03 Conclusions-Appendices Sadgrove · 2019. 3. 5. · 15.1.0 Summary . 15.1.1 Part 1 – Eremophila...
Transcript of 03 Conclusions-Appendices Sadgrove · 2019. 3. 5. · 15.1.0 Summary . 15.1.1 Part 1 – Eremophila...
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Part 4:
Thesis conclusions and appendices
‘If you want to know the end, look at the beginning’
African Proverb
‘The rule which forbids ending a sentence with a preposition is the kind of
nonsense up with which I will not put’
Sir Winston Churchill
‘If your knees aren’t green by the end of the day, you ought to seriously re-
examine your life’
Bill Watterson
‘The will to overcome a passion is in the end merely the will of another or
several other passions’
Friedrich Nietzsche
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Chapter 15 –
Conclusion
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15.1.0 Summary
15.1.1 Part 1 – Eremophila longifolia: ethnopharmacology, essential oil
chemotypes and cytogeography
With regard to the identification and delineation of essential oil chemotypes of
Eremophila longifolia, it is now clear that the first such chemotype identified in 1971
by Della and Jefferies, with an essential oil made up predominantly of the potentially
hepatotoxic carcinogenic phenyopropanoids safrole and methyl eugenol, is confined
to a small geographic region in Australia’s far west, in central-west Western
Australia. This is important since although E. longifolia has a widespread distribution
throughout the Australian landmass perceptions still prevail that this single chemotype
reflects the constituents of all individuals of the species. This is simply not true.
Further clarification reveals that this chemotype is an unusual biotype with diploid
cytology.
In all, a total of three diploid populations were identified in Australia, the other two
being geographically clustered in western New South Wales and producing terpenoid
based essential oils via the mevalonate pathway. These ketone rich chemotypes, as is
the case for the phenylpropanoid type, produce significantly high yields of essential
oils, making them potentially suitable for commercial development. The first of these
types is the isomenthone/menthone type (CT.A), which produces an essential oil yield
at an impressive range of 3-8% g/g wet weight of leaves. The second is the
karahanaenone type (CT.B), yielding at a range of 1-5% for diploid specimens, or 0.3-
0.7% for tetraploid specimens. Both these high yielding diploid types are good
candidates as cultivars for commercial plantations. Should such plantations be
established and developed this would make a significant contribution to Australia’s
essential oil industry. Essential oils and or/extracts from the high yielding CT.A
isomenthone/menthone type could be used to make ointments and lotions suitable for
topical, antifungal, aromatherapeutic and cosmeceutical/aesthetic applications (Table
1). At present it is unclear how CT.B could be utilised, but karahanaenone is already
in demand as a feedstock in the flavour and fragrance industry and may also be useful
as a chemical scaffold for further drug development.
In addition to the five essential oil chemotypes of E. longifolia identified prior to the
current study, four new types have now been characterised. One of these new
essential oils, with dominant components of bornyl- and fenchyl-acetate, is similar in
composition to the antimicrobial essential oil produced from Eremophila
bignoniiflora. Traditional ethnomedicinal use of E. bignoniiflora by Australian
Aboriginal people involved applications consistent with antispasmodic activity and
headache therapy. Because essential oils rich in esters are often associated with
antispasmodic and nervous calming activity, the essential oils from E. bignoniiflora
may have contributed to this effect. The same essential oil produced from the new
chemotype of E. longifolia, in significantly higher yields, could be marketed for
treatment of headaches, nervous tension or gastrointestinal disorders (Table 1).
Interestingly, another of the newly characterised chemotypes of E. longifolia produces
an essential oil comprised predominantly of fenchone and camphor (2-bornanone),
which are analogues of the previous mentioned fenchyl- and bornyl acetate
respectively, after removal of the acetate groups. In the case of fenchone and
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camphor, a ketone is in the place of the ester; however, in the case of the other known
chemotype, dominated by fenchol and borneol, an alcohol functional group is in the
place of the ester. Clearly, the oils produced by these three chemotypes are of very
similar biosynthetic provenance.
The essential oils dominated by the alcohols, fenchol and borneol, demonstrated high
antimicrobial activity against the yeast C. albicans, bacterial species, such as
Staphylococcus aureus, S. epidermidis, and the human pathogenic fungal species
Trichophyton rubrum, T. mentagrophytes and T. interdigitalis. Similar activity was
demonstrated by the fenchyl- and bornyl acetate oils against C. albicans and S.
epidermidis. The fenchone rich essential oil is yet to be tested for antimicrobial
activity.
The third new essential oil chemotype of E. longifolia is rich in α-pinene, sabinene,
limonene and α-terpinolene. At first this essential oil appeared to be consistent with
an earlier type reported in individual E. longifolia from Alice Springs, in the Northern
Territory. However, it’s unusually high concentration of α-terpinolene, makes this
new essential oil unique. The fourth new chemotype is dominated by p-cymen-8-ol,
along with a host of other unidentified compounds.
Currently then, at least nine chemotypes of E. longifolia have been characterised but
preliminary results suggest that others wait to be confirmed. All essential oil
chemotypes occurring outside the small regions of the safrole/methyl eugenol diploid
type, the isomenthone/menthone diploid type and the karahanaenone diploid type
show tetraploid cytology. The karahanaenone and isomenthone/menthone types also
exist as tetraploid forms but produce relatively low essential oil yields by comparison
with the diploid varieties. Such tetraploid types appear as randomly emerging
individuals in isolated patches throughout the range of E. longifolia, probably
emerging as a result of sexual reproduction and assortment of recessive allelic traits
related to biosynthesis.
Consideration within the context of proposals to cultivate commercial scale crops of
E. longifolia species, quality control of plantations of tetraploid chemotypes may
involve the elimination of karahanaenone and isomenthone/menthone chemotypes
emerging in plantations from sexual reproduction. However, in any case, this is not
expected to occur with any great frequency since this species has a preference for
reproduction by root suckers.
With regard to the emergence of unintended chemotypes in populations of known
chemotypes, one may consider the emergence of the safrole/methyl eugenol type a
potential risk in a commercial scale plantation, particularly since safrole and methyl
eugenol have been red flagged as potential hepatotoxic carcinogens. Our research
indicates that the risk of this occurring is vanishingly small. Thus far the
safrole/methyl eugenol type has not been demonstrated to occur in tetraploid form.
However, even if this did occur, the parent chemotype would produce essential oils
via the shikimic acid pathway, because emergent chemotypes may not contradict the
biosynthetic origins of the parent chemotype.
With regard to the role of volatiles in the medicinal efficacy of smoke or steam
fumigation rituals, using E. longifolia, both partially pyrolysed essential oils and the
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more hydrophilic component ‘genifuranal’ are involved. Most of the essential oil
components are present in the leaf tissue before heating, but are accompanied with
other derived artefacts in the steamy smoke that is produced when the leaves are
placed on hot embers for use in medicinal applications consistent with antibacterial or
antifungal applications, as well as lactagogue activity. The smoking procedure was
also used to prepare surgical tools, no doubt for sterilization but conceptualised as a
type of exorcism ritual. The essential oils and artefacts were also accompanied by
pyrolysed derivatives including radical essential oil fragments and other phenolic or
benzoid constituents; together producing significantly enhanced antimicrobial
activity, as demonstrated in our microtitre plate broth dilution assays.
‘Genifuranal’ itself exhibited significant antimicrobial activities, with mean inhibitory
concentrations as low as 100 μg/ml against some species. As we were not able to
detect this compound in the leaves of E. longifolia without heating it into a gaseous
state, we hypothesise that ‘genifuranal’ is the product of heat induced cleavage of a
glycosidic bond. The proposed glycoside is geniposidic acid, already demonstrated to
occur in the leaves of E. longifolia in previous studies, and demonstrated to exhibit
cardioactivity.
In traditional fumigation rituals, ‘genifuranal’ and partially pyrolysed essential oils
are delivered in warm air to the patient. Although the transdermal absorption of
components such as ‘genifuranal’ are expected to produce significant biological
activity, the first application with warm air is itself expected to have enhanced
activity, relative to cooler applications. In this regard, antimicrobial assays produced
in vitro have limited capability of capturing this enhanced activity from warm air
delivery. Thus, antimicrobial activities produced in smoke fumigation rituals are
expected to be higher than those demonstrated in the laboratory.
15.1.2 Part 2 – Ethnopharmacology of medicinal plants used traditionally by
Aboriginal Australians
The medicinal potential of the essential oil of E. bignoniiflora has already been
summarised above. In other studies a dichloromethane extract of the leaves of this
plant demonstrated calcium channel blockage that may be consistent with a number of
traditional medicinal uses. Because the calcium channel subtype was not clarified in
this earlier study, the results have implications for both therapeutic activity related to
headaches and spasmolysis of the intestine. Because activity was expected to vary
from leaves to the fruits, identification of the principal active component may be
achieved by seeking to characterise components present in both the leaves and the
fruits, but more concentrated in the fruits. Although the essential oils could have been
involved in this activity, other important components may also be identified.
Although essential oils from the fruit of Pittosporum undulatum have already been
partly characterised in an earlier study completed in 1905, our recent characterisations
enhanced and extended this earlier study. In our study we were able to tentatively
identify the optically inactive compound referred to in the earlier study, conducted
over a hundred years ago. We believe this was bicyclogermacrene.
Unlike P. undulatum, Pittosporum angustifolium was involved in a significant
number of traditional medicinal applications. The most common of these to be
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recorded in the literature are related to the treatment of coughs and colds, for
lactagogue activity and in the treatment of eczema. More recently, a number of
anecdotal reports have surfaced related to ia cancer inhibition, autoimmune conditions
in the intestines, antimicrobial activity. Previous studies have supported potentially
anticancer activity, as well as possible antiviral activity, particularly the Ross River
Fever virus.
Our study examined the chemical character of volatiles from P. angustifolium,
demonstrating a degree of variation. Compounds with structural similarities to
previously described chemosemiotic compounds identified in mother-infant
communications, were also noted, including acetic acid decyl ester or 1-dodecanol.
Accordingly, we hypothesise that these compounds are involved in the traditional
application as a lactagogue, particularly because the modality of usage involved
heating a compress of leaves to produce such volatiles, which were then used to
fumigate the breasts of the nursing woman.
In our studies most of the essential oils from Geijera parviflora and G. salicifolia
were chemically consistent with previous identified chemotypes; however some
variation was noted and new potential chemotypes were identified. One of these, from
a specimen of G. parviflora (NS374), exhibited an oil comprised of a larger
abundance of bicyclogermacrene and trans-caryophyllene (and unknown B), which
may be the first known sesquiterpene dominated essential oil from Geijera species.
Following hydrodistillation performed on this specimen a dichloromethane partition
of the hydrosol produced a residue that was rich in pyranocoumarin xanthyletine,
furanocoumarin isopsoralen and methoxy coumarin osthole. This hydrosol partition
has not been attempted using other chemotypes.
Here we also present for the first time studies on antimicrobial and free radical
scavenging activity of essential oils from Geijera species. The most active of these
oils is the green oil from G. parviflora, made up predominantly of
pregeijerene/geijerene and linalool. Previous studies on these components indicate
that this green essential oil may have applications as an insect repellent (particularly
mosquitoes) as well as a topical analgaesic agent.
Smoke condensates from G. parviflora (chemotype 3) indicated the possible
occurrence of an alkaloid in the qualitative pharmacological test. This requires further
analysis for confirmation. However, the occurrence of alkaloids in the smoke
condensate may have significance with regard to reported psychoactivity achieved in
smoking the plant. Another possibly fruitful line of investigation would be to examine
the pharmacological and chemical character of coumarins in these smoke condensates
in the context of possible psychoactivity.
In further experiments aimed at simulating traditional use, smoke condensates were
also produced from Callitris endlicheri and C. glaucophylla and these were shown to
contain γ-lactones ferruginol and pisiferal/pisiferol, along with a host of other
phenolic compounds, with high levels of antimicrobial activity.
15.1.3 Part 3 – Phytochemical and chemotaxonomic investigations
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Phytochemical investigations of Zieria species presented in this thesis corroborated
previously published data on representatives of this genus. We have expanded the
available information on this genus by, for the first time, detailing the chemical
character of essential oils from the two species, Z. odorifera subsp. williamsii and Z.
floydii. Considered within the context of the chemotaxonomic approach undertaken in
earlier studies, the remarks of the discoverer of the species, A. G. Floyd, now seem
somewhat prescient. ‘This is a quite oddity! This specimen does not match any known
Zieria taxon. It appears to be allied to 3 closely related species; Z. furfuracea, Z.
granulata and Z. smithii’. The former two species mentioned there, being Z.
furfuracea and Z. granulata, produce an essential oil rich in car-3-en-2-one. The
essential oil from Z. floydii was also dominated by this component.
Although essential oils from Zieria spp. have been previously examined for
antimicrobial activity, here we tested the essential oils against a broader range of
organisms and also compared the activity of essential oils with solvent extracts from
the same species. We found high antimicrobial activity in both solvent extracts and
essential oils. We conclude that a putative essential oil industry based on species of
Zieria would provide a novel range of essential oils, attractive to the aromatherapy
community, as well as providing purified compounds useful as scaffolds in
pharmaceutical development.
In a further chemotaxanomic approach we have for the first time addressed existing
taxanomic concerns regarding the Phebalium squamulosum heterogenous species
aggregate. The first species examined was P. squamulosum subsp. verrucosum, which
was regarded by our esteemed collaborator, Ian Telford, of the Beadle Herbarium at
the University of New England, as having greater morphological alliance with the
Phebalium glandulosum complex. Essential oils of this species were dominated by
dihydrotagetone at concentrations ranging from 95-98%. An identical essential oil,
with the same yield g/g wet weight of leaves, was produced in an earlier study from P.
glandulosum subsp. macrocalyx. In another study this was also demonstrated to be the
case with P. glandulosum subsp. glandulosum. Here we have characterised an almost
identical essential oil from P. glandulosum subsp. nitudum and P. squamulsoum
subsp. eglandulosum. We have therefore concluded that dihydrotagetone dominated
essential oils are a general characteristic of the P. glandulosum subspecies complex.
In a subsequent study other members of the P. squamulosum heterogenous species
aggregate were phytochemically investigated. We demonstrated that all apparent
subspecies currently assigned to this assemblage have separate individual essential oil
chemotypes. Interestingly, several separate chemotypes were demonstrated from
specimens currently assigned to P. squamulosum subsp. squamulosum. In this regard,
a notable chemical characteristic of oils from southern specimens (collected near
Sydney and in the Hunter Valley) was the almost total predominance of a tricyclic
sesquiterpene ketone; squamulosone. By contrast, northern specimens were
characterised by essential oils rich in elemol/hedycaryol.
Our final study aimed at identifying a range of essential oil types from select
Prostanthera species, has made a significant contribution to resolution of taxonomic
problems in this genus. This study particularly emphasised issues surrounding
taxonomy of P. rotundifolia, P. lasinathos and P. ovalifolia, and clearly demonstrated
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the need for subsequent comprehensive chemotaxonomic studies, complementing a
morphological and phylogenetic analysis, to delineate new species.
Significant numbers of morphological subtypes are known to occur in the three
species mentioned above, paralleling the existence of discrete essential oil
chemotypes. Despite such variation essential oils from these Prostanthera species
(series racemosae) were almost always characterised by a major representation of 1,8-
cineole. However the differentiating factor is the existence and relative abundances of
tricyclic sesquiterpene alcohols, such as globulol, ledol, prostantherol and maaliol,
which are characterised by a cyclopropane moiety, attached to either a decahydro-
napthalene or –azulene structure. Again, further significant differentiating
components of some essential oils were the tricyclic sesquiterpenes, but with
heterocycle substituents in place of the cyclopropane moiety. Examples include cis-
dihydroagarofuran or kessane, also on a decahydro-napthalene or –azulene structure
respectively.
As with other genera, Prostanthera essential oils were considered within the context
of possible pharmacological activities. Here we demonstrate that oils dominated by
the sesquiterpene alcohols provided the greatest antimicrobial activity against a range
of organisms, most pronounced against some Gram-positive species. Individual
components found in significant amounts in the essential oils were related to this
enhanced antimicrobial activity, particularly prostantherol. Maaliol was also found in
significant amounts in one specimen currently assigned to P. ovalifolia. This is of
considerable potential pharmacological interest, given the importance of maaliol in
the antinociceptive activity of a widely used Indian medicinal plant species
(Valeriana wallichii). This antinociceptive activity is therefore expected to be also
produced by oils from maaliol rich species of Prostanthera. Again, Prostanthera
essential oils have a great potential as novel additions to Australia’s aromatherapy
and/or natural product industry.
Table 1 - Possible commercial scale applications from essential oil yielding flora in Australia
Species Chemotype Use
Geijera parviflora geijerene/pregeijerene (and germacrene D)
Commercial plantation: Insect repellent, topical analgaesia (linalool content)
Geijera parviflora Osthole, isopsoralen, xanthyletine
Commercial plantations:
Zieria floydii car-3-en-2-one Commercial plantations: Chemical scaffold for further drug development and antimicrobial activities
Prostanthera ovalifolia maaliol Commercial plantations: Medicinal applications consistent with the Indian Valeriana willichii
Prostanthera rotundifolia
prostantherol Commercial plantations: Antimicrobial activities
Eremophila longifolia isomenthone/menthone Commercial plantation: topical, gastrointestinal for antimicrobial activities, topical for muscle aches and pains, active in applications for treatment of thrush (Candida)
Eremophila longifolia fenchyl-/bornyl acetate; Commerical plantations: possible activity in gastrointestinal disease, possible activity in aromatherapy for headache sufferers
Callitris glaucophylla NA
1) Bioactive γ-lactones; ferruginol, pisiferal, pisiferol. 2) Occurrence of hydrophilic antibiotic highly active against S. aureus and B. subtilis - requires purification and structure elucidation. Medicinal applications consistent with the Japanese species Chamaecyparis pisifera
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15.2.0 Suggested areas for further research
The demonstration of multiple chemotypes in E. longifolia emphasises the chemical
variability expressed by this species, which may be an intrinsic general character of
this genus. Thus, it is quite probable that other species from Eremophila may
demonstrate this geographical chemical variability. The observed correlation of
diploidy with higher abundances of secondary metabolites may have more general
implications. Therefore it would be worthwhile examining other species for both
chemogeography and karyotype. Perhaps this search should start in E. deserti, as this
has already been shown to possess an abundance of essential oil chemotypes with
high yields of essential oil. Another species, E. glabra, produces no essential oil at all;
however NSW specimens are either hexaploid or tetraploid, but a diploid biotype can
be found in far western WA. It may be worthwhile seeing if this diploid specimen
yields any amount of essential oil. This may be a fruitful area of investigation for all
Eremophila and its allied genus, Myoporum.
With regard to further investigation of species of Eremophila for derivatives produced
in smoke fumigation rituals, no other species was as frequently used for this purpose
as was E. longifolia, meaning that it may be less likely that volatile therapeutic
compounds could be found in other species of Eremophila. Although in Chapter 4 a
handful of other species were examined for the derivative genifuranal, thus far it has
only been produced from E. longifolia.
Other species of Eremophila were in fact used, albeit less frequently in smoke
fumigation rituals, meaning that it may be worthwhile to examine for unknown smoke
artefacts in addition to genifuranal. Other species involved in smoke fumigation
treatments were E. bignoniiflora, E. sturtii, E. mitchellii, E. dalyana, E. freelingi, and
E. duttonii.
Derivatives or larger molecular mass compounds produced/evaporated during smoke
fumigation methodology may alternatively be produced from hydrodistillation.
However, due to the less destructive nature of conventional hydrodistillation such
derivatives or larger molecules could possibly be distilled in higher abundance at
shorter time-intervals if higher temperatures and pressures are employed. In this
regard a modified pressure cooker, with a 15psi pressure release valve positioned for
horizontal airflow into an adjacent condenser, could be used to achieve this end.
At various stages throughout this thesis examination of solvent extracts demonstrated
some degree of antimicrobial activity. This was not observed using E. longifolia or E.
bignoniiflora, but Callitris glaucophylla and C. endlicheri did appear to contain a
polar component with significant discriminating bactericidal activity against two
Gram-positive organisms (Staphylococcus aureus and Bacillus subtilis). It would be
interesting to know what this component is and if it could be used to treat antibiotic
resistant infections, such as VRE or MRSA. In addition, other species of Eremophila
should be examined, particularly the highly aromatic and highly regarded E. dalyana.
Because of the intrinsic chemovariability of other species, another species worthy of
further examination is E. alternifolia, regarded as ‘highly potent’ in some places but
not others.
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An interesting and unexpected outcome of this thesis is the ‘resurrection’ of
chemotaxonomy, which was utilised by botanists in the 70’s and 80’s before
molecular fingerprinting became possible and quickly grew in popularity. Of course it
is not expected that chemotaxonomy could outperform molecular fingerprinting and
phylogenetics in species delimitation, however it certainly has proven to effectively
complement this method. Subsequently to this thesis the phylogenetic approach has
been employed for results with a quick turnaround, to resolve simple questions such
as ‘is this species the same as the one we collected previously’? Already, our
collaborative botanists have been forced to examine voucher specimens in closer
detail because the chemotaxonomic approach has compelled them to do so.
In this regard, the question still begs an answer ‘how do you define a species’?
Chemotaxonomy is challenged by the divide between ‘new species’ and ‘new
chemotype of the one species’. To complicate the matter further, in Part 1 of this
thesis we demonstrated that a correlation could be made between genetics (karyotype)
and chemotype, whilst the classical view is that chemotypes result from differences in
soil climate. In the former, seedlings from one chemotype could be transplanted into
different soil types and different climates without any serious variation to the
chemical character of its essential oil. In the latter more classical view, most certainly
there would be a difference.
The view that chemotype derives from soil type is borrowed from Europe and Great
Britain, where cultivar selection over thousands of years has caused a kind of genetic
uniformity across many species used in cultivation. However, because this cultivar
selection was not a practice employed by Australian Aboriginal people it is more
likely that unique soil types and various climates favour certain biotypes – meaning
the plant itself is different and better suited to that environment.
Over long stretches of time, geographically isolated chemotypes may diverge into
new species, but again, the challenge lies in deciding exactly what amount of
divergence warrants delimitation of a new species. Because of the inherent ambiguity
in answering such a question, the best resolution for now is that consistent
morphological differences should stand alone in defining a new species, but
chemotaxonomy and phylogenetics may be utilised to demonstrate that such
morphological variability is not merely a consequence of naturally occurring
variability within the one species.
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Appendix A –
Consolidated list of references
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Adams, R. P. (1999). Systematics of multi-seeded eastern hemisphere Juniperus based on leaf essential oils and RAPD DNA fingerprinting. Biochemical systematics and ecology 27: pp. 709-725
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Adams, R. P. (2007). Identification of essential oil components by gas chromatography/mass spectrometry (4th ed.): Allured Publishing Corporation (ISBN 978-1-932633-21-4).
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Angioni, A., Barra, A., Coroneo, V., Dessi, S., & Cabras, P. (2006). Chemical composition, seasonal variability, and antifungal activity of Lavandula stoechas L. ssp. stoechas essential oils from stem/leaves and flowers. Journal of Agricultural and Food Chemistry 54: pp. 4364-4370
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Asghari, J., Touli, K. C., & Mazaheritehrani, M. (2012). Microwave-assisted Hydrodistillation of Essential Oils from Echinophora platyloba DC. Journal of Medicinal Plants Research 6(28): pp. 4475-4480
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Bae, D. S., Kim, C. Y., & Lee, J. K. (2012). Anti-inflammatory effects of dehydrogeijerin in LPS-stimulated murine macrophages. International Immunopharmacology 14: pp. 734-739
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of NSW, Sydney. Baker, R. T., & Smith, H. G. (1912). On a new species of Prostanthera and its essential oil.
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Valeriana hardwickii Wall. rhizome are putatively mediated through calcium channel blockade. Evidence-Based Complementary and Alternative Medicine 2011: pp. 1-6
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