK, Rai S, Kumar V, Hylands PJ, Hider RC (2007) Plants of Indian origin in drug discovery. Expert Opin Drug Discov 2:637–653
Dhar ML, Dhar MM, Dhawan BN, Mehrotra BN, Ray C (1968) Screening of Indian plants for biological activity. Part I. Indian J Exp Biol 6:232–247
Bhakuni DS, Dhar ML, Dhar MM, Dhawan BN, Mehrotra BN (1969) Screening of Indian plants for biological activity. Part II. Indian J Exp Biol 7:250–262
Bhakuni DS, Dhar ML, Dhar MM, Dhawan BN, Gupta B, Srimal RC (1971) Screening of Indian plants for biological activity. Part III. Indian J Exp Biol 9:91–102
Dhar ML, Dhar MM, Dhawan BN, Mehrotra BN, Srimal RC, Tandon JS (1973) Screening of Indian plants for biological activity. Part IV. Indian J Exp Biol 11:43–54
Dhar ML, Dhawan BN, Prasad CR, Rastogi RP, Singh KK, Tandon JS (1974) Screening of Indian plants for biological activity. Part V. Indian J Exp Biol 12:512–523
Dhawan BN, Patnaik GK, Rastogi RP, Singh KK, Tandon JS (1977) Screening of Indian plants for biological activity. Part VI. Indian J Exp Biol 15:208–219
Dhawan BN, Dubey MP, Mehrotra BN, Rastogi RP, Tandon JS (1980) Screening of Indian plants for biological activity. Part IX. Indian J Exp Biol 18:594–606
Aswal BS, Bhakuni DS, Goel AK, Kar K, Mehrotra BN, Mukherjee KC (1984) Screening of Indian plants for biological activity. Part X. Indian J Exp Biol 22:312–332
Aswal BS, Bhakuni DS, Goel AK, Kar K, Mehrotra BN (1986) Screening of Indian plants for biological activity. Part XII. Indian J Exp Biol 24:48–68
Bhakuni DS, Goel AK, Jain S, Mehrotra BN, Patnaik GK, Prakash V (1988) Screening of Indian plants for biological activity. Part XIII. Indian J Exp Biol 26:883–904
Bhakuni DS, Goel AK, Goel AK, Jain S, Mehrotra BN, Srimal RC (1990) Screening of Indian plants for biological activity. Part XIV. Indian J Exp Biol 28:619–697
Aswal BS, Goel AK, Kulshreshtha DK, Mehrotra BN, Patnaik GK (1996) Screening of Indian plants for biological activity. Part XV. Indian J Exp Biol 34:444–467
Babbar OP, Joshi MN, Madan AR (1982) Evaluation of plants for antiviral activity. Indian J Med Res 76(S):54–65
Rastogi RP, Dhawan BN (1990) Anticancer and antiviral activities in Indian medicinal plants: a review. Drug Dev Res 19:1–12
Joshi MN, Chowdhary BL, Vishnoi SP, Shoeb A, Kapil RS (1987) Antiviral activity of (+)-oderinal. Planta Med 53:254–255
Vishnoi SP, Shoeb A, Kapil RS (1988) New cycloarterenol derivatives from Aglaia roxburghiana. Planta Med 54:40–41
Chowdhary BL, Hussaini FA, Shoeb A (1990) Antiviral constituents from Vicoa indica. Int J Crude Drug Res 28:121–124
Rastogi SN, Kulshreshtha DK (eds) (2001) Fifty years of research and development 1951–2001. Vol. 2 Drug development. Central Drug Research Institute, Lucknow, p 320
Mehrotra R, Rawat S, Kulshreshtha DK, Goyal P, Patnaik GK, Dhawan BN (1991) In vitro effect of Phyllanthus amarus on hepatitis B virus. Indian J Med Res 93:71–74
Mehrotra R, Rawat S, Kulshreshtha DK, Patnaik GK, Dhawan BN (1990) In vitro studies on the effect of certain natural products against hepatitis B virus. Indian J Med Res 92:133–138
CSIR-CDRI Newslett (2011) 3:2
Dhawan BN (1995) Picroliv—a new hepatoprotective agent from an Indian medicinal plant, Picrorhiza kurroa. Med Chem Res 5:595–605
Harikumar KB, Kuttan G, Kuttan R (2008) Inhibition of progression of erythroleukemia induced by Friend’s virus in BALB-C mice by natural products—berberine, curcumin and picroliv. J Exp Ther Oncol 7:275–284
Kapadia GJ, Sharma SC, Tokuda H, Nishio H, Veda S (1996) Inhibitory effect of iridoids on Epstein-Barr virus activation by a short term assay for antitumor promoters. Cancer Lett 102:223–226
Ananil K, Hudson JB, de Souzal C, Akpaganal K, Tower GHN, Arnason JT, Gbeassor M (2000) Investigation of medicinal plants of Togo for antiviral and antimicrobial activities. Pharm Biol 38:40–45
Lipipun V, Kurokawa M, Suttisri R, Taweechotipatr P, Pramyothin P, Hattori M, Shiraki K (2003) Efficacy of Thai medicinal plant extracts against herpes simplex virus type 1 infection in vitro and in vivo. Antiviral Res 60:175–180
Zandi K, Zadeh MA, Sartavi K, Rastian Z (2007) Antiviral activity of Aloe vera against herpes simplex virus type 2, an in vitro study. Afr J Biotechnol 6:170–1773
Jarukamjorn K, Nemoto N (2008) Pharmacological aspects of Andrographis paniculata on health and its major diterpinoid constituent andrographolide. J Health Sci 54:370–381
Pavitra PS, Sreevidya N, Verma RS (2009) A review of chemistry and biological activity of genus Atlantia (Rutaceae). J Med Aromat Plant Sci 31:63–72
Tewari V, Darmani NA, Yue By JT, Shykla D (2010) In vitro antiviral activity of neem (Azadirachta indica) bark extract against herpes simplex type-1 infection. Phytother Res 24:1132–1140
Suksamram S, Wongkrajang K, Kritikara K, Suksamram A (2003) Iridoid glycosides from flowers of Barleria lupulina. Planta Med 69:877–879
Jain R, Nagpal S, Jain S, Jain SC (2004) Chemical and biological evaluation of Bauhinia species. J Med Aromat Plant Sci 26:48–50
Parmar KA, Prajapati SN (2009) HPTLC-aided phytochemical finger printing analysis as a tool for evaluation and antiviral activity using Hela cell cultures of Bauhinia variegata plant. Asian J Exp Chem 4:74–77
Chiang C-C, Chang J-S, Chen C-C, Ng L-T, Lin C-C (2003) Anti-herpes simplex virus activity of Bidens pilosa and Hottuynia cordata. Am J Chin Med 31:355–362
Loizzo MR, Saab A, Tundis R, Stalli Ga, Lampronti H, Menchini F, Gambiari R, Cinalt J, Doern HW (2008) Phytochemical analysis and in vitro evaluation of the biological activity against herpes simplex type 1 (HSV-1) of Cedrus libani A. rich. Phytomedicine 15:79–83
Balasubramanian P, Jayalakshmi K, Vidhya N, Prasad R, Khaleefatullah S, Kathiravan G, Rajagopal K, Sureban SM (2010) Antiviral activity of ancient system of ayurvedic medicinal plant Cissus quadrangularis L. (Vitaceae). J Basic Clin Pharm 1:37–40
Soltan MM, Zaki AK (2009) Antiviral screening of forty-two Egyptian medicinal plants. J Ethnopharmacol 126:102–107
Hohmann J, Redei D, Mathe I, Molnar J, Musi I, Evanics F, Dombi G (2000) Diterpene polyesters with antiviral activity from Euphorbia peplus and Euphorbia serrulata. Phytomedicine 7(S II):85
Fiore C, Eisenhut M, Krausse R, Ragazzi E, Pellati D, Armanini D, Bielenberg J (2008) Antiviral effects of Glycyrrhiza species. Phytother Res 22:141–148
Singh B, Sharma PA (2007) Antineoplastic and antiviral activities of pyrrolizidine alkaloids from Heliotropium marcifolium Koen. cc Retz. Proc Natl Acad Sci India Sect B 71B:197–205
Rajbhandari M, Wegner U, Julich M, Schopke T, Mentel R (2001) Screening of Nepalese plants for antiviral activity. J Ethnopharmacol 76:251–255
Chou SC, Su CR, Ku YC, Wu TS (2009) The constituents and their bioactivities of Houttuynia cordata. Chem Pharm Bull 57:1227–1230
Vijayan P, Raghu C, Ashok G, Dhanraj SA, Suresh B (2004) Antiviral activity of medicinal plants of Nilgiris. Indian J Med Res 120:24–29
Gebre-Mariam T, Neubert R, Schimdt PC, Wutzler P, Schmidtke M (2006) Antiviral activities of some Ethiopian medicinal plants used for the treatment of dermatological disorders. J Ethnopharmacol 104:182–187
Petrera E, Cotoce CE (2009) Therapeutic effect of meliacine, an antiviral derived rom Melia azaderach L in mice genital herpes infection. Phytother Res 23:1771–1777
Alche LE, Banquero AA, Sanjuan NA, Coto CE (2002) An antiviral principle present in a purified fraction from Melia azaderach L leaf aqueous extract restrains herpes simplex virus type I propagation. Phytother Res 16:348–352
Schumacher A, Reichling J, Schnitzler P (2003) Virucidal effect of peppermint oil on enveloped viruses herpes simplex type I & II in vitro. Phytomedicine 10:504–510
Belvin A, Gbeassor M, Akpagane K, de Sousa K, Kaumaglo K, Arnason JT (2005) Ethnomedical uses of Momordia charantia (Cucurbitaceae) in Togo and relation to its phytochemistry and biological activity. J Ethnopharmacol 96:49–55
Cheng HY, Lin TC, Ishimaru Y, Yang CM, Wang KC, Lin CC (2003) In vitro antiviral activity of prodelphinirdin B-2,3,3′-Di-O-gallate from Myrica rubra. Planta Med 69:53–56
Ooi LSM, Sun SSM, Ooi VEC (2004) Purification and characterization of a new antiviral protein from the leaves of Pandanus amaryllifolius (Pandanaceae). Int J Biochem Cell Biol 36:1440–1446
Rasham IJ, Aday MH, Khazraji ALT (1989) In vitro antiviral activity of the aqueous extract from the seeds of Peganum harmala. Fitoterapia 60:365–367
Xiang Y, Rei Y, Qb C, Lai Z, Xiong S, Zhang Y, Yang C, Wang D, Liu Q, Kitazato K, Wang Y (2011) In vitro anti herpes simplex activity of 1,2,4,6-tetra-O-galloyl-β-d-glucose from Phyllanthus emblica (Euphorbiaceae). Phytother Res 25:975–982
Yang CM, Cheng HY, Lin TC, Chiang LC, Lin CC (2007) The in vitro activity of geranium and 1,3,4,6-tetra-O-galloyl-β-d-glucose isolated from Phyllanthus urinaria against herpes simplex virus type I and type II infection. J Ethnopharmacol 110:555–558
Linn CC, Cheng HY, Fang BJ (2003) Anti-herpes virus type 2 activity of herbal medicines from Taiwan. Pharm Biol 41:259–262
Ding CX, Hayashi K, Lee JB, Hayashi T (2010) Characterization of structures and antiviral effects of polysaccharides from Portulaca oleracea L. Chem Pharm Bull 58:507–510
Schnitzler P, Nolkemps S, Stintzing FC, Reichling J (2008) Comparative in-vitro study on the antiherpetic effect of phytochemically characterized aqueous and ethanolic extracts of Salvia officinalis grown at two different locations. Phytomedicine 15:62–70
Benencia F, Coureges MC (1999) Antiviral activity of sandal wood oil against herpes simplex viruses-1 and -2. Phytomedicine 6:119–123
Mandal P, Pujot CA, Carlucci MJ, Chattopadhyaya K, Damonte EB, Ray B (2008) Anti-herpetic activity of a sulfated oxylomannon from Scinaia hatei. Phytochemistry 31:2193–2199
Riel MA, Kyle DE, Milhous WK (2002) Efficacy of scopaduleic acid A against Plasmodium falciparum in vitro. J Nat Prod 65:614–615
Arthan D, Svasti J, Kiltakoop P, Pittayakhachonwu D, Tarticharoen M, Thebtaranonth Y (2002) Antiviral isoflavonoid sulfate and steroidal glycosides from the fruits of Solanum torvum. Phytochemistry 59:459–463
Filho IC, Cortez DAG, Uedo-Nakamura T, Nakamura CV, Filho BPD (2008) Antiviral activity and mode of action of a peptide isolated from Sorghum bicolor. Phytomedicine 15:202–208
Andrighetti-Frohnerv CR, Sincero TCM, de Silva AC, Savi LA, Gaido CM, Bettega JMR, Mancini M, de Almeida MTR, Barbose RA, Faries MR (2005) Antiviral evaluation of plants from Brazilian Atlantic tropical forest. Fitoterapia 76:374–378
Verma H, Patil PR, Kolhapure RM, Goplakrishna V (2008) Antiviral activity of the Indian medicinal plant extract, Swertia chirata against herpes simplex viruses: a study by in vitro and molecular approach. Indian J Med Microbiol 26:322–326
Kurokawa K, Hozumi T, Basnet P, Nakano M, Kadota S, Namba T, Kawana T, Shiraki K (1998) Purification and characterization of eugenin as an anti-herpes virus compound from Geum japonicum and Syzygium aromaticum. J Pharmacol Exp Ther 284:728–735
Abad MJ, Bermejo P, Villar A, Sanchez Palomino S, Carracis l (1997) Antiviral activity of medicinal plant extracts. Phytother Res 11:198–202
Alvarez AL, Habtemariam S, Juan-Badaturgue M, Jackson C, Parro F (2011) In vitro anti HSV-1and HSV-2 activity of Taracetum vulgare and isolated compounds. An approach to their mechanism of action. Phytother Res 25:203–296
Kambizia L, Gooseb BM, Taylorc MB, Afolayana AJ (2007) Anti-viral effects of Aloe ferox and Withania somnifera on herpes simplex virus type 1 in cell culture. S Afr J Sci 103:9–10
Khan TA, Tatke PA, Gabhe SY, Mahajan K, Tawde S, Kothari S, Deshmukh RA (2007) Screening of methanol and water extracts of Acacia nilotica for in vitro anti-HIV activity. J Res Educ Indian Med 13:47–53
Maregesi S, Mlert SV, Panrecouque C, Haddad MHF, Hermans N, Wright CW, Villetinck Aj, Alpers S, Pieters L (2010) Screening of Tanzanian plants against Plasmodium falciparum and human immunodeficiency virus. Planta Med 76:195–201
Chang YS, Moon YH, Woo ER (2003) Virus-cell fusion inhibitory compounds from Ailanthus altissima Swingle. Korean J Pharmacogn 34:28–32
Sookkongwaree K, Geitmann M, Roengsumran S, Petsom A, Danielson UH (2006) Inhibition of viral proteases by Zingiberaceae extracts and flavones isolated from Kaemfaria parviflora. Die Pharmazie 61:717–721
Alam MS, Quader MA, Rashid MA (2000) HIV-inhibitory diterpinoid from Anisomeles indica. Fitoterapia 71:574–576
Ma CM, Nakamura N, Hattori M (2001) Inhibitory effect on HIV-protease of tri-p-coumaroyl-spermidine from Artemisia caruilifolia and related amides. Chem Pharm Bull 49:915–917
Park JC, Hur JM, Park JG, Hatano T, Yoshida T, Miyashiro H, Min BS, Hattori M (2002) Inhibitory effect of Korean medicinal plants and camelliatannin H from Camellia japonica on human immunodeficiency virus type 1 protease. Phytother Res 16:422–426
Premnathan M, Rajendran S, Ramnathan T, Kathiresan K, Nakashima H, Yamamoto M (2000) A survey of some Indian medicinal plants for anti-human immunodeficiency virus (HIV) activity. Indian J Med Res 112:73–77
Lee IS, Kim HJ, Lee YS (2003) A new anti-HIV flavonoid glucuronide from Chrysanthemum morifolium. Planta Med 69:859–861
Wu JH, Wang XH, Yi YH, Lee KH (2003) Anti-aids agents 54. A potent anti-HIV chalcone and flavonoids from genus Desmos. Bioorg Med Chem Lett 13:1813–1815
Bunluepuech k, Tewtrakul S (2009) Anti-HIV integrase activity of Thai medicinal plants. Songklanakarin J Sci Technol 31:289–292
Bedoya LM, Sanchez Palomino S, Abad MJ, Bermejo P, Alcami C (2002) Screening of selected plant extracts for in vitro inhibitory activity on human immunodeficiency virus. Phytother Res 16:550–554
Song WY, Ma YB, Bai X, Zhang XM, Gu Q, Zhang YJ, Zhou J, Chen J (2007) Two new compounds and anti-HIV constituents from Illicium verum. Planta Med 73:372–375
Bedoya LM, Alvarez A, Bermejo M, Gonzalez N, Bethran M, Sanchoz-Palomina S, Cruz SM, Gaitan I, del Olmo E, Escarcena R (2008) Guatemalan plant extracts as virucides against HIV-1 infection. Phytomedicine 15:520–524
Mujovo SF, Hussein AA, Meyer JJM, Fourie B, Muthivhi T, Lall N (2008) Bioactive compounds from Lippia javanica and Hoslundia opposita. J Nat Prod Res 22:1047–1054
Sahu NP, Mandal NB, Bannerji S, Siddiqui KA (2002) Chemistry and biology of the triterpenes and saponins from the seeds of Mimusops elengi. J Herbs Spices Med Plant 24:29–37
Wang HX, Ng TB (2001) Examination of lectins, polysaccharopeptide, polysaccharide, alkaloid, coumarin and trypsin inhibitors for inhibitory activity against human immunodeficiency virus reverse transcriptase and glycohydrolase. Planta Med 67:669–672
Jinatchariyakal W, Wivat C, Vongsakul M, Somanbandhu A, Leelamanit W, Fuju I, Suwanaroj N, Ebizuka Y (2001) HIV inhibition from Thai bitter gourd. Planta Med 67:350–353
Selvan P (2010) Studies on anti-HIV activity and cytotoxicity of leaf of Morinda citrifolia. Int J Chem Sci 8:249–252
Kashiwada Y, Aoshima A, Ikeshiro Y, Chen YP, Furukawa H, Itoigawa M, Fujioka T, Mihashi K, Cosentino LM, Morris-Natschke SL, Lee KH (2005) Anti-HIV benzylisoquinoline alkaloids and flavonoids from the leaves of Nelumbo nucifera and structure–activity correlations with related alkaloids. Bioorg Med Chem 13:443–448
Pelt Gr, Ducki S, Tan R, Gardella RS, MacMahon GB, Boyd MR, Petit GR III, Blumberg PM, Lewin NE, Dinbek DL, Tackett LP, Williams MD (2002) Isolation and structure of pedilstatin from a republic of Maldives Pedilanthus species. J Nat Prod 65:1262–1265
Yan MH, Ching P, Jiang ZY, May B, Zhang XM, Zhang FX, Yang LM (2008) Periglaucines A-D, Anti-HBV and -HIV-1 alkaloids from Pericampylus glaucus. J Nat Prod 71:760–763
Tuchinda P, Pohmaktor M, Reutrakul V, Thanyachareon W, Sophason s, Yoosuk C, Sartisuk T, Pezzuto JM (2001) 2-Substituted furans from Polyalthea suberosa. Planta Med 67:572–575
Dutta BK, Datta SK, Khan TH, Kundu JK, Rashid MA, Nahar L, Sarker SD (2004) Anticholinergic, cytotoxic and anti-HIV1 activities of sesquiterpenes and a flavonoid glycoside from the aerial parts of Polygonum viscosum. Pharm Biol 42:18–23
Wang RR, Gu Q, Wang YH, Zhang XM, Yang LM, Zhou J, Chen JJ, Zheng YT (2008) Anti-HIV-1 activity of compounds isolated from medicinal plant Rhus chinensis. J Ethnopharmacol 117:249–256
Gu Q, Wang RR, Zhang XM, Wang YH, Zheng YT, Zhou T, Chen JJ (2007) A new benzofuranone and anti-HIV constituents from the stem of Rhus chinensis. Planta Med 73:279–282
Marganelli REU, Zaccaro L, Tomei PE (2005) Antiviral activity in vitro of Urtica dioica, Pariteria diffusa M. et. K. and Sambucus nigra L. J Ethnopharmacol 98:323–327
Xiao WL, Li X, Wang RR, Yang LM, Li LM, Huang SX, Zheng YT, Li RT, Sun HD (2007) Triterpinoids from Schisandra rubriflora. J Nat Prod 70:1056–1059
Porika M, Ailemi M, Kokkirala VR, Gadidasu K, Umate P, Rao AV, Devarakonda RK, Abhagani S (2009) In vitro HIV type-1 reverse transcriptase inhibitory activity from leaf extracts of Scoparia dulcis L. J Herbs Spices Med Plant 15:241–247
Khare M, Srivastava MK, Singh AK (2002) Chemistry and pharmacology of genus Sida (Malvaceae)—a review. J Med Aromat Sci 24:430–440
Ahn MJ, Kim CY, Lee JS, Kim J, Kim SH, Lee CK, Lee BB, Shin CG, Huh H, Kim L (2002) Inhibition of HIV-1 integrase by galloyl glucose from Terminalia chebula and flavonol glycoside gallates from Euphorbia pekinensis. Planta Med 68:457–459
Asres KF, Bucar F, Kartnig T, Witvrouw M, Pannecouque C, De Clen E (2001) Antiviral activity against human immunodeficiency virus (HIV-1) and type 2 (HIV-2) of ethnobotanically selected Ethopian medicinal plants. Phytother Res 15:62–69
Kown DH, Kwon HY, Kim HJ, Chang EJ, Kim MB, Yoon SK, Song EY, Yoon DY, Lee YH, Choi IS, Choi YK (2005) Inhibition of hepatitis-B virus by aqueous extract of Agrimonia eupatoria L. Phytother Res 19:355–358
Likhitwitaywuid K, Sritulanak B, Bencharak K, Lipipun V, Mathew J, Schinazi RF (2005) Phenolics with antiviral activity from Milletia erythrocalyx and Artocarpus lakoocha. Nat Prod Res 19:177–182
Jacobson JM, Feinman L, Liebes L, Ostrow N, Koslowski V, Tobia A (2001) Pharmacokinetics, safety and antiviral effects of hypericin, a derivative of St. John’s wort plant, in patients with chronic hepatitis-C virus infection. Antimicrob Agents Chemother 45:517–524
Han YQ, Huang ZM, Yang XB, Liu HZ, Wu GK (2008) In vivo and in vitro anti-hepatitis B virus activity of total phenolics from Oenanthe javanica. J Ethnopharmacol 118:148–153
Thyagarajan SP, Subramanian S, Thirumalasundari T, Venkateswaran PS, Blumberg BS (1988) Effect of Phyllanthus amarus on chronic carriers of hepatitis B virus. Lancet 2:764–766
Wang M, Cheng H, Li Y, Meng L, Zhao G, Mai K (1995) Herbs of the genus Phyllanthus in the treatment of chronic hepatitis B: observations with three preparations from different geographic sites. J Lab Clin Med 126:350–352
Zhao YL, Cai GM, Hong X, Shan LM, Xiao XH (2008) Antihepatitis-B virus activities of triterpinoid saponin compounds from Potentilla anserine L. Phytomedicine 15:253–258
Li H, Zhou CX, Pan Y, Gao X, Wu X, Bai H, Zhou L, Chen Z, Zhang S, Shi S, Luo J, Xu J, Chen L, Zheng X, Zhao Y (2005) Evaluation of antiviral activity of compounds isolated from Ranunculus seiboldi and Ranunculus scleratus. Planta Med 71:1128–1130
Li-Kang H, Ming-Jaw D, Hua-Chien C, Sheau-Farn Y, Jau-Ming C (1996) Inhibition of hepatitis B surface antigen secretion on human hepatoma cells by components from Rubia cardifolia. J Nat Prod 59:330–333
Hua-Chien C, Cen-Kung C, Shou-Dong L, Ju-Chun W, Sheau-Farn Y (1995) Active compounds from Saussurea lappa Clarks that suppress hepatitis B virus surface antigen gene expression in human hepatoma cills. Antiviral Res 27:99–109
Chung TH, Kim JC, Lee CY, Moon MK, Choe SC, Lee IS, Kim SH, Hahn KS, Lee IP (1997) Potential antiviral effects of terminalia chebula, Sanguisorba officinalis, Rubus coreanus and Rheum palmatum against duck hepatitis B virus (DHBV). Phytother Res 11:179–182
Sathyanarayanan S, Selvam P, Jose A, George RM, Revikumar KG, Neyts J (2009) Preliminary phytochemical screening and study of antiviral activity and cytotoxicity of Wrightia tinctoria. Int J Chem Sci 7:1–5
Handa SS (ed) (2008) Perspectives of Indian medicinal plants in the management of liver disorders. Indian Council of Medical Research, New Delhi
Sawamura R, Sun Y, Yasukawa K, Shimizu T, Watanabe W, Kurokowa M (2010) Antiviral activity of diaryheptanoids against influenza virus in vitro. J Nat Med 64:117–120
Chen JX, Xue HJ, Wen-Cai Y, Bing-Hu F, Ya-Hong L, Shao-Hua Y, Yu P, Yu-Quang W (2009) Activity of andrographolide and its derivatives against influenza virus in vivo and in vitro. Biol Pharm Bull 32:1385–1391
Mohamed IET, El Nur EBES, Abdelrahman MEN (2010) The antibacterial, antiviral activities and photochemical screening of some Sudanese medicinal plants. Eurasian J Biosci 4:8–16
Chen JL, Blanc P, Stoddart CA, Bogan M, Rozhon EJ, Parkinson N, Ye Z, Cooper R, Balick M, Nanakorn W, Kernan MR (1998) New iridoids from the medicinal plant Barleria prionitis with potent activity against respiratory syncitial virus. J Nat Prod 61:1295–1297
Liu AL, Shu SH, Quin HL, Lee SMY, Wang YT, Du GH (2009) In vitro anti-influenza viral activities of constituents from Caesalpinia sappan. Planta Med 75:337–339
Harikumar KB, Kuttan R (2006) Antiviral activity of Phyllanthus amarus and curcumin. Amla Res Bull 26:198–205
Martani N, Imanishi N, Kawamata H, Terasawa K, Ochiai H (2001) Inhibitory effect of (+)-catechin on the growth of influenza A/PR/8 in MDCK cells. Planta Med 67:240–243
Wang Y-Z, Cui X-L, Gao Y-J, Guo S-S, Wang X-K, Huang Y, Zhao Y (2006) Antivirus effects of extract from Gardenia. Zhongguo Zhongayo Zazhi 31:1176–1178
Lau KM, Lee KM, Koon CM, Cheung CSF, Lau CP, Ho HM, Lee MYH, Au SWN, Cheng CHK (2008) Immunomodulatory and anti-SARS activities of Houttuynia cordata. J Ethnopharmacol 118:79–85
Vidal A, Fallarero A, Pena BR, Medina ME, Gra B, Rivera F, Guttierrz Y, Vuorela PM (2003) Studies on the toxicity of Punica granatum L (Punicacaeae) whole fruit extracts. J Ethnopharmacol 89:295–300
Ho W-S, Xue J-Y, Sun VEC, Li YL (2010) Antiviral activity of daphnoretin isolated from Wikstroemia indica. Phytother Res 24:657–661
Tandon N (ed) (2011) Quality standards of Indian medicinal plants, vol 9. Indian Council of Medical Research, New Delhi, p 5
Jassim SAA, Naji MA (2003) Novel antiviral agents: a medicinal plants perspective. J Appl Microbiol 95:412–427
Dhawan BN, Patnaik GK (1993) Pharmacological studies for therapeutic potential. In: Randhawa NS, Parmar BS (eds) Neem research and development. Society of Pesticide Science, India, New Delhi, pp 242–249
Bhanuprakash V, Hosamani M, Balamurugan V, Singh RK, Swarup D (2007) In vitro antiviral activity of Eugenia jambolana plant extract on buffalo pox virus: conventional and qPCR methods. Int J Trop Med 2:3–9
Pompei R, Pari A, Flore O, Marcialis MA, Lodd OB (1980) Antiviral activity of glycyrrhizic acid. Experientia 36:304–305
Sunday OA, Munir AB, Akeeb OY, Bolanle AA, Badaru SO (2010) Antiviral effect of Hibiscus sabdariffa and Celosia argentea on measles virus. Afr J Microbiol Res 4:293–296
Badam L, Bedekar S, Sonawane KB, Joshi SP (2002) In vitro antiviral activity of bael (Aegle marmalos) upon human Coxsackie virus B1–B6. J Commun Dis 34:88–99
Goncalves JLS, Lopes RC, Oliviera DB, Costa SS, Mirandas MMFS, Romanos MTV, Santo NSO, Wigg MD (2005) In vitro anti-rotavirus activity of some medicinal plants used in Brazil against diarrhea. J Ethnopharmacol 99:403–407
Badam L, Bedekar SS, Joshi SP (1999) ‘In-vitro’ antiviral activity of neem (Azadirachta indica A. Juss) leaf extract against group B Coxsackie viruses. J Commun Dis 31:79–90
Akihisa T, Tokuda H, Ukiya M, Suzuki T, Erjo F, Koike K, Nikaido T, Nishino H (2004) 3-Epicabrale hydroxylactone and other triterpinoids from Camellia oil and their inhibitory effects on Epstein-Barr virus activation. Chem Pharm Bull 52:153–156
Krishnaswamy K (2008) Turmeric: the salt of orient is the spice of life. Allied Publishers Private Ltd, Mumbai, pp 175–178
Badam L (1997) In vitro antiviral activity of indigenous glycyrrhizin, licorice and glycyrrhizic acid on Japanese encephalitis virus. J Commun Dis 29:91–98
Badam L (1994) In vitro studies on the effect of glycyrrhizin from Indian Glycyrrhiza glabra Linn on some RNA and DNA viruses. Indian J Pharm 26:194–199
Ito C, Itoigaiva M, Ogata M, Mou XY, Tokuda H, Nishino HF (2001) Lignans as anti-tumor promoter from the seeds of Hernandia ovigera. Planta Med 67:166–168
Supratman U, Fujita T, Akiyama K, Hayashi H, Murakami A, Sakai H, Koshimitzu K, Obigashi H (2001) Anti-tumor promoting activity of bufadienolids from Kalanchoe pinnata and Kalanchoe daigremontiana × tubiflora. Biosci Biotechnol Biochem 65:947–951
Tanaka R, Nakata T, Yamaguchi C, Wada SI, Yamada T, Tokude H (2008) Potential anti-tumor activity of 3-alpha-hydroxy-D: a-friesdooleanan-2-one from stem bark of Mallotus philippensis. Planta Med 74:413–416
Premnathan M, Nakashima H, Kathiresan K (1996) In vitro anti-human immunodeficiency virus activity of mangrove plants. Indian J Med Res 103:278–281
Chang RS, Ding L, Chen GQ, Pan QC, Zhao ZI, Smith KM (1991) Dehydroandrographolide succinic acid monoester as an inhibitor against the human immunodeficiency virus. Proc Soc Exp Biol Med 197:59–66
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Dhawan, B.N. Anti-Viral Activity of Indian Plants. Proc. Natl. Acad. Sci. Sect B. Biol. Sci. 82, 209–224 (2012). https://doi.org/10.1007/s40011-011-0016-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40011-011-0016-7