South African Journal of Botany 72 (2006) 232 – 237

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Antibacterial, antifungal and antitubercular activity of (the roots of)

Pelargonium reniforme (CURT) and Pelargonium sidoides (DC)
(Geraniaceae) root extracts
S.P.N. Mativandlela, N. Lall *, J.J.M. Meyer
Department of Botany, University of Pretoria, Pretoria 0002, South Africa

Received 10 May 2005; accepted 26 August 2005

Abstract

Root extracts of Pelargonium reniforme CURT and Pelargonium sidoides DC were evaluated for antibacterial and antifungal assays using the
agar dilution while antitubercular assays were done using the BACTEC method at concentrations ranging from 5  103 to 500.0 mg/L. The ethanol
and acetone extracts of the roots of P. sidoides inhibited the growth of Haemophilus influenzae, Moraxella catarrhalis and Streptococcus
pneumoniae at a concentration of 5  103 mg/L. Both acetone and ethanol extracts of P. reniforme and only the ethanol extract of P. sidoides
inhibited the growth of Aspergillus niger and Fusarium oxysporum significantly at a concentration of 5  103 mg/L. Growth of Rhizopus
stolonifer was suppressed by the ethanol extract of P. reniforme and P. sidoides at 5  103 and 1 103 mg/L, respectively. Acetone, chloroform
and ethanol extracts of P. reniforme showed activity against M. tuberculosis exhibiting a minimum inhibitory concentration of 5  103 mg/L.
D 2006 SAAB. Published by Elsevier B.V. All rights reserved.

Keywords: Antibacterial; Antifungal; Extracts; Mycobacterium tuberculosis; Pelargonium

1. Introduction Africa use these species to treat coughs, diarrhoea and

tuberculosis (Watt and Breyer-Brandwijk, 1962). The medic-
The importance of Pelargonium species (Geraniaceae) is inally active ingredients are found in the bitter tasting roots of
well documented (Watt and Breyer-Brandwijk, 1962; Hutch- the plants (Helmstadter, 1996). A commonly used medicine
ings, 1996). The genus Pelargonium comprises more than 250 produced in Germany, named, FUmckaloabo_ originates from
natural species of perennial small shrubs, which are limited in the roots of P. sidoides and P. reniforme (Helmstadter, 1996;
their geographical distribution. About 80% of Pelargonium Kayser et al., 1998). This herbal medicine is extensively used
species are confined to the southern parts of Africa, while in Germany for bronchitis, antibacterial and antifungal infec-
others occur in Australia, New Zealand and the Far East. These tions. Although this herbal medicine (UmckaloaboR) is
species usually grow in short grassland and sometimes with successfully employed in modern phytotherapy in Europe to
shrubs and trees on stony soil varying from sand to clay-loam, cure infectious diseases of the respiratory tract, the scientific
shale or basalt. The plants are evergreen when cultivated, but basis of its remedial effect is still unclear (Kayser and
die back in nature during droughts and winter (May to August) Kolodziej, 1995).
(Van der Walt and Vorster, 1985). Bacteria, which are associated with either primary or
Pelargonium reniforme CURT and Pelargonium sidoides secondary infections of bronchitis, are Streptococcus pneumo-
DC are highly valued by traditional healers for their curative niae, Haemophilus influenzae and Moraxella catarrhalis. H.
properties and they are well known to generations of Khoi/San influenzae, a Gram-negative bacterium, is an obligate human
and Xhosa (South African tribes) traditional healers (Wagner parasite that is passed from person to person by way of the
and Bladt, 1975). The Xhosa and the Zulu tribes of South respiratory route. M. catarrhalis, a Gram-negative bacterium,
causes bronchitis and pneumonia in children and adults. S.
* Corresponding author. pneumoniae, a Gram-positive bacterium, infects the upper
E-mail address: [email protected] (N. Lall). respiratory tract and can cause pneumonia, also it can infect the
0254-6299/$ - see front matter D 2006 SAAB. Published by Elsevier B.V. All rights reserved.
doi:10.1016/j.sajb.2005.08.002
 S.P.N. Mativandlela et al. / South African Journal of Botany 72 (2006) 232 – 237 233

lining of the brain-spinal cord (meningitis), bones (osteomy- respectively. Seider and Taylor (2004) investigated the two
elitis), joints (arthritis), ears (otitis media) and sinuses (sinusitis plant species against rapidly growing mycobacteria (M.
and bronchitis) (Benjamin et al., 1991). aurum and M. fortuitum, M. phlei, M. abscessus and M.
Apergillus niger, Fusarium oxysporum and Rhizopus smegmatis). This is the first report on antitubercular activity
stolonifer are some of the fungal pathogens that can affect of these plants extracted using various solvents such as
the respiratory tract. A. niger, is a causative agent of pulmonary chloroform, acetone and ethanol against M. tuberculosis using
diseases including aspergillosis, bronchial asthma and acute BACTEC radiometric method.
allergic alveolitis. The fungus colonizes old tuberculosis or
bronchiostatic cavities, in which it forms a large colony 2. Materials and methods
(aspergilloma); or it may actually invades the lung tissue to
produce haemorrhagic and necrotizing pneumonia (MacSween 2.1. Plant material
and Whaley, 1992). F. oxysporum is responsible for fusariosis,
skin infection, respiratory tract infections (tuberculosis and Roots of P. reniforme and P. sidoides were collected from
bronchitis) and arthritis and produces a 76% mortality rate in Qwaqwa, a region in the Free State province of South Africa.
hospitalised immunocompromised patients (Monier et al., Voucher specimens of P. reniforme (P 092558) and P. sidoides
1994). R. stolonifer causes mucorosis disease and it has been (P 092559) were deposited and identified at the H.G.W.J.
reported that exposure to large numbers of Rhizopus spores can Schweickerdt Herbarium (PRU), University of Pretoria, South
cause respiratory complications (Alexopoulos et al., 1996). Africa.
Previously, researchers have reported antimicrobial activity
of extracts of Pelargoniums and their constituents against a few 2.2. Preparation of extracts
bacterial (Staphylococcus aureus, S. pneumoniae, Escherichia
coli, Klebsiella pneumoniae, Proteus mirabilis, Pseudomonas Air-dried and powdered roots of P. reniforme and P.
aeruginosa and H. influenzae), and fungal (Microsporum sidoides (300 g each) were extracted three times with 1 L of
canis, M. gypseum, A. fumigatus, Mucor racemosus, R. acetone, chloroform and ethanol separately for 2 h at room
nigricans) pathogens as well as opportunistic yeasts such as temperature. The extracts were filtered through Whatman No.
Candida albicans, C. glabrata, C. krusei and Cryptococcus 1 filter paper and concentrated with a rotary vacuum
neoformans (Kolodziej, 2000; Kolodziej et al., 2003; Latté and evaporator (Büchi Laboratoriums, Technik AG, Germany) to
Kolodziej, 2000). Plant extracts of P. reniforme and P. sidoides dryness at reduced pressure. For antibacterial and antifungal
have not been tested against the fungal pathogens, A. niger, F. assays, acetone and ethanol extracts were dissolved in
oxysporum, R. stolonifer and the Gram-negative bacteria M. acetone to a concentration of 5  104 and 1 105 mg/L,
catarrhalis, which are indirectly responsible for secondary respectively. For the antitubercular assay, all (3) extracts were
infections in cases of bronchitis and tuberculosis. In the present dissolved in dimethyl sulphoxide (DMSO) to a concentration
study, we have investigated their antimicrobial activity against of 5  105 mg/L.
the bacteria and fungi mainly responsible for bronchitis. We
have also confirmed the findings of other researchers on the 2.3. Microorganisms and in vitro antimicrobial assays
antibacterial activity of these species against S. pneumoniae
and H. influenzae. 2.3.1. Bacteria
Tuberculosis (TB) kills approximately 2 million people The bacteria used in this investigation H. influenzae (UPM
each year, the global epidemic is growing and becoming more 2), M. catarrhalis (UPM 4), and S. pneumoniae (UPM 9) were
problematic. The breakdown in health services, the spread of clinical isolates which were obtained from the Department of
HIV/AIDS and the emergence of multidrug-resistant strains of Pathology, University of Pretoria, South Africa. Cultures were
Mycobacterium tuberculosis (MDR) TB are contributing to maintained on Colombia agar (Oxoid, Basingstoke, UK) slants
the worsening impact of this disease. It is estimated that supplemented with 5% horse blood to form chocolate agar. For
between 2002 and 2020, approximately a billion people will assays, organisms were subcultured once and incubated at
be newly infected, more than 150 million people will get sick, 37 -C on Mueller-Hinton (MH), (BIOLAB, Merck, South
and 36 million will die of TB. The current threat in TB Africa) agar for 24 h.
treatment lies in the emergence of strains resistant to two of
the best antitubercular drugs, isoniazid (INH) and rifampicin 2.3.2. Antibacterial assay
(RIF). The current TB-treatment comprises of 3– 4 drugs for a For the antibacterial assay, the minimum inhibitory con-
period of 6 –9 months (Bloom, 2002). Novel drugs are centrations (MIC which is defined as the lowest concentration
required which can shorten this long-treatment period and of the extract that inhibits more than 99% of the bacterial
target multidrug resistant strains of TB. Previous studies have population) of the acetone and ethanol extracts were deter-
investigated the anti-TB and antimycobacterial activity of the mined by incorporating various amounts (5  103, 1 103 and
two Pelargonium species. Kolodziej (2000) and Kolodziej et 500.0 mg/L) of the extracts into chocolate agar in sterile bottles
al. (2003) tested acetone extract of both plant species against and placed in a water bath (50 -C) to prevent solidification,
M. tuberculosis using Alamar blue assay and acetone extracts then withdrawn into Petri dishes and left to solidify for 4 h. The
of P. sidoides using the BACTEC radiometric system, bacterial colonies were transferred into the sterile screw-capped
234 S.P.N. Mativandlela et al. / South African Journal of Botany 72 (2006) 232 – 237

round tubes with glass beads to which 5 ml of the saline (0.9% BACTEC 12B vials containing 4 ml of 7H12 medium broth to
w/v NaCl) was added for achieving McFarland No. 1 turbidity achieve the desired final concentrations of 5000.0, 2500.0,
standard (108 CFU/ml). A hundred microlitres of each 1000.0 and 500.0 mg/L together with PANTA (Becton
suspension was smeared on Petri dishes containing the extracts Dickinson and Company, Ferndale, South Africa), an antimi-
and the chocolate agar. The plates (three replications) were crobial supplement.
incubated at 37 -C for 24 h and antimicrobial activity was Control experiments showed that a final concentration of
evaluated thereafter. Streptomycin sulphate (Sigma Chemical DMSO (1%) in the medium had no adverse effect on the
Co., South Africa) was added to the chocolate agar plates (final growth of M. tuberculosis. Streptomycin, isoniazid, rifampicin
concentrations of 500.0, 10.0 and 50.0 mg/L) and served as a and ethambutanol (Sigma Chemical Co., South Africa), were
positive control. Three Petri dishes containing only 200 Al used as positive drug controls. A homogenous culture (0.1 ml)
acetone mixed with chocolate agar served as negative controls. of M. tuberculosis, yielding 1 104 to 1 105 colony-forming
The highest concentration of acetone (4%) did not affect the units per millilitre (CFU ml 1), was inoculated in the vials
growth of any of the organisms. containing the extracts as well as in the control vials (Heifets et
al., 1985). Three extract-free vials were used as controls
2.3.3. Fungi (medium + 1% DMSO): two vials (V1) were inoculated in the
The fungal pathogens used in the study, A. niger (UPFC same way as the vials containing the extracts, and one (V2) was
13), F. oxysporum (UPFC 97) and R. stolonifer (UPFC 312) inoculated with a 1:100 dilution of the inoculum (1:100
were from culture collection at the Department of Microbiol- control) to produce an initial concentration representing 1%
ogy and Plant Pathology, University of Pretoria, South Africa. of the bacterial population (1 102 to 1 103 CFU ml 1). The
Each fungus was maintained on Potato Dextrose Agar (PDA), MIC was defined as the lowest concentration of the extract that
(BIOLAB, Merck, South Africa) for 7 days at T25 -C. inhibited > 99% of the bacterial population.
Mycobacterium growing in 7H12 medium containing 14C-
2.3.4. Antifungal assay labelled substrate (palmitic acid) use the substrate and
For the antifungal assay, the required amount of acetone and produced 14CO2. The amount of 14CO2 detected (reflecting
ethanol extracts were added to sterile PDA in 5 ml Petri dishes the rate and amount of growth occurring in the sealed vial) is
before congealing to yield final concentrations of 5  103, expressed in terms of the growth index (GI) (Middlebrook et
1 103 and 500.0 mg/L. PDA plates with acetone alone al., 1977). Inoculated bottles were incubated at 37 -C and each
inoculated with fungi served as growth controls. Once the agar bottle was assayed everyday to measure GI, at about the same
had solidified, a 5-mm plug of a 7-day-old fungal culture was hour(s) until cumulative results were interpretable. The
placed in the centre of the Petri dish containing the extract- difference in the GI values of the last two days is designated
amended and unamended PDA plates. The plates were sealed as DGI. The GI readings of the vials containing the test extracts
with parafilm and placed in a 25 -C incubator. Fungal growth were compared with the control vials (V2). Readings were
was measured on two diametric lines after 3, 6 and 9 days of taken until the control vials, containing a hundred times lower
growth. Each treatment was replicated three times and results dilution of the inoculum than the test vials, reached a GI of 30
expressed as the mean of three replicates. The results of 6 days or more. If the DGI values of the vials containing the test
growth was statistically analysed using analysis of variance extracts were less than the control vials, the population was
(ANOVA) and comparison of means by Duncan’s Multiple reported to be susceptible to the compound. Each test was
Range Test. The antifungal agent amphotericin B (Fluka, replicated three times.
Germany) added to the agar plates (final concentration of 0.5, Whenever results suggested contamination (e.g. large, rapid
1.0 and 2.0 mg/L) served as a positive control. The highest increase in GI), bottles were inspected and the organisms were
concentration of acetone (4%) did not affect any of the stained by Ziehl-Neelsen stain to determine whether the visible
organisms. microbial growth was a mycobacterial organism (Kleeberg et
al., 1980). With this stain, the bacilli appear as brilliantly
2.4. M. tuberculosis stained red rods against a deep sky-blue background. Organ-
isms often have a beaded appearance because of their
A drug-susceptible strain of M. tuberculosis, H37Rv polyphosphate content and unstained vacuoles (Joklik et al.,
obtained from American Type, MD, USA Culture Collection 1968).
(ATCC, 27294), was used (to investigate the activity of the Since anecdotal evidence suggests the use of a combination
plant extracts). of ethanol extracts of two Pelargonium species (1:1) combined
ethanol and acetone root extracts from both species were
2.4.1. Antitubercular assay screened for antitubercular activity.
The radiometric respiratory technique using the BACTEC
system was used for susceptibility testing against M. tubercu- 3. Results and discussion
losis as described previously (Lall and Meyer, 2001; Lall et al.,
2003). Solutions of all the extracts were prepared in DMSO to It was found from the antibacterial assay that the ethanol
obtain a concentration of 5  105 mg/L and stored at 4 -C until and acetone extracts of P. sidoides and its combination (1:1 to
used. Subsequent dilutions were made in DMSO and added to investigate additive effect) with P. reniforme was active at
 S.P.N. Mativandlela et al. / South African Journal of Botany 72 (2006) 232 – 237 235

5  103 mg/L against H. influenzae, M. catarrhalis and S. positive bacteria such as S. aureus, Proteus vulgaris, Bacillus
pneumoniae. Complete inhibition activity of three bacteria on cereus, and S. epidermidis (Lis-Balchin et al., 1998a, 2003).
exposure to Streptomycin sulphate was observed at 10.0 mg/L. The acetone and ethanol root extracts of P. reniforme and
Kayser and Kolodziej (1997), found moderate activity of P. ethanol root extract of P. sidoides showed activity against the
sidoides against S. pneumoniae and H. influenzae at concen- fungal pathogens at a concentration of 5  103 mg/L (Fig. 1a –
trations of 7.5  103 and 5  103 mg/L, respectively, by ethanol b). Activity of amphotericin B was observed on each fungi at
(70%) root extracts. There have been few reports of these 0.5 mg/L. Previous in vitro antifungal assays Latté and
bacterial organisms being susceptible to other plant extracts. Kolodziej (2000) had revealed that the aqueous acetone
Christoph et al. (2001) found antibacterial activity of Austra- extracts of the roots of P. reniforme were less potent exhibiting
lian tea tree oil from Melaleuca alternifolia (Cheel) and niaouli a MIC of 8  103 mg/L against the filamentous fungi
oil isolated from M. quinquenervia at 0.01 (%v v 1) against M. (Aspergillus fumigatus, Rhizopus nigricans, Penicillium itali-
catarrhalis. We found that acetone extracts of P. reniforme cum) and opportunistic yeasts tested. Lis-Balchin and Deans
were not active against these bacteria at the highest concen- (1996) assessed the methanolic extracts of representative
tration (5  103 mg/L) tested, similar to the findings of Magama species and cultivars of Pelargonium for activity against 25
et al., 2002, when testing Euclea crispa. Essential oils of P. different species of bacteria and A. niger. All samples were
graveolens were found to be inactive against Moraxella sp. active against at least 18 bacterial species and some were active
(Lis-Balchin et al., 1998b). Gram-negative bacteria have been against all 25 species, although there was very poor antifungal
found to be less susceptible to plant extracts in earlier studies action. Other plant extracts have been found to be antifungal
done by other researchers (Kuhnt et al., 1994; Afolayan and against the fungi tested in this study. Chandrasekaran and
Meyer, 1995). Essential oils from leaves of scented Pelargo- Venkatesalu (2004), investigated the water and methanol
nium species such as P. graveolens, P. tomentosum, P. extracts of Syzygium jambolanum for antifungal activity
odaratissimum, P. denticulatum and P. ficifolium have been against A. niger and R. stolonifer and the highest zones of
found to possess good antibacterial activity against Gram- inhibition were recorded at 1 103 and 500.0 mg/L, respec-

(a)
60
*a
A.niger
50 a a
F.oxysporum
b
R.stolonifer
40 b
Growth (mm)

b bc

30 c c bc
c c
d
d
d d
20 d

10
e
0
Ac/Control Ac/500.0 Ac/1000.0 Ac/5000.0 Et/500.0 Et/1000.0 Et/5000.0
Sample (concentration mg/L)
(b)
60
*a a
a
A.niger
50 a
a a F.oxysporum
ab
ab R.stolonifer
a
40 ab
Growth (mm)

b b b b
b

30 c
c
20
c
10

0
Ac/Control Ac/500.0 Ac/1000.0 Ac/5000.0 Et/500.0 Et/1000.0 Et/5000.0
Sample (concentration mg/L)

Fig. 1. Antifungal activity of (a) P. reniforme acetone and ethanol extract and (b) P. sidoides acetone and ethanol extract. Results are expressed as a mean of three
replicates and are significantly different. *Values of the bars within the sample concentration not followed by the same letter are significantly different, P < 0.01.
Ac = acetone; Et = ethanol.
236 S.P.N. Mativandlela et al. / South African Journal of Botany 72 (2006) 232 – 237

Table 1 Acknowledgements
Antitubercular activity of Pelargonium root extracts against the drug sensitive
strain of Mycobacterium tuberculosis (H37Rv) determined by the BACTEC
radiometric method Thanks to Dr, Bernard Fourie and the technical assistants of
the Medical Research Council (Pretoria) and Mahdi Ziaratnia
Plant species Sensitive strain
for their assistance. The National Research Foundation
MICa (mg/L) DGIb values (mg/L)
supported the research financially.
3
Pelargonium reniforme (acetone) 5  10 1.5 T 0.7 (Sc)
P. reniforme (chloroform) 5  103 0.5 T 0.7 (S)
P. reniforme (ethanol) 5  103 2.5 T 0.7 (S) References
P. reniforme+P. sidoides (acetone) 5  103 1.0 T 2.8 (S)
P. reniforme+P. sidoides (chloroform) 5  103 1.0 T 0.0 (S) Afolayan, A.J., Meyer, J.J.M., 1995. Antibacterial activity of Helichrysum
P. reniforme+P. sidoides (ethanol) 5  103 1.5 T 0.7 (S) aureonitens (Asteraceae). Journal of Ethnopharmacology 47, 109 – 111.
P. sidoides (acetone) nad 35.5 T 6.3 (Re) Alexopoulos, C.J., Mims, C.W., Blackwell, M., 1996. Introductory Mycology,
P. sidoides (ethanol) na 276.0 T 9.89 (R) 4th ednR John Wiley and Sons, New York, USA, pp. 868 – 869.
P. sidoides (chloroform) na 18.5 T 4.94 (R) Benjamin, D.C., Kadner, R.J., Volk, W.A., 1991. Essential of Medical
Streptomycin 4.0 5.0 T 0.0 (S) Microbiology. (4th edn)J.B. Lippincott Company, Philadelphia, pp. 41 – 65.
Ethambutol 6.0 0.33 T 0.0 (S) Bloom, B.R., 2002. Tuberculosis—the global view. Journal of Medicine 346,
Rifampicin 0.2 0.0 T 0.0 (S) 1434 – 1435.
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Not active at highest concentration tested.
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