Advance Access Publication 25 October 2007eCAM 2009;6(4)517–522
Antiviral Activity of Some Plants Used in Nepalese Traditional
M. Rajbhandari1, R. Mentel2, P. K. Jha3, R. P. Chaudhary3, S. Bhattarai3, M. B. Gewali1,
N. Karmacharya1, M. Hipper4and U. Lindequist4
1Research Center for Applied Science and Technology, Tribhuvan University, Kathmandu, Nepal,
2Friedrich-Loeffler-Institute of Medical Microbiology, Ernst-Moritz-Arndt-University Greifswald,
Martin-Luther-Strasse 6, 17487 Greifswald, Germany,3Central Department of Botany, Tribhuvan University,
Kathmandu, Nepal and4Institute of Pharmacy, Ernst-Moritz-Arndt-University Greifswald,
Friedrich-Ludwig-Jahn-Strasse 17, 17487 Greifswald, Germany
Methanolic extracts of 41 plant species belonging to 27 families used in the traditional medicine
in Nepal have been investigated for in vitro antiviral activity against Herpes simplex virus type 1
(HSV-1) and influenza virus A by dye uptake assay in the systems HSV-1/Vero cells and
influenza virus A/MDCK cells. The extracts of Astilbe rivularis, Bergenia ciliata, Cassiope
fastigiata and Thymus linearis showed potent anti-herpes viral activity. The extracts of Allium
oreoprasum, Androsace strigilosa, Asparagus filicinus, Astilbe rivularis, Bergenia ciliata and
Verbascum thapsus exhibited strong anti-influenza viral activity. Only the extracts of A. rivularis
and B. ciliata demonstrated remarkable activity against both viruses.
Keywords: anti-herpes–anti-influenza–anti-viral–medicinal plant
Plants have long been used as a source of medicine from
ancient time to today all over the world. In developing
countries the availability of modern medicines is limited.
So traditional medicine is still the mainstay of health care
and most drugs come from plants. Although many plants
have long been recognized and widely used in Nepalese
traditional medicine, some are relatively unexplored and
not arrived to mainstream medicine (1). Therefore, the
search on new drugs must be continued and natural
products from plants, microorganisms, fungi and animals
can be the source of innovative and powerful therapeutic
agents for newer, safer and affordable medicines (2,3).
On the other hand the screening of plants as a possible
source of antiviral drugs has led to the discovery of
potent inhibitors of in vitro viral growth (4–11).
Therefore, the present investigation was carried out to
assess the antiviral effects of some native plants used by
the local people belonging to Gurungs and Thakalis of
Manang and Mustang districts that lie in the Annapurna
Conservation Area Project (ACAP). Permission for the
field study as well as the collection of voucher specimens
was received from the headquarters of ACAP in Pokhara.
The plants were selected on the basis of ethnopharma-
cological records, so the prospect of finding new bio-
active compounds is always promising.
Plant Materials and Preparation of Extracts
The plants were collected in the Manang and Mustang
district of Nepal during summer 2004 and 2005 and
dried in shady place. The plants were authenticated by
Prof. Ram P. Chaudhary, Central Department of Botany,
Tribhuvan University, Kathmandu, Nepal and voucher
specimens were deposited in the Tribhuvan University
For reprints and all correspondence: U. Lindequist, Institute of
Pharmacy, Ernst-Moritz-Arndt-University Greifswald, Friedrich-
Ludwig-Jahn-Strasse 17, 17487 Greifswald, Germany. Tel: 0049-3834-
864868; Fax: 0049-3834-864885; E-mail: email@example.com
? 2007 The Author(s).
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/
licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is
Central Herbarium (TUCH), Kirtipur, Nepal. The name
of the plants, respective families, the parts used for the
extract preparation and traditional uses of the plants are
listed in Table 1.
The dried and powdered plant material (each 10g) was
extracted successively with n-hexane, dichloromethane
and methanol in a soxhlet extractor for each 8h.
Evaporation of the solvent followed by drying in
vacuum gave the respective crude dry extract. Only
methanol extract was used for the antiviral assay,
n-hexane and dichloromethane extracts were not included
because of their insolubility in medium and high toxicity
to the cells. Each 2mg of the extract was dissolved in
10ml dimethylsulfoxide (DMSO) before adding tissue
culture medium supplemented with 2% fetal calf serum
(FCS, GIBCO Life science technologies, Paisley, UK)
and stocked at a concentration of 2mgml?1.
Cells and Viruses
Madine–darby canine kidney (MDCK) and African green
monkey kidney (Vero) cells (cell bank of the Friedrich-
Loeffler-Institute, Federal Research Institute for Animal
Health, Greifswald-Insel Riems, Germany) were main-
tained in Eagle’s minimal essential medium (MEM)
supplemented with 5% FCS (GIBCO, Paisley, UK).
The exponentially growing cells were harvested and
seeded at a cell density of 60000/well in a 96 well
microtiter plate (8mm diameter, Falcon Plastic, NJ) and
incubated for 24h at 37?C with 5% carbondioxide in
a 90% humidified chamber so as to form confluent
Human influenza virus A/WSN/33 (H1N1) London
was obtained from the strain collection of the Institute of
Medical Microbiology, University Greifswald, Germany,
and propagated in embryonated hen eggs for 72h. The
infected allantoic fluids were harvested, the hemaggluti-
nation (HA) titer and virus infectivity were determined
on MDCK cells and the virus stock was stored at ?70?C.
Herpes simplex virus type 1 (HSV-1, strain KOS) was
obtained from the strain collection of the Consiliar and
Reference Center for Alpha Herpes Virus Infection,
Institute of Virology and Antiviral Therapy, University
Jena, Germany and propagated in Vero cells. The virus
infected cells were frozen and thawed and the virus
suspension was titrated on Vero cells and stored at
The cellular toxicity of extracts on Vero and on MDCK
cells was assessed by dye uptake method using neutral
red (12) in 96-well tissue culture plates (8mm diameter,
Falcon Plastic, NJ). Only living cells are able to manage
the active uptake of neutral red. Confluent monolayers of
cells were treated with 100ml 2-fold serial dilutions of
extracts prepared at concentrations of 200, 100, 50 and
25mgml?1in four replicates and incubated at 37?C in a
humidified atmosphere of 5% CO2for 72h. The super-
natant was removed and 200ml neutral red solution
(0.005%) in optimum was added. The microtiter plate
was further incubated for 3h at 37?C. After removal of
the supernatant, the dye incorporated by the viable cells
was extracted with 100ml ethanol/water/glacial acetic acid
solution (50:50:1) by shaking for 15min. The absor-
bance was measured on an ELISA reader using Ascent
software at 540nm. The cytotoxic concentration that
caused the reduction of viable cells by 50% [CC50] was
calculated from dose–response curve.
Antiviral activity was determined by dye uptake assay
using neutral red as described by Mothana et al. (7).
Non-cytotoxic extracts were tested in concentrations of
100, 50, 25, 12.5 and 6.25mgml?1. The antiviral tests of
cytotoxic extracts started with the half of the individual
CC50. The extracts were diluted 1:2 by medium. Con-
fluent monolayers of Vero and MDCK cells were treated
with 100ml of extracts in four replicates for 30min. After
that Vero cells were infected with 30 TCID50of HSV-1
and MDCK cells with 30 TCID50of influenza virus A
and incubated for 72h at 37?C. TCID50(tissue culture
infectious dose) is the virus dose that leads to the
infection of 50% of the cells. The virus suspension and
dilution medium without samples were added, respec-
tively, to the cell cultures to serve as the virus control and
cell control. The supernatant was replaced by 200ml
incubated for 3h at 37?C. After removal of the super-
natant, the dye incorporated by viable cells was eluted
with 100ml ethanol/water/glacial acetic acid solution
(50:50:1) by shaking for 15min. The absorbance was
measured at 540nm and the percentage protection was
calculated by the following formula (13):
ðODTÞV? ðODCÞV=ðODCÞM? ðODCÞV? 100 ð%Þ:
where, (ODT)V, (ODC)V and (ODC)M correspond to
absorbances in virus infected cells with test compounds,
virus infected cells without test compounds and the mock
infected control (assay without viruses), respectively.
Amantadine HCl and acyclovir were used as reference
Cytotoxicity of Extracts for Vero Cells
In this study, 43 methanolic extracts from 41 different
plant species belonging to 27 families (Table 1) were
518Antiviral Nepalese Plants
Table 1. Name of the plants, respective families, parts used for extraction and major traditional use(s)
Name of plant FamilyCollected
Major traditional use(s)
Abies spectabilis Spach.PinaceaeLeavesKye 342Bone fracture
Allium oreoprasum SchrenkAlliaceae Whole plantLungho2104Cough, cold, sore throat
Allium prattii C.H. WrightAlliaceae Whole plantBanlasun493 Vegetables
Anaphalis busua DC. AsteraceaeLeaves Phosorosan 463Cough, cold, sore throat
Anaphalis busua DC. Asteraceae FlowersPhorosan 463Cough, cold, sore throat
Androsace strigilosa Franch. PrimulaceaeWhole plant Gadhikanakyo169 Fever, edema
Anemone rivularis Buch.-Ham. ex DC.Ranunculaceae RootsAngsoup 492Cough, cold, stomachache
Arisaema flavum SchottAraceae TubersTimtry618Skin disease, wounds
Artemisia caruifolia Roxb.AsteraceaeWhole plantsBajha421Incense
Asparagus filicinus Buch.-Ham.
ex D. Don
AsparagaceaeTubersNirshing2125Tonic, menstrual problem
Astilbe rivularis Buch.-Ham. ex D. DonSaxifragaceaeRhizomes Bhadhangoo2070Headache, improve fertility
Bergenia ciliata (Haw.) Sternb.SaxifragaceaeRhizomes Pakhanved2075 Diarrhea, dysentery, stomachache
Bistorta affinis GreenePolygonaceaeRoot Khaldi 203Cough, cold, tonsillitis, fever
Cassiope fastigiata D. DonEricaceae Aerial partsSunpathi433 Incense
Clinopodium umbrosum MatsumLamiaceae Aerial partsSarshang 155High blood pressure, pain,
inflammation of body
Cotoneaster integrifolius (Roxb.) KlotzRosaceae FruitsTsharsin168 Edible
Delphinium brunonianum RoyleRanunculaceaeWhole plantPonmar 262Fever, jaundice
Dicranostigma lactucoides Hook.f.
PapaveraceaeWhole plantRhafendhi 105Easy delivery of baby
Euphorbia longifolia D. DonEuphorbiaceaeRootDhurbi2018 Cough, cold, fever, skin disease
Geranium donianum SweetGeraniaceaeAerial partKagheshurti 153Gingivitis, toothache
Hyoscyamus niger var. agrestis
Juniperus squamata Buch.-Ham.
CupressaceaeAerial partSukri 265Fever, cough, cold, skin disease
Maharanga emodi DC. BoraginaceaeRootsMaharangi
2071 Ear pain
Morina longifolia Wall. ex DC.MorinaceaeRoots Changtser goepaEdema, stomachache, headache
(Pennell) D.Y. Hong
ScrophulariaceaeRootsKutki431Fever, cough, cold, tonsillitis
Oxytropis williamsii I. T. Vassilchenko FabaceaeWhole plants Sinshi329Wound healing, coagulate blood
Primula involucrata Sw. ex DubyPrimulaceae Whole plantsChyonker 178 Vegetable
Rhododendron anthopogon D. Don EricaceaeAerial partPalu, Sangalin 210Reduce blood pressure, fever,
Rhododendron lepidotum Wall. & G. DonEricaceae Aerial partBhaiunakpo2122Fever, cough, cold, tonsillitis
Rosa macrophylla Lindl.RosaceaeFlowerSeghu343 Fever, diarrhea, dysentery
Rosa macrophylla Lindl.Rosaceae FruitsSeghu 343Nutrition in cold, cough
Rosa sericea Lindl.RosaceaeFruitsSewa 102Diarrhea, dysentery, stomachache,
Rubus foliolosus D. DonRosaceaeRoot Mapalan2019 Fever, dyspepsis, cough, cold, vertigo
Salix serpyllum AnderssonSalicaceaeAerial partLangmanackpo2015Stomachache, diarrhea, dysentery
Saussurea auriculata (DC.) Sch. Bip.AsteraceaeWhole plantTa283Blood circulation
Saussurea fastuosa (Decne) Sch. BipAsteraceaeAerial partSingamindro303Cut, bleeding
Swertia ciliata (G. Don) B. L. BurttGentianaceaeWhole plantTiktha 311 Fever due to stomach and
Thalictrum cultratum Wall.Ranunculaceae Roots and stemNagghunensa121Fever, diarrhea (for animal only)
Thymus linearis Benth. LamiaceaeWhole plant Akhino 126Eye infection
Urtica dioica L.UrticaceaeLeavesPolo409 Cough, cold
Valeriana jatamansi JonesValerianaceaeRootsNappu2072Sedative, headache
Verbascum thapsus L.ScrophulariaceaeAerial partYugisingh 195Wound healing, urinary
Zanthoxylum armatum DC.Rutaceae FruitsPrumo2183 Cough, cold, tonsillitis
screened for their antiviral activity against herpes simplex
virus and influenza virus A by dye uptake assay. By
methanolic extraction, a broad spectrum of compounds
with different polarity can be obtained. As prerequisite
for antiviral tests, the cytotoxicity of the extracts against
virus-host cells was investigated. The results are summa-
rized in Table 2.
The extracts of Androsace strigilosa, Anemone rivularis,
Thalictrum cultratum exhibited strong cytotoxicity in
Vero cells with CC50(the concentration that causes the
reduction of viable cells by 50%) ranging from 12.5 to
25mgml?1. A moderate cytotoxicity was observed for the
extracts of Asparagus filicinus, Bergenia ciliata, Primula
involucrata and Saussurea auriculata with CC50ranging
from 30 to 50mgml?1. Other eight extracts showed very
mild toxicity while rest of the extracts were non-toxic at
Cytotoxicity of Extracts for MDCK Cells
Similarly, in MDCK cells extracts of Artemisia caruifolia,
D. brunonianum and E. longifolia showed strong toxicity
with CC50ranging from 19 to 25mgml?1. A moderate
toxicity was exhibited by the extracts of A. strigilosa,
A. rivularis, Asparagus filicinus, Dicranostigma lactucoides,
Hyoscyamus niger, Thymus linearis and Zanthoxylum
armatum with CC50ranging from 30 to 50mgml?1. Other
three extracts demonstrated very low toxicity while rest of
the extracts were non-toxic at 100mgml?1.
Antiviral Activity of Extracts Against HSV-1
Antiviral activity against HSV-1 was shown by 11
extracts at non-cytotoxic
values (the concentration that protects 50% of the cells
against destruction by viruses) ranged from <6.25 to
82mgml?1. The highest activity against HSV-1 with IC50
values <6.25mgml?1was observed for the extracts of
A. rivularis, B ciliata, Cassiope fastigiata and T. linearis.
Moderate activity was shown by Cotoneaster integrifolius
19mgml?1). Weak activity (IC50 50–82mgml?1) was
found in the extracts of Bistorta affinis, Juniperus
squamata, Oxytropis williamsii, Rhododendron anthopogon
and Rubus foliolosus.
Antiviral Activity of Extracts Against Influenza Virus A
extracts at non-cytotoxic concentrations. The IC50values
ranged from <6.25 to 97mgml?1. The highest activity was
shown by the extracts of A. filicinus, A. rivularis and
Verbascum thapsus with IC50< 6.25mgml?1. In addition,
the extracts of Allium oreoprasum, A. strigilosa and
B. ciliata also exhibited high activity (IC50values from
8 to 10mgml?1). Moderate activity (IC50values from 17 to
50mgml?1) was demonstrated by 11 extracts. Weak activity
(IC50values from 78 to 97mgml?1) was shown by three
extracts (Table 2).
The extracts of A. rivularis and B. ciliata were found to
be highly active against both viruses.
The results of this work justify the potential of some
of the investigated plants for the production of bioactive
compounds. The phytochemical knowledge about these
plants is so far very limited. The active principles present
in A. rivularis are still unknown. Phytochemical investi-
gation of A. rivularis revealed the presence of flavonoids,
terpenoids and bergenin (14,15).
Bergnia ciliata is known to contain phenolic com-
pounds (16). Polyphenols, especially high polymeric
procyanidines possess strong anti-influenza viral activity
(17), which is in agreement with our previous study (18).
In our previous study (19), methanol–water extract of
Bergenia ligulata, which is taxonomically closely related
to B. ciliata, inhibited the growth of influenza virus A in
cell culture with IC50 of 10mgml?1. The extract also
inhibited the viral protein and nucleic acid synthesis (18).
In the present study, the methanol extract of B. ciliata
inhibited the influenza virus A and HSV-1 indicating that
the genus Bergenia could be the source of potent antiviral
drugs. Again potent activity of A. rivularis against both
viruses indicated the high prospect of finding antiviral
drugs in Saxifragaceae family.
No antiviral compounds have previously been isolated
from A. filicinus. The plant is known to contain steroidal
saponins (20,21), furostanol glycosides (22) and furosta-
nosides (23,24). The phytochemicals possibly responsible
for the high activity of C. fastigiata against HSV are not
described. Some Cassiope species are reported to contain
flavonoid glycosides (25). Similarly, the compounds
responsible for the high anti-influenza viral activity of
Likewise, no antiviral constituents have been isolated
from C. integrifolius, C. umbrosum and T. linearis. Other
members of the genus Cotoneaster, have been found to
possess phenolic glycosides (Cotoneaster orbicularis, 26),
flavonols and isoflavones (Cotoneaster simonsii, 27).
From the other member of the genus Clinopodium,
C. chinensis var. parviflorum, oleanane triterpene saponins
have been isolated (28).
Whereas for the extract of V. thapsus, antiherpes
activity has been reported (29); our study revealed only
the strong anti-influenza viral activity. However, no
antiviral compounds have previously been isolated.
The plant is known to contain phenylethanoid and
520Antiviral Nepalese Plants
Table 2. Antiviral activities of plants used in Nepalese ethnomedicine
Plant extractsPercentage yield
of MeOH extract
Antiviral activity HSV-1/Vero cellsAntiviral activity Influenza A/MDCK cells
17 Abies spectabilis23.4
Allium oreoprasum 17.8>100– >1008
Allium prattii7.5 >100– >100 97
Anaphalis busua Leaves12.2 >100– >100–
Anaphalis busua Flower 13.6>100–>100–
Androsace strigilosa18.212.5–40 10
Anemone rivularis14.521– 40–
Arisaema flavum14.1 >100– >100–
Artemisia caruifolia 12.392– 22–
Asparagus filicinus18.740– 30 <6.25
Astilbe rivularis 52.167 <6.25>100 <6.25
Bergenia ciliata33.2 35<6.25 >1009
Bistorta affinis14.3 >10080 >10050
Clinopodium umbrosum 14.0 76 19>100–
Cotoneaster integrifolius22.0>100 18>10044
Delphinium brunonianum 12.3 11– 25–
Dicranostigma lactucoides 21.172–50–
Euphorbia longifolia18.5 25–19–
Geranium donianum24.4 89– 69–
Hyoscyamus niger18.7 >100– 50 40
Juniperus squamata16.7>100 82>100–
Maharanga emodi14.7>100– >10029
Morina longifolia5.9>100– >100–
Oxytropis williamsii 27.5 >100 78>100 33
Primula involucrata31.7 50– 63–
Rhododendron anthopogon22.1>100 50>100 44
Rhododendron lepidotum 18.9100–>10058
Rosa macrophylla Flower11.2 86–>10045
Rosa macrophylla Fruits10.5 74–>100–
Rosa sericea 14.2>100–>100–
Rubus foliolosus 21.2>10050>100–
Salix serpyllum26.2 >100– >100–
Saussurea auriculata 11.431– 100 42
Saussurea fastuosa8.3>100– >100–
Swertia ciliata 6.2>100– >100–
Thymus linearis5.26912.5 45–
Valeriana jatamansi50.1 >100– >10020
Verbascum thapsus 12.3>100–>100<6.25
Zanthoxylum armatum6.7>100– 36–
*CC50=the concentration that causes the reduction of viable cells by 50%;
destruction by viruses; – No measurable effect.
The values are the mean of four experiments.
yIC50=the concentration that protects 50% of the cells against
phytochemicals responsible for anti-influenza viral activ- Download full-text
ity could be different from anti-herpes activity and also
the amount of active constituents present in the plants
depends on the geographical distribution, season of
collection and climatic and ecological condition at the
Looking at the chemical structures of the already
identified compounds, most of these substances should be
extracted by methanol. The foregoing extraction by more
lipophilic solvents (n-hexane and dichlormethane) alle-
viates themethanolic extraction
Comparing the use of plants in traditional medicine
and their antiviral activity, a direct correlation could
be established for some plants, e.g. A. oreoprasum,
A. strigilosa (anti-influenza activity) and T. linearis
(antiherpes activity). For other plants, e.g. C. fastigiata,
which exhibited potent anti-herpes activity, this cannot be
recognized till now.
The extracts that exhibited only medium and low
activity, could also be the source of potential antiviral
drugs because the bioactive compounds may be present in
too low concentrations to show effective antiviral activity
at non-toxic concentration. Further fractionation and
separation of extract(s) may reveal potent antiviral
Our results indicate that several plants used in Nepalese
traditional medicine could be the lead to potential
antiviral drugs, which possibly provide molecules with
drug-like properties and with incredible structural diver-
sity. Besides, the results are useful for rationalizing the
use of medicinal plants in primary health care in Nepal.
The phytochemical characterization of the extracts, the
identification of the responsible bioactive compounds and
the elucidation of the mode of action and quality
standards are necessary.
Volkswagen Foundation, Germany, is gratefully acknow-
ledged for financial support. We would like to thank
Dr. Susanne von der Heide, HimalAsia foundation, for her
valuable suggestion for grant application and further
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522Antiviral Nepalese Plants