Post on 26-Feb-2023
Molecules 2013, 18,1-x manuscripts; doi:10.3390/molecules180x0000x
molecules ISSN 1420-3049
www.mdpi.com/journal/molecules Review
Medicinal Plants with Antitumor Potential against Lung Cancer
Luara de Sousa Monteiro, Katherine Xavier Bastos, José Maria Barbosa-Filho, Petrônio Filgueiras de Athayde-Filho, Margareth de Fátima Formigo Melo Diniz, and Marianna Vieira Sobral Castello-Branco*,
Department of Pharmaceutical Sciences, Federal University of Paraiba, 58051-900, João Pessoa, PB, Brazil; E-Mails: luaramonteiro@hotmail.com (L.S.M.); katherine_xb@hotmail.com (K.X.B.); jbarbosa@ltf.ufpb.br (J.M.B.-F.); athayde-filho@quimica.ufpb.br (P.F.A.-F.); margareth@ltf.ufpb.br (M.F.F.M.D.)
* Author to whom correspondence should be addressed; E-Mail: mariannavbs@gmail.com (M.V.S.C.B.); Tel.: +55-83- 3216-7003; Fax: +55-83-3216-7364.
Received: / Accepted: /Published:
Abstract: Lung cancer is a disease with a high morbidity and high mortality rates. As a result, it is
often associated with a significant amount of suffering and a general decrease in the quality of life.
Herbal drugs are recognized as one of attractive approaches for lung cancer therapy with little side
effects and are the main sources of new drugs. The aim of this review is to review the medicinal plants
with antitumor potential against lung cancer. The assays were conducted with humans and animals,
and Lewis lung carcinoma was the most used experimental model. Considering all the countries
covered in the study, India, China, Japan, and South Korea were the countries with the highest number
of species with antitumor activity on different experimental models. Of the 47 plants evaluated, 35
demonstrated antitumor activity. This review was based on NAPRALERT data bank, Web of Science
and Chemical Abstracts. This work shows that the natural products from plants continue being a rich
source of herbal medicines or biologically active compounds against cancer.
Keywords: medicinal plants; antitumor activity; lung cancer; review
1. Introduction
OPEN ACCESS
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Cancer is a collection of heterogeneous genetic diseases united by common alterations in multiple
cellular signaling pathways [1]. Different hallmarks are proposed to cancer cells. Evasion of
programmed cell death or apoptosis has been recognized as one of the main alterations that dictate
malignant growth [2]. Furthermore, other hallmarks include self-sufficiency in growth signal,
deregulating cellular energetics, sustained angiogenesis, evasion immune detection, and tissue invasion
and metastasis [1-3]. In addition, have been described two characteristics of cancer that facilitate
acquisition of the hallmarks: genome instability and mutation tumor-promoting inflammation [2].
Coordinated processes such as cell proliferation, differentiation and apoptosis are modified producing
altered cellular phenotype with these specific characteristics [1,2].
According to the World Health Organization (WHO), the cancer are non-communicable diseases
responsible for 63% of deaths worldwide, being characterized as the second cause of death in western
countries [4,5]. Its incidence is strongly affected by demographics aspects, such as population aging,
feeding habits and, in particular, environmental factors such as the incidence of ultra-violet rays. The
International Agency for Research on Cancer (IARC) estimates that there were 12.7 million new
cancer cases in 2008 and is expected by 2030 to grow to 21.4 million [6,7].
Lung cancer is currently the malignant tumor with the highest rate of mortality worldwide, often
because it is not detected until there has been significant progression of the illness, which leads to a
significant reduction in quality of life of the patient [8]. Different factors are classified as possible
causes for lung cancer, including active cigarette smoking; exposure to secondhand cigarette smoke
(passive smoking); pipe and cigar smoking; exposure to indoor and outdoor air pollution; exposure to
radiation; and occupational exposure to agents such as asbestos, nickel, chromium, and arsenic [9].
The most important factor is smoking [10] and the incidence rates of lung cancer are generally higher
among men than among women [11]. The lung cancer is classified into non-small cell lung carcinoma
(NSCLC): squamous cell carcinoma, adenocarcinoma or large cell carcinoma, which represents 80%
of all lung cancer cases, and the remaining cases are small cell lung carcinoma (SCLC) [11,12].
Recently, it was published a new classification that defined ‘‘molecular subtypes’’ of lung cancer
based on specific actionable genetic aberrations [13]. New opportunities for targeted therapy are under
development based on the discovery of multiple molecular mechanisms underlying the development,
progression, and prognosis of lung cancer.
Surgery, chemotherapy, radiation, hormones and immunotherapy are the main cancer treatment
often supplemented by other complementary and alternative therapies. Although chemotherapy is the
method most used, several problems are associated with its use as limited efficacy, toxicity severe and
multi-drug resistant [14].
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Plants have a long history of use in the treatment of cancer and continue to be the main source of
new drugs [15]. Herbal drugs have been recognized as one of attractive approaches for lung cancer
therapy because they have proven to be useful and effective in sensitizing conventional agents,
prolonging survival time, preventing side effects of chemotherapy, and improving quality of life in
lung cancer patients [16]. Recent cohort study with 453 cancer patients revealed that the percentage of
patients using herbal medicines in combination with conventional treatment was as high as 77% [17].
These data demonstrate the importance of natural products as complementary therapy for the treatment
of lung cancer, mainly with the aims of reduction of toxicity, improvement of cancer-related
symptoms, fostering of the immune system, and even direct anti-cancer effects [18].
Many natural products or synthetic analogs are still widely used in clinical, for example, the so-
called vinca alkaloids, vinblastine and vincristine, isolated from the Madagascar periwinkle,
Catharanthus roseus, the paclitaxel (Taxol®), obtained of the leaves of various Taxus species, and the
two clinically-active agents, etoposide and teniposide, which are semisynthetic derivatives of the
natural product epipodophyllotoxin [15]. In addition, other promising agents, natural or synthetic
analogs, are in clinical development phase, including flavopiridol [19] and combretastatin A4 [20].
In the course of our continuing search for bioactive natural plant products, we have published
reviews on crude plant extracts and plant-derived compounds with potential uses [21-38]. Moreover,
our group has also reviewed the medicinal and poisonous plants of Northeast Brazil [39-40], among
others [41-53].
The search was carried out on data banks such as Web of Science, Chemical Abstracts, and
NAPRALERT (acronym for the University of Illinois Natural Products ALERT service). The
references found in the searches were later consulted. For details on the mechanism-based bioassays
utilized for antitumor activity, the original references should be consulted.
2. Results and Discussion
Herbal medicines and phytochemicals can be potent anti-cancer agents for lung cancer treatment
and prevention by regulating multi-molecular targets involved in angiogenesis, metastasis and severe
side effects, only provided quality control and reproducibility issues were solved [16].
In the current review we present medicinal plants, distributed in diverse parts of the world, with
antitumor activity against different lung tumor models. The effectiveness of the medicinal plants
depended on the type of drug studied and the bioassay models. Thus, it was possible to classify the
extracts as active or inactive. In this study, we chose more species referenced in data collected in the
NAPRALERT natural products database and the scientific literature databases ScienceDirect and
PubMed.
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Euphorbiaceae and Fabaceae were the most cited families for antitumor activity against lung tumor
models, respectively. Croton macrostachys, Euphorbia esula, Euphorbia fischeriana and Euphorbia
ingens were the most studied Euphorbiaceae species. All of them showed significant antitumor activity
against lung tumor models. Among the Fabaceae active species were cited Caesalpinia gilliesii, Cassia
garrettiana, and Sophora flavescens.
Eleven mentions were described for the specie Ganoderma lucidum (Ganodermataceae), being
considered the most studied specie for antitumor activity against lung tumor models. One of these
studies showed that an aqueous extract of Ganoderma lucidum, called ‘Ling-Zhi or holy mushroom’ in
Chinese traditional medicine, significantly increased the life span of Lewis lung carcinoma-implanted
syngeneic C57BL/6 mice, when administered intraperitoneally alone or in combination with cytotoxic
antitumor drugs (Adriamycin, fluorouracil, thioguanine, methotrexate, cisplatin) or a synthetic
immunomodulator (Imexon) [54]. In another study, the authors suggest that the antitumor and
antimetastatic activities of the triterpenoid fraction of G. lucidum against Lewis lung carcinoma
(LLC)-implanted might be due to the inhibition of tumor-induced angiogenesis [55].
The species Undaria pinnatifida, Panax ginseng red type, Brucea javanica and Camellia sinensis
were also active against lung tumor models. To Undaria pinnatifida specie, four studies showed
significant activity against Lewis lung carcinoma. Among the four mentions for Panax ginseng red
type, one of the studies showed the antitumor activity of this specie against lung adenoma induced by
different carcinogenic agents.
The Brucea javanica species showed the anti-carcinoma effect against brain metastasis as a
complication of lung cancer. The results of this study showed that the median survival duration (15
months in the test group, 10 months in the control group) and the quality of life of the patients in the
combined group (radiotherapy and intravenous injection of 10% Brucea javanica emulsion) was much
better than in the radiotherapy alone (control) group. The results suggest the Brucea javanica emulsion
exhibits a synergic action with the radiotherapy in the treatment of brain metastasis as a complication
of lung cancer [56]. Another study with this species showed that the preoperative intravenous emulsion
of 10% Brucea javanica oil emulsion may improve surgical treatment of non-small cell lung cancer
[57].
Considering all the countries covered in the study, India, China, Japan, and South Korea were the
countries with the highest number of species with antitumor activity on different experimental models.
The most used cellular model for investigation of antitumor activity against lung cancer was the
Lewis lung carcinoma. Of the 58 studies that show this cell line being used as an experimental model,
44 showed its sensibility to the samples tested. This shows that this cell line is the most used model
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worldwide to evaluate the antitumor activity in lung cancer cells. Other models cited in few studies
include Small cell lung, Lung cancer and adenomas.
3. Conclusions
Several countries study medicinal plants with antitumor potential, including against lung cancer.
Many species are active in different experimental models. This shows that the natural products from
plants continue being a rich source of herbal medicines or biologically active compounds. There is a
need for further studies on the standardization or chemical characterization of the extracts used. With
respect to pharmacological studies, the most of them it was performed on mice. However studies with
human were also observed for different species of plants. Therefore, new research findings could lead
to greater safety and benefits to people contributing to a better access to health care and thereby a
better quality of life of patients with lung cancer.
Acknowledgments
The authors thank the University of Illinois at Chicago, USA for the use of the NAPRALERT
database for this study and A. Leyva for the English revision of the manuscript. Thanks are in order
also for the financial support provided by CAPES/CNPq/PRONEX-FAPESQ.
Conflicts of Interest
The authors declare no conflict of interest.
Table 1. Medicinal plants and other organisms with antitumor potential against lung cancer.
Family and botanical name
Origin
Part used
Extract
Model
Mammal tested
Result
Reference
AGAVACEAE Yucca aloifolia
USA
Flowers
MeOH Ext
Ca-lewis lung
Mouse
Active
[58]
ALARIACEAE
Undaria pinnatifida
Hawaii
Commercial sample of thallus pacific
Type ext not stated
Ca-lewis lung
Mouse
Active
[59]
Hawaii
Commercial sample of thallus pacific
H2O- Insoluble Extract
Ca-lewis lung
Mouse
Active
[59]
Japan
Commercial sample of thallus pacific
H2O Ext
Ca-lewis lung
Mouse
Active
[60]
Japan
Dried thallus pacific
Polysaccharide fraction
Ca-lewis lung
Mouse
Active
[61]
ANACARDIACEAE
Semecarpus anacardium
India
Dried fruit
CHCl3 Ext
Ca-lewis lung
Mouse
Inactive
[62]
APIDAE
Apis mellifera
Croatia
Fresh venom
Venom
Decreased number of lung
metastases
Mouse
Active
[63]
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APOCYNACEAE
Ervatamia heyneana
India
Leaf
MeOH Ext
Ca-lewis lung
Mouse
Inactive
[64]
ARALIACEAE
Eleutherococcus senticosus
USSR
Root
EtOH (16%) Ext
Chem. induced tumor
Mouse
Active
[65]
Panax ginseng
South Korea
Dried root
H2O Ext
Mice exposed
to benzopyrene Male
mouse Active
[66]
South Korea
Dried root
H2O Ext
Aflatoxin-induced
lung adenoma Mouse
Active
[67]
South Korea
Dried root
H2O Ext
Fluorenyl-induced Lung adenoma
Mouse
Inactive
[67]
South Korea
Dried root
H2O Ext
DMBA-induced lung adenoma
Mouse
Inactive
[67]
South Korea
Dried root
H2O Ext
Urethane-induced lung adenoma
Mouse
Active
[67]
ARECACEAE
Calamus rotang
India
Aerial parts
EtOH-H2O (50%) Ext
Ca-lewis lung
Mouse
Active
[68]
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ASTERACEAE
Tagetes minuta
Ethiopia
Aerial parts
H2O Ext
Ca-lewis lung
Mouse
Active
[69]
CARCHARHINIDAE
Carcharhinus plumbeus
USA
Serum chesapeake bay
-
Ca-lewis lung
Male mouse
Active
[70]
CELASTRACEAE
Maytenus serrata
Ethiopia
Fruit
EtOH (95%) Ext
Ca-lewis lung
Mouse
Active
[71]
Ethiopia
Stemwood
EtOH (95%) Ext
Ca-lewis lung
Mouse
Active
[71]
Ethiopia
Root
EtOH (95%) Ext
Ca-lewis lung
Mouse
Active
[71]
Kenia
Root
EtOH (95%) Ext
Ca-lewis lung
Mouse
Active
[71]
Kenia
Stemwood
EtOH (95%) Ext
Ca-lewis lung
Mouse
Active
[71]
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CHLORELLACEAE
Chlorella vulgaris
Pacific (Japan)
Dried cells
Chromatographic fraction
Ca-lung-3LL
Female mouse
Active
[72]
CLADONIACEAE
Cladonia leptoclada
New Zealand
Thallus
EtOH-H2O (1:1) Ext
Ca-lewis lung
Mouse
Active
[73]
EUPHORBIACEAE
Croton macrostachys
Ethiopia
Fruit
EtOH (95%) Ext
Ca-lewis lung
Mouse
Active
[74]
Ethiopia
Fruit
EtOH (95%) Ext
Ca-lewis lung
Mouse
Active
[75]
Euphorbia esula
USA
Aerial parts
EtOH (95%) Ext
Ca-lewis lung
Mouse
Inactive
[76]
USA
Entire plant
EtOH (95%) Ext
Ca-lewis lung
Mouse
Active
[77]
Euphorbia fischeriana
China
Dried entire plant
EtOH (95%) Ext
Ca-lewis lung
Mouse
Active
[78]
Euphorbia ingens
South Africa
Fresh stem
EtOH-H2O (1:1) Ext
Ca-lewis lung
Mouse
Inactive
[79]
Jatropha gossypiifolia
Costa Rica
Root
H2O Ext
Ca-Lewis lung
Mouse
Inactive
[80]
Costa Rica
Root
EtOH (95%) Ext
Ca-Lewis lung
Mouse
Inactive
[81]
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FABACEAE
Caesalpinia gilliesii USA Dried fruit H2O Ext Ca-lewis lung Mouse Active [82]
Cassia garrettiana Thailand Dried heartwood MeOH Ext Ca-lewis lung Mouse/ip Active [83]
Thailand Dried heartwood MeOH Ext Ca-lewis lung Mouse/ig Active [84]
Sophora flavescens
China
Dried root
Type ext not stated
Ca-lewis lung
Mouse
Active
[85]
Sutherlandia frutescens
South Africa
Fresh flowers
EtOH-H2O (1:1) Ext
Ca-lewis lung
Mouse
Inactive
[86]
GANODERMATACEAE
Ganoderma lucidum Taiwan Dried fruitbody H2O Ext Ca-lewis lung Mouse Active
[87]
Taiwan Dried fruitbody EtOH (95%) Ext Ca-lewis lung Mouse Active
[87]
Taiwan
Dried fruitbody
H2O Ext in
combination with adriamycin
Ca-lewis lung
Mouse
Active
[87]
Taiwan
Dried fruitbody
H2O Ext in combination with
cisplatin
Ca-lewis lung
Mouse
Active
[87]
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Taiwan
Dried Fruitbody
H2O Ext in combination with
fluorouracil
Ca-lewis lung
Mouse
Active
[87]
Taiwan
Dried fruitbody
H2O Ext in
combination with methotrexate
Ca-lewis lung
Mouse
Active
[87]
Taiwan
Dried fruitbody
H2O Ext in combination with
imexon
Ca-lewis lung
Mouse
Active
[87]
Taiwan
Dried fruitbody
H2O Ext in combination with
thioguanine
Ca-lewis lung
Mouse
Active
[87]
Taiwan
Dried mycelium
Hot H2O Ext
Ca-lewis lung
Mouse
Active
[88]
South Korea
Mycelium
Hot H2O Ext
Ca-lewis lung
Mouse
Active
[89]
Japan
Dried fruitbody
H2O Ext
Ca-lewis lung
Mouse
Active
[90]
GERANIACEAE
Pelargonium graveolens
China
Dried root
Type Ext not stated
Ca-lewis lung
Mouse
Active
[85]
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HYMENOCHAETACEAE
Phellinus linteus South Korea Mycelium Polysaccharide fraction
Cancer cell line NCI-H23 Mouse Active [91]
LILIACEAE Allium sativum
Japan
Aged bulb
Aged garlic extract
used
Sarcoma-180 and LL/2 lung
carcinoma cells
Mouse
Active
[92, 93]
LORANTHACEAE
Viscum album
Germany
Dried aerial parts
H2O soluble fraction
Ca-lewis lung
Female mouse
Inactive
[94]
England
Commercial sample of leaf + stem
Type ext not stated
Small cell lung
Human adult
Active
[95]
Switzerland
Commercial sample of entire plant
H2O Ext
Ca-lewis lung
Mouse
Active
[96]
MALVACEAE
Hespesia populnea India Fruit EtOH-H2O (1:1) Ext Ca-lewis lung Mouse Active [68] Hibicus syriacus
Taiwan
Dried rootbark
Acetone Ext
Ca-human-lung
Mouse
Inactive
[97]
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MELASTOMATACEAE
Memecylon umbellatum
India
Leaf
EtOH-H2O (1:1) Ext
Ca-lewis lung
Mouse
Inactive
[68]
NYCTAGINACEAE
Mirabilis multiflora USA Root H2O Ext Ca-lewis lung Mouse Inactive [98]
NYSSACEAE
Nyssa sylvatica Not stated Stembark H2O Ext Ca-lewis lung Mouse Inactive [99]
OCHNACEAE
Lophira lanceolata Nigeria Rootbark EtOH-H2O (1:1) Ext Ca-lewis lung Mouse Inactive [100]
OSCILLATORIACEAE
Oscillatoria acutissima strain B.1 Hawaii Freeze-dried organism Type ext not stated Ca-lewis lung Mouse Inactive [101]
PAPAVERACEAE
Chelidonium majus
Austria
Dried entire plant
Alkaloid fraction
Lung cancer
Human adult
Active
[102]
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PECTINIDAE
Patinopecten yessoensis
Pacific (Japan)
Fresh organism
Polysaccharide fraction
Cells-human-embryonic-lung
Mouse
Inactive
[103]
RANUNCULACEAE
Nigella sativa India Seed EtOH-H2O (50%) Ext Ca-lewis lung Mouse Active [68]
Singapore
Commercial sample
of seed Chromatographic
fraction Ca-lewis lung
Mouse
Active
[104]
RUBIACEAE Morinda citrifolia
Hawaii
Dried fruit juice
EtOH insoluble fraction
Ca-lewis lung
Mouse
Active
[105]
RHIZOPHORACEAE
Bruguiera sexangula
Papua-New Guinea
Stembark
EtOH (95%) Ext
Ca-lewis lung
Mouse
Active
[106]
SCHISANDRACEAE
Schisandra propinqua
China
Dried root + Stem
Hot H2O Ext
Ca-human-lung
Human adult
Active
[107]
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SIMAROUBACEAE
Brucea javanica
China
Dried part not specified
Type ext not stated
Lung cancer
Human adult
Active
[108]
China
Seed
Seed oil
Squamous carcinoma and
adenocarcinoma
Human adult
Active
[109]
China
Seed
Seed oil
The extract showed a
therapeutic effect for lung cancers
Human adult
Active
[110]
China
Seed
Fixed oil
Patients with lung cancer
Human adult
Active
[111]
SOLANACEAE
Withania somnifera
India
Dried root
EtOH (95%) Ext
Lung adenomas
Mouse Male
Active
[112]
India
Dried entire plant
EtOH (95%) Ext
Lung adenomas
Mouse
Active
[113]
SQUALIDAE
Squalus acanthias
Not stated
Cartilage
H2O Ext
Ca-lewis lung
Mouse
Active
[114]
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THEACEAE
Camellia sinensis
China
Dried leaf
Polyphenolic fraction
Lung cancer
Female mouse
Active
[115]
China
Green leaf
Tea
Lung cancer
Human adult
Active
[116]
China
Black leaf
Leaves
Reduced tumor multiplicity and volume in nnk treated mice
Female mouse
Active
[117]
TRICHOLOMATACEAE
Hypsizigus marmoreus Japan Dried fruit H2O Ext
Ca-lewis lung
Mouse Active [118]
Lentinus edodes
Japan
Dried fruit body
H2O Ext
Ca-lewis lung Mouse
Active
[119]
VIOLACEAE
Viola odorata
South Africa
Fresh leaf
EtOH-H2O (1:1) Ext
Ca-lewis lung Mouse
Inactive
[79]
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