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332 CHAPTER 16 Zanthoxylum armatum
https://t.me/med1917
FIGURE 16.2
(a) T. S. leaf of Zanthoxylum armatum. (b) T. S. leaf midrib of Zanthoxylum armatum. T.S.,
transverse section.
From Ullah, B., Ibar, M., Ghulam, J., Ahmad, I., 2014. Leaf, stem bark and fruit anatomy of Zanthoxylum
armatum (Rutaceae). Pakistan J. Bot. 46 (4), 1343e1349.
FIGURE 16.3
(a) Adaxial surface of Zanthoxylum armatum. (b) Abaxial surface Zanthoxylum armatum.
From Ullah, B., Ibar, M., Muhammad, N., Khan, A., Khan, S.A., Zafar, S., Jan, S., Riaz, N., Ullah, Z., Farooq, U.,
Hussain, J., 2017. Pharmacognostic and phytochemical studies of Zanthoxylum armatum DC. Pakistan J.
Pharm. Sci. 30 (2), 429e438.
16.4 Biochemical analysis 333
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FIGURE 16.4
(a)T.S.ofbarkofZanthoxylum armatum. (b) T. S. of fruit of Zanthoxylum armatum.(c)T.S.
of fruit wall of Zanthoxylum armatum.
From Ullah, B., Ibar, M., Ghulam, J., Ahmad, I., 2014. Leaf, stem bark and fruit anatomy of Zanthoxylum
armatum (Rutaceae). Pakistan J. Bot. 46 (4), 1343e1349.
16.4.1.1 Leaf
In Z. armatum (leaf) carbohydrates, alkaloids, flavonoids, glycosides, sterols, terpenoids, tannins, and saponins were reported (Upreti et al., 2013; Dabral et al., 2019;
Khan et al., 2020). Ranawat et al. (2010) reported that isoquinoline alkaloid,
berberine, and flavonoids as well as phenolic compounds were found in the ethanol
extract of Z. armatum.
16.4.1.2 Fruit and seed
High-performance liquid chromatography (HPLC) was used to assess the identity of
phytoconstituents in the aqueous extract of whole fruit (fruit with seeds) of
Z. armatum. The major constituents were identified as phenolic acids, some flavonoid aglycones, and glycosides in Z. armatum fruit extract (Sabir et al., 2017). In
an ethanol extract of Z. armatum seeds, terpenoids, saponins, steroids, flavonoids,
alkaloids, phenols, volatile oils, amino acids, and fatty acids were found (Boggula
et al., 2018).
16.4.1.3 Stem and bark
In Z. armatum (bark), the existence of compounds such as saponins, tannins, sterols,
terpenes, flavonoids, coumarins, lignins, alkaloids, glycosides, carbohydrates, phenols, fixed oils, and fats was reported (Ranawat et al., 2013; Jothi et al., 2019). A
new amide was identified as armatamide, alon g with two lignans, asarinin and fargesin; others were isolated from the bark of Z. armatum (e.g., amyrins, lupeol, and
sitosterol
and 4
Z. armatum. All three lignans were found to have cytotoxic/anticancer activity
against A540 and MIA-PaCa cell lines. Among the three lignans, 4
D-glucoside) (Kalia et al., 1999).
Mukhija et al. (2014) reported three prominent lignans (e.g., sesamin, kobusin,
0
-O-dimethyl magnolin [novel]) in a petroleum-ether extract of stem-bark of
0
-O-dimethyl
334 CHAPTER 16 Zanthoxylum armatum
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Table 16.3 Microscopic features of Zanthoxylum armatum leaf.
Leaf anatomy (Fig. 16.2a)
Characteristics Observation
Upper epidermis Nonstomatiferous, thin cuticle, compactly arranged
Palisade mesophyll Single-layered, cylindrically shaped, compactly
Spongy mesophyll Rounded to somewhat elongated, loosely arranged with
Lower epidermis Stomatiferous, rectangular, elongated, or irregularly
Vascular tissues Present
Leaf midrib anatomy (Figs. 16.2b, 16.3a and b)
Adaxial surface Planoconvex
Abaxial surface Semicircular
Upper epidermis Single layered, cuticle, oval to rectangular shaped cells
Hypodermis Thick-walled collenchymatous cells.
Cortex Round, thin-walled parenchymatous cells,
Vascular tissues:
Surrounded by
iodioblast cells
containing Caoxalate crystals
Lower epidermis Rectangular cells
Leaf surface characters
Palisade Compact, elongated, and large cells
Vein islets Prominent distinct, wide, squarish, elongated,
Vein termination Arboreous
Types of stomata Anomocytic, actinocytic, actinostephanocytic,
Bark anatomy (Fig. 16.4a)
Cork (outer phellem) Few layers of brown color, lignified thick-walled,
Cork cambium (middle
phellogen)
Cortex (phelloderm) Compound and simple globular, ovoid starch grains,
xylem Arc-shaped in which xylem was in adaxial position,
phloem Arc shaped in which phloem was in abaxial position,
rectangular shaped cells
arranged cells
large intercellular spaces, schizogenous and
lysischizogenous cells
shaped cells
schizogenous oil cavities
appeared in radial rows
rounded cells
polyhedral, thick boundaries, forked and unforked
vascular branches and randomly oriented
staurocytic, laterocyclocytic, brachyparacytic,
brachyparatetracytic, hemiparacytic, and stomatal
cluster
rectangular, or squared cells
Continuous layer of small, elongated, rectangular, thin-
walled parenchymatous cells
closely packed large parenchymatous cells, iodioblast
cells
16.4 Biochemical analysis 335
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Table 16.3 Microscopic features of Zanthoxylum armatum leaf.dcont’d
Medullary rays It was passing through the phloem
Phloem Consist of intact and crushed phloem elements
Bast fibers Present
Tracheids Present
Fruit anatomy (Fig. 16.4b and c)
Fruit
Epicarp Outermost layer, closely arranged thick-walled
wall
Mesocarp Middle layer, irregular thin-walled parenchymatous cells,
Endocarp Outer
layer
Inner
layer
Seed Oval shaped, outer pigmented layer of testa followed by
From Alam, F., Us Saqib, Q.N., 2015. Pharmacognostic study and development of quality control parameters for fruit, bark and leaves of Zanthoxylum armatum (Rutaceae). Ancient Sci. Life 34 (3), 147
e155. Ullah, B., Ibar, M., Ghulam, J., Ahmad, I., 2014. Leaf, stem bark and fruit anatomy of Zanthoxylum
armatum (Rutaceae). Pakistan J. Bot. 46 (4), 1343e1349. Ullah, B., Ibar, M., Muhammad, N., Khan, A.,
Khan, S.A., Zafar, S., Jan, S., Riaz, N., Ullah, Z., Farooq, U., Hussain, J., 2017. Pharmacognostic and
phytochemical studies of Zanthoxylum armatum DC. Pakistan J. Pharm. Sci. 30 (2), 429e438.
rectangular cells
large schizogenous, lysoschizogenous oil cavities
Small isodiametric or rectangular, thin-walled
parenchymatous cells
Larger, thin-walled rectangular cells
a layer of thin-walled small cells, nonendospermic and
small elongated embryo
magnolin was found to have strong cytotoxic activity. An ethyl acetate fraction of
Z. armatum stem-bark was used for phytochemical and cytotoxic studies. Two
pure flavonoids (apigenin and kaempferol-7-O-glucoside) were isolated from column chromatography of an ethyl acetate extract of Z. armatum. Apigenin and
kaempferol isolated from other plants were shown to have anticancer activity (Muh-
kija et al.,2015). Flavonoids were reported to inhibit cell growth and proliferation
(Adhami et al., 2007) and induce cell toxicity in cancer cells.
HPLC was employed on an ethyl acetate fraction of Z. armatum (stem and roots).
The researchers reported eight lignans (eudesmin, horsfieldin, fargesin, kobusin, sesamin, asarinin, planispine, and pinoresinol-di-3,3-dimethylallyl) in Z. armatum.
These lignan constituents showed antiinflammatory properties (Guo et al., 2011).
Two new phenolic glycosides were isolated from the stem of Z. armatum (e.g., 2methoxy-4-hydroxylphenyl-1-O-a-
L-rhamnopyranosyl-[1
side and threo-3-methoxy-5-hydroxy-phenylpropanetriol-8-O-b-
00/600
]-b-D-glucopyrano-
D-glucophyano-
side) (Guo et al., 2017a). A new lignan, (7S,8R)-guaiacylglycerol-ferulic acid
ether-7-O-b-
D-glucopyranoside, along with 12 known compounds (i.e., five known
phenylpropanoids (2e6) and seven phenylpropanoid glycosides (7 e 13), were isolated from the stems of Z. armatum, which were analyzed by UV-nuclear magnetic
resonance spectrophotometry (Guo et al., 2017b).
336 CHAPTER 16 Zanthoxylum armatum
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16.4.2 Quantitative studies
16.4.2.1 Leaf
Phytochemicals (e.g., sterols, tannins, saponins, alkaloids, flavonoids, and phenols)
from Z. armatum leaves were investigated quantitatively (Ullah et al., 2013a,b,
2017). Essential oil obtained from Z. armatum (syn. Z. alatum) leaves was analyzed
by GC-MS spectroscopy. The major components identified were bornyl acetate
(Negi et al., 2012) and linalool (Ullah et al., 2013b; Guleria et al., 2013). It was
revealed that the presence of linalool, 2-undecanone, and b-phellandrene were the
major compound not previously found for Z. armatum leaves (Bhatt et al., 2017;
Singh et al., 2019). The three major components, linalool, limonene, and unde-
can-2-one, were isolated from the essential oil of Z. armatum leaves (Phuyal
et al., 2019).
Two major compounds (i.e., 2-undecanone and 2-tridecanone) were identified
through GC-MS analysis; an n-hexane extract of Z. armatum leaves showed
maximum larvicidal activity (Kumar et al., 2015). In phytochemical analysis, fargsin
was identified as the major constituent in methanolic and chloroform extracts of
Z. armatum leaves (Singh et al., 2020).
16.4.2.2 Fruit and seed
The highest percentage of major compounds (e.g., 3-borneol, iso-bornyl acetate and
dihydro carveol) was isolated from the essential oil of Z. armatum seeds and identified through GC-MS (Waheed et al., 2011). A total of 36 compounds were identified through GC-MS; few of them were reported to be major constituent (i.e., 2hydroxy cyclopentadecanone followed by palmitic acid and piperitone) (Kayat
et al., 2016). Two new compounds were identified by column chromatography
and isolated from the methanolic extract of Z. armatum fruits and characterized
as 2a-methyl-2b-ethylene-3b-isopropyl-cyclohexan-1b,3a-diol and phenol-O-b-
D-arabinopyranosyl-4
et al., 2017). Linalool from Dharchula and Z)-b-ocimene from Pithoragarh were re-
ported to be major compounds isolated from the essential oil of Z. armatum seeds.
They were identified through the combination of GC and GC-MS (Dhami et al.,
2018). Z. alatum fruit was reported to have major phenolic acids, flavonoid agly-
cone, and glycosides, which were analyzed by HPLC; the major compounds were
identified as ellagic acid, chlorogenic acid, gallic acid, chrysin, quercetin, and epicatechin. The observed antioxidant activity and protective ability of Z. alatum
against liver damage results from the phenolic acids (ellagic acid, gallic acid, chlorogenic acid, caffeic acid, and coumaric acid) and flavonoids (chrysin, catechin, epicatechin, rutin, and quercetin) (Sabir et al., 2017). GC-MS analysis of the seed oil
of Z. armatum (Syn. alatum) revealed linalool and limonene to be the main constituents (Jain et al., 2001; Tiwary et al., 2007; Kwon et al., 2011). Singh et al. (2016)
performed a proximate quantitative analysis of the total phenolic and flavonoid content of Z. armatum seeds.
0
-(300,700,1100,1500-tetramethyl)-hexadecan-100-oate (Nooreen
16.5 Mineral elemental analysis 337
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16.4.2.3 Stem and bark
Two major compounds were characterized as apigenin and kaempferol-7-O-glucoside, which was isolated from the ethyl acetate extract of Z. alatum stem bark and
identified through column chromatography ( Mukhija et al., 2015). Five major compounds were isolated and identified as (E)-anethole, 1.8-cineole, 2-tridecanone,
limonene and piperitone from the essential oil of Z. armatum twigs through GC
and GC-MS analysis (Wang et al., 2015). The two new major compounds (N-[31,
41-methylenedioxyphenyl ethyl]-3,4-methylenedioxycinnamoyl amide and N[31,41-dimethoxyphenylethyl]-3,4- methylenedioxydihydrocinnamoyl amide),
were isolated from a methanol extract of Z. armatum bark through spectroscopic
techniques (Siddhanadham et al., 2017b). a-Pinene and 2-undecanone were isolated
from the essential oil of Z. armatum bark through GC-MS (Dhami et al.,2019). In a
methanol extract of bark of Z. armatum, t-butylamine was the dominant compound
followed by others such as 1-[(trimethylsilyl) oxy]propan-2-ol, propylene glycol, 2TMS derivative, glycerol, 1-tert-butyl 3-trimethylsilyl ether, doxepin, acetin, bis1,3-trimethylsilyl ether, laudanosine, and 2-methyl-1,2-butanediol 2-TMS, respectively. In a chloroform extract of Z. armatum bark, benzoxazole, 2-(isobutylamino),
was found to be more strongly present than the other constituents (e.g., [Z,Z]-6,9cis-3,4-epoxy-nonadecadiene, [þ]-eudesmin, thujaplicatin, tri-O-methyl, [þ]-sesamine, [(2E)-3,7-dimethyl-2,6-octadienyl-2,6-octadienyl] benzene and 1,3,14,16nonadecatetraene) (Singh et al. 2020).
The secondary metabolites were isolated from Z. armatum bark and the total alkaloids were reported (2.73 0.23 mg/g), as were the total flavonoids (0.05 0.02
QE equivalent), terpenoids (153 3.21 mg/g), saponins (0.13 0.01 mg/g), tannins (0.041 0.01 mg/g), and phenols (25.92 1.36 GAE (gallic acid equivalent))
of their respective concentrations (Jothi et al. 2019).
Two different samples (wild and cultivated type) were isolated from seeds of
Z. armatum for their total phenolic and flavonoid contents. In wild and cultivated
seeds of Z. armatum, the mean total phenolic content value was reported to be
185.15 and 171.13 mg GAE/g weight of the dried extract, whereas the mean total
flavonoid content value was reported to be 91.27 and 111.2 mg QE/g dried weight
of the sample (Phuyal et al. 2020a).
16.5 Mineral elemental analysis
Histochemical analysis showed the presence of lignin, calcium, carbonate, mucilage, resins, starch, fats, fatty oils, and volatile oils in Z. armatum leaf, bark, and
fruit. Cellulose was detected in the bark and fruit of Z. armatum, but not in the
leaf. Aleurones were detected only in the fruit. The presence of hydroxyanthraquinones was reported only in the leaf and fruit of Z. armatum, but not in the bark.
HPLC was used for analytical studies; it showed the presence of rutin and gallic
acid in a leaf and bark extract of Z. armatum ( Alam and Saqib, 2015). Crude protein,
338 CHAPTER 16 Zanthoxylum armatum
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phosphorus, calcium, zinc, and copper were reported in Z. armatum seeds (Singh
et al., 2016). The results of a mineral analysis of leaf of Z. armatum revealed the
presence of calcium, chlorine, potassium, magnesium, silicon, sulfur, phosphorus,
iron, sodium, manganese, strontium, zinc, molybdenum, copper, and nickel of their
respective concentrations in leaf extract (Khan et al. 2020).
16.6 Genomics
Wang et al. (2019) performed the first study on complete chloroplast sequences of
Z. armatum. The results showed that Z. armatum contains a chloroplast DNA
(cpDNA) 158,579 base pairs (bp) long. The cpDNA was found to contain a pair
of inverted repeat regions of 27,598 bp between the large single copy region of
85,780 bp and a small copy region of 17,598 bp. Among 133 genes of genome,
88 were protein-coding, eight were ribosomal RNA genes, and 37 were found to
be transfer RNA genes. The comprehensive guanine-cytosine content of the whole
genome was found 38.5%. Phylogenetic analysis was performed on 18 chloroplast
genomes that were native to the family Rutaceae; Z. armatum was closely related
to Zanthoxylum schinifolium.
Fluorescence in situ hybridization was employed to detect (GAA) six loci and
ribosomal DNA in Z. armatum using oligonucleotide probes. Both (GAA) six loci
and 5S ribosomal DNA were detected on pericentromeric regions of chromosomes,
but the presence of (GAA) six loci was detected in five chromosome pairs, and ribosomal DNA was detected in another two chromosomal pair s. The variation in densities and locations of (GAA) 6 and 5S rDNA signals was observed by means of
individual chromosome. High-intensity (GAA) six signals were detected at the centromeres of two large and two smaller metacentric chromosomes. Strong (GAA) six
signals were found at the centromeres of two relatively small metacentric chromosome, whereas weak (GAA) six signals were detected at the centromeres of four
large metac entric chromosomes. In the case of 5S rDNA, the strong 5S rDNA signals
were detected at the centromere of two other smaller metacentric chromosomes
(exclude the small metacentric chromosomes, which were found in strong [GAA]
six signals), whereas weak 5S rDNA signals were detected at the centromere of
two smaller metacentric chromosomes. No signals were detected in the remaining
chromosomes. The approximate 2n number for Z. armatum was 128. The range
of length of the mitotic metaphase chromosome was recorded as 1.22e2.34 mm
(Luo et al., 2018).
Gupta and Kumar (2014) evaluated Z. armatum for karyotypic studies. A slight
asymmetric 2B type of karyotype in Z. armatum was identified. The somatic chromosome number was 66 in the case of Z. armatum. The arm’s ratio was reported for
about 12% of the whole set of chromosomes was 2:1. The total length and volume of
whole set of chromosome were 28 and 0.079 mm
est chromosome ratio was 2.8. The range of centromeric index was 26e50 and the
variation in total length of chromatin was reported to be 3.43 to 9.86.
3
, respectively. The largest to small-
16.7 Medical significance 339
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This study claim to perform the de novo transcriptome assembly for five major
parts of Z. armatum, including the roots, stems, leaf buds, mature leaves, and fruit.
Comprehensively 111,318 UniGenes were generated from an average length of
1014 bp DNA. GO (gene ontology) and KEGG (Kyoto encyclopedia of genes and
genomes) enrichment analysis of Z. armatum parts was done by means of organspecific UniGenes . A total of 53 and 34 UniGenes found from whole-fruit samples
were recorded as candidate UniGenes in the case of many biological pathways (i.e.,
terpenoid biosynthesis or fatty acid biosynthesis) and their elongation and degradation pathways, respectively. The prominent period for accumulating terpenoid compounds was recorded after 40 days of fertilization (Fr4 stage) of the plant, when the
development and maturation of fruit of Z. armatum were observed. The Fr4 stage
was found to be the initial stage that induced the process of fatty acid biosynthesis;
catalysis of subsequent reactions was reported up to 62 days after fertilization (Fr6
stage) (Hui et al., 2020).
16.7 Medical significance
Z. armatum demonstrated pharmacological and biological activities that showed
highly potent antiinflammatory (Dhami et al., 2019), hepatoprotective (Barua
et al., 2018, 2019; Ullah et al., 2011), cytotoxic (Ullah et al., 2013b; Alam et al.,
2017), antispasmodic (Ullah et al., 2013a, analgesic (Pathakala et al., 2018), antidi-
abetic (Khan et al., 2020), and anthelmintic (Singh et al., 2016)(Table 16.4).
16.7.1 Antimicrobial activity
Different explants (fruit, leave, and bark) of Z. armatum were employed for the
assessment of in vitro antibacterial activity using of agar well diffusion methods
against gram-positive bacteria (Mi crococcus luteus, Bacillus subtilis, Staphylo-
coccus aureus and Streptococcus faecalis) and gram-negative bacteria (Escherichia
coli, Proteus vulgaris, Klebsiella pneumoniae, Streptococcus viridans, Pseudomonas multocida, and Pseudomonas aeruginosa). It was found that an acetone
extract showed a maximum zone of inhibition against S. aureus (42.3 mm), followed
by a methanolic extract against S. aureus (28.7 mm) as gram-positive bacteria,
whereas maximum activity was found in a chloroform extract against P. vulgaris
(28.3 mm) as gram-negative bacteria (Ullah et al., 2013b; Srivastava et al., 2013).
It was concluded that gram-positive bacteria showed more sensitivity to the essential
oil than did gram-negative bacteria. For most bacterial species, minimum inhibitory
concentration values were 0.65 mg/mL (Ullah et al., 2013b). The ethanol is the most
potent extract and had a maximum inhibitory potential at 25% concentration (Dabral
et al., 2019).
In another study, among the different extracts used (e.g., petroleum ether,
acetone, essential oil, n-hexane, chloroform, ethanol, and methanol), the essential
oil of Z. armatum was most effective against various tested gram-positive and
Table 16.4 Pharmacological properties of Zanthoxylum armatum.
https://t.me/med1917
Plant
parts
Antibacterial activity
Fruits Crude ethanolic In vitro Ciprofloxacin Positive Micrococcus
Leaves Essential oil In vitro Ciprofloxacin Positive Streptococcus
Leaves Essential oil In vitro Ciprofloxacin Positive Micrococcus
Leaves Essential oil In vitro Chloramphenicol Positive Bacillus subtilis
Leaf Essential oil In vitro Chloramphenicol Positive Micrococcus
Bark Acetone,
Leaf Ethanol In vitro - Positive Pseudomonas
Fruits Crude
Extracts
used
methanol, and
chloroform
ethanolic, nhexane,
chloroform, and
aqueous
methanol
In vitro/
In vivo Standard used Samples
luteus
Negative Pasteurella
Negative Klebsiella
Negative Streptococcus
Negative Streptococcus
Negative Enterobacter
In vitro Tetracycline,
streptomycin,
and ampicillin
In vitro Imipenem Positive Bacillus subtilis **30% Agar well diffusion Alam and Saqib
Positive Staphylococcus
Negative Proteus vulgaris *28.3 mm
Negative Enterococcus
Negative Escherichia coli ,
multocida
faecalis
pneumoniae
luteus
Bacillus subtilis
viridians
Micrococcus
luteus
Staphylococcus
aureus
viridians
Escherichia coli
roseus
aerogenes,
Escherichia coli
aureus
aeruginosa
faecalis
Shigella flexnari,
Pseudomonas
aeruginosa, and
Salmonella
Typhi
Value of
Detection Method References
*21.33 mm Agar well diffusion Ullah et al. (2012)
*18.33 mm
*23 mm Agar well diffusion Negi et al. (2012)
*12 mm
*28.45 mm
*20.45 mm
*18.54 mm
*15 mm
*21 mm
*19 mm
*18.54 mm
*18 mm
*22 mm Agar well diffusion Mehmood et al.
*21 mm
*22 mm
*28.7 mm Agar well diffusion Srivastava et al.
*33 1 mm Agar well diffusion Akbar et al.
*14 1mm
***-
Agar well diffusion Ullah et al.
(2013b)
Agar well diffusion Guleria et al.
(2013)
(2013)
(2013)
(2014)
(2017)
Bark Methanol In vitro Benzyl penicillin Positive Staphylococcus
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Negative Escherichia coli *15 mm
Seeds Essential oil In vitro Gentamicin sulfate Positive Staphylococcus
Negative Escherichia coli *14.330.58 mm
Stem bark Essential oil In vitro Gentamicin sulfate
Leaves Petroleum ether
and chloroform
Fruits Methanolic In vitro Chloramphenicol Positive Staphylococcus
Leaves Methanol In vitro Gentamicin sulfate Positive Staphylococcus
In vitro Positive Bacillus subtilis
(20.330.58 mm to
40.330.58 mm)
Positive Staphylococcus
Negative Escherichia coli *14.330.58 mm
Negative Pseudomonas
Negative Proteus vulgaris
Negative Escherichia coli
aureus
aureus
aureus
Staphylococcus
aureus
aeruginosa
aureus
Pseudomonas
aeruginosa
Salmonella typhi
Shigella
dysenteriae
aureus
Antifungal activity
Bark Ethanolic In vitro Miconazole Fusarium solani
Candida albicans
Microsporum
canis
Leaf Essential oil In vitro Miconazole Microsporum
canis
Candida albicans
Candida glabrata
**66.67%
**56.33%
**54.33%
**84%
**83%
**79%
*13 mm Agar well dilution
*15.660.58 mm
and
6.330.58 mm
*14.660.58 mm
and
15.660.58 mm
*18 mm
*18 mm
*15 mm
*20.72 mm (wild)
*18.10 mm
(cultivated)
No Inhibition
Zone
*17.67 mm Agar well diffusion Singh et al.
*17.67 mm
method
Agar well diffusion Dhami et al.
Agar well diffusion Dhami et al.
Disk diffusion Dabral et al.
Disk diffusion Phuyal et al.
Agar dilution method Ullah et al. (2012)
Agar dilution method Ullah et al.
Siddhanadham
et al. (2017a)
(2018)
(2019)
(2019)
(2020b)
(2020)
(2013b)
Continued
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