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Open access peer-reviewed chapter

Taraxacum Genus: Potential Antibacterial and Antifungal Activity

Written By

María Eugenia Martínez Valenzuela, Katy Díaz Peralta, Lorena Jorquera Martínez and Rolando Chamy Maggi

Submitted: 14 June 2017 Reviewed: 11 October 2017 Published: 05 November 2018

DOI: 10.5772/intechopen.71619

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Abstract

Plants have been used in traditional medicine for centuries as antibacterial and antifungal agents. Taraxacum spp., commonly known as dandelion, is a well-known herbal remedy with a long history; however, limited scientific information is available to explain its traditional use. This review aims to provide current information and a general overview of the available literature concerning the antibacterial and antifungal properties of the Taraxacum genus to support its potential as a powerful herbal medicine. Though Taraxacum has demonstrated that it is capable of inhibiting the growth of a wide range of bacteria and fungi, the technical aspects of methodology lack standardization, and, therefore, the overall results of processing are difficult to compare between studies. Phytochemical composition and antimicrobial activity in Taraxacum are neither directly related, nor does the published data provide sufficient information for identifying the group of unique extraction conditions that are optimal against specific microorganisms. Antimicrobial research indicates that this plant is a promising species for treating several common infections in humans, animals, and plants.

Keywords

  • antimicrobial
  • antifungal
  • ethnopharmacology
  • extraction
  • Taraxacum species

1. Introduction

Plants have been used in traditional medicine for centuries due to the synthesis of several molecules that provide antibacterial and antifungal properties, the majority of which probably evolved as defenses against infection or predation [1]. The medicinal potential of many plants is still largely unexplored. Among the estimated 250,000–500,000 plant species, a relatively small percentage have been investigated phytochemically and the fraction submitted for biological or pharmacological screening is even smaller [2]; approximately 20% of the plant species in the world have been investigated for these properties [3]. In this context, dandelion serves as an interesting species with which to unify decades-old information regarding its biological potential against diverse microorganisms. This review gathers the existing results to advance the search for products that could strengthen the domestication and mass production of this plant.

The Taraxacum spp. commonly called dandelion is an herbaceous perennial plant of the Asteraceae (Compositae) family. This common weed is found worldwide, though originally introduced from Eurasia, and can be found growing in parks, gardens, pastures, orchards, roadsides, vegetable gardens, and among agricultural and horticultural crops [4]. Primarily used as food, the role of Taraxacum in traditional medicine was mentioned during ancient times by the Greek physician Dioscorides in the first century and during the renaissance by monks in Cyprus [5]. This plant has been used to treat cystitis, liver and gastric ailments, hepatic and renal detoxification, diabetes, as an anti-inflammatory and anticarcinogenic agent, and, to a lesser extent, as an antimicrobial and antiviral agent, as described in several reviews [6, 7]. Ethnopharmacologically, its use as an antimicrobial agent has been known worldwide among varying cultures, though it has always been administered as a cataplasm (poultice) or infusion. The traditional antimicrobial uses of Taraxacum worldwide are displayed in Table 1.

SpeciesCommon useCountryPart usedConsumptionReferences
T. cypriumCatarrh and common cold, coughGreeceRoots, leaves[5]
T. mongolicumUrinary tract infectionsChinaLeafInfusion[8]
T. officinaleMalariaVenezuelaRoots, leavesDecoction[9]
TuberculosisItaly[10]
CoughItaly[11]
Bacterial infectionMexico[12]
DiureticChikarRootsTonico[13]
T. panalpinumMalariaPortugalRoots, leaves, juice[14, 15]
T. platycarpumPleurodyniaKoreaLeaf, stemInfusion
Brewing
[16, 17]

Table 1.

Ethnopharmacological information of Taraxacum genus used as an antimicrobial traditional medicine.

Asia and Europe have an important historical background regarding the traditional uses of Taraxacum, primarily T. officinale, T. mongolicum, and T. coreanum. This traditional knowledge has been the principal reason for studying the potential uses and crop requirements of Taraxacum; studies in America remain scarce [18]. Due to the unscientific approach often present in oral traditions, uncertainty surrounds whether Taraxacum use effectively treats microbial infection or, instead, treats only the symptoms. Therefore, scientific research is extremely important in avoiding misinterpretation and myths regarding Taraxacum or any other plant.

The first antibacterial scientific study for Taraxacum was reported a mere 35 years ago [19]. More than a decade later, studies related to Taraxacum antimicrobial activity gained significant relevance as part of an Italian program between the University of Ferrara and the University of Naples for screening medicinal plants [20]. Nowadays, this plant is becoming a promising species in the treatment of several bacterial and fungal diseases due to the results of various antimicrobial-related studies. This chapter seeks to elucidate both the traditional uses and current state of Taraxacum in antimicrobial research to determine the potential that this genus has to become an industrial medicinal crop worldwide. Due to the high potential value that could be derived from the use of new technologies and industrial products developed from this type of plant species, the conservation and protection of the crop should be considered and sustainable global production strategies are developed in accordance with assessments of ecological, economic, and social factors.

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2. Antimicrobial properties of the Taraxacum genus

Literature reviews providing information on the antimicrobial aspects of natural products, which had until now only been considered empirical, have been recently scientifically confirmed as a means of countering the increasing reports of pathogenic microorganisms resistant to synthetic antimicrobial agents. Some plant-derived compounds can control microbial growth, either separately or in association with conventional antimicrobials [21]. Currently, numerous studies seek to improve pathogen prevention by combining the application of medicinal herb extracts with an antibiotic or effective antipathogenic pesticide to reduce the active synthetic ingredient and resistant pathogenic strains.

2.1. Taraxacum species tested for antimicrobial properties

Among the Taraxacum genus, T. officinale is the most frequently reported species, with almost 80% of mentions in documents related to antimicrobial properties (see Table 2), followed by T. mongolicum and T. coreanum, though over 2500 Taraxacum species are currently identified [67]. Other, less studied species include T. platycarpum, T. farinosum, T. ohwianum, and T. phaleratum; however, the relevance of these species is confined to specific areas (mostly in Asia) in which they grow naturally since they are not deliberately cultivated for medicinal benefit. This indicates that the microbial properties of less than 1% of all Taraxacum species discovered have been studied, revealing the enormous research potential of this genus.

SpeciesAutentification/VoucherC: Collected
P: Purchase
ZoneSeasonPlant part*Sample manipulationRatioSolventExtraction timeTemp.AgitationInhibition activity**Ref.
T. officinale Wigg.No/NoNININIFlowerNI1:10Acetic acid 10%1 hRTHomog.+[22]
T. officinale Wigg.No/NoCNIYesSeedsGrounded1:10Acetic acid 10%1 hRTNI+[23]
T. officinale WeberYes/NoCYesYesNIDriedNIWater, ethanol and ethyl acetate1 h80°CMaceration+[24]
T. officinaleYes/YesCYesNINIAir-dried1:14Acetone30 minNINI+[25]
Taraxacum spp.No/NoCYesNININI1:10Dichloromethane3 h20°CHomog.+[26]
T. officinaleNo/YesCYesYesNININIDichloromethane3 daysNIHomog.+[27]
T. coreanumNo/NoNININININI1:3.3Ethanol 75%9 h60°CReflux+[28]
T. mongolicumNo/NoCNINIAerialFrezee-dried and grounded 20-mesh1:5Ethanol 75%2 daysNISoaked+[29]
T. officinale WeberNo/YesCYesYesRootDried and groundedNIEthanol 80%NINIReflux+[20]
T. officinale F. H. WiggYes/YesCNINIAerialAir-dried and crushed1:1Ethanol 90%2 daysRTIntermitent shaking+[30]
T. mongolicum H.NI1:10Ethanol 95%3 h80°C+[31]
T. ohwianumNo/NoNINININIFreeze-dried, air-dried (40°C, 24 h), grounded 24-mesh1:16Ethanol 95%24 hRT (23°C)Shaking+[32]
T. officinaleYes/NoNININILeavesAir-dried1:5Ethylacetate24 hRT150 rpm+[22]
T. officinale F.H. Wigg.Yes/YesPNINIRootFreeze-dried and blended1:10HexaneOvernightRT70 rpm+[33]
T. officinaleNo/NoNININILeavesAir-dried 1 month and grounded1:1.4Methanol 75%NININI+[34]
T. officinale WeberNo/NoCYesNIAerialAir-dried a 40°C (36–48 h) and grounded1:5Methanol 80%1 h100°CReflux+[35]
T. officinale Weber ex. F.H. WiggNo/YesNININILeavesNI1:4Methanol5 daysRTNI+[36]
T. officinale WeberNo/NoCNINIAerialDry under shade and ground1:10Methanol3 weeks25°CHomog.+[37]
T. platycarpumNo/NoNINININIDriedNIMethanol3 h80°CNI+[38]
T. platycarpumNo/NoNINININIDriedNIMethanol3 h80°CNI+[39]
T. officinaleNINIMethanol16 h50°C+[40]
T. officinaleNo/NoCNINILeavesDried under shade and grounded1:2.5Methanol24 h37°C120 rpm+[41]
T. mongolicum Hand-MazzYes/YesCYesYesNIAir-dried and groundedNIWater3 h100°CBy boiling+[36]
T. officinaleNI1:05WaterNINIHomog.+[42]
T. officinaleNo/NoNINININIDried at 25–30°C for 1 week., ground with a mortar1:20Water24 h35°CShaking+[43]
T. officinale F.H. (Webb)No/NoC/PNINIRootCleaning prior freeze-dried, grounded1:10Water3 hRT170 rpm+[44]
T. officinaleNo/NoNININININI1:04Water45 min100°CNI+[45]
T. officinale Weber ex WiggerNo/NoNININIleavesGrounded1:01Water5 minNINI+[46]
T. mongolicumNo/NoNINININIGroundedNIWater1 h100°CBy boiling+[47]
T. officinaleNo/NoNINININIDried at 60°C × 2 h and grounded 60-mesh1:10WaterNININI+[48]
T. officinale H.NI/NINININININI+[49]
T. officinale F.H. WiggNI/NICYesYesHoneyNINININININI+[50]
T. farinosum Hausskn. & BornmNI/NICNIYesRootNINININININI+[51]
T. officinaleYes/NoCYesYesNIDried 40°C × 5 days and groundedNINININIReflux+[52]
T. officinaleNI/NININININININININININI+W[53]
T. officinaleNo/NoPNININININIEthanol 35%NININI+W[54]
T. platycarpumNo/NoPNININIGrounded 50-mesh1:10Ethanol24 hRTHomog.+W[55]
Taraxacum sp.No/NoNININIAerialGrounded1:10Water4 h100°CBy boiling+W[56]
T. officinale F.H. Wigg.No/NoCYesYesAerialFrozen, cut and grounded1:01Ethanol 20%24 hRTNI[57]
T. officinaleNo/NoNININILeavesDriedNIEthanol 40%NININI[58]
T. officinaleNo/NoExtract (P)NININIDilutedNIethanol 45%NININI[59]
T. phaleratum G. Hagl et RechYes/YesCYesNIAerialAir-dried and groundedNIEthanol 70%NIRTNI[60]
T. officinale Cass.No/NoPNINIRootDried1:04Ethanol24 hNI[61]
T. officinaleNo/NoCYesNIflowerChopped and frozenNIMethanol 90%30 min4°CHomog.[62]
T. officinale WeberYes/YesNINININIDried and grounded1:40MethanolOvernightRTNI[63]
T. mongolicum Hand-MazzNo/YesCNINIWholeNI1:10WaterOvernightNIHomog.[64]
T. officinaleNo/NoPNINIRootGrounded1:8.3Water30 min100°CBy boiling[65]
T. officinaleNo/NoCYesYesLeafs, rootsNI1:03WaterRTHomog.[66]

Table 2.

Physical parameters on Taraxacum extracts for testing antimicrobial activity.

NI, No indicated.


2.2. Bacterial and fungi strains tested

Taraxacum extracts have been tested on different bacterial and fungal strains affecting humans, animals, and plants to determine its antimicrobial profile, confirm its traditional usage, and expand its known uses. Antimicrobial agents are categorized based on the spectrum of action, namely “narrow” and “broad” spectrum, which indicates whether its use is specific for certain bacterial strains or active on a wider range. Bacterial infections can result in mild to life-threatening illnesses that require immediate antibiotic intervention. Alternatively, a superficial fungal infection is rarely life-threatening but can have debilitating effects and may spread to other people or become invasive or systemic, resulting in a life-threatening infection. The widespread, and sometimes inappropriate, use of chemical compounds can create antibiotic resistance. Due to this issue, the potential of Taraxacum as a useful, broad-spectrum antimicrobial and antifungal agent that can be “easily and worldwide grown,” is highly valuable. A list of the strains against which Taraxacum’s antimicrobial activity has been tested is displayed in Table 3.

Bacterial strainsFungi strains
Aeromonas hydrophila (−) [22]Alternaria alternata (+) [46, 68]
Agrobacterium tumefaciens (+) [24]Aspergillus carbonarius (+) [35]
Bacillus cereus (+) [22, 33, 36, 44] (−) [66]A. niger (+) [23, 35, 37, 68, 69] (−) [27, 66]
B. pumilus (−) [66]A. flavus (+) [37] (−) [66]
B. subtilis (+) [20, 24, 25, 27, 29, 34, 38, 39, 41, 48, 69] (−) [37, 64, 66]A. fumigatus (+) [37](−) [66]
Campylobacter jejuni (+) [54, 59]Bipolaris sorokiniana (+) [23, 67] (−) [68]
Chromobacterium violaceum (+) [66] (−) [65]Botrytis cinerea (+) [23, 35, 67]
Clavibacter michiganense (+) [69]Candida albicans (+) [27, 34, 36, 52] (−) [55, 57, 66]
Cupriavidus sp. (−) [66]C. glabrata (−) [55, 66]
Enterobacter coccus (−) [37]C. krusei (−) [66]
Enterococcus faecalis (+) [53] (−) [37, 66]C. parapsilesis (−) [55, 66]
Erwinia carotovora (+) [24]C. utils (−) [55]
Escherichia coli (+) [22, 24, 25, 27, 29, 34, 36, 38, 39, 41, 43, 45, 47, 48, 58, 70]
(−) [20, 32, 33, 37, 44, 57, 62, 64, 66]
C. tropicalis (+) [55]
Cladosporium herbarum (+) [71]
Helicobacter pylori (+) [31, 54]Cochliobolus sativus (+) [68]
Klebsiella aerogenes (−) [66]Colletotrichium gloesporoides (−) [68]
K. penumoniae (+) [29, 36] (−) [20, 37, 45, 66]C. lagenarium (+) [42]
Listeria monocytogenes (+) [38, 39] (−) [66]Cryptococcus neoformans (+) [36]
Micrococcus kristinae (+) [25]Exophiala (Wangiella) dermatitidis (−) [66]
M. luteus (+) [37, 41]Fusarium avenaceum (+) [68]
Mycobacterium aurum (−) [63]F. graminearum (−) [69]
M. bovis (−) [63]F. oxysporum (+) [23, 56, 69]
M. smegmatis (−) [63]Microsporum canis (+) [51]
M. tuberculosis (−) [60]Monilinia laxa (+) [35]
Propionihacterium acnes (+) [49]Mucor piriformis (+) [46]
Proteus mirabilis (+) [43] (−) [20]Penicillium sp. (−) [66]
P. vulgaris (+) [25, 29] (−) [70]P. digitatum (+) [35]
Pseudomonas sp. (−) [50]P. expansum (+) [26, 46] (−) [35]
P. aeruginosa (+) [24, 27, 29, 36, 41, 49, 70] (−) [20, 37, 57, 64, 66]P. italicum (+) [35]
P. fluorescens (+) [24]Ph. betae (+) [23, 68]
P. syringae (+) [69]Phytophthora infestans (+) [69]
Serratia/Rahnella sp. (−) [66]Pityrosporum ovale (+) [49]
Salmonella typhimurium (+) [36] (−) [33, 44]Pythium debaryanum (+) [69]
S. abony enterica (+) [58]Rhizoctonia solani (+) [37, 56]
S. poona (−) [66]Saccharomyces cereviseae (+) [34]
S. typhi (+) [44, 51] (−) [20]Saprolegnia australis (−) [61]
Sarcina lutea (+) [24]Scedosporium apiospermum (−) [66]
Serratia marcescens (+) [25] (−) [66]Trichophyton longifusus (+) [51]
Shigella fiexeri (−) [70]T. mentagrophytes (+) [27]
S. sonnei (+) [36]Verticillium albo-atrum (+) [23] (−) [68]
Staphylococcus aureus (+) [22, 24, 25, 28, 29, 32, 33, 34, 36, 38, 39, 41, 43, 44, 45, 48, 49, 50, 51, 52, 70] (−) [20, 27, 37, 57, 58, 62, 64, 66]
S. epidermidis (+) [28] (−) [66]
Streptococcus haemolyticus (+) [20]
S. agalactiae (+) [47]
S. dysgalactiae (+) [47]
Vibrio cholerae (+) [37]
V. parahaemolyticus (+) [38, 39]
Xanthomonas campestris (+) [69]

Table 3.

Bacterial and fungal strains on which Taraxacum extracts have been tested.

(+) Extracts of Taraxacum active against the pathogen; (−) extracts of Taraxacum inactive against the pathogen.

2.2.1. Human pathogens

In the study of antibacterial properties of these plants, most attention has been focused on human pathogenic strains, including S. aureus, E. faecalis, V. cholerae, B. subtilis, P. aeruginosa, K. pneumonia, and E. coli. These are the pathogens commonly responsible for infections in gastrointestinal and massive organ systems such as the lungs and skin. Taraxacum officinale is the species generally studied to combat these pathogens, but it has demonstrated diverse results depending on the extraction characteristics or the bioassay performed. For instance, a methanolic extract of T. officinale at 0.2 mg/mL was as effective as an antibacterial agent against M. luteus and V. cholera with minimum inhibitory concentration (MIC) values of 1.0 and 12.5 mg/mL, respectively, but displayed no activity against S. aureus, E. faecalis, E. bacter, V. cholerae, B. subtilis, P. aeruginosa, K. pneumonia, or E. coli [37]. In the same study, the inhibition percentages achieved for mycelial growth of A. niger, A. flavus, A. fumigatus, and R. solani were 37, 71, 85, and 78%, respectively. Other works indicate that methanolic T. officinale leaf extracts ranging from 0.003 to 0.5 mg/mL were active against S. aureus, P. aeruginosa, B. cereus, S. sonnei, S. enterica serovar typhimurium, E. coli, K. pneumonia, C. albicans, and C. neoformans with MIC values ranging from 0.04 to 5.0 mg/mL [36]. A similar extract at 10 mg/mL displayed moderate growth diameter inhibition for S. typhi, but was highly active for S. aureus, B. cereus, and E. coli, even when no activity was observed for A. hydrophila [22]. Ethanolic extracts of 2.0 mg/mL were active against A. aureus, MRSA clinical, and B. cereus, with MIC values between 0.38 and 0.5 mg/mL, but were not effective against E. coli or S. typhi. In the same work, a water extract at the same concentration showed no activity against any strain tested [33]. Moreover, 21 ethanolic extracts from various plants were tested against 20 Salmonella serovars. Taraxacum inhibited only 5% of these, and was therefore not considered for additional antimicrobial studies [72].

Recently, methanolic and chloroformic leaf extracts of T. officinale were found to be effective against M. luteus, P. aeruginosa, B. subtilis, E. coli, and S. aureus with MIC values of 0.3 mg/mL and no observable activity for water extracts [41]. In this study, the highest impact was noted with methanol and chloroform extracts against S. aureus and E. coli, respectively, and the lowest with both extracts against P. aeruginosa. Furthermore, an ethanolic extract was effective against E. coli and S. aureus, but no activity was observed for either extract against K. pneumonia and P. aeruginosa at 50, 100, and 200 mg/mL. Nevertheless, a water extract was effective only for E. coli at 100 and 200 mg/mL [45]. Water and ethanolic extracts at 1.0 mg/mL exhibit effective inhibition against S. aureus and fewer inhibitory effects were observed for P. mirabilis; against S. aureus, an ethanolic extract was active at 0.5 mg/mL, but a water extract was only active at 1.0 mg/mL; and inhibition was not achieved for either extracts at 0.1 mg/mL [73]. An ethanolic extract was slightly active against B. subtilis and S. haemolyticus, but was inactive against other Gram positive and Gram negative strains, resulting in no further studies with this extract [20]. Furthermore, only weak activity was achieved by methanolic extracts of this plant against P. syringae [74].

Both ethanolic and water extracts of T. officinale were active for S. marcescens and M. kristinae. The ethanolic extract alone was active on P. vulgaris, E. coli, B. subtilis, and S. aureus with MIC values ranging from 1.0 to 7.0 mg/mL for all strains tested [25]. Similar extracts had antimicrobial effects on four species that induce acne (P. ovale, P. acnes, P. aeruginosa, and S. aureus) in broth dilution tests with effects depending on the extract concentration, but no further information was available [49]. Moreover, a leaf extract (0.04 mg/well) was reported as a bactericidal agent against S. aureus and fungistatic against C. albicans [52]. Contrarily, extracts of 130 and 200 mg/mL from aerial parts were unable to prevent the growth of 34 microorganisms from genera Bacillus, Enterobacter, Klebsiella, Listeria, Pseudomonas, Salmonella, Staphylococcus, Aspergillus, and Candida, among others; therefore, it was considered inactive at these concentrations in a disc diffusion assay [66]. A methanolic T. officinale flower extract was not active against E. coli or S. aureus at 1.0 mg/mL in a diffusion agar assay [62] and no activity was found on S. aureus, E. coli, P. aeruginosa, or C. albicans using a leaf ethanolic extract when 0.05 mL were placed in sterile discs [57]. Furthermore, an ethanolic extract of leaves displayed no activity against S. aureus, E. coli, or S. abony by the serial dilution method [58], with the same results for root and leaf extracts on M. aurum and M. smegmatis at 0.5 mg/mL [63].

Raw extracts of T. officinale have been widely tested, as well as solvent fractions. In a study in which the methanolic leaf extract was fractioned by different solvents, the methyl chloride, ethyl acetate, and butanol fractions were active on E. coli, S. aureus, B. subtilis, C. albicans, and S. cerevisiae at 50 mg/mL, with inhibition percentages ranging from 13 to 76%. The water fraction showed moderate inhibition via the broth dilution method (10 and 14% for E. coli and B. subtilis, respectively) but no effect on the disc diffusion assay [34]. The only report in which a Taraxacum extract was compared to another natural antibacterial substance besides other plants extracts evaluated the use of T. officinale extract as an irrigation agent in endodontic treatments against E. faecalis in root canal infections. Leaf and root extracts at 0.7% were slightly active but propolis was more effective for this purpose [53]. In the case of commercial preparations, high activity has been reported for a commercial T. officinale ethanolic extract, showing antibacterial activity against H. pylori at 20 mg/mL with 26% inhibition but no observable activity for C. jejuni [54].

Considering other Taraxacum species, T. platycarpum anticandidal activity was determined against five different Candida sp. by agar diffusion assay. An ethanolic extract at 0.2 mg/mL weakly inhibited C. tropicalis but no other Candida strains [55]. A methanolic extract was active against B. subtilis, S. aureus, L. monocytogenes, E. coli, and V. parahaemolyticus at concentrations ranging from 0.5 to 2.0 mg/mL, with growth inhibition ranging from 5.1 to 100%, correlating to the concentration. In that study, chloroform, butanol, and ethyl acetate fractions were active in the disc diffusion assay for almost every strain tested, but an aqueous extract was inactive [38, 39].

An ethanolic extract of T. mongolicum at 0.2 mg/mL was not able to achieve growth inhibition in a microdilution assay for B. subtilis, S. aureus, E. coli, or P. aeruginosa [64]. In contrast, an ethanolic extract of this species was active for E. coli, S. aureus, and P. aeruginosa in the disc diffusion assay with MIC values between 0.05 and 0.1 mg/mL, which was three times higher than the values obtained for erythromycin. However, no activity was achieved for S. fiexneri or P. vulgaris [75]. Another report indicated that only the butanol fraction of an ethanolic extract of this plant was active on H. pylori, but water and methyl chloride fractions were inactive. Nevertheless, a different report indicated that a butanol fraction exerted higher inhibition (13%) than the aqueous fraction, possibly due to the flavonoid and luteolin content (28 and 1.1%, respectively) [31]. Against S. aureus and S. epidermis, an acetyl acetate fraction of an ethanolic T. coreanum extract was active at 0.5, 1.0, and 3.0 mg/disc, a chloroform fraction was active at 1.0 and 3.0 mg/disc, and a butanol fraction at 1.0 mg/mL, but displayed no activity against MRSA displayed [28]. An ethanolic T. ohwianum extract was active against E. coli at 240 and 320 mg/mL, but not against S. aureus [32]. These authors indicate that the pH and temperature of the bioassay were important parameters in the antimicrobial performance of the extract. An extract of the aerial parts of T. phaleratum was inactive at 0.2 mg/mL against M. tuberculosis, even when several solvent fractions were tested [60].

Limited studies have been conducted on humans establishing the antimicrobial potential of Taraxacum extracts. Chinese language studies have reported the effects of various formulas containing T. mongolicum for medical treatment. An herbal formula known as “fu zheng qu xie” was just as effective as the antibiotic gentamycin in 75 cases of gastric disease caused by H. pylori. Furthermore, an herbal formula called “jie du yang gan gao,” which includes T. mongolicum, was significantly more effective than another botanical formulation in lowering elevated liver enzymes and curing patients with hepatitis B in a 96-person, double-blind trial [76].

2.2.2. Plant pathogens

Plant extracts have also been tested on bacteria and fungi that affect fruits and vegetables, causing rot diseases during postharvest handling, to find an alternative to chemical pesticides, which are harmful to the environment and human health. An aqueous T. officinale root extract (S) at different dilutions (S, S/2 to S/100) caused significant inhibition to mycelial growth in A. alternata (70% for S to 17% for S/100), P. expansum (67% for S to 5.3% for S/100), and M. piriformis (70% for S to 16% for S/100) [46]. In the case of R. solani and C. sativus, a Taraxacum acetyl acetate extract at a concentration of 100 mg/mL exhibited a weak effect on the growth of these plant pathogens and no inhibition of F. oxysporum [22]. A methanolic extract of Taraxacum at 0.2 mg/mL was not effective against A. niger, A. flavus, A. fumigates, or R. solani [37]. A methanolic extract of Taraxacum sp. displayed weak activity against C. sativus, F. oxysporum, and R. solani at 5 mg/disc and a water extract displayed no activity at all [56].

A T. officinale hydro-methanolic extract tested the inhibition of conidial germination and inhibition of germ tube elongation for several plant pathogens at several dilutions (0.25×, 0.5×, and 0.75×) using a microassay method on slides. Dilution at 0.75× showed inhibition of conidial germination values of 2, 3, 4, 9, 11, and 12% for P. italicum, A. niger, A. carbonarius, B. cinerea, M. laxa, and P. digitatum, respectively. For these same strains, excluding A. carbonarius, inhibition of germ tube elongation values were 56, 45, 38, 5 and 42%, respectively. For P. expansum, the plant extract did not show positive results for inhibition of conidial germination or inhibition of germ tube elongation. In artificially inoculated fruits, the extract applied to nectarines was not protective against brown rot development from M. laxa, while for apricots effects were similar to those of the negative control for P. digitatum [35]. Dichloromethane and diethyl ether T. officinale extracts were tested on P. expansum by applying either a solution or its vapor to paper discs. The dichloromethane extract was more active of the two models, though direct inoculation in apples offered no observable inhibition [26]. Water extracts of T. officinale and T. platycarpum were tested against C. lagenarium in cucumber, exhibiting inhibition rates of the anthracnose lesions of 1.9 and 13% in treated leaves, and 11 and 5.3% in untreated leaves, respectively. These results were not significant compared to other plant extracts [42]. In vivo evaluation of protective effects in plant tissue has not been as successful as the in vitro assays, which is typical in cases of inhibitory activity validation. To avoid these ineffective results, concentrations are increased to demonstrate the pathogen control effect.

2.2.3. Animal pathogens

Regarding animal pathogens, Saprolegnia infections can account for significant salmonid losses. Treatment is difficult and there are reservations regarding efficacy, prompting a search for suitable alternatives. A T. officinale root extract was not as effective as a fungistatic at 10, 100, 1000, or 10,000 mg/mL [61]. The effects of Taraxacum polysaccharides were studied on the preservation of white shrimp (Penaeus vannamei) during refrigerated storage (10 days at 4°C) by soaking the shrimps in aqueous extracts (1–3% w/v). Samples were periodically evaluated for total viable count, pH value, and total volatile basic nitrogen, which resulted in 2–3% of shrimp in fresh conditions (<30 mg/100 mg of total volatile basic nitrogen) and a total viable count that only increased slightly during storage. This indicated that the treatment effectively retarded bacterial growth during refrigerated storage, prolonging shrimp shelf life for up to 10 days [76].

In the case of the meat industry, an herb mixture including T. officinale as a substitute for fodder antibiotics in pig feeding revealed positive growth of the animal and no change in meat quality, confirming the possibility of using herbs as an antibiotic substitute in pig feed [77, 78]. Aqueous and ethanolic extracts of T. mongolicum could also inhibit four pathogenic bacteria responsible for cow mastitis, a serious disease in the cow industry, at concentrations of 0.13, 0.25, and 0.5 g/mL. In this case, the ethanolic extracts displayed slightly better antibacterial activities than aqueous extracts. For E. coli, S. aureus, S. agalactiae, and S. dysgalactiae, inhibition zone diameters were slightly larger for aqueous than for ethanolic extracts but showed between medium and high sensitivity [79]. Dandelion extract can not only be used to control pathogens but also to supplement the diet of animals, which could result in increased meat, milk, whey, and other yields, contributing to the food industry. Alternatively, the extracts could be utilized in the agricultural industry as biofertilizers to promote plant growth and strengthen the plant against biotic and abiotic stress.

2.3. Taraxacum antimicrobial action mechanisms

Innate plant immunity involves various defense responses, including cell wall reinforcements, lytic enzyme biosynthesis, secondary metabolite production, and pathogenesis-related proteins. To protect themselves from non-beneficial microorganisms, plants accumulate secondary metabolites that form chemical barriers to microbial attacks (phytoanticipins) and produce antimicrobials (phytoalexins) [80]. Phenolics and terpenoids are considered the primary mechanisms for plant defenses because these reduce microbial attacks by disrupting the cell membranes in microorganisms, bind to adhesins and cell wall compounds, and inactivate enzymes, among other roles [81]. The action mechanisms of natural compounds are related to the disintegration of the cytoplasmic membrane and destabilization of the proton motive force, electron flow, active transport, coagulation of the cell content, inhibition of protein synthesis, inhibition of DNA synthesis, and the synthesis of metabolites used for DNA synthesis [82]. Some action mechanisms are specific to certain targets and some targets may also be affected by more than one mechanism [83]. A general scheme of the action’s sites and antimicrobial potential mechanism is presented in Figure 1 of Supporting Information.

Figure 1.

Main action mechanisms for antimicrobial agents (adapted from Mulvey and Simor [84]).

Even though Taraxacum is a plant with extremely high pathogen resistance, the underlying molecular mechanisms of antimicrobial activity are poorly studied [68]. Until now, most of the research on Taraxacum has focused on elucidating the compounds present in the extract, and, to a lesser extent, on the mechanism involved in the antimicrobial activity itself. One study specifically illustrated the effect of four proteins from T. officinale flowers on fungi by light microscopy and distinguished two modes of antimicrobial action, depending on the fungus tested. Taraxacum proteins completely blocked conidia germination or induced thickening of multiple local hyphae and irreversible cytoplasm plasmolysis [68, 69]. Different extracts from this genus showed positive inhibitory activity in controlled studies and were characterized by protein synthesis inhibition (e.g. chloramphenicol, tetracycline, gentamicin, and kanamycin) and cell wall synthesis (e.g. amphotericin, cefixime, cephalothin, and penicillin). These mechanisms need to be addressed to elucidate the Taraxacum active compound action mechanisms because a direct relation with the positive controls cannot be pursued.

Another response that has been studied is the modulation of microbe adherence to body tissues. Adhesion to epithelial cells has been represented as the first step in the subsequent bacterial invasion of host cells [59]. These authors reported the partial inhibition of intestinal adherence of C. jejuni HT-29 cells using a commercial ethanolic Taraxacum extract. Cytotoxic activity was less than 10%, but no antibacterial activity was observed. Moreover, Taraxacum has been tested with the aim of controlling bacterial diseases by inhibiting communication between bacteria. An ethanolic extract of T. officinale aerial parts disturbed bacterial communication systems (or quorum sensing) for C. violaceum, showing the moderately positive effect of the extract on the attenuation of microbial pathogenicity [30]. In contrast, an ethanolic and water extract of the rhizomes of the same plant showed no significant activity in the same assay [65].

2.4. Taraxacum compounds related to antimicrobial action

Several studies have named a wide range of compounds, including terpenes, flavonoids, and phenolic compounds, as responsible for the medicinal activity of different plants [85, 86]. For Taraxacum, only a few studies concerning its antimicrobial properties have considered chemical identification of the obtained extracts and this identification is chiefly qualitative (e.g. using colorimetric methods indicating presence or absence). Authors report the presence of terpenoids, triterpenoids, steroids, coumarins, phenols, saponins, flavonoids, flavones, flavonols, chalcones, phlobatannins, and cardiac glycosides in antimicrobial extracts [22, 27, 34, 36, 37, 43, 44, 45, 87, 88] but neither compound isolation nor further identification were performed.

Taraxasterol acetate, lupeol acetate, tranexamic acid, and squalene, among others, were identified in the dichloromethane extract of T. officinale leaves, which show low activity against E. coli, P. aeruginosa, B. subtilis, C. albicans, and T. mentagrophytes in an agar well assay at 30 μg but no observed activity against S. aureus or A. niger [27]. Terpenoids and flavonoids were identified in the ethanolic extracts of the T. farinosum root, which displayed antibacterial activity against S. aureus, S. typhi, M. canis, and T. longifusus in an agar well diffusion and agar tube dilution, while the herb extract was active only against the latter two strains [51]. Fractions of a methanolic root extract indicated the significant presence of phenolic-based compounds and hydroxyl-fatty acids with liquid and mass spectrometry, and were active against S. aureus, MRSA clinical, and B. cereus at 2 mg/mL, with MIC values ranging from 0.05 to 0.19 mg/mL, and crude extracts indicating values of 0.25–0.5 mg/mL [33]. An oligosaccharide extract (DOs) from this species exhibited high antibacterial activity against E. coli, B. subtilis, and S. aureus at 100 mg/mL, indicating that these oligosaccharides could potentially be used as antibacterial agents [48].

Concerning specific compounds, isolated Taraxacum peptides displayed antimicrobial activity at 6 μg/μL, corresponding to 52–79% of kanamycin activity against P. syringae, B. subtilis, and X. campestris at the same concentration [69], which is a promising value that warrants further experiments. These authors indicated that though A. niger appeared sensitive to four proteins (ToAMP1, ToAMP2, ToAMP3, and ToAMP4) from T. officinale flowers, F. graminearum was not susceptible to any of these proteins. All proteins displayed inhibition activity against B. cinerea, B. sorokiniana, A. niger, P. debaryanum, F. oxysporum, and P. infestans, with IC50 values ranging between 1.2 and 5.8 μM. The ToAMPs were also active against P. syringae, B. subtilis, and X. campestris, similar to a kanamycin control. Additionally, ToAMP2 was active against C. michiganensis at up to 0.5 μg/μL. The disease development of P. infestans was inhibited by ToAMP2 at 1.3 μM (20–40%) to 5.2 μM (10–20%). In further studies, B. sorokiniana, C. gloeosporioides, and V. albo-atrum were insensitive to ToAMP4, another peptide isolated from the seed extract of T. officinale, at concentrations below 15 mM. The IC50 values for the agent-sensitive fungi A. alternata, A. niger, F. avenaceum, and P. betae ranged from 2.9 to 13.1 mM, with MIC values from 1.0 to 8.0 mM; no activity was observed for P. syringae, B. subtilis, E. coli, or C. michiganensis [68, 69]. Peptides supposedly have broad-spectrum activity, lack of microbial resistance, and high efficacy [69], but some action mechanisms in these molecules are still poorly defined [89]. Peptides related to albumin 2S from Taraxacum seeds are active against phytopathogenic fungi and bacteria. Antifungal assays displayed different activities for the 2S isoforms (ToA1, ToA2, and ToA3). The spore germination of B. cinerea, A. niger, and P. debaryanum were the most tolerant, and H. sativum, P. betae, and V. albo-atrum were the most sensitive at concentrations ranging from 0.063 mg/mL to 0.25 mg/mL. H. sativum and P. betae were inhibited by ToA1, ToA2, and ToA3, but F. oxysporum and V. albo-atrum were only inhibited by ToA2 and ToA3, respectively. In potato tubers, P. infestans was inhibited by ToA3 at 0.06 mg/mL at 96 and 120 h, but at 144 h ToA2 inhibited better at 0.13 mg/mL [23]. Interestingly, an antimicrobial filtrate isolated from the fungal strains of P. betae (PG23) from T. mongolicum was proven active against E. coli, S. aureus, A. hydrophila, E. tarda, and P. multocida, and proposed as a potential antimicrobial product for poultry and aquatic disease control [88].

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3. Driving forces and tendencies in Taraxacum antimicrobial research

Between 2000 and 2010, approximately 40 new drugs originating from terrestrial plants, terrestrial microorganisms, marine organisms, and terrestrial vertebrates and invertebrates against different bacteria, fungi, and viruses were launched on the market [90]. This follows distinct research tendencies. Studies related to antimicrobial and antifungal properties generally aim, in developing and developed countries, to respond to the necessity of finding new drugs or products based on traditional medicine at a low cost, confirming already established activity originating from oral tradition. The driving force behind studying new antimicrobial alternatives is the necessity of finding new drugs or natural products that act against diseases due to the increased drug resistance in the latter. Furthermore, the toxicity of synthetic compounds currently utilized in farming and agricultural industries has created a market for natural compounds that are safer, cheaper, and more effective against pathogens.

Modern phytochemistry, scientific equipment, and technology have had a significant impact on natural product chemistry, including isolation, extraction, purification, and structure determination. However, this discipline still demands that research investigators establish the clinical significance of natural compounds and recognize them as drugs or industrial products (pesticides, bactericides, pharmaceutical products, etc.) [91]. Bioactive compounds in botanical drugs are purportedly superior to monosubstances because of synergistic effects. Similarly, multidrug therapy is highly important against resistant microbial strains due to the enhanced efficacy, reduced toxicity, decreased adverse side effects, increased bioavailability, lowered dosage, and reduced evolution of antimicrobial resistance [92].

Even when antibiotics have been effective in treating infectious diseases, resistance to the action mechanisms has led to the emergence of new and the re-emergence of old infectious diseases. Several plant extracts exhibit synergistic activity against microorganisms, with natural products (including flavonoids and essential oils) and synthetic drugs effectively combating bacterial, fungal, and mycobacterial infections. The mode of action of combinations differs significantly from the individual use of the same drugs; hence, isolating a single component may not highlight its importance, simplifying the task of the pharmacological industries [93].

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Acknowledgments

This work has been supported by Innova Chile CORFO Code FCR-CSB 09CEII-6991 and a doctoral fellowship awarded by the Pontifical Catholic University of Valparaíso, Chile Project DI Iniciación COD 039.454/2017 Pontificia Universidad Católica de Valparaíso.

References

  1. 1. Modi C, Modi S, Patel H, Dudhatra G, Kumar A, Awale M. Herbal Antibacterials: A review. Journal Intercultural Ethnopharmacology. 2012;1:52-61. DOI: 10.5455/jice.20120207113423
  2. 2. Mahesh B, Satish S. Antimicrobial activity of some important medicinal plant against plant and human pathogens. World Journal Agricola Science. 2008;4:839-843. DOI: 10.1556/EuJMI.3.2013.4.6
  3. 3. Vashegyi I, Marozsán-Tóth Z, Galiba G, Dobrev P, Vankova R, Tóth B. Cold response of dedifferentiated barley cells at the gene expression, hormone composition, and freezing tolerance levels: Studies on callus cultures. Molecular Biotechnology. 2013;54:337-349. DOI: 10.1007/s12033-012-9569-9
  4. 4. Stewart-Wade S, Neumann S, Collins L, Boland G. The biology of Canadian weeds. 117. Taraxacum officinale G.H. Weber ex Wiggers. Canadian Journal Plant Science. 2002;82:825-853. DOI: org/10.4141/P01-010
  5. 5. Lardos A. The botanical materia medica of the Iatrosophikon – A collection of prescriptions from a monastery in Cyprus. Journal of Ethnopharmacology. 2006;104:387-406. DOI: 10.1016/j.jep.2005.12.035
  6. 6. González-Castejón M, Visioli F, Rodríguez-Casado A. Diverse biological activities of dandelion. Nutrition Reviews. 2012;70:534-547. DOI: 10.1111/j.1753-4887.2012.00509.x
  7. 7. Schütz K, Carle R, Schieber A. Taraxacum – A review on its phytochemical and pharmacological profile. Journal of Ethnopharmacology. 2006;107:313-323. DOI: 10.1016/j.jep.2006.07.021
  8. 8. Li G.Pharmacology, toxicity and clinic of traditional Chinese medicine. In: Tianjin Science and Technique. Tianjin, China: Translation Publishing House; 1992. pp. 207-208
  9. 9. Ou M, Li YW. The Traditional Chinese Drug and Its Usage. Hong Kong, China: Hai Feng Press; 1994. pp. 49-51
  10. 10. Zhu M, Wong P, Li R. Effects of Taraxacum mongolicum on the bioavailability and disposition of ciprofloxacin in rats. Journal of Pharmaceutical Sciences. 1999;88:632-634. DOI: 10.1021/js980367q
  11. 11. Caraballo A, Caraballo B, Rodríguez-Acosta A. Preliminary assessment of medicinal plants used as antimalarials, in the southeastern Venezuelan Amazon. Revista da Sociedade Brasileira de Medicina Tropical. 2004;37:186-188. DOI: 10.1590/S0037-86822004000200016
  12. 12. Guarino C, De Simone L, Santoro S. Ethnobotanical study of the Sannio area, Campania, Southern Italy. Ethnobotany Research and Applications. 2008;6:255-317. DOI: 10.17348/era.6.0.255-317
  13. 13. Saghir I, Awan A, Majid S, Khan M, Qureshi S, Bano S. Ethnobotanical studies of Chikar and its allied areas of district Muzaffarabad. Journal of Biological Sciences. 2001;1:1165-1170
  14. 14. Guarrera P, Savo V. Perceived health properties of wild and cultivated food plants in local and popular traditions of Italy: A review. Journal of Ethnopharmacology. 2013;146:659-680. DOI: 10.1016/j.jep.2013.01.036
  15. 15. Neves J, Matos C, Moutinho C, Queiroz G, Gomes L. Ethnopharmacological notes about ancient uses of medicinal plants in Trás-os-Montes (northern of Portugal). Journal of Ethnopharmacology. 2009;124:270-283. DOI: 10.1016/j.jep.2009.04.041
  16. 16. Rodriguez-Fragoso L, Reyes-Esparza J, Burchiel S, Herrera-Ruiz D, Torres E. Risks and benefits of commonly used herbal medicines in Mexico. Toxicology and Applied Pharmacology. 2008;227:125-135. DOI: 10.1016/j.taap.2007.10.005
  17. 17. Song M, Kim H. Ethnomedicinal application of plants in the western plain region of North Jeolla Province in Korea. Journal of Ethnopharmacology. 2011;137:167-175. DOI: 10.1016/j.jep.2011.05.001
  18. 18. Martinez M, Poirrier P, Chamy R, Prüfer D, Schulze-Gronover C, Jorquera L, Ruiz G. Taraxacum officinale and related species – An ethnopharmacological review and its potential as a commercial medicinal plant. Journal of Ethnopharmacology. 2015;169:244-262. DOI: 10.1016/j.jep.2015.03.067
  19. 19. Wat C, Johns T, Towers G. Phototoxic and antibiotic activities of plants of the Asteraceae used in folk medicine. Journal of Ethnopharmacology. 1980;2:279-290. DOI: 10.1016/S0378-8741(80)81006-3
  20. 20. Izzo A, Di Carlo G, Biscardi D, De Fusco R, Mascolo N, Borrelli F, Capasso F, Fasulo M, Autore G. Biological screening of Italian medicinal plants for antibacterial activity. Phythotherapy Research. 1995;9:281-286. DOI: 10.1002/ptr.2650090410
  21. 21. Silva N, Fernandes A. Biological properties of medicinal plants: A review of their antimicrobial activity. Journal of Venomous Animals and Toxins including Tropical Diseases. 2010;16:402-413. DOI: 10.1590/S1678-91992010000300006
  22. 22. Ghaima K, Hashim N, Ali S. Antibacterial and antioxidant activities of ethyl acetate extract of nettle (Urtica dioica) and dandelion (Taraxacum officinale). Journal of Applied Pharmaceutical Science. 2013;3:96-99. DOI: 10.7324/JAPS.2013.3518
  23. 23. Odintsova T, Rogozhin E, Sklyar I, Musolyamov A, Kudryavtsev A, Pukhalsky V, Smirnov A, Grishin E, Egorov T. Antifungal activity of storage 2S albumins from seeds of the invasive weed dandelion Taraxacum officinale Wigg. Protein and Peptide Letters. 2010;17:522-529. DOI: 10.2174/092986610790963591
  24. 24. Stanojković A, Ceković J, Čomić L, Pivić R, Stanojković A. Antibacterial properties of some plants from the family Asteraceae growing wild in Serbia. Lekovite sirovine. 2008;26/27:11-20
  25. 25. Jaca T, Kambizi L. Antibacterial properties of some wild leafy vegetables of the Eastern Cape Province, South Africa. Journal of Medicinal Plants.2011;5:2624-2628.DOI: http://www.academicjournals.org/journal/JMPR/article-abstract/3CA6E7916006
  26. 26. Ikeura H, Somsak N, Kobayashi F, Kanlayanarat S, Hayata Y. Application of selected plant extracts to inhibit growth of Penicillium expansum on apple fruits. Plant Pathology Journal. 2011;10:79-84. DOI: 10.3923/ppj.2011.79.84
  27. 27. Ragasa C, Apuada M, Rideout J. Terpenoids from Taraxacum officinale. NRCP Research Journal. 2009;10:17-26
  28. 28. Im D, Lee K. Antioxidative and antibacterial activity and Tyrosinase inhibitory activity of the extract and fractions from Taraxacum coreanum Nakai. Korean Journal of Medicinal Crop Science. 2011;19:238-245. DOI: 10.7783/KJMCS.2011.19.4.238
  29. 29. Qiao H, Sun T. Antibacterial activity of ethanol extract and fractions obtained from Taraxacum mongolicum flower. Research Journal of Pharmacognosy. 2014;1:35-39. Available from: http://rjpharmacognosy.ir/article_6336_609.html
  30. 30. Zaki A, Shaaban M, Hashish N, Amer M, Lahloub M. Assessment of anti-quorum sensing activity for some ornamental and medicinal plants native to Egypt. Scientia Pharmaceutics. 2013;81:251-258. DOI: 10.3797/scipharm.1204-26
  31. 31. Han S, Hwang J, Park S, Lee K, Ko K, Kim K, Kim K. Potential effect of solvent fractions of Taraxacum mongolicum H. on protection of gastric mucosa. Korean Journal of Medicinal Crop Science. 2005;37:84-89
  32. 32. Sun H, Li Z, Liu W, Wang X, Zhang T, Feng Z. In vitro antibacterial activities of antibiotics and traditional chinese medicinal herb extracts on Escherichia coli and Staphylococcus aureus. Asian Journal of Chemistry. 2014;26:298-302. DOI: 10.14233/ajchem.2014.16174
  33. 33. Kenny O, Brunton N, Walsh D, Hewage C, Mcloughlin P, Smyth T. Characterisation of antimicrobial extracts from dandelion root (Taraxacum officinale) using LC-SPE-NMR. Phytotherapy Research. 2015;29:526-532. DOI: 10.1002/ptr.5276
  34. 34. Tettey C, Ocloo A, Nagajyothi P, Lee K. An in vitro analysis of antiproliferative and antimicrobial activities of solvent fractions of Taraxacum officinale (dandelion) leaf. Journal of Applied Pharmaceutical Science. 2014;4:41-45. DOI: 10.7324/JAPS.2014.40309
  35. 35. Gatto M, Ippolito A, Linsalata V, Cascarano N, Nigro F, Vanadia S, Di Venere D. Activity of extracts from wild edible herbs against postharvest fungal diseases of fruit and vegetables. Postharvest Biology and Technology. 2011;61:72-82. DOI: 10.1016/j.postharvbio.2011.02.005
  36. 36. Fabri R, Nogueira M, Dutra L, Bouzada M, Scio E. Potencial antioxidante e antimicrobiano de espécies da família Asteraceae. Revista Brasileira de Plantas Medicinais. 2011;13:183-189. DOI: 10.1590/S1516-05722011000200009
  37. 37. Khan A, Qureshi R, Gillani S, Ullah F. Antimicrobial activity of selected medicinal plants of Margalla Hills, Islamabad, Pakistan. Journal of Medicinal Plants Research. 2011;5:4665-4670
  38. 38. Kim K, Chun H, Han Y. Screening of antimicrobial activity of the dandelion (Taraxacum platycarpum) extract. Korean Society of Food Science and Nutrition. 1998;14:114-118
  39. 39. Kim K, Min K, Lee S, Han Y. Isolation and identification of antimicrobial compound from dandelion (Taraxacum platycarpum D.). Journal of the Korean Society of Food Science and Nutrition. 1999;28:822-829
  40. 40. Park J, Jang J, Lee M, Park E. Effect of dandelion (Taraxacum officinale) extracts on the intestinal microorganisms of streptozotocin-induced diabetic rats. Journal of the Korean Society of Food Science and Nutrition. 2002;31:1112-1118. DOI: 10.3746/jkfn.2002.31.6.1112
  41. 41. Sohail Z, Afzal M, Afzal A, Rahman I, Shad S, Ahmed B, Anjum N, Qureshi K, Bibi A. In vitro antibacterial study of Taraxacum officinale leaves extracts against different bacterial pathogenic strains. Journal of Pharmacognosy and Phytochemistry. 2014;3:15-17
  42. 42. Inagaki H, Yamaguchi A, Kato K, Kageyama C, Iyozumi H, Oki Y. Screening of weed extracts for antifungal properties against Colletotrichum lagenarium, the causal agent of anthracnose in cucumber. Weed Biology and Management. 2008;8:276-283. DOI: 10.1111/j.1445-6664.2008.00308.x
  43. 43. Jassim A, Farhan S, Noori O. Identification of dandelion Taraxacum officinale leaves components and study its extracts effect on different microorganisms. Journal of Al-Nahrain University – Science. 2012;15:7-14
  44. 44. Kenny O, Smyth T, Walsh D, Kelleher C, Hewage C, Brunton N. Investigating the potential of under-utilised plants from the Asteraceae Family as a source of natural antimicrobial and antioxidant extracts. Food Chemistry. 2014;161:79-86. DOI: 10.1016/j.foodchem.2014.03.126
  45. 45. Lateef O, Issah Y. Screening ethanolic and aqueous leaf extracts of Taraxacum offinale for in vitro bacteria growth inhibition. Journal of Pharmaceutical and Biomedical Sciences. 2012;20:06
  46. 46. Parveen S, Wani A, Ganie A, Pala S, Mir R. Antifungal activity of some plant extracts on some pathogenic fungi. Archives of Phytopathology and Plant Protection. 2013;47:279-284. DOI: 10.1080/03235408.2013.808857
  47. 47. Peng S, Dai W, Yu H, Wang Y, Wang X, Sun S. Antibacterial activity of aqueous and ethanolic extracts of Portulaca oleracea L and Taraxacum mongolicum against pathogenic bacteria of cow mastitis. International Journal of Applied Research in Veterinary Medicine. 2014;12:210-213. DOI: 10.18805/ijar.5960
  48. 48. Qian Z, Jiang L. Preparation and antibacterial activity of the oligosaccharides derived from Rhizoma phragmites. Carbohydrate Polymers. 2014;111:356-358. DOI: 10.1016/j.carbpol.2014.04.043
  49. 49. Chan G, Kim H. Antimicrobial effects of extracts of Taraxacum officinale H. on acnes strains. 국제통합보완대체의학회지 [International Journal of Integrated CAM]. 2011;7:3-16. DOI: 10.4172/1948-5948.1000287
  50. 50. Redzic S, Kurtagic H, Prazina N, Tuka M, Avdagic T. The antimicrobial activity of honey in relation to the composition of pollen (Bosnia-Herzegovina, W. Balkan). Planta Medicinal. 2011;77:SL62. DOI: 10.1055/s-0031-1282185
  51. 51. Sarer E, Sahin A, Gökbulut A. The investigation on the terpenoids and flavonoids of an endemic Taraxacum species from Turkey. Planta Medicinal. 2010;76:P303. DOI: 10.1055/s-0030-1264601
  52. 52. Sharma V, Sharma H, Mehta D, Chhabra B, Thakur D, Sourirajan A, Dev K. Comparative analysis of antibacterial and antifungal properties of traditional medicinal plants of Shimla and Solan, Himachal Pradesh. International Journal of Pharmacy and Pharmaceutical Research. 2014;6:18-26. DOI: 10.1016/j.jtcme.2017.04.002
  53. 53. Shafiq N, Al-Hashimi M. The antibacterial evaluation of dandelion extracts as root canal irrigating solutions (A comparative study). Journal of Bagdhdad College of Dentistry. 2014;26:35-40
  54. 54. Cwikla C, Schmidt K, Matthias A, Bone K, Lehmann R, Tiralongo E. Investigations into the antibacterial activities of phytotherapeutics against Helicobacter pylori and Campylobacter jejuni. Phytotherapy Research. 2010;24:649-656. DOI: 10.1002/ptr.2933
  55. 55. Kim J, Yi Y, Lim Y. Biological and antifungal activity of herbal plant extracts against Candida species. Korean Journal of Microbiology and Biotechnology. 2009;37:42-48
  56. 56. Bahraminejad S, Abbasid S, Fazlali M. In vitro antifungal activity of 63 Iranian plant species against three different plant pathogenic fungi. African Journal of Biotechnology. 2011;10:16193-16201. DOI: 10.5897/AJB11.1203
  57. 57. Borchardt J, Wyse D, Sheaffer C, Kauppi K, Fulcher R, Ehlke N, Biesboer D, Bey R. Antimicrobial activity of native and naturalized plants of Minnesota and Wisconsin. Journal of Medicinal Plants Research. 2008;2:98-110
  58. 58. Ionescu D, Mihele D, Predan G, Rizea G, Dune A, Ivopol G. Antimicrobial activity of some hydroalcoholic extracts of artichoke (Cynara scolymus), burdock (Arctium lappa) and dandelion (Taraxacum officinale). Agricultural Food Engineering. 2013;6:113-120 Available from: http://webbut.unitbv.ro/Bulletin/Seri
  59. 59. Bensch K, Tiralongo J, Schmidt K, Matthias A, Bone KM, Lehmann R, Tiralongo E. Investigations into the antiadhesive activity of herbal extracts against Campylobacter jejuni. Phytotherapy Research. 2011;25:1125-1132. DOI: 10.1002/ptr.3384
  60. 60. Tosun F, Vural M, Palittapongarnpim P. Antimycobacterial screening of some Turkish plants. Journal of Ethnopharmacology. 2004;95:273-275. DOI: 10.1016/j.jep.2004.07.011
  61. 61. Caruana S, Yoon G, Freeman M, Mackie J, Shinn A. The efficacy of selected plant extracts and bioflavonoids in controlling infections of Saprolegnia australis (Saprolegniales; Oomycetes). Aquaculture..2012;358–359:146-154. DOI: 10.1016/j.aquaculture.2012.06.035
  62. 62. López-García J, Kuceková Z, Humpolícek P, Mlcek J, Sáha P, Humpolíček P, Mlček J, Sáha P. Polyphenolic extracts of edible flowers incorporated onto atelocollagen matrices and their effect on cell viability. Molecules. 2013;18:13435-13445. DOI: 10.3390/molecules181113435
  63. 63. Newton S, Lau C, Gurcha S, Besra G, Wright C. The evaluation of forty-three plant species for in vitro antimycobacterial activities; isolation of active constituents from Psoralea corylifolia and Sanguinaria canadensis. Journal of Ethnopharmacology. 2002;79:57-67. DOI: 10.1016/S0378-8741(01)00350-6
  64. 64. Liu Y, Nielsen M, Staerk D, Jäger A. High-resolution bacterial growth inhibition profiling combined with HPLC-HRMS-SPE-NMR for identification of antibacterial constituents in Chinese plants used to treat snakebites. Journal of Ethnopharmacology. 2014;155:1276-1283. DOI: 10.1016/j.jep.2014.07.019
  65. 65. Tolmacheva A, Rogozhin E, Deryabin D. Antibacterial and quorum sensing regulatory activities of some traditional Eastern-European medicinal plants. Acta Pharmaceutica. 2014;64:173-186. DOI: 10.2478/acph-2014-0019
  66. 66. Woods-Panzaru S, Nelson D, McCollum G, Ballard L, Millar B, Maeda Y, Goldsmith C, Rooney P, Loughrey A, Rao J, Moore J. An examination of antibacterial and antifungal properties of constituents described in traditional Ulster cures and remedies. Ulster Medical Journal. 2009;78:13-15. PMCID: PMC2629014
  67. 67. The Plant List. Version 1.1. Published on the Internet. Available from: http://www.theplantlist.org/ [Accessed: May 2015]
  68. 68. Astafieva A, Rogozhin E, Andreev Y, Odintsova T, Kozlov S, Grishin E, Egorov T. A novel cysteine-rich antifungal peptide ToAMP4 from Taraxacum officinale Wigg. flowers. Plant Physiology and Biochemistry. 2013;70:93-99. DOI: 10.1016/j.plaphy.2013.05.022
  69. 69. Astafieva A, Rogozhin E, Odintsova T, Khadeeva N, Grishin E, Egorov T. Discovery of novel antimicrobial peptides with unusual cysteine motifs in dandelion Taraxacum officinale Wigg. flowers. Peptides. 2012;36:266-271. DOI: 10.1016/j.peptides.2012.05.009
  70. 70. Gao D. Analysis of nutritional components of Taraxacum mongolicum and its antibacterial activity. Pharmacognosy Journal. 2010;2:502-505. DOI: 10.1016/S0975-3575(10)80039-2
  71. 71. Hanawa F, Kanauchi M, Tahara S, Mizutani J. Lettucenin A as a phytoalexin of dandelion and its elicitation in dandelion cell cultures. Journal of the Faculty of Agriculture, Hokkaido University. 1995;66:151-162
  72. 72. Voss-Rech D, Klein C, Techio V, Scheuermann G, Rech G, Fiorentin L. Antibacterial activity of vegetal extracts against serovars of Salmonella. Ciência Rural, Santa Maria. 2011;41:314-320. DOI: 10.1590/S0103-84782011000200022
  73. 73. Al-kalby J, Alwan N. Effects of ethanolic extract of Taraxacum officinale leaves on some physiological and reproductive parameters of local adult male rabbits.Basrah Journal of Veterinary Research. 2007;6:42-55
  74. 74. Elkhalfi B, Essari A, Serrano A, Soukri A. Antibacterial activity of plant methanolic extracts on a field isolate of Pseudomonas syringae pv tomato from the Casablanca region (Morocco). Advancesin Bioscience of Biotechnology. 2013;4:1-9. DOI: 10.4236/abb.2013.47A2001
  75. 75. Chen Z. Clinical study of 96 cases with chronic hepatitis B treated with jiedu yanggan gao by a double-blind method. Zhong Xi Yi Jie He Za Zhi. 1990;10:71-74
  76. 76. Wang H. Effect of dandelion polysaccharides on the retardation of the quality changes of white shrimp. International Journal of Biological Macromolecules. 2014;68:205-208. DOI: 10.1016/j.ijbiomac.2014.05.002
  77. 77. Urbanczyk J, Hanczakowska E, Swiatkiewicz M. Herb mixture as an antibiotic substitute in pig feeding. Medycyna Weterynaryjna. 2002;58:887-889
  78. 78. Yan L, Meng QW, Kim IM. The effects of dietary Houttuynia cordata and Taraxacum officinale extract powder on growth performance, nutrient digestibility, blood characteristics and meat quality in finishing pigs. Livestock Science. 2011;141:188-193. DOI: 10.1016/j.livsci.2011.05.017
  79. 79. Yang L, Lü J, Feng Y. Partition and extraction of total flavonoids from Taraxacum mongolicum in PEG/(NH4)2SO4 aqueous two-phase system. Chemical Industry and Engineering Progress. 2014;33:1992-1996
  80. 80. González-Lamothe R, Mitchell G, Gattuso M, Diarra M, Malouin F, Bouarab K. Plant antimicrobial agents and their effects on plant and human pathogens. International Journal Molecular of Science. 2009;10:3400-3419. DOI: 10.3390/ijms10083400
  81. 81. Cowan M. Plant products as antimicrobial agents. Clinical Microbiology Reviews. 1999;12:564-582. PMCID: PMC88925
  82. 82. Singh S, Barrett J. Empirical antibacterial drμg discovery – Foundation in natural products. Biochemical Pharmacology. 2006;71:1006-1015. DOI: 10.1016/j.bcp.2005.12.016
  83. 83. Burt S. Essential oils: Their antibacterial properties and potential applications in foods – A review. International Journal of Food Microbiology. 2004;94:223-253. DOI: 10.1016/j.ijfoodmicro.2004.03.022
  84. 84. Mulvey M, Simor A. Antimicrobial resistance in hospitals: How concerned should we be? Canadian Medical Association Journal. 2009;180:408-415. DOI: 10.1503/cmaj.080239
  85. 85. Chadwick M, Trewin H, Gawthrop F, Wagstaff C. Sesquiterpenoids lactones: Benefits to plants and people. International Journal of Molecular Science. 2013;14:12780-12805. DOI: 10.3390/ijms140612780
  86. 86. Mir M, Sawhney S, Jassal M. Qualitative and quantitative analysis of phytochemicals of Taraxacum officinale Wucpecker. Journal of Pharmacy and Pharmacology. 2013;2:1-5
  87. 87. Khan A, Qureshi R, Ullah F, Gilani S, Nosheen A, Sahreen S, Laghari M, Laghari M, Hussain I, Murad W. Phytochemical analysis of selected medicinal plants of Margalla Hills and surroundings. Journal of Medicinal Plants Research. 2011;5:6017-6023. DOI: 10.5897/JMPR11.869
  88. 88. Zhang H, Xiong Y, Zhao H, Yi Y, Zhang C, Yu C, Xu C. An antimicrobial compound from the endophytic fungus Phoma sp. isolated from the medicinal plant Taraxacum mongolicum. Journal of the Taiwan Institute of Chemical Engineers. 2013;44:177-181. DOI: 10.1016/j.jtice.2012.11.013
  89. 89. Barbosa P, Del Sarto R, Silva O, Franco O, Grossi-De-Sa M. Antibacterial peptides from plants: What they are and how they probably work. Biochemistry Research International. 2011. 9 pp. Article ID: 250349. DOI: 10.1155/2011/250349
  90. 90. Brahmachari G. Natural products in drμg discovery: Impacts and opportunities – An assessment. Bioactive Natural Products: Opportunities and Challenges in Medicinal Chemistry. 2012;1:1-199
  91. 91. Mahmood Z, Mahmood S. Antibiotic natural products: Opportunities and challanges. In: Microbial Pathogens and Strategies for Combating Them: Science, Technology and Education. Formatex Research Center. 2013;2:823-833
  92. 92. Radulović N, Blagojević P, Stojanović-Radić Z, Stojanović N. Antimicrobial plant metabolites: Structural diversity and mechanism of action. Current Medicinal Chemistry. 2013;20:932-952. DOI: 10.2174/092986713805219136
  93. 93. Hemaiswarya S, Kruthiventi A, Doble M. Synergism between natural products and antibiotics against infectious diseases. Phytomedicine. 2008;15:639-652. DOI: 10.1016/j.phymed.2008.06.008

Written By

María Eugenia Martínez Valenzuela, Katy Díaz Peralta, Lorena Jorquera Martínez and Rolando Chamy Maggi

Submitted: 14 June 2017 Reviewed: 11 October 2017 Published: 05 November 2018

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