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The Genus Terminalia (Combretaceae): An Ethnopharmacological, Phytochemical and Pharmacological Review

  • Xiao-Rui Zhang
  • Joseph Sakah Kaunda
  • Hong-Tao Zhu
  • Dong Wang
  • Chong-Ren Yang
  • Ying-Jun ZhangEmail author
Open Access
Review
  • 180 Downloads

Abstract

Terminalia Linn, a genus of mostly medium or large trees in the family Combretaceae with about 250 species in the world, is distributed mainly in southern Asia, Himalayas, Madagascar, Australia, and the tropical and subtropical regions of Africa. Many species are used widely in many traditional medicinal systems, e.g., traditional Chinese medicine, Tibetan medicine, and Indian Ayurvedic medicine practices. So far, about 39 species have been phytochemically studied, which led to the identification of 368 compounds, including terpenoids, tannins, flavonoids, phenylpropanoids, simple phenolics and so on. Some of the isolates showed various bioactivities, in vitro or in vivo, such as antitumor, anti HIV-1, antifungal, antimicrobial, antimalarial, antioxidant, diarrhea and analgesic. This review covers research articles from 1934 to 2018, retrieved from SciFinder, Wikipedia, Google Scholar, Chinese Knowledge Network and Baidu Scholar by using “Terminalia” as the search term (“all fields”) with no specific time frame setting for the search. Thirty-nine important medicinal and edible Terminalia species were selected and summarized on their geographical distribution, traditional uses, phytochemistry and related pharmacological activities.

Keywords

Terminalia Combretaceae Ethnomedicine Traditional uses Phytochemistry Hydrolyzable tannins Pharmacology 

Abbreviations

A.

Aspergillus

BCG

Bacillus Calmette Guerin

BMM

Broth microdilution method

Ca.

Candida

Cr.

Cryptococcus

CC50

Cytotoxic concentration of the extracts to cause death to 50% of host’s viable cells

DPPH

2,2-Diphenyl-1-picrylhydrazyl

E.

Escherichia

EC50

Half maximal effective concentration

FRAP

Ferric reducing/antioxidant power

GABA

Neurotransmitter gamma-aminobutyric acid

IC50

Minimum inhibition concentration for inhibiting 50% of the pathogen

K.

Klebsiella

MIC

Minimum inhibitory concentration

MTT

3-(4,5-Dimethylthiazol-2-yl)-2,5-diphenyl tetrazolium bromide

Ps.

Pseudomonas

Sa.

Salmonella

Sta.

Staphylococcus

Str.

Streptomyces

1 Introduction

Terminalia Linn, comprising about 250 species in the world mostly as medium or large trees, is the second largest genus in the family Combretaceae. The name “Terminalia” is derived from Latin word “terminus”, which means the leaves are located at the tip of the branch. The bark of Terminalia plants usually has cracks and branches tucked into layers. Most of the Terminalia plants’ leaves are large, leathery with solitary or clustered small green white flowers. Their fruits are yellow, dark red or black; drupe, usually angular or winged. Some fruits are edible, highly nutritious and possess medicinal values.

Terminalia species are widely distributed in the southern Asia, Himalayas, Madagascar, Australia, and the tropical and subtropical regions of Africa. Terminalia plants in southern Asia have been intensively studied phytochemically due to their wide usage in Asian (India, Tibetan, and Chinese) traditional medicine systems [1]. For example, the fruits of Terminalia bellirica and Terminalia chebula, together with Phyllanthus emblica (Euphorbiaceae) which form the herbal remedy, Triphala, in Tibetan medicine, have received much attention because of its extensive and remarkable effectiveness in the treatment of anticancer, antifungal, antimicrobial, antimalarial, antioxidant.

So far, 39 Terminalia species have been investigated for their phytochemical constituents, which resulted in the identification of terpenes, tannins, flavonoids, lignans and simple phenols, amongst others. Pharmacological studies suggest that they have exhibited activity on liver and kidney protection, antibacterial, antiinflammatory, anticancer, and have displayed a positive effect on immune regulation, cardiovascular disease and diabetes, and acceleration of wound healing.

This paper features 39 important medicinal and edible Terminalia species and summarizes their traditional usage, geographical distribution, structures of isolated chemical constituents and pharmacological activities.

2 Species’ Description, Distribution and Traditional Uses

So far, 50 Terminalia species have been documented, 39 of which have been reported to possess medicinal properties and/or being edible. Among them, eight species and four varieties including T. argyrophylla, T. bellirica, T. catappa, T. chebula, T. franchetii, T. hainanensis, T. myriocarpa, T. intricate, T. chebula var. tomentella, T. franchetii var. membranifolia, T. franchetii var. glabra, and T. myriocarpa var. hirsuta are distributed in China (Yunnan, southeast Tibet, Taiwan, Guangdong, south Guangxi and southwest Sichuan). Their distribution and traditional applications are shown in Table 1.
Table 1

Local names, distributions and traditional uses of Terminalia plants

No.

Plants

Local names

Distributions

Traditional uses

T1

T. alata

Unknown

Southern Vietnam [2, 3]

Anti-diarrhea, ulcer, diuretics, supplements [3]

T2

T. amazonia

White olive

Southern Costa Rica [4]

Wood

T3

T. arborea

Jaha Kling

Indonesia

Cardiovascular disease, myocardial infarction, atherosclerosis, diabetes, cancer, stroke, cataract, shoulder stiffness, cold allergy, hypertension, senile dementia, inflammation, gum disease (e.g. gingivitis, pneumonia), Alzheimer’s, skin conditions [5]

T4

T. arjuna

Arjuna, White Marudah, Koha

India, South Asia, Sri Lanka [6]

Cardiotonic, sores, bile infection, poison antidote [6]

Coughs, dysentery, fractures, contusions, ulcers, hypertension ischaemic heart diseases [23]

T5

T. argyrophylla

Silver leaves Chebula, Xiao Chebula (Yunnan), Manna (Yunnan Dai language)

China (Yunnan) [7]

Autoimmune diseases [7]

T6

T. australis

Tanimbu, palo amarillo

Punta Lara, Argentina (Buenos Aires) [8]

Hemostasis

T7

T. avicennioides

kpayi, Kpace, baushe

Nigeria [9, 10]

Malaria, worms, gastric peptic ulcer [9], scorpion bites [10], tuberculosis, cough [90]

T8

T. bellirica

Beleric

China (southern Yunnan), Vietnam, Laos, Thailand, Cambodia, Myanmar, India (except West), Malaysia, Indonesia

Laxative, edible

Edema, diarrhea, leprosy, bile congestion, indigestion, headache [11]

Fever, diarrhea, cough, dysentery, skin diseases [12]

Wine, palm sugar [23]

Diarrhea [94]

T9

T. bentzoe

Unknown

Rodrigues [13]

Essential oil [13]

T10

T. bialata

Indian silver greywood

India, South Asia

Wood [14]

T11

T. brachystemma

Kalahari cluster leaf

Southern Africa

Shistosomiasis, gastrointestinal disorders [15]

T12

T. brownii

kuuku, muvuku (Kamba, Kenya), koloswa (northern region, Kenya), weba (Ethiopia), lbukoi (Samburu, Kenya), orbukoi (Maasai, Tanzania), and mbarao or mwalambe, in Kiswahili

Southern and central Africa

Diarrhea, stomach pain, gastric ulcer, colic, heartburn

Genitourinary infection, urethral pain, endometritis, cystitis, leucorrhea, syphilis, gonorrhea, malaria, dysmenorrhea, nervousness, hysteria, epilepsy, athlete’s foot, indigestion, stomach pain, gastric ulcer, colitis, cough, vomiting, hepatitis, jaundice, cirrhosis, yellow fever [16]

T13

T. bursarina

Yellow wood

Australia, South Asia [17]

Unknown

T14

T. calamansanai

Phillipine almond, Anarep

Philippines, Southeast Asia

Lithontriptic [18], horticultural plant [102]

T15

T. calcicola

Unknown

Madagascar Rain Forest [19]

Unknown

T16

T. catappa

Indian almond, umbrella tree, tropical almond

China (Guangdong, Taiwan, SE Yunnan), Australia and SE Asia, Africa, South America Tropical Coast

Blood stasis, liver injury [20]

Diarrhea, dysentery, biliary inflammation [23], dermatitis, hepatitis [106]

T17

T. chebula

Black Mytrobalan, Inknut, Chebulic Myrobalan

Nepal, northern India, Myanmar, Sri Lanka, Thailand, Bangladesh, China (Yunnan), Himalayan

Digestion appetizers, vomiting, infertility, asthma, sore throat, vomiting, urticaria, diarrhea, dysentery, bleeding, ulcers, gout, bladder disease [21]

T18

T. chebula var. tomentella

Weimaohezi (variant)

China (western Yunnan), Myanmar

Unknown

T19

T. citrina

Manahei, Yellow myrobalan

India, Bangladesh [22]

Dysmenorrhea, bleeding, heart disease, dysentery, constipation [22]

T20

T. elliptica

Indian laurel

SE Asia, India, Bangladesh, Laos, Myanmar, Nepal, Thailand, Cambodia, Vietnam

Wine, palm sugar

Ulcers, fractures, bleeding, bronchitis, diarrhea [23]

T21

T. franchetii

Dianlanren

SW China [24]

Unknown

T22

T. franchetii var. membranifolia

Baoyedianlanren (variant)

China [western Guangxi (Longlin), central to SE Yunnan]

Unknown

T23

T. franchetii var. glabra

Guang yedianlanren (variant)

China (Sichuan and Yunnan Jinsha River Basin)

Unknown

T24

T. ferdinandiana

Gubinge, Bbillygoat plum, Kakadu plum, green plum, salty plum, murunga, mador

Australia [25]

Dietary supplements, skin care [25]

T25

T. glaucescens

Unknown

Nigeria [26]

Amenorrhea, vaginal infections, syphilis, sores, neurological disorders

Anti-plasma, antiparasitic, antiviral, antimicrobial [26, 27]

T26

T. hainanensis

Ji zhenmu, Hainan lanren

China (Hainan)

Antioxidant [28]

T27

T. intricate

Cuozhilanren

China (NW Yunnan and SW Sichuan)

Unknown

T28

T. ivorensis

Idigbo, Black Afara, Shingle Wood, Brimstone Wood, Blackbark

Cameroon, West Africa, Ivory Coast, Liberia, Nigeria, Sierra Leone, Ghana

Rheumatism, gastroenteritis, psychotic analgesics [29]

Syphilis, burns and bruises [30]

T29

T. kaernbachii

Okari Nut

Solomon Islands, Papua New Guinea

α-Glucosidase inhibitor activity [31]

T30

T. kaiserana

Unknown

Tanzania

Diarrhea, gonorrhea vomiting [44]

T31

T. laxiflora

Unknown

West Africa, Sudan Savannah

Malaria, cough [32]

Fumigant, rheumatic pain, smoothen skin, body relaxation [33]

T32

T. macroptera

Bayankada

Tropical (West Africa)

Wound, hepatitis, malaria, fever, cough, diarrhea, tuberculosis, skin diseases [34]

T33

T. mantaly

Unknown

Africa, Madagascar

Dysentery

T34

T. mollis

Bush willow

Africa

Diarrhea, gonorrhea, malaria, AIDS adjuvant therapy [35]

T35

T. muelleri

Ketapang kencana

Indonesia, SE Asia, South Asia

Antibacterial [36], antioxidants [37]

T36

T. myriocarpa

Qianguolanren

China [Guangxi (Longjin), Yunnan (central to the south), and Tibet (Medog)], northern Vietnam, Thailand, Laos, northern Myanmar, Malaysia, NE India, Sikkim

Antioxidant, liver protection [38]

T37

T. myriocarpa var. hirsuta

Yingmaoqianguolanren (variant)

Yunnan, China; Thailand

Unknown

T38

T. oblongata

Rose wood, yellow wood

Central Queensland [39]

Unknown [39]

T39

T. paniculata

Vellamaruth

India

Cholera, mumps, menstrual disorders, cough, bronchitis, heart failure, hepatitis, diabetes, obesity [40]

T40

T. parviflora

Tropical almond, umbrella tree, Indian almond

Sri Lanka and India [41]

Diarrhea [41]

T41

T. prunioides

Hareri, Sterkbos, Purple pod Terminalia, Mwangati

Southern Africa

Postnatal abdominal pain

T42

T. sambesiaca

Unknown

Southern Africa

Cancer, gastric ulcer, appendicitis

Bloody diarrhea [45]

T43

T. schimperiana

Idi odan

Africa, Sierra Leone, Guinea, Uganda, Ethiopia

Local burns, bronchitis, dysentery [42]

T44

T. sericea

Monakanakane, Mososo, Mogonono, Amangwe, Vaalboom, Mangwe, Silver clutter-leaf

Northern South Africa, Botswana (except central Kalahari), southern Mozambique, Tanzania, Namibia, Zimbabwe, Northern Democratic Republic of Congo, tropical Africa [43]

Diarrhea, sexually transmitted infections, rash, tuberculosis [43]

Fever, high blood pressure [44]

T45

T. spinosa

Musosahwai, spiny cluster leaf, Kasansa

Southern Africa

Malaria, fever [46]

Epilepsy, poisoning [47]

T46

T. stenostachya

Rosette leaf Terminalia

Southern Africa

Epilepsy, poisoning [47]

T47

T. stuhlmannii

Unknown

Acacia [48]

Unknown

T48

T. superba

Limba

Tropical Western Africa

Gastroenteritis, diabetes, female infertility, abdominal pain, bacteria/fungi/viral infections [49], diabetes remedies, anesthetic, hepatitis [50]

T49

T. triflora

Lanza, lanza amarilla, amarillo derío, paloamarillo

Tropical (South America)

Northern and Northwest Argentina [149]

Making posts, furniture, weapons, fuel [149]

T50

T. tropophylla

Unknown

Madagascan [51]

Unknown

SE southeastern, NE northeastern, SW southwestern, NW northwestern

Terminalia species are broadly used in many aspects. Some are employed as drugs, while others can provide high quality wood, tannin or dyes. For example, fruits of T. ferdinandiana, a species largely distributed in Australia, are rich in vitamin C, and possess strong antioxidant activity [25]. T. bellirica and T. chebula are not only recorded in every version of Chinese pharmacopoeia, but are also the important and most commonly applied drugs in Han, Tibetan, Mongolian and many other folk medicinal systems in India, Burma, Thailand, Malaysia, Vietnam and other southeast asian countries. T. catappa is a commonly used medicinal plant for liver protection in China [20].

3 Chemical Composition

Since 1930s, the chemical compositions of the genus Terminalia have been vastly studied. T. arjuna, T. bellirica, T. catappa and T. chebula, having been frequently used in the Ayurvedic, Chinese and Tibetan medicines, attracted scholars’ attention. To date, 368 compounds, largely terpenoids (1–104), tannins (105–196), flavonoids (197–241), lignans (242–265), phenols and glycosides (268–318) were reported from the genus (Tables 2, 3).
Table 2

Chemical constituents isolated from the genus Terminalia and the studied plant organs

No.

Compounds

Plants

Organs

References

Triterpenes (86)

 1

2α,3β,19α-Trihydroxyolean-12-en-20-oic acid 3-O-β-d-galactosyl-(1 → 3)-β-d-glucoside

T1

R

[3]

 2

2α,3β,19α-Trihydroxyolean-12-en-28-oic acid methylester 3β-O-rutinoside

T1

R

[53]

 3

2α,3β,19β,23-Tetrahydroxyolean-12-en-28-oic acid 3β-O-β-d-galactosyl-(1 → 3)-β-d-glucoside-28-O-β-d-glucoside

T1

R

[52]

 4

3-Acetylmaslinic acid

T1

RB

[54]

 5

Arjunic acid

T1

T4

T17

T25

T28

T32

T44

B

SB, F

F

SB

B

B

R

[55, 74]

[60, 79, 124]

[146]

[130]

[132]

[145]

[133]

 6

Arjunoside I

T4

SB

[61]

 7

Arjunoside II

T4

SB

[61]

 8

Arjunoside III

T4

R

[62, 63]

 9

Arjunoside IV

T4

R

[62, 63]

 10

Arjunetin

T1

T4

T8, T16, T17, T20, T39

B

B, L, S, R, F

B, L, S, R, F

[55, 74]

[23, 67]

[23]

 11

Oleanolic acid

T1

T9

T4, T16, T20

T8, T17

T39

T28

T36

H

L

B, L, S, R, F

B, L, S, R

L, S, R, F

B

B

[56]

[97]

[23]

[23]

[23]

[132]

[140]

 12

Ursolic Acid

T4, T16, T20

T8, T17

T39

B, L, S, R, F

L, S, R

B, L, S, F

[23]

[23]

[23]

 13

Maslinic acid

T1

T9

T17

T36

H

L

F

B

[56]

[97]

[21, 116]

[140]

 14

2α,3α,24-Trihydroxyolean-11,13(18)-dien-28-oic acid

T33

SB

[158]

 15

Terminoside A

T4

B

[58]

 16

Arjungenin

T4

T25

T12

T8, T16, T20, T39

T17

T25

T28

T32

T33

T44

SB,L,R,F

R

B

B, L, S, R, F

B, L, S, R, F

R, SB

B

B

SB

RB

[23, 60, 70, 74]

[60]

[99]

[23]

[23, 146]

[69, 130]

[132]

[145]

[158]

[133, 152]

 17

Hypatic acid

T25

R

[69]

 18

Arjunglucoside I

T4

T17

T50

T32

B, R

F

R

B

[70, 74, 78]

[146]

[72]

[145]

 19

Sericoside

T4

T25

T28

T44

T32

T50

B

SB

B

R, L, SB

B

R

[71]

[130]

[76, 131]

[43, 133, 149]

[145]

[72]

 20

Crataegioside

T4

T17

B

F

[75]

[146]

 21

23-O-neochebuloylarjungenin 28-O-β-d-glycosyl ester

T17

F

[146]

 22

23-O-4′-epi-neochebuloylarjungenin

T17

F

[146]

 23

23-O-galloylarjunic acid

T39

T32

B

B

[144]

[145]

T17

F

[146]

 24

Quercotriterpenoside I

T32

B

[145]

T17

F

[146]

 25

Sericic acid

T28

T32

T44

B

B

R

[132]

[145]

[150]

 26

24-Deoxy-sericoside

T32

B

[138]

 27

Arjunolic acid

T1

T4

T7

T9

T8

T16, T17, T20, T39

T34

T36

B, H

B, H, L, S, R, F

RB

L

B, L, S, R

B, L, S, R, F

L

B

[55, 56, 74]

[23, 77, 78, 91]

[97]

[23]

[23]

[23, 144]

[35]

[140]

 28

Terminolic acid

T1

T17

T7, T16, T31

T25

T32

H

F

H

H, Rl

H, B

[56]

[146]

[128]

[128]

[128, 145]

 29

Arjunglucoside II

T4

T17

B

F

[70, 74]

[146]

 30

23-O-galloylarjunolic acid

T17

F

[146]

 31

23-O-galloylarjunolic acid 28-O-β-d-glucosyl ester

T17

F

[146]

 32

23-O-galloylterminolic acid 28-O-β-d-glucosyl ester

T17

F

[146]

 33

Arjunolitin

T4

SB

[80]

 34

Terminolitin

T4

F

[80]

 35

Arjunglucoside III

T4

B

[74]

 36

Methyl oleanate

T4

R, F

[80, 124]

 37

Olean-3α,22β-diol-12 en-28-oic acid 3-O-β-d-glucosyl-(1 → 4)-β-d-glucoside

T4

B

[81, 84]

 38

Arjunetoside

T4

R, SB

[82]

 39

Olean 3β,6β,22α-triol-12en-28-oic acid-3-O-β-d-glucosyl-(1 → 4)-β-d-glucoside

T4

B

[84]

 40

2α,19α,Dihydroxy-3-oxo-olean-12-en-28-oic acid-28-O-β-d-glucoside

T4

R

[85]

 41

Ivorengenin A (2α,19α,24-trihydroxy-3-oxoolean-12-en-28-oic acid)

T28

B

[132]

 42

Chebuloside I

T17

F

[115]

 43

Chebuloside II

T17

T32

F

B

[115]

[138]

 44

Arjunglucoside

T17

T44

T33

F

R, SB

SB

[115]

[133]

[158]

 45

Glaucescic acid (2α,3α,6α,23-tetrahydroxyolean-2-en-28-oic acid)

T25

R

[69]

 46

Glaucinoic acid (2α,3β,19α,24-tetrahydroxyolean-12-en-30-oic acid)

T25

SB

[130]

 47

Termiarjunoside I (olean-1α,3β,9α,22α-tetraol-12-en-28-oic acid-3-β-d-glucoside)

T4

SB

[156]

 48

Termiarjunoside II (olean-3α,5α,25-triol-12-en-23,28-dioic acid-3α-d-glucoside)

T4

SB

[156]

 49

β-Amyrin

T25

T36

SB

B

[129]

[140]

 50

Ivorenoside A

T28

B

[131]

 51

Ivorenoside B

T28

B

[131]

 52

Ivorenoside C

T28

B

[131]

 53

Ivorengenin B (4-oxo-19α-hydroxy-3,24-dinor-2,4-secoolean-12-ene-2,28-dioic acid)

T28

B

[132]

 54

1α,3β-Hydroxyimberbic acid 23-O-α-l-4-acetylrhamnoside

T47

SB

[48]

 55

1α,3β,3,23-Trihydroxy-olean-12-en-29-oate-23-O-α-[4-acetoxyrhamnosyl]-29-α-rhamnoside

T47

SB

[48]

 56

2α,3β-Dihydroxyolean-12-en-28-oic acid 28-O-β-d-glucoside

T48

SB

[49]

 57

2α,3β,21β-Trihydroxyolean-12-en-28-oic acid 28-O-β-d-glucoside

T48

SB

[49]

 58

2α,3β,29-Trihydroxyolean-12-en-28-oic acid 28-O-β-d-glucoside

T48

SB

[49]

 59

2α,3β,23,27-Tetrahydroxyolean-12-en-28-oic acid 28-O-β-d-glucoside

T48

SB

[49]

 60

Terminaliaside A ((3β,21β,22α)-3-O-(3′-O-angeloylglucosyl)-21,22-dihydroxy-28-O-sophorosyl-16-oxoolean-12-ene)

T50

R

[72]

 61

2, 3, 23-Trihydroxylolean-12-ene

T7

RB

[91]

 62

2α,3β,23-Trihydroxylolean-12-en-28-oic acid

T48

SB

[49]

 63

23-O-galloylpinfaenoic acid 28-O-β-d-glucosyl ester

T17

F

[146]

 64

Pinfaenoic acid 28-O-β-d-glucosyl ester

T4

T17

B

F

[76]

[146]

 65

2α,3β-Dihydroxyurs-12,18-dien-28-oic acid 28-O-β-d-glucosyl ester

T4

B

[76]

 66

Quadranoside VIII

T4

B

[76]

 67

Kajiichigoside F1

T4

B

[76]

 68

2α,3β,23Trihydroxyurs-12,19-dien-28-oic acid 28-O-β-d-glucosyl ester

T4

B

[76]

 69

α-Amyrin

T7

RB

[91]

 70

2α,3β,23-Trihydroxy-urs-12-en-28-oic acid

T34

L

[35]

 71

2α-Hydroxyursolic acid

T34

T17

L

F

[35]

[115, 116]

 72

Ursolic acid

T11

L

[35]

 73

2α-Hydroxymicromeric acid

T17

F

[115, 116]

 74

Betulinic acid

T1

T11

T12

T4, T16, T17, T20, T39

T8

T25

T28

T36

B

L

B

B, L, S, R, F

B, L, S, R

SB

B

B

[55]

[35]

[99]

[23]

[23]

[129]

[132]

[140]

 75

Terminic acid

T4

R, H

[57, 62]

 76

Lupeol

T4

T25

T44

SB

SB

SB, R

[80]

[129]

[43]

 77

Monogynol A

T12

B

[99]

 78

Triterpenes

T25

T44

SB

R, SB

[129]

[133]

 79

Friedelin

T4

T7

T25

T34

F

RB

SB

SB

[83]

[93]

[129, 130]

[35]

 80

Maslinic lactone

T1

H

[56]

 81

Terminalin A

T25

SB

[129]

 82

Arjunaside A

T4

B

[68]

 83

Arjunaside B

T4

B

[68]

 84

Arjunaside C

T4

B

[68]

 85

Arjunaside D

T4

B

[68]

86

Arjunaside E

T4

B

[68]

Mono- (14) and sesqui- (4) terpendoids

 87

α-Pinene

T9

L

[13]

 88

Sabinene

T9

L

[13]

 89

Myrcene

T9

L

[13]

 90

β-Pinene

T9

L

[13]

 91

1,8-Cineole

T9

L

[13]

 92

Linalool

T9

L

[13]

 93

Menthone

T9

L

[13]

 94

γ-Terpineol

T9

L

[13]

 95

α-Terpineol

T9

L

[13]

 96

Limonene

T9

L

[13]

 97

Neral

T9

L

[13]

 98

Geraniol

T9

L

[13]

 99

Thymol

T9

L

[13]

 100

Isomenthone

T9

L

[13]

 101

β-Copaene

T9

L

[13]

 102

β-Caryophyllene

T9

L

[13]

 103

Caryophyllene

T9

L

[13]

 104

α-Humulene

T9

L

[13]

Hydrolysable (89) and condensed tannins (2)

 105

1,2,3,6-Tetra-O-galloyl-β-d-glucose

T17

F

[159]

 106

Gallotannin (1,2,3,4,6 penta galloyl glucose)

T4

T17

T19

T30

T45, T46

SB, L

F

F

R

L

[86]

[21, 118, 119]

[120]

[133]

[133]

 107

1,3,4,6-Tetra-O-galloyl-β-d-glucose

T17

F

[159]

 108

2,3,4,6-Tetra-O-galloyl-d-glucose

T3

T4

F

SB, L

[154]

[86]

 109

1,2,6-Tri-O-galloyl-β-d-glucose

T31

R

[101]

 110

Sanguiin H-1

T14

L

[102]

 111

1,6-Di-O-galloyl-β-d-glucose

T3

T17

T40

F

F

B

[154]

[21, 119]

[41]

 112

1,3,6-Tri-O-galloyl-β-d-glucose

T3

T40

T19

T17

F

B

F

F

[154]

[41]

[120]

[159]

 113

Methyl 3,6-di-O-galloyl-β-d-glucoside

T40

B

[41]

 114

4,6 Bis hexahydroxydiphenyl-1-galloyl-glucose

T4

SB, L

[86]

 115

Sanguiin H-4

T14 

L

[18, 102]

 116

Corilagin

T3

T31

T16

T17

T19

T24

T32

F

R

L, B

F

F

F

L

[154]

[101]

[41, 106, 107]

[21, 118, 119, 159]

[120]

[126]

[135, 136]

 117

Tercatain

T16

T17

B, L

F

[41, 106, 107]

[159]

 118

1,3-Di-O-galloyl-β-d-glucose

T17

F

[159]

 119

2,3-O-(S)-HHDP-d-glucose

T3

T14

T4

T16

T40

T36

F

L

B

B, L

B

L

[154]

[102]

[104]

[41, 107]

[41]

[38]

 120

2,3-(S)-HHDP-6-O-galloyl-d-glucose

T3

T4

T40

T32

F

B

B

B

[154]

[104]

[41]

[137]

 121

3,6-Di-O-galloyl-d-glucose

T3

T40

T17

F

B

F

[154]

[41]

[159]

 122

3,4-Di-O-galloyl-d-glucose

T3

F

[154]

 123

6-O-galloyl-d-glucose

T17

F

[159]

 124

3,4,6-Tri-O-galloyl-d-glucose

T17

F

[159]

 125

Tellimagrandin I

T35

T17

L

F

[139]

[159]

 126

Gemin D

T17

F

[159]

 127

Arjunin

T4

T17

L

F

[65, 86]

[115]

 128

Punicalin

T3

T4

T14

T40

T16

T17

T28

T49

F

L, B

L

B

L

L, F

SB

L

[154]

[65, 86, 104]

[102]

[41]

[106, 107]

[21, 155]

[29]

[149]

 129

Casuarinin

T4

T16

T17

L, B

B

F

[88, 104]

[41]

[21, 118, 119]

 130

Casuariin

T4

B

[90, 104]

 131

Terchebulin

T3

T4

T7

T12

T17

T31

F

B

SB

B

F

W

[154]

[90, 104]

[92]

[100]

[21]

[134]

 132

Castalagin

T4

T16, T40

B

B

[90, 104]

[41]

 133

Grandinin

T16, T40

B

[41]

 134

Castalin

T16, T40

B

[41]

 135

α/β-Punicalagin

T3

T7

T4

T11

T12

T31

T14

T16

T17

T40

T19

T28

T32

T35

T36

T38

F

SB

B

L

B

R

L

B

L, F

B

F

SB

B

L

L

L

[154]

[92]

[104]

[35]

[100]

[101]

[18, 103]

[41]

[21, 106, 119, 155]

[41]

[120]

[29]

[137]

[139]

[38]

[39]

 136

1-α-O-galloylpunicalagin

T14 

L

[18, 102, 103]

 137

6′-O-methyl neochebulagate

T17

F

[159]

 138

Dimethyl neochebulagate

T17

F

[159]

 139

Neochebulagic acid

T17

F

[159]

 140

Dimethyl 4′-epi-neochebulagate

T17

F

[159]

 141

Methyl chebulagate

T17

F

[159]

 142

Chebulagic acid

T3

T4

T8

T17

T16

T39

T20

T19

T32

T35

F

B, L, S

F, B, L, S

F, B, L, S, R

F, B, L, S, R

F, B, L, S, R

F, B, L, R

F

L

L

[154]

[23]

[23]

[23, 96]

[3, 4, 9, 21, 110]

[23]

[23]

[120]

[135, 136]

[139]

 143

Chebulinic acid

T3

T4, T8, T16, T20, T39

T17

T32

T35

F

F, B, L, S, R

F, B, L, S, R

L

L

[154]

[23]

[3, 4, 21, 110, 119, 155]

[23]

[110, 135, 139]

 144

Chebulanin

T34, T11

T17

L

F

[35]

[21, 119, 155, 159]

 145

1,3-Di-O-galloyl-2,4-chebuloyl-β-d-glucose

T3

F

[154]

 146

1,6-Di-O-galloyl-2,4-chebuloyl-β-d-glucose

T17

F

[155, 159]

 147

2-O-galloylpunicalin

T14

T40

T32

T49

L

B

B

L

[18]

[41]

[137]

[149]

 148

1-Desgalloyleugeniin

T14

T16

L

L

[102]

[107]

 149

Eugeniin

T14 

L

[102]

 150

Rugosin A

T14 

L

[102]

 151

1(α)-O-galloylpedunculagin

T14 

L

[102]

 152

Praecoxin A

T14 

L

[102]

 153

Calamansanin

T14 

L

[102]

 154

Calamanin A

T14 

L

[102]

 155

Calamanin B

T14 

L

[102]

 156

Calamanin C

T14 

L

[102]

 157

Terflavin C

T4

T14

T17

B

L

L

[104]

[103]

[21]

 158

Terflavin A

T16

T17

T32

L

F

B

[106, 107]

[21]

[137]

 159

Terflavin B

T16

T17

T32

L

L, F

B

[106, 107]

[21, 155]

[137]

 160

3-Methoxy-4-hydroxyphenol-1-O-β-d-(6′-O-galloyl)-glucoside

T16

B

[41]

 161

3,5-Di-methoxy-4-hydroxyphenol-1-O-β-d-(6′-O-galloyl)-glucoside

T16

B

[41]

 162

Acutissimin A

T16

B

[41]

 163

Eugenigrandin A

T16

B

[41]

 164

Catappanin A

T16

B

[41]

 165

Castamollinin

T40

B

[41]

 166

Tergallagin

T16

L

[106, 107]

 167

Geraniin

T16

L

[107]

 168

Granatin B

T16

L

[107]

 169

Gallotannic (tannic acid)

T17,T8

T38

F

L

[113]

[141]

 170

Chebulin

T17

F

[113, 114]

 171

Terchebin

T17

F

[113, 119]

 172

Neochebulinic acid

T3

T17

F

F

[154]

[21, 119, 155]

 173

Chebumeinin A

T17

F

[118]

 174

Chebumeinin B

T17

F

[118]

 175

Isoterchebulin

T32

B

[137]

 176

Punicacortein C

T3

T32

T17

F

B

F

[154]

[137]

[159]

 177

Punicacortein D

T17

F

[159]

 178

4,6-O-Isoterchebuloyl-d-glucose

T32

B

[137]

 179

Trigalloyl-β-d-glucose

T35

L

[139]

 180

Tetragalloyl-β-d-glucose

T35

L

[139]

 181

Pentagalloyl-β-d-glucose

T35

L

[139]

 182

1,2,3-Tri-O-galloyl-6-O-cinnamoyl-β-d-glucose

T17

F

[159]

 183

1,2,3,6-Tetra-O-galloyl-4-O-cinnamoyl-β-d-glucose

T17

F

[159]

 184

1,6-Di-O-galloyl-2-O-cinnamoyl-β-d-glucose

T17

F

[159]

 185

1,2-Di-O-galloyl-6-O-cinnamoyl-β-d-glucose

T17

F

[159]

 186

4-O-(2′′, 4′′-di-O-galloyl-α-l-rhamnosyl) ellagic acid

T17

F

[159]

 187

4-O-(4′′-O-galloyl-α-l-rhamnosyl) ellagic acid

T17

F

[159]

 188

4-O-(3′′, 4′′-di-O-galloyl-α-l-rhamnosyl) ellagic acid

T17

F

[159]

 189

1′-O-methyl neochebulanin

T17

F

[159]

 190

Dimethyl neochebulinate

T17

F

[159]

 191

Phyllanemblinin E

T17

F

[159]

 192

1′-O-methyl neochebulinate

T17

F

[159]

 193

Phyllanemblinin F

T17

F

[159]

 194

Procyanidin B-1

T16

B

[41]

 195

3′-O-galloyl procyanidin B-2

T16

B

[41]

Flavonoids (45)

 196

5,7,2′-Tri-O-methylflavanone4′-O-α-l-rhamnosyl-(1 → 4)-β-d-glucoside

T1

R

[52]

 197

Arjunone

T4

B, F

[83, 89]

 198

8-Methyl-5,7,2′,4′-tetramethoxy-flavanone 

T1

T39

R

B

[53]

[144]

 199

Naringin

T4

T8

T17

T39

T20

L, S, F

B, F

L, R, F

R, F

B, L, S, R

[23]

[23]

[23]

[23]

[23]

 200

Eriodictyol

T4, T8, T17, T20, T39

T16

B, L, S, R, F

L, S, R, F

[23]

[23]

 201

Hesperitin

T24

F

[122]

 202

Flavanone

T24

F

[122]

 203

Arjunolone (6,4-dihydroxy-7-methoxy flavone)

T4

SB

[64]

 204

Bicalein (5,6,7-trihydroxy flavone)

T4

SB

[64]

 205

Scutellarein

T4

T8, T17, T20

T16

T39

B, R

B, L, S, R, F

L, F

B, L, R, F

[23]

[23]

[23]

[23]

 206

Luteolin

T4

T8, T20

T17

T16

T39

T24

B, L

L, S

R, L

L

L, S, F

F

[23, 65]

[23]

[23]

[23]

[23]

[122]

 207

Apigenin

T4

T8, T16, T17, T20, T39

B, L, S, R, F

B, L, S, R, F

[23, 66]

[23]

 208

Isoorientin

T11

T4, T8, T17, T16, T20, T39

T35

T36

L

B, L, S, R, F

L

L

[35]

[23]

[139]

[38]

 209

Orientin

T11

T4

T8

T17

T16

T39

T20

T35

T36

L

L, F

B, S

B, L, S, R, F

L, R, F

B, S, F

L, S, F, R

L

L

[35]

[23]

[23]

[23]

[23]

[23]

[23]

[139]

[38]

 210

Isovitexin

T11

T4

T17

T16

T39

T20

T35

T36

L

L, F

L, R, F

L

S, F

L, S, F

L

L

[35]

[23]

[23]

[23, 105]

[23]

[23]

[139]

[38]

 211

Apigenin-6-C-(2″-O-galloyl)-β-d-glucoside

T16

L

[105]

 212

Apigenin-8-C-(2″-O-galloyl)-β-d-glucoside

T16

T34

L

L

[105]

[35]

 213

Vitexin

T4, T17, T20

T8

T16

T39

T35

T36

B, L, S, R, F

B, L, S, R

L, S, R, F

B, L, S, F

L

L

[23]

[23]

[23]

[23]

[139]

[38]

 214

Amentoflavone

T8

T17

T20

L, S

L, R, F

L

[23]

[23]

[23]

 215

Neosaponarin

T36

L

[38]

 216

(−)-Epicatechin

T4

B

[76]

 217

Epicatechin 

T4, T8, T17, T20, T39

T16

T34

B, L, S, R, F

L, S, R, F

SB

[23]

[23]

[35]

 218

Catechin

T34

T11

T4, T8, T16, T17, T20, T39

T44

SB

L

B, L, S, R, F

R

[35]

[35]

[23]

[133]

 219

Catechin–epicatechin

T44

R

[43]

 220

Catechin–epigallocatechin

T44

R

[43]

 221

Epigallocatechin

T34

SB

[35]

 222

(−)-Epicatechin-3-O-gallate

T16

B

[41]

 223

(−)-Epigallocatechin-3-O-gallate

T16

B

[41]

 224

Flavanol

T24

F

[122]

 225

Gallocatechin

T34

T24

SB

F

[35]

[126]

 226

Quercetin

T4

T8

T17

T16

T39

T20

T24

T49

B, L, R

R

S, R, F

L, S, F

L, B

F

F

L

[23]

[23]

[23]

[23]

[23, 142]

[23]

[124]

[124]

 227

Kaempferol

T4

T8

T16, T17

T20, T39

T24

B, L, S, R, F

B, L, S, F

B, L, S, R, F

L, S, R, F

F

[23, 66]

[23]

[23]

[23]

[122]

 228

Kaempferol-3-O-β-d-rutinoside

T4, T8, T17

T16

T39

T20

T36

B, L, S, R, F

L, S, F

L, R, F

L, S, R

L

[23]

[23]

[23]

[23]

[38]

 229

Afzelin (kaempferol 3-O-rhamnoside)

T49

L

[124]

 230

Rutin

T4, T16

T8

T17, T39

T20

T32

T36

B, L, S, F

L, S

B, L, S, R, F

L, S, F

L

L

[23]

[23]

[23]

[23]

[135, 136]

[38]

 231

Narcissin

T32

L

[135, 136]

 232

Quercetin-3,4′-di-O-glucoside

T4

T8

T16, T17, T20, T39

B, L, S, F

B, S, F

B, L, S, R, F

[23]

[23]

[23]

 233

Quercetin-7-O-rhamnoside

T4

F

[80]

 234

2-O-β-glucosyloxy-4,6,2′,4′-tetramethoxychalcone

T1

R

[53]

 235

Cerasidin

T4

F

[80]

 236

Genistein

T4

T8, T16, T17, T20, T39

B, L, S, R, F

B, L, S, R, F

[23, 80]

[23]

 237

Cyaniding

T4

B

[66]

 238

Pelargonidin

T4

B

[66]

 239

Leucocyanidin

T4

B

[80]

 240

7-Hydroxy-3′,4-(methylenedioxy)flavan

T8

FR

[12]

Lignan (27)

 241

Termilignan

T8

T39

FR

B

[12]

[144]

 242

Anolignan B

T8

T44

FR

R

[12]

[43, 151]

 243

Thannilignan

T8

FR

[12]

 244

Termilignan B

T44

R

[133]

 245

Ferulic acid dehydrodimer

T24

F

[125]

 246

(7S,8R,7′R,8′S)-4′-hydroxy-4-methoxy-7,7′-epoxylignan

T48

SB

[50]

 247

Meso-(rel7S,8R,7′R,8′S)-4,4′-dimethoxy-7,7′-epoxylignan

T48

SB

[50]

 248

4′-O-cinnamoyl cleomiscosin A

T50

R

[72]

 249

Diethylstilbestrol monosulphate

T24

F

[126]

 250

Terminaloside A

T19

L

[22]

 251

Terminaloside B

T19

L

[22]

 252

Terminaloside C

T19

L

[22]

 253

Terminaloside D

T19

L

[22]

 254

Terminaloside E

T19

L

[22]

 255

Terminaloside F

T19

L

[22]

 256

Terminaloside G

T19

L

[22]

 257

Terminaloside H

T19

L

[22]

 258

Terminaloside I

T19

L

[22]

 259

Terminaloside J

T19

L

[22]

 260

Terminaloside K

T19

L

[22]

 261

2-Epiterminaloside D

T19

L

[22]

 262

6-Epiterminaloside K

T19

L

[22]

 263

Terminaloside L

T19

L

[121]

 264

Terminaloside M

T19

L

[121]

 265

Terminaloside N

T19

L

[121]

 266

Terminaloside O

T19

L

[121]

 267

Terminaloside P

T19

L

[121]

Phenols and glycosides (52)

 268

Ellagic acid

T1

T7

T10, TM, TT

T12

T40

T4, T8, T20

T17

T16

T39

T24

T25

T31

T28, T32

T35

T42

T30, T44

T36, T45, T46

T48

T49

B

SB

SB

B

B

B, L, S, R, F

L, SB, R F

SB, L, R, F

B, L, S, R, F, H

F

B, R, Rl

B

H

L, F

R, SB

R

L

SB

L

[55]

[92, 127]

[14]

[100]

[41]

[23, 80, 83, 86]

[3, 9, 21, 23, 111, 119]

[14, 23, 41, 108, 144]

[23, 142]

[123]

[70, 127, 128]

[127, 134]

[128]

[37, 38]

[133]

[133]

[133]

[50]

[124]

 269

Methyl ellagic acid

T4

B

[90]

 270

3-O-methylellagic acid

T33

SB

[158]

 271

3,3′-Di-O-methylellagic acid

T28

T39

T48

SB

H,B

SB

[29]

[8, 9, 143, 144]

[50]

 272

3,3′-Di-O-methylellagic acid 4-mono glucoside

T39

H

[147, 148]

 273

Tetra-O-methyl ellagic acid

T39

H

[148]

 274

3,3′-Di-O-methylellagic acid 4-O-β-d-glucosyl-(1 → 4)-β-d-glucosyl-(1 → 2)-α-l-arabinoside

T1

R

[52]

 275

3,4,3′-Tri-O-methylflavellagic acid

T7

T12

T24

T25

T31

T28

T32

T39

B

B

F

L, B, R, Rl

B

SB, H

H, B

H

[126]

[100]

[126]

[26, 70, 127, 128]

[127]

[29, 128]

[128, 138]

[143, 148]

 276

3,3′,4-O-trimethyl-4′-O-β-d-glucosylellagic acid

T28

SB

[29]

 277

3,3′-Di-O-methyl ellagic acid 4′-O-β-d-xyloside

T48

SB

[50]

 278

3,4′-Di-O-methylellagic acid 3′-O-β-d-xyloside

T48

SB

[153]

 279

4′-O-galloy-3,3′-di-O-methylellagic acid 4-O-β-d-xyloside

T48

SB

[153]

 280

Flavogallonic acid

T7

T40

T31

T12

T36

SB

B

W

R

L

[92]

[41]

[134]

[101]

[38]

 281

Methyl (S)-flavogallonate

T36

L

[38]

 282

Vanillic acid 4-O-β-d-(6′-O-galloyl) glucoside

T32

B

[138]

 283

3-O-methylellagic acid 4′-O-α-l-rhamnoside

T4

T34

T33

B

SB

SB

[76]

[35]

[158]

 284

Eschweilenol C (ellagic acid 4-O-α-l-rhamnoside)

T12

T17

B

F

[100]

[164]

 285

3-O-methylellagic acid 4′-O-xyloside

T31

R

[101]

 286

Brevifolincarboxylic acid

T35

L

[139]

  

T17

F

[159]

 287

Terflavin D

T17

L

[21]

 288

Gallic acid

T3

T4, T8, T20, T39

T10, TM, TT

T17

T16

T34

T12

T31

T40

T24

T30

T35

T36

T38

T42

T44

T45, T46

T48

T49

F

B, L, S, R, F

SB

SB, F, R, L

SB, F, R, L

L

B

R, W

B

F

R

L

L

L

R, SB

R

L

SB

L

[154]

[23, 80, 83, 86]

[14]

[14, 21, 23, 118, 119]

[14, 23, 41, 108]

[35]

[100]

[101, 134]

[41]

[123, 125]

[133]

[139]

[38]

[141]

[133]

[133]

[133]

[50]

[124]

289

Phyllemblin (ethyl gallate isomers1 progallin A)

T4

T8

T24

T28

T36

B

F

F

SB

L

[86]

[96, 113]

[126]

[29]

[38]

290

Monogalloyl glucose

T3

T8

T17

T31

F

F

F

R

[154]

[113]

[21]

[101]

 291

Methyl gallate

T14

T8

T32

T36

T48

T49

L

F

L

L

SB

L

[18]

[113]

[135, 136]

[38]

[50]

[124]

 292

Shikimic acid

T32

L

[135, 136]

 293

5-O-galloyl-(−)-shikimic acid

T3

T17

F

F

[118]

[154, 159]

 294

4-O-galloyl-(−)-shikimic acid

T17

F

[159]

 295

3,5-Di-O-galloyl-(−)-shikimic acid

T3

F

[154]

 296

Digallic acid

T17

F

[159]

 297

Ethyl gallate isomers2

T24

F

[126]

 298

Ethyl gallate isomers3

T24

F

[126]

 299

Dimethyl gallic acid

T35

L

[139]

 300

Chebulic acid

T3

T17

T24

T35

F

F

F

L

[154]

[4, 9, 112, 119, 159]

[125, 126]

[139]

 301

6′-O-methyl chebulate

T17

F

[159]

 302

7′-O-methyl chebulate

T17

F

[159]

 303

Chebulic acid trimethyl ester

T32

L

[135, 136]

 304

Terminalin

T38

L

[39]

 305

Decarboxyellagic acid

T3

F

[154]

 306

3-O-galloyl-d-glucose

T3

F

[154]

 307

6-O-galloyl-d-glucose

T3

T17

F

F

[154]

[159]

 308

Vanillic acid

T4, T8, T20, T39

T17

T16

T44

B, L, S, R, F

B

S, R, B, F

R

[23]

[23, 117]

[23]

[43]

 309

Benzoic acid

T44

T24

R

F

[43]

[122]

 310

Hydrocinnamic acid

T44

R

[43]

 311

Gentisic acid

T16

L

[108]

 312

Protocatechuic acid

T4, T8, T16, T17, T20, T39

B, L, S, R, F

[23]

 313

2,3-Di-hydroxyphenyl β-d-glucosiduronic acid

T24

F

[125]

 314

Quinic acid

T4, T8, T16, T17, T20, T39

T24

B, L, S, R, F

[23]

[125]

 315

p-Coumaric acid

T17

T44

WP

R

[117]

[43]

 316

Caffeic acid

T4, T8

T17

T16

T39

T20

T44

L, S

L, S, R

L

B, L, S, R, F

B

R

[23]

[23]

[23]

[23]

[23]

[43]

 317

Chlorogenic acid

T4

T17

T16, T39

T20

L, S

S, R, F, L

L

B

[23]

[23]

[23]

[23]

 318

Ferulic acid

T4

T8, T17, T20, T39

T16

B, L, S, F

B, L, S, R, F

L, S, R

[23]

[23]

[23]

 319

Sinapic acid

T4, T16, T20, T39

T8

T17

B, L, S, R, F

S, R, F

B, S, R, F

[23]

[23]

[23]

Steroids (8), polyols (9) and esters (6)

 320

β-Sitosterol

T1

T4

T8

T12

T16

T48

T25

T36

T39

T44

B, H

S, F

F

F

B, SB

H

H

SB

B

H, SB, R

[55, 56]

[57, 83]

[96, 113]

[99]

[128]

[128]

[129]

[140]

[147, 148]

[43, 133, 152]

 321

β-Sitosterol-3-acetate

T44

SB, R

[43]

 322

β-Sitosteryl palmitate

T16

T25, T31

SB, H

L,F

[128]

[128]

 323

Stigmasterol 3-O-β-d-glucoside

T4

T33

F

SB

[80]

[158]

 324

Stigmasterol

T12

T25

T33

T44

B

SB

SB

RB

[99]

[129]

[158]

[133, 152]

 325

Stigma-4-ene-3-one

T44

RB

[43]

 326

16,17-Dihydroneridienone 3O-β-d-glucosyl-(1 → 6)-O-β-d-galactoside

T4

R

[59]

 327

Cannogenol 3-O-β-d-galactosyl-(1 → 4)-O-α-l-rhamno-side

T8

Se

[94]

 328

2-Hexanol

T9

L

[13]

 329

Octanol

T9

L

[13]

 330

Methoxycarbonyloxymethyl methylcarbonate

T24

F

[125]

 331

Ribonolactone

T24

F

[125]

 332

Apionic acid

T24

F

[125]

 333

Ascorbic acid

T24

F

[125]

 334

Gluconolactone

T24

F

[125]

 335

Glucohepatonic acid-1,4-lactone

T24

F

[125]

 336

Galacturonic acid

T44

R

[43]

 337

Geranyl formate

T9

L

[13]

 338

Citronellyl acetate

T9

L

[13]

 339

Geranyl acetate

T9

L

[13]

 340

Geranyl tiglate

T9

L

[13]

 341

Laxiflorin

T31

RB

[127]

 342

(1S,5R)-4-oxo-6,8-dioxabicyclo[3.2.1]oct-2-ene-2-carboxylic acid

T24

F

[125]

Others (26)

 343

Glucuronic acid

T24

F

[125]

 344

Coumarin

T45

L

[133]

 345

Eujavonic acid

T24

F

[125]

 346

Purine

T24

F

[125]

 347

5-(4-Hydroxy-2,5-dimethylphenoxy)-2,2-dimethylpentanoic acid (gemfibrozil M1)

T24

F

[125]

 348

p-Hydroxytiaprofenic acid

T24

F

[125]

 349

Cis-polyisoprene

T32

L

[135]

 350

Arachidic acid

T17

F

[113]

 351

Behenic acid

T8, T17

F

[113]

 352

Arjunaphthanoloside

T4

SB

[87]

 353

Resveratrol (3′,4,5′-trihydroxystilbene)

T24

T44

F

R

[126]

[43]

 354

Resveratrol glucoside (piceid)

T24

T44

F

RB

[126]

[152]

 355

Resveratrol-β-d-glucoside

T44

RB

[152]

 356

Combretastatin

T24

F

[126]

 357

Combretastatin A1

T24

F

[126]

 358

(Z)-Stilbene

T44

R

[133]

 359

(E)-Stilbene

T44

R

[133]

 360

3′5′-Dihydroxy-4-(2-hydroxyethoxy) resveratrol-3-O-β-rutinoside

T44

R, RB

[43, 152]

 361

Resveratrol-3-β-rutinoside glycoside

T44

R, RB

[43, 152]

 362

1,4-Cineole

T9

L

[13]

 363

Terpinen-4-ol

T9

L

[13]

 364

Terminalianone

T12

B

[98]

 365

Termicalcicolanone A

T15

WP

[19]

 366

Termicalcicolanone B

T15

WP

[19]

 367

Mangiferin

T4

T8

T17

T16

T39

T20

B, S, F

B, R, F

B, L, S, R, F

L, R, F

B, L, S, F

L, S, R

[23]

[23]

[23]

[23]

[23]

[23]

 368

Benzoyl-β-d-(4′ → 10″geranilanoxy)-pyranoside

T8

F

[160]

R root, SB stem bark, B bark, F fruit, S stem, H heartwood, RB root bark, Rl rootlet, Se seed, FR fruit rind, WP whole plant, T1T50 plants from Table 1, TM T. manii, TT T. tomentosa

Table 3

The numbers and main types of compounds reported from different Terminalia species

No.

Plant

Plant organs

Numbers

Main types

T1

T. alata

Roots, barks

18

Triterpenes

T3

T. arborea

Fruits

24

Hydrolysable tannin

T4

T. arjuna

Whole plants

93

Triterpenes, tannins, flavonoids

T7

T. avicennioides

Barks

10

Triterpenes, tannins

T8

T. bellirica

Fruits, barks

45

Triterpenes, flavonoids, lignin, simple phenols

T9

T. bentzoe

Leaves

29

Monoterpenoids, sesquiterpenoid

T11

T. brachystemma

Leaves

8

Flavonoids

T12

T. brownii

Leaves

13

Triterpenes

T14

T. calamansanai

Leaves

18

Hydrolysable tannin

T16

T. catappa

Whole plants

64

Triterpenes, tannins, flavonoids, simple phenols

T17

T. chebula

Whole plants

120

Triterpenes, tannins, flavonoids, simple phenols

T19

T. citrina

Fruits, leaves

23

Lignan

T20

T. elliptica

Whole plants

36

Flavonoids

T24

T. ferdinandiana

Fruits

35

Flavonoids, simple phenols, polyols

T25

T. glaucescens

Barks

19

Triterpenes

T28

T. ivorensis

Barks

18

Triterpenes

T31

T. laxiflora

Roots

13

Tannins

T32

T. macroptera

Whole plants

28

Triterpenes, tannins, simple phenols

T33

T. mantaly

Stem barks

7

Triterpenes, simple phenols

T34

T. mollis

Barks

12

Triterpenes, flavonoids

T35

T. muelleri

Leaves

16

Hydrolysable tannin, flavonoids, simple phenols

T36

T. myriocarpa

Leaves, barks

21

Triterpenes, flavonoids, simple phenols

T39

T. paniculata

Barks

43

Triterpenes, flavonoids, simple phenols

T40

T. parviflora

Barks

16

Tannins

T44

T. sericea

Roots

32

Triterpenes, simple phenols, other compounds

T48

T. superba

Barks

15

Triterpenes, simple phenols

Chemical components identified from the other 12 species, including T. bialata (T10), T. calcicola (T15), T. kaiserana (T30), T. manii (TM), T. macroptera (T32), T. oblongata (T38), T. sambesiaca (T42), T. spinosa (T45), T. stenostachya (T46), T. stuhlmannii (T47), T. triflora (T49), T. tropophylla (T50) were less than 6 compounds

3.1 Terpenoids

So far, 104 terpenoids (Fig. 1) including 86 triterpenes (1–86), 14 monoterpenes (87–100), 4 sesquiterpenes (101–104) have been reported from the genus Terminalia. The triterpenoids are mainly oleanane, ursane and lupine types, and their glycosides. Particularly, Atta-ur-Rahman et al. isolated a new seco-triterpene terminalin A (81) possessing a novel rearranged seco-glutinane structure with a pyran ring-A and an isopropanol moiety from the stem barks of T. glaucescens [129]. Ponou et al. found two dimeric triterpenoid glucosides, ivorenosides A and B (49–50) possessing an unusual skeleton [131], and two new oleanane type triterpenes, 3-oxo-type ivorengenin A (41) and 3,24-dinor-2,4-secooleanane-type ivorengenin B (53) from the barks of T. ivorensis [132]. Compounds 41, 49 and 53 showed significant anticancer activities. Wang et al. isolated five new 18,19-secooleanane type triterpene glycosyl esters, namely arjunasides A–E (82–86) from the MeOH extract of T. arjunas barks, TaBs [68]. Moreover, five ursane type triterpene glucosyl esters (64–68) were also obtained for the first time [76]. From the fruits of T. chebula, 23-O-neochebuloylarjungenin 28-O-β-d-glycosyl ester (21) and 23-O-4′-epi-neochebuloylarjungenin (22) with novel substituents at C-23 were reported, in addition to compounds 23–24, 30–32 and 63, whose C-23 substituents were gallate. Compounds 30 and 31 had strong hypoglycemic effect [146]. Furthermore, compound 40 was obtained from the barks of T. arjuna [85], while friedelin (79) with 3-oxo moiety was reported from the fruits of T. arjuna [83], the root barks of T. avicennioides [93], and the stem barks of T. glaucescens [130] and T. mollis [35].
Fig. 1

The structures of terpenoids 1–104

3.2 Tannins

As the main secondary metabolites, 91 tannins (105–195) were reported from the genus Terminalia (Fig. 2), including ellagitannins, gallotannins, dimeric, and trimeric tannins. Four cinnamoyl-containing gallotannins (182–185) were discovered firstly from the fruits of T. chebula, and 1,2,3,6-tetra-O-galloyl-4-O-cinnamoyl-β-d-glucose (183) and 4-O-(2″,4″-di-O-galloyl-α-l-rhamnosyl) ellagic acid (186) showed significant inhibitory activity on α-glucosidase with IC50 values of 2.9 and 6.4 μM, respectively [159].
Fig. 2

The structures of tannins 105–195

Tannins possess not only liver and kidney protection properties, but also anti-diarrhea, anticancer, antibacterial and hypoglycemic activities [133]. However, a condensed tannin terminalin (186) from T. oblongata was reported to have severe hepatorenal toxicity and even caused renal necrosis [39].

3.3 Flavonoids

The Terminalia genus are rich in flavonoids (Fig. 3) comprising of flavanones (196–202), flavones (203–215), flavan-3-ols (216–225), and flavonols (226–233). Among them, cerasidin (235) of chalcone, genistein (236) of isoflavone, and leucocyanidin (239) of flavan-3,4-diol from T. arjuna [80] were described as rare structural types in the Terminalia genus. Moreover, a new chalcone glycoside 2-O-β-glucosyloxy-4,6,2′,4′-tetramethoxychalchone (234) was reported from the roots of T. alata [53]. In addition, anthocyanidin cyanidin (237) and pelargonidin (238), flavanoid 7-hydroxy-3′,4-(methylenedioxy)flavan (240) and other structure were reported [12, 23, 66]. Compounds 209–213, 215 were C-glycosides at C-6 or C-8 of ring A.
Fig. 3

The structures of flavonoids 197–240

3.4 Lignans

Twenty-seven lignans (241–267) were reported from the genus Terminalia (Fig. 4). A new lignan 4′-O-cinnamoyl cleomiscosin A (248) was reported from the ethanol extract of T. tropophylla roots [72]. Moreover, 13 new furofuran lignan glucosides, terminalosides A–K (250–260), 2-epiterminaloside D (261), 6-epiterminaloside K (262) and 5 new polyalkoxylated furofuranone lignan glucosides, terminalosides L–P (263–267) were obtained from the leaves of T. citrina. All of them were tested for their estrogenic and/or antiestrogenic activities using estrogen responsive breast cancer cell lines T47D and MCF-7, and showed varying degrees of inhibitory activity. Among them, terminalosides B (251), G (256), L (263) and M (264) inhibited cell growth by up to 90% at a minimum concentration of 10 nM [22, 121].
Fig. 4

The structures of lignans 241–267

3.5 Phenols and Glycosides

There are 52 phenols and glycosides reported in the Terminalia genus (Fig. 5), in which ellagic acid (268) and gallic acid (289) are present in almost all species. Studies have shown that most of the simple phenolic compounds have antioxidant, antibacterial, hypoglycemic, liver and kidney protection [23].
Fig. 5

The structures of phenols and glycosides (268–319)

3.6 Sterols and Cardiac Glycosides

Only 6 sterols (320–325) and 2 cardiac glycosides (326-327) were isolated from the genus Terminalia before 2001 (Fig. 6).
Fig. 6

The structures of steroids (320–325) and cardiac glycosides (326–327)

3.7 Polyols and Esters

Polyols and lipids were reported to be abundant in the genus Terminalia and concentrated mainly in fruits and leaves [125]. So far, 9 polyol (328–336) and 6 esters (337–342) have been documented (Fig. 7).
Fig. 7

The structures of polyols and esters (328–342)

3.8 Other Compounds

Other compounds featured in the Terminalia genus are shown in Fig. 8 and are mostly styrenes. Cao et al. isolated two new cytotoxic xanthones - termicalcicolanone A (365), termicalcicolanone B (366) in T. calcicola, and found an inhibitory effect on ovarian cancer [19]. Hiroko Negishi et al. obtained a new chromone derivative - terminalianone (364) from the barks of Terminalia brownii [98]. Ansari et al. isolated the novel compound, 4′-substituted benzoyl-β-d glycoside (368), from the fruits of T. bellirica and illustrated its potential for anticoagulation [160].
Fig. 8

The structures of other compounds (343–368)

Moreover, chlorophyll and various vitamins were reported from the genus Terminalia.

4 Pharmacological Activities

The pharmacological activities of the genus Terminalia, mainly including antimicrobial, antioxidant, cytotoxicity, anti-inflammatory, hypoglycemic, cardiovascular, mosquitocidal and antiviral, have been extensively studied.

4.1 Antimicrobial

Extracts of several Terminalia species exhibit antimicrobial activity against various microbes. For example, methanol and aqueous extracts of T. australis were demonstrated antimicrobial activity against Ca. albicans (MIC = 180 and 250 µg/mL, resp.) and Ca. kruzzei (MIC = 250 and 300 µg/mL, resp.) [8]. Aqueous extracts of the stem barks, woods and whole roots of T. brownii showed antibacterial activity against standard strains of Sta. aureus (14.0 ± 1.1 µg/mL), Escherichia coli, Ps. aeruginosa (12.0 ± 1.1 µg/mL), Klebsiella pneumonia (6.0 ± 1.0 µg/mL), Sa. typhi and Bacillus anthracis (13.0 ± 1.0 µg/mL), as well as fungi Ca. albicans (12.3 ± 1.5 µg/mL) and Cr. neoformans (9.7 ± 1.1 µg/mL) [16]. Ethanol extracts of the root barks and leaves of T. schimperiana were against Sta. aureus, Ps. aeruginosa and Sa. typhi (MIC = 0.058–2.089 mg/mL), with inhibition zone diameters (IZDs) of 17.2 to 10.0 mm, compared to gentamicin (IZD = 21.8–10 mm). The results supported the efficacy of the extracts in the folkloric treatment of burns wounds, bronchitis and dysentery, respectively [42]. Antibacterial tests on Mycobacterium smegmatis ATCC 14468 showed that methanol extract of T. sambesiaca roots and stem barks had promising effects (MIC = 1.25 mg/mL, both) [133].

Ellagitannin punicalagin (133) obtained from the stem barks of T. mollis demonstrated crucial activity against Ca. parapsilosis and Ca. krusei (MIC = 6.25 μg/mL), as well as Ca. albicans (MIC = 12.5 μg/mL) [35]. 7-Hydroxy-3′,4′-(methylenedioxy) flavan (240), termilignan (241), anolignan B (242) and thannilignan (243) isolated from the fruit rinds of T. bellirica displayed significant antifungal activity against Penicillium expansum (MIC = 1.0, 2.0, 3.0 and 4.0 µg/mL, resp.), also with 240 and 241 against Ca. albicans at 10 and 6 µg/mL, resp. [12]. The antimycobacterial activity of friedelin (79) furnished from the root barks of T. avicennioides was 4.9 μg/mL in terms of MIC value [93]. β-Arjungenin (16), betulinic acid (74), sitosterol (319) and stigmasterol (323) from T. brownii were proved to possess antibacterial activity, with 74 the most active against A. niger and S. ipomoea (MIC = 50 μg/ml) [99].

4.2 Antioxidant

Terminalia species have also illustrated some interesting antioxidant properties [161]. By a 2,2-diphenyl-1-picrylhydrazyl (DPPH) radical scavenging assay, relatively high anti-oxidant activities of the methanol extracts of T. alata, T. bellirica and T. corticosa trunk-barks were found (IC50 = 0.24, 1.02 and 0.25 mg/mL, resp.), compared to the positive control, l-ascorbic acid (IC50 = 0.24 mg/mL) [2].

Flavonoid glycosides, apigenin-6-C- (211) and apigenin-8-C- (212) (2″-O-galloy1)-β-d-glucoside, isolated from dried fallen leaves of T. catappa, showed significant antioxidative effects (IC50 = 2.1 and 4.5 µM, resp.) on Cu2+/02-induced low density lipoprotein lipid peroxidation, with probucol (IC50 = 4.0 µM) as positive control [105].

Arjunaphthanoloside (351), isolated from the stem barks of T. arjuna showed potent antioxidant activity and inhibited nitric oxide (NO) production in lipopolysaccharide (LPS)-stimulated rat peritoneal macrophages [87], while ivorenosides B (51) and C (52), two triterpenoid saponins from T. ivorensis, exhibited scavenging activities against DPPH and ABTS+ radicals [131].

The antioxidant potential of T. paniculata (TPW) was investigated by DPPH, ABTS2−, NO, superoxide (O2−), Fe2+ chelating and ferric reducing/antioxidant power (FRAP) assays. TPW showed maximum superoxide, ABTS2−, NO, DPPH inhibition, and Fe2+-chelating property at 400 µg/mL, resp. FRAP value was 4.5 ± 0.25 µg Fe(II)/g, which demonstrated the efficacy of aqueous barks extract of T. paniculata as a potential antioxidant and analgesic agent [142].

TaB contains various natural antioxidants and has been used to protect animal cells against oxidative stress. The alleviating effect of TaB aqueous extract against Ni toxicity in rice (Oryza sativa L.) suggested that TaB extract considerably alleviated Ni toxicity in rice seedlings by preventing Ni uptake and reducing oxidative stress in the seedlings [162]. Behavioral paradigms and PCR studies of TaB extract against picrotoxin-induced anxiety showed that TaB supplementation increased locomotion towards open arm (EPM), illuminated area (light–dark box test), and increased rearing frequency (open field test) in a dose dependent manner, compared to picrotoxin (P < 0.05). Furthermore, alcoholic extract of TaB showed protective activity against picrotoxin in mice by modulation of genes related to synaptic plasticity, neurotransmitters, and antioxidant enzymes [174].

4.3 Cytotoxicity

70% Acetone extracts of T. calamansanai leaves inhibited the viability of human promyelocytic leukemia HL-60 cells. Sanguiin H-4 (115), 1-α-O-galloylpunicalagin (136), punicalagin (135), 2-O-galloylpunicalin (147) and methyl gallate (290) were the main components isolated from T. calamansanai with the IC50 values of 65.2, 74.8, 42.2, 38.0 and > 100 µM, respectively, for HL-60 cells. Apoptosis of HL-60 cells treated with 1-α-O-galloylpunicalagin, 115, 135, and 147 was noted by the appearance of a sub-G1 peak in flow cytometric analysis and DNA fragmentation by gel electrophoresis. 115 and 147 induced a decrease of the human poly (ADP-ribose) polymerase (PARP) cleavage-related procaspase-3 and elevated activity of caspase-3 in HL-60 cells, but not normal human peripheral blood mononuclear cells, PBMCs [18].

Terminaliaside A (60), an oleanane-type triterpenoid saponin isolated from the roots of T. tropophylla showed antiproliferative activity against the A2780 human ovarian cancer cell line with an IC50 value of 1.2 µM [72]. The 70% methanolic extract of T. chebula fruits was found to decrease cell viability, inhibit cell proliferation, and induce cell death of human (MCF-7) and mouse (S115) breast cancer, human osteosarcoma (HOS-1), human prostate cancer (PC-3) and a non-tumorigenic, immortalized human prostate (PNT1A) cell lines. Flow cytometry and other analyses showed that some apoptosis was induced by the extract at lower concentrations, but at higher concentrations, necrosis was the major mechanism of cell death. Chebulinic acid (143) and ellagic acid (186) were tested by ATP assay on HOS-1 cell line in comparison with three known antigrowth phenolics of Terminalia, gallic acid (287), methyl gallate (290), luteolin (206), and tannic acid (169). Results showed that the most growth inhibitory phenolics in T. chebula fruits were chebulinic acid (IC50 = 53.2 µM ±/0.16) >/tannic acid (IC50 = 59.0 mg/mL ±/0.19) > ellagic acid (IC50 = 78.5 µM ±/0.24) [111].

Aqueous and ethanolic extracts of T. citrina fruits were revealed to exhibit significant mutagenicity in tested strains of baby hamster kidney cell line (BHK-21). Ethanolic extract showed higher mutagenicity in TA 100 strain, whereas aqueous extract exhibited higher mutagenicity in TA 102 strain than TA 100. Both extracts showed dose-dependent mutagenicity. Fifty percent cell viability was exhibited by 260 and 545 μg/mL of ethanolic and aqueous extracts respectively [169]. Moreover, ivorenoside A (50) showed antiproliferative activity against MDA-MB-231 and HCT116 human cancer cell lines with IC50 values of 3.96 and 3.43 µM, respectively [131].

4.4 Anti-inflammatory

Inflammation has been considered as a major risk factor for various kinds of human diseases. Macrophages play substantial roles in host defense against infection. It can be activated by LPS, the major component of the outer membrane of Gram-negative bacteria. An investigation was carried out to determine anti-inflammatory potential of ethyl acetate fraction isolated from T. bellirica (EFTB) in LPS stimulated RAW 264.7 macrophage cell lines. EFTB (100 μg/mL) inhibited all inflammatory markers in dose dependent manner. Moreover, EFTB down regulated the mRNA expression of TNF-α, IL-6, COX-2 and NF-κB against LPS stimulation. These results demonstrated that EFTB is able to attenuate inflammatory response possibly via suppression of ROS and NO species, inhibiting the production of arachidonic acid metabolites, proinflammatory mediators and cytokines release [165].

Anolignan B (242) isolated from roots of T. sericea was tested for anti-inflammatory activity using the cyclooxygenase enzyme assays (COX-1 and COX-2) It showed activity against both COX-1 (IC50 = 1.5 mM) and COX-2 (IC50 = 7.5 mM) enzymes [151]. Termiarjunosides I (47) and II (48) isolated from stem barks of T. arjuna inhibited aggregation of platelets and suppressed the release of NO and superoxide from macrophages [156].

The anti-inflammatory activities of a polyphenol-rich fraction (TMEF) obtained from T. muelleri was assessed using carrageenan-induced paw edema model by measuring PGE2, TNF-α, IL-1b, and IL-6 plasma levels as well as the paw thickness. The group treated with 400 mg/kg of TMEF showed a greater inhibition in the number of writhes (by 63%) than the standard treated group (61%). TMEF pretreatment reduced the edema thickness by 48, 53, and 62% at the tested doses, respectively. TMEF administration inhibited the carrageenan-induced elevations in PGE2 (by 34, 43, and 47%), TNF-α (18, 28, and 41%), IL-1β (14, 22, and 29%), and IL-6 (26, 31, and 46%) [166].

4.5 Hypoglycemic

Some species and isolates from Terminalia have indicated possession of α-glucosidase inhibitory capabilities. Gallic acid (287) and methyl gallate (290), from stem barks of T. superba, showed significant activity (IC50 = 5.2 ± 0.2 and 11.5 ± 0.1 μM, resp.). Arjunic acid (5) and glaucinoic acid (46) from stem barks of T. glaucescens showed significant β-glucuronidase inhibitory activity with IC50 value 80.1 and 500 μM, resp., against β-glucuronidase [130].

In a study to investigate α-glucosidase inhibition of extracts and isolated compounds from T. macroptera leaves, chebulagic acid (142) showed an IC50 value of 0.05 µM towards α-glucosidase and 24.9 ± 0.4 µM towards 15-lipoxygenase (15-LO), in contrast to positive controls (acarbose: IC50 = 201 ± 28 µM towards α-glucosidase, quercetin: IC50 = 93 ± 3 µM towards 15-LO). Corilagin (116) and narcissin (231) were good 15-LO and α-glucosidase inhibitors. Rutin (230) was a good α-glucosidase inhibitor (IC50 ca. 3 µM), but less active towards 15-LO [136].

From the fruits of T. chebula, 23-O-galloylarjunolic acid (30) and 23-O-galloylarjunolic acid 28-O-β-d-glucosyl ester (31) were afforded and showed potent inhibitory activities with IC50 values of 21.7 (30) and 64.2 (31) µM, resp., against Baker’s yeast α-glucosidase, compared to the positive control, acarbose (IC50 174.0 µM) [146].

Hydrolyzable tannins, 1,2,3,6-tetra-O-galloyl-4-O-cinnamoyl-β-d-glucose (183) and 4-O-(2″,4″-di-O-galloyl-α-l-rhamnosyl) ellagic acid (186) from the fruits of T. chebula, showed significant α-glucosidase inhibitory activities with IC50 values of 2.9 and 6.4 µM, resp. In addition, inhibition kinetic studies showed that both compounds have mixed-type inhibitory activities with the inhibition constants (Ki) of 1.9 and 4.0 µM, respectively [159].

4.6 Cardiovascular

A few species of Terminalia have demonstrated cardiovascular activities. It was reported that the barks of T. arjuna possessed significant inotropic and hypotensive effect, mild diuretic, antithrombotic, prostaglandin E2 enhancing and hypolipidaemic activities [66].

Ethanolic extract of T. pallida fruits (TpFE) were studied to determine their cardioprotection against isoproterenol (ISO)-administered rats. The supplementation of TpFE dose-dependently exerts notable protection on myocardium by virtue of its strong antioxidant activity. It could be used as a medicinal food for the treatment of cardiovascular ailments [163].

4.7 Mosquitocidal

Insect-borne diseases remain to this day a major source of illness and can cause death worldwide. The resistance to chemical insecticides among mosquito species has been a major problem in vector control. The larvicidal and ovicidal activities of crude benzene, hexane, ethyl acetate, chloroform and methanol extracts of T. chebula were tested for their toxicity against three important vector mosquitoes, viz., Anopheles stephensi, Aedes aegypti and Culex quinquefasciatus. All extracts showed moderate larvicidal effects, the highest larval mortality was found in the methanol extract of T. chebula against the larvae of A. stephensi, A. aegypti, and C. quinquefasciatus with the LC50 values of 87.13, 93.24 and 111.98 ppm, respectively. Mean percent hatchability of the ovicidal activity was observed 48 h post treatment. All the five solvent extracts showed moderate ovicidal activity. The maximum egg mortality (zero hatchability) was observed in the methanol extract of T. chebula at 200 and 250 ppm against A. stephensi, while A. aegypti and C. quinquefasciatus showed 100% mortality at 300 ppm. No mortality was observed in the control group. The finding of the investigation revealed that the leaf extract of T. chebula possesses remarkable larvicidal and ovicidal activity against medically important vector mosquitoes [167, 168].

4.8 Antiviral

Termilignan (241) and anolignan B (242), obtained from T. bellirica exhibited antimalarial activity against the chloroquine-susceptible strain 3D7 of Plasmodium falciparum (IC50 = 9.6 ± 1.2 μM)[12]. Casuarinin (129), chebulagic acid (142) from the fruits of T. chebula possessed hepatitis C virus inhibition activities (IC50 = 9.6 and 5.2 μM, resp.) [118]. Punicalin (128) and 2-O-galloylpunicalin (147), isolated from aqueous extract of T. triflora leaves, showed inhibitory activity on HIV-1 reverse transcriptase with IC50 of 0.11 μg/mL (0.14 μM) and 0.10 μg/mL (0.11 μM), resp. [149].

In vitro anti-HIV-1 activity of acetone and methanol extracts of T. paniculata fruits was studied by Durge A. et al. Cytotoxicity tests were conducted on TZM-bl cells and PBMCs, the CC50 values of both extracts were ≥ 260 μg/mL. By using TZM-bl cells, the extracts were tested for their ability to inhibit replication of two primary isolates HIV-1 (X4, Subtype D) and HIV-1 (R5, Subtype C). The activity against HIV-1 primary isolate (R5, Subtype C) was confirmed by using activated PBMC and quantification of HIV-1 p24 antigen. Both the extracts showed anti-HIV-1 activity in a dose-dependent manner. The EC50 values of the acetone and methanol extracts of T. paniculata were ≤ 10.3 μg/mL. Furthermore, the enzymatic assays were performed to determine the mechanism of action which indicated that the anti-HIV-1 activity might be due to inhibition of reverse transcriptase (≥ 77.7% inhibition) and protease (≥ 69.9% inhibition) enzymes [172].

Kesharwani A. et al. investigated anti-HSV-2 activity of T. chebula extract and its constituents, chebulagic acid (142) and chebulinic acid (143). Cytotoxicity assay using Vero cells revealed CC50 = 409.71 ± 47.70 μg/mL for the extract whereas 142 and 143 showed more than 95% cell viability up to 200 μg/mL. The extract from T. chebula (IC50 = 0.01 ± 0.0002 μg/mL), chebulagic (IC50 = 1.41 ± 0.51 μg/mL) and chebulinic acids (IC50 = 0.06 ± 0.002 μg/mL) showed dose dependent in vitro anti-viral activity against HSV-2, which can also effectively prevent the attachment and penetration of the HSV-2 to Vero cells. In comparison, acyclovir showed poor direct anti-viral activity and failed to significantly (p > 0.05) prevent the attachment as well as penetration of HSV-2 to Vero cells when tested up to 50 μg/mL. Besides, in post-infection plaque reduction assay, T. chebula extract, chebulagic and chebulinic acids showed IC50 values of 50.06 ± 6.12, 31.84 ± 2.64, and 8.69 ± 2.09 μg/mL, resp., which were much lower than acyclovir (71.80 ± 19.95 μg/mL) [173].

4.9 Others

Terminalia species were also reported to be used in the treatment of diarrhea [95], Alzheimer’s disease [112], psoriasis [164], liver disease [170], kidney disease [171], etc. Terminalosides A–K (249–259) from the leaves of the Bangladeshi medicinal plant T. citrina possess estrogen-inhibitory properties. Among them, Terminaloside E (253) showed inhibitory activity against the T47D cell line, such terminalosides C (252), F (255), and I (258). Besides, 6-epiterminaloside K (262) displayed antiestrogenic activity against MCF-7 cells [22].

5 Conclusion and Future Prospects

The genus Terminalia contains not only a large number of tannins, simple phenolics, but also a lot of terpenoids, flavonoids, lignans and other compounds. Most tannins, simple phenolics and flavonoids have antioxidation, antibacterial, antiinflammatory and anticancer activities. The plants of the genus Terminalia have exhibited positive effect on immune regulation, cardiovascular disease and diabetes, and can accelerate wound healing [157]. Therefore, the Terminalia genus has great medicinal potential. However, most of the chemical composition of species is still unknown, we should use modern advanced technology such as LC–MS to continue to isolate its compounds, and determine their pharmacological activities and mechanism of action, to explore other possible greater medicinal value.

Notes

Acknowledgements

This work was supported by the Key Projects of Yunnan Science and Technology, and Yunnan Key Laboratory of Natural Medicinal Chemistry (S2017-ZZ14).

Conflict of interest

All authors declare no conflict of interest.

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Authors and Affiliations

  1. 1.State Key Laboratory of Phytochemistry and Plant Resources in West China. Kunming Institute of BotanyChinese Academy of SciencesKunmingPeople’s Republic of China
  2. 2.University of Chinese Academy of SciencesBeijingPeople’s Republic of China
  3. 3.Yunnan Key Laboratory of Natural Medicinal Chemistry, Kunming Institute of BotanyChinese Academy of SciencesKunmingPeople’s Republic of China

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