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CHAPTER
13
Antiviral potential of medicinal
plants: a case study with guava tree
against dengue virus using a
metabolomic approach
Thomas Vial
1,2
, Chiobouaphong Phakeovilay
1,3,
*,
Satoru Watanabe
2
, Kitti Wing Ki Chan
2
, Minhua Peng
2
,
Eric Deharo
1,4
, Franc¸ois Chassagne
1
, Subhash G. Vasudevan
2
and Guillaume Marti
1,3
1
UMR 152 PharmaDev, IRD, UPS, Universite
´
de Toulouse, Toulouse, France
2
Programme in
Emerging Infectious Diseases, Duke-NUS Medical School, Singapore
3
Laboratoire de
Recherche en Sciences Ve
´
ge
´
tales and Metatoul-AgromiX Platform, MetaHUB, National
Infrastructure for Metabolomics and Fluxomics, LRSV, Universite
´
de Toulouse, CNRS, UPS,
Toulouse, France
4
Institut de Recherche pour le De
´
veloppement, Vientiane, Lao PDR
Introduction
Dengue disease
Dengue is an arthropod-borne viral disease (arbovirus) that currently infects about
400 million people every year throughout the tropical and subtropical world (
Bhatt et al.,
2013
). Dengue virus (DENV) is the most widespread arbovirus. It emerged in the second
part of the 20th century (
Gubler, 2002), and ever since its incidence has increased 30-fold,
* Contributed equally.
439
Medicinal Plants as Anti-infectives
DOI:
https://doi.org/10.1016/B978-0-323-90999-0.00010-0 Copyright © 2022 Elsevier Inc. All rights reserved.
according to World Health Organization (WHO). DENV is transmitted by the bite of an
infected female mosquito of the genus Aedes. Due to the Aedes geographical distribution,
more than 40% of the global population, living in more than 120 countries, is at risk to
contract dengue (
Kraemer et al., 2018; Simmons, Farrar, Van Vinh Chau, & Wills, 2012).
Aedes distribution which now extends to North America and Europe (Kraemer et al.,
2018
), in addition to the subtropical regions, where it is normally prevalent, has significant
implications for increasing the burden of dengue (
Fig. 13.1). DENV belongs to genus
Flavivirus. There are four DENV serotypes: DENV-1, DENV-2, DENV-3, and DENV-4
(
Simmons et al., 2012). Dengue is classified as a neglected tropical disease and develop-
ment of many vaccines and novel antidengue drugs as well as novel vector control mea-
sures have been investigated in the last decade (
Horstick, Tozan, & Wilder-Smith, 2015).
However, although research activity has increased substantially in the past decade, find-
ings for antiviral therapy have so far been unsatisfactory.
About 75% of people infected with DENV remain asymptomatic (not registered in hospital).
The other 25% represents around 100 million patients that experience a range of different
symptoms from mild flu-like illness to more severe dengue characterized by vascular leakage,
hemorrhages, organ failure, and shock (
Fig. 13.2)(Bhatt et al., 2013). WHO Dengue Guideline
described the clinical manifestations of dengue fever with an incubation period of 37days
after viral infection by the mosquito. Dengue has a broad range of clinical symptoms and in
some cases no symptoms appear up to 14 days. The most common symptom is the immediate
onset of fever together with headaches, myalgia, arthralgia, pain behind the eyes, abdominal
pain, nausea, and flushing of the face. A rash is often seen and can be maculopapular, morbilli-
form, macular, and scarlatiniform. WHO classified dengue fever manifestation into dengue
FIGURE 13.1 The global distribution of dengue. Source: Adapted from CDC Dengue heatmap (http://www.health-
map.org/dengue), and data from the European Centre for Disease Prevention and Control (ECDC) (http://www.ecdc.europa.
eu/en/dengue
). National and local consensus of complete presence (red) or absence (blue) reported by local transmission. This
map was created with
mapchart.net and does not take into account imported dengue cases by travelers.
440 13. Antiviral potential of medicinal plants: a case study with guava tree against dengue virus using a metabolomic approach
Medicinal Plants as Anti-infectives
and severe dengue. Dengue is characterized by abdominal pain, vomiting, clinical fluid accu-
mulation, mucosal bleeding, lethargy, liver enlargement, and increase in hematocrit concurrent
with a rapid decrease in platelet number. Severe dengue signs comprise severe plasma leakage
leading to shock, severe bleeding, and severe organ impairment. Secondary infection from other
serotypes increases the risk of developing severe dengue (
World Health Organization, 2012).
Conventional treatment
No antiviral against DENV is currently available and only symptomatic care is provided to
patients (
Malina, Boon, Aurapa, & Azmath, 2019). It is recommended to stay hydrated and
avoid anticoagulant such as aspirin-containing drugs. For severe dengue patients with shock
syndrome, intravenous fluid supplementation is essential and prophylactic platelet transfusion
is performed, although the latter does not prevent bleeding (
Lye et al., 2017).
Multiple drugs with in vitro antivi ral activity against DENV have been tested in clinical
trials (chloroquine, balapiravir, celgosivir, lovastatin, prednisolone, ribavirin, zinc bis-
glycinate, vitamin E, and UV-4B), without success in preventing disease or lowering vire-
mia (
Wilder-Smith, Ooi, Horstick, & Wills, 2019). Several clinically approved drugs for
other diseases have been evaluated for antidengue activity (
Dighe et al., 2019 ). For exam-
ple, ivermectin went in clinical trial in phase II/III in children and adult patients
FIGURE 13.2 Dengue clinical phases and classification. Source: Adapted from WHO Dengue Guidelines 2009.
https://apps.who.int/iris/handle/10665/44188.
441Introduction
Medicinal Plants as Anti-infectives
(ClinicalTrials.gov number NCT02045069) and shown also a 50% decrease in infection rate
of DENV-2-infected Aedes albopictus mosquito treated with ivermectin and almost complete
clearance of DENV RNA (
Xu et al., 2018). Ivermectin also inhibits in vitro replication of flavi-
viruses, mainly YFV and DENV with a lower effect for the latter, by targeting viral nonstruc-
tural (NS) protein NS3 helicase activity (
Mastrangelo et al., 2012). Other drugs that target NS
have been studied, but none reached clinical trials (
Hernandez-Morales et al., 2017; Luo,
Vasudevan, & Lescar, 2015
). Neutralizing monoclonal antibodies are also candidates for den-
gue treatment (
Sun, Chen, & Lai, 2018). However, none of them have been approved as anti-
dengue drugs (
Beesetti, Khanna, & Swaminathan, 2016; Dighe et al., 2019).
Medicinal plants
Given the lack of efficacy of repurposed drugs against the DENV and the difficulty in
developing a universal vaccine with no contraindications, it is necessary to find new direc-
tions in the search for antivirals. The medicinal plants are an important source of active
compounds for various diseases in the world, also for viral infections. The medicinal plant
extracts and their derivatives have been suggested by WHO in the fight against dengue dis-
ease as they are comparatively less harmful, and cheaper than synthetic drugs. Currently,
the identification of the active compounds against DENV from medicinal plants has
attracted the researchers’ interests. The use of medicinal plants in the management of den-
gue is widely reported, aiming to demonstrate antiviral effects of plant extracts or isolated
compounds (
Abd Kadir, Yaakob, & Mohamed, 2013; Ali, Chorsiya, Anjum, Khasimbi, & Ali,
2020
; Ferreira et al., 2017; Qadir et al., 2015; Tang, Ling, Koh, Chye, & Voon, 2012).
Although several studies have methodological variations in the experimental design, the
biological model, or limited to an in silico model, medicinal plants products have the poten-
tial for anti-DENV development (Ferreira et al., 2017). An overview of the main natural
extracts and their respective biosources depicted as active against dengue fever are pre-
sented in
Table 13.1 (Kaushik, Kaushik, Sharma, & Yadav, 2018).
Case study: metabolomics reveal antidengue compounds isolated from
Psidium guajava
Introduction
Psidium guajava: a potential antidengue medicinal plant
Psidium guajava Linn. or guava has been reported for its potential antidengue activity as
mentioned in our literature review. In this context, studying the ethanolic leaf extract of guava
should be of interest to find new active compounds against DENV. Guava belongs to the
Psidium genus and Myrtaceae family. Guava is native to Mexico (
Gutie
´
rrez, Mitchell, & Solis,
2008
), and distributed throughout the tropical and subtropical areas. Moreover, guava has
been reported in traditional medicine in many regions, and its pharmacological activities have
been widely studied for various diseases. Finally, some bioactive compounds were also
reported from this plant species (
Gutie
´
rrez et al., 2008).
442 13. Antiviral potential of medicinal plants: a case study with guava tree against dengue virus using a metabolomic approach
Medicinal Plants as Anti-infectives
TABLE 13.1 Summary of reported antidengue medicinal plants.
Plant species Family Active form Activity
Andrographis paniculata
(Burm.f.) Nees
Acanthaceae Methanolic extract Inhibited the activity of DENV-1 in in vitro assays (doi:
10.1186/1472-6882-12-3)
Azadirachta indica A. Juss. Meliaceae Leaves aqueous extract Inhibited the DENV-2 replication by the absence of Dengue-related clinical
symptoms in suckling mice confirmation (doi:
10.1016/S0378-8741(01)00395-6)
Boesenbergia rotunda (L.)
Mansf.
Zingiberaceae 4-hydroxypanduratin A
and panduratin A
Inhibited the DENV-2 NS3 protease (doi:
10.1016/j.bmcl.2005.12.075)
Carica papaya L. Caricaceae Leaves aqueous extracts Exhibited potential activity against dengue fever in 45-year-old patient by
increasing the platelets count, WBC, and neutrophils (doi:
10.1016/S2221-1691(11)
60055-5
)
Castanospermum australe
A. Cunn. & C. Fraser
Fabaceae Castanospermine Castanospermine inhibited at the level of secretion and infective of virus
particles (doi:
10.1128/JVI.79.14.8698-8706.2005)
Cissampelos pareira L. Menispermaceae Ethanolic extracts Showed antiviral activity against all types of dengue virus and reduced the
production of TNF-α in Wistar rats-induced severe dengue disease
(doi:
10.1371/journal.pntd.0004255)
Cryptonemia crenulata
(J. Agardh) J. Agardh
Halymeniaceae Carrageenan G3d and DL-
galactan hybrid C2S-3
Active against DENV-2 at the early infection stage means these compounds
target virus absorption and internalization (doi:
10.1016/j.antiviral.2005.02.001)
Euphorbia hirta L. Euphorbiaceae Leaf extract Inhibited the viral serotype 1 and increased platelet count in the animal study
(doi:
10.1155/2018/2048530)
Gastrodia elata Blume Orchidaceae
D-glucans sulfated
derivatives
Strongly interfering with the DENV-2 infections mainly in virus adsorption, in
a very early stage of the virus cycle (doi:
10.1016/j.carres.2007.06.021)
Gymnogongrus griffithsiae
(Turner) C. Martius
Phyllophoraceae Carrageenan G3d and
DL-
galactan hybrid C2S-3
Active against DENV-2 at the early infection stage means these compounds
target virus absorption and internalization (doi:
10.1016/j.antiviral.2005.02.001)
Gymnogongrus torulosus (J.D.
Hooker & Harvey) F. Schmitz
Phyllophoraceae
DL-galactan hybrid Inhibited the DENV-2 serotype in Vero cells (doi:10.1177/095632020201300202)
Houttuynia cordata Thunb. Saururaceae Aqueous extract
(hyperoside)
Significantly reduce intracellular DENV-2 RNA production in HepG2 cells
(doi:
10.1111/j.1745-4514.2010.00514.x)
Hippophae rhamnoides L. Elaeagnaceae Leaf extract Be able to maintain cell viability of dengue infected cells, decreases in TNF-α,
and increases IFN-γ (doi:
10.1016/j.phymed.2008.04.017)
Lippia alba (Mill.) N.E.Br. ex
Britton & P. Wilson
Verbenaceae Essential oil Inactivated virus before adsorption on host cells (doi:
10.1590/S0074-
02762010000300010
)
(Continued)