Medical Importance of Helianthus Tuberosus - A Review

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IAJPS 2018, 05 (04), 2159-2166 Ali Esmail Al-Snafi ISSN 2349-7750

CODEN [USA]: IAJPBB ISSN: 2349-7750

INDO AMERICAN JOURNAL OF


PHARMACEUTICAL SCIENCES
http://doi.org/10.5281/zenodo.1214984

Available online at: http://www.iajps.com Review Article

MEDICAL IMPORTANCE OF HELIANTHUS TUBEROSUS- A


REVIEW
Ali Esmail Al-Snafi
Department of Pharmacology, College of Medicine, University of Thi qar, Iraq.
Cell: +9647801397994. E mail: [email protected]
Abstract:
Phytochemical analysis of Helianthus tuberosus showed that it contained coumarins, unsaturated fatty acids,
polyacetylenic derivatives, phenols, flavonoids, sesquiterpenes, protein, amino acid, reducing sugars, organic acids,
lactones and cardiac glycoside. The pharmacological investigations revealed that Helianthus tuberosus exerted
antioxidant, anticancer, antidiabetic, antifungal and α-Glucosidase inhibitory activity, as well as it produced inulin
which used as functional food and possessed many medical benefits. This review will highlight the chemical
constituents and pharmacological and therapeutic effects of Helianthus tuberosus.
Keywords: Helianthus tuberosus, pharmacology, therapeutic, chemical constituents
Corresponding author:
Ali Esmail Al-Snafi QR code
Department of Pharmacology,
College of Medicine,
University of Thi qar, Iraq
Cell: +9647801397994.
E mail: [email protected]

Please cite this article in press Ali Esmail Al-Snafi., Medical Importance of Helianthus Tuberosus- A Review, Indo
Am. J. P. Sci, 2018; 05[04].

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IAJPS 2018, 05 (04), 2159-2166 Ali Esmail Al-Snafi ISSN 2349-7750

INTRODUCTION:
Medicinal plants are the Nature’s gift to human Distribution:
beings to help them pursue a disease-free healthy life. It was native to Canada and United states, and
Plants have been used as drugs by humans since naturalized in Africa, Asia [Russian Federation,
thousands of years ago. As a result of accumulated Turkey, Iraq, Republic of Korea, China and Japan].
experience from the past generations, today, all the Australasia [Australia and New Zealand], Europe
world’s cultures have an extensive knowledge of [Belarus, Estonia, Latvia, Lithuania, Moldova, Russia
herbal medicine. Plants are a valuable source of a n Federation- European part, Ukraine,
wide range of secondary metabolites, which are used Austria, Belgium, Czech Republic, Germany,
as pharmaceuticals, agrochemicals, flavours, Hungary, Netherlands,
fragrances, colours, biopesticides and food Poland, Slovakia, Switzerland,
additives[1-20]. Phytochemical analysis of Norway, Sweden, United Kingdom, Albania,
Helianthus tuberosus showed that it contained Bulgaria, Croatia, Italy,
coumarins, unsaturated fatty acids, polyacetylenic Macedonia, Romania, Slovenia, France and Spain],
derivatives, phenols, flavonoids, sesquiterpenes, Southern America [Argentina and Uruguay], and it
protein, amino acid, reducing sugars, organic acids, was cultivated widely in the temperate regions[22-
lactones and cardiac glycoside. The pharmacological 23].
investigations revealed that Helianthus tuberosus
exerted antioxidant, anticancer, antidiabetic, Description:
antifungal and α-Glucosidase inhibitory activity, as Robust, erect, perennial herb, in cultivation usually
well as it produced inulin which used as functional grown as an annual, up to 3 m tall, scarcely to
food and possessed many medical benefits. This moderately branched in upper half of stem, hirsuta in
review was designed to highlight the chemical most above-ground parts. Roots adventitious [in
constituents and pharmacological and therapeutic plants not grown from seed], fibrous, spreading
effects of Helianthus tuberosus. deeply. Tubers formed by thickening of short and
Plant profile: stout or long and slender underground stolons,
ellipsoid to globose, 2-8[-15] x 3-6 cm, whitish,
Synonyms: yellow, red or purple, with small scale leaves and
Helianthus esculentus Warsz., Helianthus serotinus axillary buds. Leaves opposite or in whorls of three in
Tausch, Helianthus tomentosus Michx., Helianthus lower plant part, in upper part alternate, simple;
tuberosus var. subcanescens A. Gray, Helianthus petiole 2-4 cm long, winged above; blade ovate to
tuberosus f. tuberosus and Helianthus tuberosus var. ovate-lanceoliate, 10-20 cm long, base tapering into
tuberosus[21]. petiole, margin irregularly serrate, apex acute, veins
prominent with three main veins. Inflorescence a
Taxonomic classification: head, 4-8 cm in diameter, few together in a leafy
Kingdom: Plantae; Phylum: Spermatophyta, panicle 8-20 cm long; involucral bracts in several
Subphylum: Angiospermae, Class: Dicotyledonae, rows, lanceolate, long acuminate, subequal, 15-17 x 4
Order: Asterales, Family: Asteraceae, Genus: mm, ciliate, blackish outside; receptacle flat, 1.5-2
Helianthus, Species: Helianthus tuberosus[22]. cm in diameter; outer ray florets sterile, with golden-
yellow, ligulate corolla, elliptical to oblong, 2.5-4.5 x
Common names: 1 cm; disc florets bisexual, with tubular bright yellow
corolla, 6-7 mm long; sterile bracts pale, 8-9 mm
Arabic: Taffahh Al-Ardh; Tartuf; English: Earth-
long, with greenish-yellow apex; five stamens; style
apple, Jerusalem-artichoke, Sunchoke, Topinambur;
French: Artichaut de Jérusalem, Topinambour; slender, with two-lobed stigma. Fruit an achene,
German: Erdbirne, Indianerknolle, Topinambur; oblongoid, 5-7 mm long, flattened at the sides,
Italy: Girasole di Canadá, Tartufo diCanna, brownish with dark stripes, thinly hairy[22].
Topinambur; Japanese: Kiku-imo; Portuguese:
Batata-tupinambá, Girassol-de-batata, Tupinambá, Traditional uses:
Tupinambor; Russian: Podsolnečnik Klubenosnij, Jerusalem artichoke was considered as one of the
Topinambur, Zemljanaja gruša; primary sources for inulin in higher plants. Its protein
Spanish: Aguaturma, Castaña de tierra, Námara, has high food value due to the presence of almost all
Pataca, Patata de caña; Swedish: Jordärtskocka; essential amino acids, it was used as livestock
Thailand: Thantawan-hua; Vietnam: Quyf doji[22- feed[24]. Tubers of Helianthus tuberosus were
23]. utilized as a diuretic, spermatogenic, tonic,

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galactagogue, aphrodisiac, antihemorrhoidal, crude protein of Helianthus tuberosus tubers [% of


collagogue and to decrease diabetes symptoms[25- dry weight] were: asparatic acid 0- 0.86, threonine
27]. Leaves were used as a natural medicine for the 0.20- 0.30, serine 0- 0.19, glutamic acid 0-0.83,
treatment of skin wound, bone fracture and glycine 0- 0.21, alanine 0- 0.23, cysteine 0-0.06 ,
swelling[28-29]. valine 0.22- 1.33, methionine 0- 0.06, isoleucine 0-
Part used medicinally: 0.19, leucine 0.27- 0.85, tyrosine 0.12, phenylalanine
Whole plant, tubers and leaves [24-29]. 0- 0.23, histidine 0.17- 0.21, lysine 0.30- 0.33,
arginine 0.46- 0.65 and proline 0- 0.30[37-39].
Chemical constituents:
Phytochemical analysis of Helianthus tuberosus However, the contents of essential amino acids in
showed that it contained coumarins, unsaturated fatty Jerusalem artichoke tubers of Rote Zonenkugel
acids, polyacetylenic derivatives, phenols, flavonoids, variety [mg/g protein] were included: histidine: 17,
sesquiterpenes, protein, amino acid, reducing sugars, isoleucine : 29, leucine: 40, lysine: 45, methionine +
organic acids, lactones and cardiac cystine: 23, phenylalanine + tyrosine: 44, threonine:
glycoside[25,28,30-31]. 29, valine: 33 and the sum of essential amino acids
was 260[40].
The tubers comprised about 80% water, 15%
carbohydrate, and 1 to 2% protein. The tubers The chemical constituents of the leaf, stem and total
contained little or no starch and small amount of fat aerial parts [% dry weight] were: leaf protein 26.9-
included trace amounts of monounsaturated and 29.4, stem protein: 8.8-11.9, total aerial parts
polyunsaturated fatty acids, but no saturated fatty protein: 7-9; leaf sugars: 0.8-2.4 stem sugar: 5-6;
acids. The polyunsaturated fatty acids linoleic [24 total aerial parts fructose: 1.8-2.2; total aerial parts
mg/100g raw tuber] and α-linoleic acid [36 mg /100g glucose: 1.2-2.1; total aerial parts sucrose: 1.2-2.1;
raw tuber][32-33]. total aerial parts inulin [fructan] 2-4.5; leaf cellulose:
It contained inulin 7 to 30% of fresh weight [ 8 and 6.6-7.3, stem cellulose: 13.1-14.2, total aerial parts
21% inulin of fresh weight is considered typical][34- cellulose 17-20; leaf hemicelluloses: 4.3-4.5, stem
35]. hemicelluloses: 9.3-9.6, total aerial parts
The root of Helianthus tuberosus contained inulin hemicelluloses: 21; leaf lignin: 17.9-21.7, stem
20%, fructose amount 91.9 %, glucose amount 8.1 lignin 10.8-14.1, total aerial parts lignin: 12-14; leaf
%[36]. uronides: 13.2-15.8 , stem uronides: 9.2-10.9, leaf
ash: 13.4-14.9, stem ash: 6.8-9.4 , total aerial parts
The composition of Helianthus tuberosus tubers [per ash: 8-10[37, 41-42].
100 g fresh weight]: water: 7-80.1%, energy: 38-76
kcal, protein: 0.5- 8.0 g, total carbohydrate: 10.6-17.3 The total phenol content of the ethanol extract of
g, dietary fiber: 1.3-4g, total sugars: 1-1.6g, sucrose: tubers of Helianthus tuberosus was 7.91 mg GAE/g
0.6 g, lactose: 0 g, total starch: trace- 7.2g, total fat: and total flavonoid content was 29.60 ± 5.23 mg
0.1- <1 g, total fatty acids: <0.1- <1 g, saturated fatty QE/g[27].
acids: 0-0.17g, monounsaturated fatty acids: <0.1- <1
g, polyunsaturated fatty acids: <0.1- <1 g, The 70 % ethanol extracts of tubers of different
cholesterol: 0-0.3 mg, total sterols: 5.2 mg, ash: 1.2 g, varieties and wild populations of Helianthus
nitrogen: 0.25-0.38g, calcium: 14-37 mg, iron: 0.4- tuberosus grown on territory of Bulgaria, possessed
3.7 mg, magnesium: 14.4-17 mg, potassium: 420- the highest total phenolic content [6-17 mg GAE/g
657 mg, sodium: 1.8- 4mg, phosphorus: 63-78 mg, dry weight][43].
copper: 0.10-0.12 mg, boron: 0.21-0.24 mg,
manganese 0- 0.3 mg, sulfur: 22-27mg, chlorine: 0 Ethyl acetate fraction of Helianthus tuberosus leaves
mg, zinc: 0.1-12 mg, aluminum:4 mg, barium: contained the highest total phenolic content [266.69 ±
0.33mg, silicon: 4.4mg, nickel: 0-16μg, iodine: 0-0.1 2.51 mg GAE/g dry extract]. Six phenolic
μg, chromium: 0-6.4 μg, selenium: 0-0.2 μg, lead compounds were also isolated, among them 3-O-
6.3μg, cadmium 1.1μg, vitamin A [retinol]: 0.6-1μg, caffeoylquinic acid and 1,5-dicaffeoylquinic acid.
carotenoids: 9-28.9 μg, vitamin B1 [thiamin]: 0.07- The content of 3-O-caffeoylquinic acid in n-butanol
0.2 mg, vitamin B 2[riboflavin]: 0-0.16 mg, niacin fraction was 74.58 ± 1.05 mg/g, while 1,5-
0.5-1.3mg , vitamin B6: 0.09 mg, pantothenic acid: dicaffeoylquinic acid in ethyl acetate fraction was
0.38 mg, biotin: 0.5 μg, folates: 13-22 μg, vitamin B 104.51 ± 2.86 mg/g[44].
12 [cobalamin]: 0 μg, vitamin C: 2-6 mg, vitamin D:
0 μg, vitamin E: <0.1-2 mg, vitamin K: 1.44 μg and Ten chlorogenic acids were identified from the
tryptophan: 0.23mg. Amino Acid composition of leaves of three Helianthus tuberosus [3-O-

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caffeoylquinic acid, two isomers of caffeoylquinic hexahydrofarnesylacetone[1.68%]. However,


acid, caffeic acid, p-coumaroyl-quinic acid, chemical constituents of the essential oil from leaves
feruloylquinic acid, 3,4-dicaffeoyquinic acid, 3,5- and tubers of Helianthus tuberosus [ g/100g]
dicaffeoylquinic acid, 1,5-dicaffeoylquinic acid, and respectively were included: p-mentha-1,5- dien-8-ol :
4,5-dicaffeoylquinic acid][45] - and 0.00013, Verbenone: - and 0.00020, Bornyl
acetate: – and 0.00017, α-Copaene: 0.00074 and - ,
Naturally occuring isomers of caffeoylquinic acid Phenylacetaldehyde: – and 0.00011, β-bourbonene:
namely neo-chlorogenic acid, chlorogenic acid and 0.00029 and - , [E]-α-bergamoten: 0.00023 and -,
crypto-chlorogenic acid, 4 isomeric di-caffeoylquinic Geranyl acetone: 0.00019 and -, Calarene : – and
acids [3,5-O-dicaffeoyl, 3,4-O-dicaffeoyl, 4,5-O- 0.00027, β-ionone: 0.00116 and -, -]-[β-bisabolene:
dicaffeoyl and 1,3-O-dicaffeoyl esters] were 0.03486 and 0.00205, β-sesquiphellandrene: 0.00157
identified from Helianthus tuberosus tubers[46]. and -, Caryophyllene oxide: 0.00244 and -, [Z]-α-
bisabolene epoxide: 0.00624 and - , neophytadiene:
Eleven sesquiterpene lactone and two flavones were 0.00079 and - , hexahydrofarnesylacetone: 0.00083
isolated from Helianthus tuberosus leaves[47]. and - and squalene: - and 0.00032[49].
Pharmacological effects:
Eight components were detected in the methanolic
extract of Jerusalem Artichoke tuber extract from Antioxidant effect:
Folurd region included: cyclopentanol, hexadecanoic The radical scavenging activities of Jerusalem
acid, 9-octadecenoic acid, 9-octadecenoic acid, 9- artichoke [Helianthus tuberosus] leaves were
octadadecinoic acid, octadeconic acid, 13- investigated in vitro. The results indicated that the
octadecenal and 9-octadeconic acid. Ten components ethyl acetate fraction contained the highest total
were identified in the methanolic extract of phenolic content [266.69 ± 2.51 mg GAE/g dry
Jerusalem Artichoke tuber extract from Polsefid extract] accompanied with strongest free radical
region included: utero-noenen-1-ol-3; 2-propen-1-ol; scavenging abilities. Following an in vitro radical
3-deoxy-d-manneolclactone; heyadecanic acid; 1- scavenging activity-guide fractionation procedure, six
pyrrolin,3-ethyl; 9-octadecnoic acid; octadelenoic phenolic compounds which strongly quenched free
acid; 13-octa decnal; 1,2-epoxy-1-vinylcyclode coene radicals were separated from ethyl acetate fraction.
and cycloprtadecanon c, 2-hydroxy, and ten Among them, 3-O-caffeoylquinic acid and 1,5-
compounds were isolated from the methanolic extract dicaffeoylquinic acid played a dominant role due to
of Jerusalem artichoke tuber extract from Bandar their strong free radical scavenging abilities and their
Torkaman region included: 2-furan carboxaldehyde; high contents. The content of 3-O-caffeoylquinic acid
2-furan carboyaldehyde; Dodecane1,1-oxybis; in n-butanol fraction was 74.58 ± 1.05 mg/g, while
Glycine,n-methyl-n-1-oxadodecyl; hexa-decaneic 1,5-dicaffeoylquinic acid in ethyl acetate fraction was
acid; 9-octadecenoic acid; oleic acid; 9-octadecenal; 104.51 ± 2.86 mg/g[44].
9-octadecenal and phthalic acid disoo ctyl ester[48]. Antioxidant activity of the ethanol extract of tubers
Nine compounds: ent-17-oxokaur-15[16]-en-19-oic of Helianthus tuberosus was evaluated in vitro.
acid, ent-17-hydroxykaur-15[16]-en-19-oic acid, ent- ABTS cation radical scavenging activity of the
15β-hydroxykaur-16[17]-en-19-oic acid methyl ester, ethanol extract of tubers of Helianthus tuberosus was
ent-15-nor-14-oxolabda-8[17],12E-dien-18-oic acid, 20.25 ± 4.97 and 1.38 ± 0.58 at concentration of
4,15-isoatriplicolide angelate, 4,15-isoatriplicolide 1000 and 570 µg/ml respectively, DPPH radical
methylacrylate, [+]-pinoresinol, [−]-loliolide, and scavenging activities of ethanol extract was 13.58 ±
vanillin were isolated from the chloroform-soluble 2.54 18.24±1.80% at concentration of 1000 and 570
subfraction of a methanol extract of the whole plant µg/ml respectively. Reducing power [absorbance] of
of Helianthus tuberosus collected in Ohio, USA[25]. the ethanol extract of tubers of Helianthus tuberosus
was 0.0030 ± 0.0010, 0.0038±0.0001 and
The major component in leaves and tubers oils was[- 0.0089±0.0003 at concentration of 3000, 1000 and
]-β-bisabolene with the highest concentration among 570 µg/ml respectively, and the metal chelating
other volatile compounds concentrations of 70.7% capacity [Inhibition] was >100, 95.12±1.33 and
and 63.1%, respectively. Other components in leaves 94.27±2.33 at concentration of 3000, 1000 and 570
present in significant contents being: α-copaene µg/ml respectively[27].
[1.50%], β-bourbonene [0.59%], [E]-α-bergamoten
[0.47%], geranyl acetate [0.39%], β- The total fructans, phenolic content and radical
sesquiphellandrene [3.18%], β-ionon [2.35%], scavenging activities of the extracts were investigated
caryophyllene oxide [4.95%], [Z]-α-bisabolene using ABTS and CUPRAC methods. The 70%
epoxide [12.65%], neophytadiene [1.60%], and ethanol extracts possessed the highest total phenolic

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content [6-17 mg GAE/g dry weight]. The water Effect on carbohydrate digestive enzymes:
extracts characterized by higher fructan levels, 32 to α-Glucosidase inhibitory activity of the tubers of
69 g/100 g/ dry weight. The flour obtained from Helianthus tuberosus was 13.60 ± 2.54% and α-
tubers of Scorospelcu variety and wild population of amylase inhibitory activity was 0.49 ± 0.03%[27].
Helianthus tuberosus were evaluated as a valuable
source of total polyphenols and soluble dietary fibers, Antifungal effect:
because of the rich fructan content. The results The extracts and phenolic acids from Helianthus
revealed that flours possessed radical scavenging tuberosus leaves were investigated for antifungal
activity and were suitable for human and animal effect and potential use in enhancing preservation of
nutrition to prepare foods with health benefits[43]. fruits and vegetables in storage. Either crude leaf
extract or n-butanol fraction was active against
Anticancer effect: Botrytis cinerea, Colletotrichum gloeosporioides,
The cytotoxic activities of eleven sesquiterpene Phytophthora capsici Leonian and Rhizoctonia
lactone and two flavones compounds isolated from cerealis, with the values of IC50 ranging from 2.166
the leaves of Helianthus tuberosus were tested to 2.534 g/l for the crude leaf extract and 0.232–1.911
against MCF-7, A549 and HeLa cancer cells lines. g/l for n-butanol fraction. The severity of grey mould
The results revealed that sesquiterpene lactones caused by B. cinerea was significantly reduced by n-
exhibited consistent cytotoxicity against all three butanol fraction applied at 1 and 2 g/l [the control
cancer cell lines, while flavones showed selective efficiency of 71.3% and 77.8%, respectively,
inhibitory activity against HeLa cell lines. Among compared with commercial preparation carbendazim.
them, one of the sesquiterpene lactone compounds, Six phenolic acids were separated from n-butanol
exhibited strong growth inhibitory activity against all fraction. Among them, caffeic acid, 3,4-
three cell lines. Its IC50 values against MCF-7, A549 dicaffeoylquinic acid and 1,5-dicaffeoylquinic acid
and HeLa were 1.97 ± 0.04, 7.79 ± 0.44, played a dominant role and were active in bioassays
9.87 ± 0.20 μg/ml, respectively[47]. against Gibberella zeae, with respective minimum
inhibitory concentrations [MIC] being 108, 60 and
Nine compounds [ent-17-oxokaur-15[16]-en-19-oic 4.2 µg/ml respectively[52].
acid, ent-17-hydroxykaur-15[16]-en-19-oic acid, ent-
15β-hydroxykaur-16[17]-en-19-oic acid methyl ester, The antifungal activities of Helianthus tuberosus
ent-15-nor-14-oxolabda-8[17],12E-dien-18-oic acid, leaves extracts was studied against Rhizoctonia
4,15-isoatriplicolide angelate, 4,15-isoatriplicolide solani, Gibberella zeae, Alternaria solani and
methylacrylate, [+]-pinoresinol, [−]-loliolide, and Botrytis cinerea. The results showed that the extracts
vanillin] isolated from the chloroform-soluble exerted antifungal activity against Rhizoctonia
subfraction of a methanol extract of the whole plant solani, Alternaria solani and Botrytis cinerea, the
of Helianthus tuberosus were tested for cytotoxic inhibitory effects of aqueous extracts were
activity against MCF-7 human breast cancer cell significantly less than those of extracts of organic
line. The results revealed that two germacrane-type solvents, the extract of ethyl acetate possessed the
sesquiterpene lactones [4,15-isoatriplicolide angelate highest inhibitory activity, and its lowest inhibitory
and 4,15-isoatriplicolide methylacrylate] possessed rates were 77.91%, 100 and 100% to Rhizoctonia
cytotoxic activity[25]. solani, Alternaria solani and Botrytis cinerea
respectively at a concentration of 20 mg/ml[30].
Cytotoxic effects of different substances isolated
from Helianthus tuberosus were tested against four Medical benefit of inulin:
cell lines [Hp G2- cells, HCT-116, MCF-7 and 1301- Inulin was used as functional food. Functional food
cells]. Total sesquiterpenes were potent cytotoxic was defined as food that demonstrated to affect at
followed by heliangine, while inulin did not exhibit least one target function in the body beyond basic
cytotoxic effect[50]. nutritional effects, in a way to either enhance stage of
well-being and health and/or reduce the risk of
Antidiabetic effect: disease. Experimental studies have shown that inulin,
The ethanol extracts of tubers of Helianthus stimulating the immune system of the body,
tuberosus [ 250 and 500 mg/kg bw] showed decreasing the pathogenic bacteria in the intestine,
antidiabetic effect in streptozotocin induced diabetic relieving constipation, decreasing the risk of
rats, it also possessed an inhibitory effect on kidney osteoporosis by increasing mineral absorption,
tissue TBARS levels [24.5%][51]. especially of calcium, reducing the risk of

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atherosclerosis by lowering the synthesis of The effect of Jerusalem artichoke [JA], as a source of
triglycerides and fatty acids in the liver and inulin, was evaluated on intestinal pH, some blood
decreasing their level in serum, modulating the parameters and liver enzymes. Inulin effectively
hormonal level of insulin and glucagon, thereby modified intestinal characteristics, blood metabolites
regulating carbohydrate and lipid metabolism by and liver enzymes. Furthermore, 10% JA reduced
lowering the blood glucose levels, lowering the serum glucose as well as fructose levels. Serum ALP
blood urea and uric acid levels, thereby maintaining levels was decreased [P<0.05] by 10% JA[65].
the nitrogen balance and also reduced the incidence
of colon cancer. Furthermore, inulin with the β [2,1] CONCLUSION:
linkages between the fructose monomers cannot be This review discussed the chemical constituent,
digested by human intestinal enzymes, giving rise to pharmacological and therapeutic effects of
important applications in functional foods suitable for Helianthus tuberosus as promising herbal drug
management of type 2 diabetes, obesity and other because of its safety and effectiveness.
blood sugar-related health conditions[53-57].
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