A multifaceted peer reviewed journal in the field of Pharmacognosy and Natural Products
Vol 6, Issue 2, Apr-Jun, 2016
Clostridium perfringens is a gram positive pathogen which
is an etiological agent in Clostridial myonecrosis and enteritis necroticans.
Unless promptly treated, C. perfringens infections may result in tissue
necrosis and death. Syzygium australe (brush cherry) and Syzygium lu-
ehmannii (riberry) fruit and leaves have documented therapeutic proper-
ties as general antiseptic agents against an extensive panel of bacteria.
Despite this, studies are yet to test the growth inhibitory activity of these
species against C. perfringens. Methods: S. australe and S. luehmannii
fruit and leaf extracts were investigated by disc diffusion assay for growth
inhibitory activity against a clinical strain of Clostridium perfringens. Their
MIC values were determined to quantify and compare their efficacies.
Toxicity was determined using the Artemia franciscana nauplii bioassay.
Results: Methanolic and aqueous
S. australe and S. luehmannii fruit and
leaf extracts as well as the corresponding fruit ethyl acetate extracts,
displayed growth inhibitory activity in the disc diffusion assay against
C. perfringens. The aqueous and methanolic extracts were particularly
potent growth inhibitors, each with MIC values substantially <500 µg/mL. The
S. australe fruit extracts were nontoxic in the Artemia franciscana bioassay
values <1000 µg/mL). All ethyl acetate extracts were also nontoxic. In
contrast, the S. luehmannii aqueous and methanolic extracts (fruit and leaf),
as well as the S. australe leaf extracts displayed substantial toxicity in the
assay. Conclusion: The potent growth inhibitory bioactivity of the fruit and
leaf aqueous and methanolic Syzygium spp. extracts against C. perfringens
indicates their potential as medicinal agents in the treatment and prevention
of clostridial myonecrosis and enteritis necroticans.
Syzygium australe, Syzygium luehmannii, Riberry, Brush cher-
ry, antioxidant, Myonecrosis, Enteritis necroticans, Gas gangrene.
Ian Edwin Cock,
School of Natural Sciences, Nathan Campus,
Griffith University, 170 Kessels Rd, Nathan,
Queensland 4111, AUSTRALIA.
Tel no.: +61 7 37357637; Fax no: +61 7 37355282.
E-mail: email@example.com (I. E. Cock).
DOI : 10.5530/pc.2016.2.7
The genus Clostridium comprises a large group of sporulating, Gram-
positive, fermentative saprophytes. Generally existing in nature as part
of the natural bacterial flora, the genus is clinically significant as several
members of the genus have been linked to a number of diseases in
humans.These include C. botulinum (botulism), C. difficile (pseudomem-
branous colitis), C. sordellii (pneumonia, endocarditis) and C. perfrin-
gens (food poisoning, clostridial myonecrosis).
can infect a host and cause disease through the production of various
The diseases vary greatly in both associated symptoms and
depending on the route of infection. The best known example within the
genus is C. perfringens, which can cause food poisoning if ingested, or
clostridial myonecrosis (gas gangrene) through the infection of deep-
accounting for up to a million infections annually in the United States.
Present in air, soil, water, faeces and as part of the human gut microbiota,
can propagate to infectious levels. Whilst proper food preparation
can significantly reduce the likelihood of infection, the sporulating
nature of C. perfringens can result in the organism’s survival.
food poisoning, with only by nontyphoidal Salmonella causing more
Antibiotic therapy can offer an effective means of treatment,
search is ongoing for alternative antimicrobial agents. In addition to
the design and synthesis of new agents, the probing of natural resources
for antimicrobial agents offers an appealing alternative to traditional
means of drug development. The geographical isolation and unique flora
positions Australia to be an ideal environment for such investigations
with several previous studies reporting antimicrobial activity against
a number of other microorganisms.
Syzygium (family Myrtaceae) is a
tropical regions of Africa, Southern and South-East Asia, and throughout
Australia. The greatest diversity of Syzygium spp. occurs in South-East
Asia and Northern Australia. Most species are evergreen trees or large
shrubs, with glossy green foliage. Several species have culinary and
therapeutic uses. In the commercially most important species Syzygium
aromaticum (clove), the unopened flower bud is used as a spice. This
plant also has uses in traditional medicine due to its anaesthetic
The antibacterial activity of S. aromaticum is also well
activities of oils and extracts from this plant.
Syzygium luehmannii) produce edible fruit which have very high antioxi-
associated with a decreased incidence of chronic diseases.
School of Natural Sciences, Nathan Campus, Griffith University, 170 Kessels Rd, Nathan, Queensland 4111, AUSTRALIA.
Environmental Futures Research Institute, Nathan Campus, Griffith University, 170 Kessels Rd, Nathan, Queensland 4111, AUSTRALIA.
the development of degenerative diseases such as cancer,
diabetes and obesity.
high antioxidant Australian plants.
Particularly noteworthy, the
have potent growth inhibitory activity against a broad panel of
inhibitory activity of Australian Syzygium spp., numerous pathogens are
yet to be evaluated for their susceptibility to Australian Syzygium spp.
extracts. The current study was undertaken to test the ability of to
S. australe and S. luehmannii fruit and leaf extracts to inhibit the growth
of the Gram-positive anaerobic bacterium Clostridium perfringens.
Plant source and extraction
S. luehmannii and S. australe fruit and leaves were collected from verified
trees in suburban regions of Brisbane, Australia and voucher specimens
deposited in the School of Natural Sciences, Griffith University, Aus-
tralia. The plant materials were comprehensively dried using a Sun-
beam food dehydrator and the dried material stored at -30
into a coarse powder. Individual 1 g quantities of the ground plant ma-
terial were weighed into separate tubes and 50 mL of deionised water,
methanol or ethyl acetate were added. All solvents were obtained from
Ajax, Australia and were AR grade. The ground plant materials were
independently extracted in each solvent for 24 h at 4
C through gentle
(Whatman No. 54) under vacuum, followed by drying using rotary
evaporation in an Eppendorf concentrator 5301. The resultant dry ex-
tract was weighed and dissolved in 10 mL deionised water (containing
Qualitative phytochemical studies
Phytochemical analysis of the extracts for the presence of alkaloids,
cardiac glycosides, tannins, saponins, phenolic compounds, flavonoids,
polysteroids and triterpenoids was achieved as previously described.
The antioxidant capacity of each sample was assessed using a modified
DPPH free radical scavenging method.
Ascorbic acid (0-25 µg per
recorded at 515 nm. All tests were completed alongside controls on each
plate and all were performed in triplicate. The antioxidant capacity based
on DPPH free radical scavenging ability was determined for each extract
and expressed as µg ascorbic acid equivalents per gram of original plant
Clinical Clostridium perfringens screening
A clinical strain of Clostridium perfringens was supplied by Ms. Jane
Gifkins (Griffith University) which was originally isolated and verified
by Dr. John Bates (Department of Health, Queensland, Australia).
Cultures were grown and maintained using a thioglycollate liquid media
(Oxoid Ltd., Australia). All growth studies were performed using
nutrient agar (Oxoid Ltd., Australia) under induced anaerobic conditions
through the use of anaerobic jars and AnaeroGen™ 3.5 L atmospheric
generation systems (Thermo Scientific). All studies were performed at
C and the stock culture was subcultured and maintained in thiogly-
Antimicrobial activity of Syzygium spp. extracts was determined
using a modified disc diffusion assay.
was grown in 10 mL of fresh thioglycollate media until an approximate
count of 10
cells/mL was reached. A volume of 100 µL of the bacterial
antibacterial activity using 6 mm sterilised filter paper discs. Discs were
impregnated with 10 µL of the extracts, allowed to dry and placed onto
the inoculated plates. The plates were left to stand at 4°C for 2 h before
incubation at 30°C for 24 h. The diameters of the inhibition zones were
measured to the closest whole millimetre. Each assay was performed
in at least triplicate. Mean values (± SEM) are reported in this study.
Standard discs of penicillin (2 µg) and ampicillin (10 µg) were obtained
from Oxoid Ltd., Australia and used as positive controls to compare
antibacterial activity. Filter discs impregnated with 10 µL of distilled water
were used as a negative control.
Minimum inhibitory concentration (MIC) determination
The minimum inhibitory concentrations (MIC) of the extracts was deter-
mined as previously described.
Briefly, the plant extracts were diluted
were impregnated with 10 µL of the extract dilutions, allowed to dry and
placed onto inoculated plates. The assay was performed as outlined above
and graphs of the zone of inhibition versus concentration were plotted.
Determination of MIC values were achieved using linear regression.
Reference toxin for toxicity screening
Potassium dichromate (K
) (AR grade, Chem-Supply, Australia)
seawater for use in the Artemia franciscana nauplii bioassay.
Artemia franciscana nauplii toxicity screening
Toxicity was tested using a modified Artermia franciscana nauplii
n=155, SD 14.5) A. franciscana nauplii were added to wells of a 48 well
plate and immediately used in the bioassay. Volumes of 400 µL of refer-
ence toxin or the diluted plant extracts were transferred to the wells and
incubated at 25 ± 1°C under artificial light (1000 Lux). For each plate, a
negative control (400 µL seawater) was run in triplicate. All treatments
were also performed in at least triplicate. The wells were assessed at
regular intervals and the number of dead counted. The nauplii were
deemed dead if no movement of the appendages was detected within
10 sec. After 24 h, all nauplii were sacrificed and counted to determine
the total % mortality per well. The LC
with 95% confidence limits for
Data is expressed as the mean ± SEM of at least three independent
Liquid extraction yields and qualitative phytochemical
Extraction of Australian Syzygium spp. plant materials (1 g) with various
solvents yielded dried plant extracts ranging from 62 mg (S. luehmannii
leaf ethyl acetate extract) to 560 mg (S. luehmannii fruit methanolic
extract) (Table 1). Methanolic extracts provided significantly greater
yields of extracted material relative to the corresponding aqueous and
Mass of dried extract (mg)
resuspended extract (mg/
Water insoluble phenolics
by DPPH reduction
(expressed as mg AA
equivalence per 1 g plant
M=methanolic extract; E=ethyl acetate extract; AA=ascorbic acid.
triplicate determinations. - indicates that MIC or LC
values were not obtained as the bacterial growth inhibition
ethyl acetate extracts, which gave low to moderate yields. The dried
extracts were resuspended in 10 mL of deionised water (containing 1%
DMSO), resulting in the concentrations presented in Table 1.
Antioxidant capacity for the plant extracts (Table 1) ranged from 1.5 mg
(S. luehmannii fruit ethyl acetate extract) to a high of 94.6 mg ascorbic
acid equivalence per gram of dried plant material extracted (S. luehman-
nii fruit methanolic extract). The antioxidant capacities for the aqueous
and methanolic extracts of each plant part were generally similar for both
species and were substantially higher than the corresponding ethyl acetate
To determine the ability of the crude fruit and leaf extracts to inhibit
C. perfringens growth, 10 µL of each extract were screened using a disc
diffusion assay. Bacterial growth was inhibited by 10 of the 12 extracts
screened (83%) (Figure 1). The methanolic extracts were the most po-
tent inhibitor of growth (as judged by zone of inhibition), with inhibition
zones as much as 19.3 ± 0.6 mm (S. australe fruit methanolic extract).
This compares favourably with the penicillin (2 µg) and ampicillin
controls (10 µg), with the zones of inhibition of 12.3 ± 0.3 and 13 ± 1.0 mm
respectively. Indeed, the methanolic fruit and leaf extracts of both
Syzygium spp. displayed inhibition zones > 12 mm. The aqueous S. australe
Growth inhibitory activity of S. australe and S. Luehmannii fruit and leaf extracts against the C. perfringens environmental isolate measured as
zones of inhibition (mm). SAFW=aqueous S. australe fruit extract; SAFM=methanolic S. australe fruit extract; SAFE=ethyl acetate S. australe fruit extract;
SALW=aqueous S. australe leaf extract; SALM=methanolic S. australe leaf extract; SALE=ethyl acetate S. australe leaf extract; SLFW=aqueous S. luehman-
nii fruit extract; SLFM=methanolic S. luehmannii fruit extract; SLFE=ethyl acetate S. luehmannii fruit extract; SLLW=aqueous S. luehmannii leaf extract;
SLLM=methanolic S. luehmannii leaf extract; SLLE=ethyl acetate S. luehmannii leaf extract; PC=penicillin (2 µg); AMP=ampicillin (10 µg). Results are expressed
as mean zones of inhibition ± SEM.
The lethality of the S. australe and S. luehmannii fruit and leaf extracts (2000 µg/mL) and the potassium dichromate control (1000 µg/mL) towards
Artemia franciscana nauplii after 24 h exposure. SAFW=aqueous S. australe fruit extract; SAFM=methanolic S. australe fruit extract; SAFE=ethyl acetate
S. australe fruit extract; SALW=aqueous S. australe leaf extract; SALM=methanolic S. australe leaf extract; SALE=ethyl acetate S. australe leaf extract;
SLFW=aqueous S. luehmannii fruit extract; SLFM=methanolic S. luehmannii fruit extract; SLFE=ethyl acetate S. luehmannii fruit extract; SLLW=aqueous
S. luehmannii leaf extract; SLLM=methanolic S. luehmannii leaf extract; SLLE=ethyl acetate S. luehmannii leaf extract; PC=potassium dichromate control;
SW=seawater control. Results are expressed as mean % mortality ± SEM.
fruit and S. luehmannii leaf extracts also displayed good inhibition of
The antimicrobial efficacy of the extracts was further quantified through
the determination of MIC values (Table 2). The aqueous and methanolic
fruit extracts of both Syzygium spp., were particularly effective at
inhibiting C. perfringens growth with MIC values generally <300 µg/mL
(<3 µg impregnated in the disc). Similarly, the aqueous and methanolic
S. luehmannii leaf extracts, as well as the methanolic S. australe leaf
extract, were good growth inhibitors with MIC values <900µg/mL
(<9 µg infused into the disc). These results compare well with the growth
inhibitory activity of the penicillin and ampicillin controls which were
tested at 2 µg and 10 µg respectively. All other extracts were either of only
low efficacy in the assay, or did not inhibit C. perfringens growth at all.
Quantification of toxicity
All extracts were initially screened in the assay at 2000 µg/mL (Figure 2).
As a reference toxin, potassium dichromate was also tested in the bio-
assay. The potassium dichromate reference toxin was rapid in its onset
of mortality, inducing nauplii death within the first 3 h of exposure and
100% mortality was evident within 4-5 h (unpublished results). With the
exception of the ethyl acetate leaf extracts of both species, all extracts
showed > 50% mortality rates at 24 h.
To further quantify the effects of toxin concentration on Artemia nau-
plii mortality, the extracts were serially diluted in artificial seawater to
test across a series of concentrations in the Artemia nauplii bioassay. The
24 h LC
values of the Syzygium spp. extracts towards A. franciscana
are presented in Table 2. No LC
values are reported for the fruit or leaf
in all tested concentrations. Extracts with an LC
>1000 μg/mL towards
The S. australe
Interestingly, the aqueous and methanolic extracts of S. australe leaf
and of S. luehmannii fruit and leaf, displayed LC
result as S. australe and S. luehmannii fruit are considered nutritious,
high antioxidant foods. However, it is noteworthy that the bioassay
organism (Artemia franciscana) is sensitive to extreme pH ranges.
Our study reported that all of the extracts with LC
values < 1000 μg/mL
reported that the high antioxidant capacities of these Syzygium
spp. is largely due to their high ascorbic acid contents. Therefore, it is
possible that the apparent toxicity reported in this study may instead be
a result of the extracts high ascorbic acid contents.
Previous studies have reported potent growth inhibitory activities for
S. australe and S. leuhmannii fruit and leaf extracts against a panel of
pathogenic bacterial species.
Both Gram-positive and Gram-
negative bacteria were screened in previous studies. Whilst the Syzygium
spp. extracts had broad spectrum growth inhibitory activity, a greater
susceptibility of Gram-positive bacteria was noted. Indeed, the previous
studies reported that the aqueous and methanolic S. australe and S. leuh-
mannii extracts inhibited the growth of 40-80% of the gram positive
bacterial species tested, with the methanolic extracts generally having a
broader specificity. In light of this broad spectrum gram positive growth
inhibitory activity, the potent
growth inhibition evident in
our study is perhaps not surprising.
Whilst an investigation of the phytochemistry of the Syzygium spp.
extracts was beyond the scope of our study, high flavonoid, terpenoid and
tannin contents are characteristics of this genus.
Flavonoids have well
Relatively high levels
taxonomically related species Syzygium aromaticum (clove).
ferol, myricetin and a methanolic S. aromaticum leaf extract against a
panel of bacteria. Similarly, quercetin, rutin and their corresponding
glycosides inhibit the growth of Pseudomonas maltophilia and Enterobacter
The antimicrobial activity of terpenoids hasbeen extensively
mycrene, terpinene, limonene, piperitone and β-phellandrene inhibit the
growth of a panel of bacteria including several nitrofurantoin resistant
strains of Enterobacteriaceae.
Similarly, the antibacterial activities for
lene have been reported.
Furthermore, many tannin compounds have
broad spectrum of bacterial species
through a variety of mechanisms
proline-rich cell surface proteins,
and by inhibiting glucosyltransferase
Elligitannins are also highly potent inhibitors of bacterial
been reported to function via several antibiotic mechanisms including
interaction with cytoplasmic oxidoreductases and by disrupting bacterial cell
Thus, it is likely that multiple compounds within the Syzygium
spp. extracts are contributing to the growth inhibition of C. perfringens.
The findings reported here also indicate that the majority of the
Syzygium spp. extracts examined in this study displayed significant
toxicity (<1000 µg/mL) in the Artemia nauplii bioassay. Indeed, the most
promising aqueous and methanolic S. luehmannii fruit extracts (MIC
values of 275 and 161 µg/mL respectively) had LC
values of approxi-
would impact on the usefulness of these extracts as a medicinal anti-
septic agent. Similar extracts prepared from fruits of these species have
previously been reported to have high ascorbic acid levels.
may also be responsible (at least in part) for the toxicity reported here.
Whilst A. franciscana have generally been reported to be a robust and
hardy organism for toxicity screening, they are susceptible to pH changes.
The levels of ascorbic acid previously reported in S. australe and S. leuh-
pH of the seawater in the tests and this change may be responsible for the
mortality induction reported in our study.Indeed, studies in our labora-
tory have shown that testing pure ascorbic acid in the concentrations
previously reported to be in these extracts results in mortality similar to
that reported in our study (unpublished results).
Whilst toxicity was assessed in this study with the test organism
A. franciscana, toxicity towards A. franciscana has previously been
shown to correlate well with toxicity towards human cells for many toxins.
true for the Syzygium spp. extracts examined in these studies. Toxic
anti bacterial extracts may still be useful as non-medicinal antibacterial
agents (eg. surface disinfectants and topical antiseptics). Likewise, toxic
plant extracts may also still have medicinal potential even if they are not
antimicrobial. Previous studies have demonstrated that toxicity in the
A. franciscana bioassay may indicate anti-cancer potential.
extracts has been reported against CaCo2 and HeLa human cancer cell
indicating that these extracts may also have potential in the devel-
The results of this study indicate that the Syzygium spp. extracts examined
warrant further study due to their
activity. Conversely, the toxicity detected for these extracts indicates
that further toxicity studies are required to evaluate the safety of these
extracts for medicinal usage. Whilst the extracts examined in this report
have potential as
growth inhibitory agents, caution is
needed before these compounds can be applied to medicinal purposes.
Purification and identification of the bioactive components is needed to
examine the mechanisms of action of these agents.
The results of this study demonstrate the potential of S. australe and
S. leuhmannii fruit and leaf extracts to inhibit C. perfringens growth.
As the fruit and leaves of these Syzygium species are edible and are used
as a culinary agent, they have potential in the prevention and treatment
of clostridial myonecrosis and enteritis necroticans. However, before
being acceptable for therapeutic uses, further cell line toxicity studies
are required to verify the safety of these extracts. Furthermore, studies
aimed at the purification and identification of the bioactive components
arerequired to examine the mechanisms of action of these extracts.
Financial support for this work was provided by the Environmental
Futures Research Institute and the School of Natural Sciences, Griffith
The authors report no conflicts of interest.
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S. australe and S. luehmannii leaf and fruit extracts inhibit C. perfringens
Aqueous and methanolic extracts were particularly potent with MIC’s
S. australe fruit extracts and the ethyl acetate extracts from both Syzy-
All S. luehmannii aqueous and methanolic extracts as well as the S. aus-
trale leaf extracts, displayed substantial toxicity.
Syzygium spp. extracts have therapeutic potential in the prevention and
oxidation characteristics of environmental bacteria. He is currently a postdoctoral researcher at Griffith University,
Australia, where he is working on several projects both in the areas of Geomicrobiology and Pharmacognosy.
His present research interests are the use of bacteriogenic manganese oxides in the bioremediation of metal-
contaminated sites as well as the use of Australian native plants in the treatment and prevention of various patho-
genic bacteria. Dr Wright’s interests include wearing silly hats and supporting bad football teams.
his PhD in Microbiology from the University of New South Wales and focuses on extreme environments, bio-
remediation and Geomicrobiology. His specific interests include the microbial ecology of thermophilic, saline
and alkaliphilic environments and the mechanisms and industrial potential of extremophilic bacteria contained
Dr. Ian Cock: Leads a research team in the Environmental Futures Research Institute and the School of Natural
Sciences at Griffith University, Australia. His research involves bioactivity and phytochemical studies into a
variety of plant species of both Australian and international origin, including Aloe vera, South Asian and South
American tropical fruits, as well as Australia plants including Scaevola spinescens, Pittosporum phylliraeoides,
Terminalia ferdinandiana (Kakadu plum), Australian Acacias, Syzygiums, Petalostigmas and Xanthorrhoea john-
sonii (grass trees). This range of projects has resulted in nearly 200 scientific publications in a variety of peer
reviewed journals. Unlike Dr Wright who enjoys wearing silly hats, Dr Cock is wearing the hat in this photo due
to a lost wager.