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Hindawi International Journal of Zoology Volume 2018, Article ID 9407962, 6 pages https://doi.org/10.1155/2018/9407962 Research Article In Vitro Antibacterial Potential of Extracts of Sterculia africana, Acacia sieberiana,and Cassia abbreviata ssp. abbreviata Used by Yellow Baboons (Papio cynocephalus) for Possible Self-Medication in Mikumi National Park, Tanzania 1,2 3 2 4 Irene Kirabo , Faith P. Mabiki, Robinson H. Mdegela, and Christopher J. D. Obbo Natural Chemotherapeutics Research Institute, Ministry of Health, Kampala, Uganda Faculty of Veterinary Medicine, Sokoine University of Agriculture, Morogoro, Tanzania Department of Chemistry and Physics, Solomon Mahlangu College of Science and Education, Sokoine University of Agriculture, P.O. Box 3038, Morogoro, Tanzania Department of Biological Sciences, Kyambogo University, P.O. Box 1, Kampala, Uganda Correspondence should be addressed to Irene Kirabo; firstname.lastname@example.org Received 12 July 2017; Revised 27 November 2017; Accepted 29 January 2018; Published 22 February 2018 Academic Editor: George A. Lozano Copyright © 2018 Irene Kirabo et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. In the animals in general and nonhuman primates in particular self-medication has been widely reported; however, little is still known about the pharmacological activity of the extracts present in their daily diet. eTh in vitro antibacterial activity of the stem, root bark, and leaf extracts of three selected plants on which yellow baboons feed in an unusual manner in Mikumi National Park, Tanzania, was evaluated. Crude plant extracts were tested against Gram positive and Gram negative bacteria of medical and veterinary importance employing a modified agar well diffusion method and Minimum Inhibitory Concentration (MIC) technique. The lowest MIC value for Gram positive strains was 0.31 mg/ml demonstrated by Cassia abbreviata ssp. abbreviata against Staphylococcus aureus (ATCC 25923). The highest susceptibility to the ethanol plant extracts was exhibited by Pseudomonas aeruginosa, Escherichia coli, and Staphylococcus aureus, examples of microbes that affect both human and nonhuman primates. These findings demonstrate that the plant extracts from Sterculia africana, Acacia sieberiana, and Cassia abbreviata ssp. abbreviata have antibacterial activity and may be used as feed for their prophylactic benefits. Remarkably, the lowest MIC of 0.16 mg/ml was only 16-fold weaker than Gentamicin, a standard drug. 1. Introduction infection of the individual at the time of ingestion of a putative medicinal plant [5, 6, 8], and a subsequent positive There is a growing body of evidence to support the theory change in this condition following ingestion [7, 9, 10]. Fur- that animals are self-medicated by ingesting plants of both thermore, it has been suggested that compounds found in the nutritional and medicinal value [1–5]. A Tanzanian medicine ordinary diet of animals may have important positive eeff cts man, Babu Kalunde, almost a century ago, was able to on health and may prevent risks of infection and illness [2, 11]. treat a dysentery-like illness by observing a porcupine with Chemical investigations of the self-medication hypothesis similar symptoms ingesting the roots of mulengelele,a plant have found that the bitter pith of Vernonia amygdalina has previously believed to be toxic . Some of the evidence for chemical compounds that apparently are responsible for the self-medication by African great apes includes the infrequent control of nematode infections . Diospyros abyssinica, intake of plant species which are not a regular part of the diet, Uvariopsis congensis, Albizia grandibracteata, and Trichilia rubescens are only a few of the plants present in the nonpri- restriction of plant use to seasons or other periods associated with high risk of parasitic infection [5–7], illness, or parasite mate diet that have been tested for biological activity [13, 14]. 2 International Journal of Zoology Among the plants eaten by yellow baboons (Papio uterine problems and to improve lactation after child birth cynocephalus) inside Mikumi National Park, Tanzania, are . Laboratory studies on Acacia sieberiana reveal that it is Acacia sieberiana (Mimosaceae family), Sterculia africana effective against Bacillus subtilis, Staphylococcus epidermidis, Escherichia coli, Staphylococcus aureus, Klebsiella pneumo- (Sterculiaceae family), and Cassia abbreviate ssp. abbreviata (Caesalpiniaceae family), the focus of this study. The leaves niae, and Mycobacterium avium. Preliminary phytochemical and stem bark of Acacia sieberiana and the stem bark of screening showed presence of saponins, tannins, cardiac gly- cosides, flavonoids, and anthraquinones [31, 32]. The crushed Cassia abbreviata ssp. abbreviata and Sterculia africana were observed to be feed of the yellow baboons. On three separate pods are used in the treatment of hypertension in the Blue occasions while observing yellow baboons, only one or two, Nile state in Sudan . as opposed to the whole group, would stop and feed on the This study was undertaken to establish the antibacterial leaves or stem bark of these plants and then join up with the activity of Cassia abbreviata ssp. abbreviata, Acacia sieberi- an rest of the group. A video of this phenomenon was recorded a,and Sterculia africana against Gram positive and Gram on one of these visits. However, though not observed to be negative bacteria of medical and veterinary concern. Results consumed, the roots of all three plants and leaves of Cassia observed may contribute to knowledge on the range of abbreviata ssp. abbreviata were analysed as well. microbes susceptible to these plant extracts using a single A number of studies have been conducted on Cassia solvent. abbreviata Oliv. , a close relative of Cassia abbreviata Furthermore, results from this study may shed more light ssp. abbreviata, endemic to Morogoro region from where on the existing knowledge gap about the therapeutic benefits this sample was taken [16, 17]; however there is a dearth of of plant metabolites present in the nonhuman primates’ literature on Cassia abbreviata ssp. abbreviata.In Bukoba diet. A combined understanding of the underlying wildlife and Morogoro, Tanzania, the root bark of Cassia abbreviata behaviour with long-term dietary data, antimicrobial studies, ssp. abbreviata is used in the treatment of oral and vaginal and analysis of plant chemistry will contribute to better candidiasis particularly in HIV/AIDS patients [18, 19]. understanding of the animal self-medication theory. Sterculia africana is valued in the study area for traditional worship and is one of the plants associated with ancestral 2. Materials and Methods sacrifices in Tanzania . Sterculia africana root is used to 2.1. Plant Collection and Processing. Plant materials were col- treat asthma in communities around Lake Victoria region in lected from areas around Sokoine University of Agriculture Tanzania  and also possesses strong antifungal activity main campus and areas around Mikumi National Park in . The Maale and Ari communities in Ethiopia utilize Morogoro region, Tanzania, the location of which is shown Sterculia africana as an antiemetic and to treat food poisoning in Figure 1. The samples were collected in the month of as well as treating fever in the Blue Nile state, Sudan [22, 23]. September during a dry spell when Sterculia africana had Sterculia africana is one ofthe sourcesofnontraditional seed shed its leaves and therefore these were not studied. oils in Botswana  and is widely used in African traditional The samples were collected during morning hours and medicine. In Somalia a decoction of the crushed fresh root authenticated with the help of Mr. Frank Mbago, a Botanist is drunk as an anthelmintic. In Tanzania a root decoction is from the University of Dar es Salaam. They were assigned taken to treat back pain, hernia, and dizziness, a root infusion voucher specimen numbers FMM 3704, 3705, and 3706 for is drunk as an aphrodisiac, and leaf decoctions are drunk for Acacia sieberiana, Sterculia africana, and Cassia abbreviata treating fungal infections and convulsions . In parts of ssp. abbreviata, respectively. From Sterculia africana, the root East Africa the roots, bark, and leaves are boiled and the vapor bark and stem bark were collected while Cassia abbreviata is inhaled for the treatment of influenza and fever. In Namibia ssp. abbreviata and Acacia sieberiana samples consisted of the a root or bark decoction is drunk by women for the treatment stem bark, root bark, and leaves. The 8 samples were cleaned; of postnatal and stomach pains, a leaf infusion is drunk for the stem bark and root bark were cut into smaller pieces to treating cough and chest complaints, and a fruit decoction allow for better drying in air. After drying, the samples were is drunk to relieve pain during pregnancy and aer ft giving pulverised to a particle size of 1 mm. birth. In Malawi the irritant hairs along the splitting point of the fruits are reported to be burnt and the ash is used in an ointment for the treatment of eye infections, especially in 2.2. Extraction of Samples. In the chemistry laboratory at babies . Mazimbu Campus, Sokoine University of Agriculture, Tanza- Acacia sieberiana has been utilized traditionally for treat- nia, one sample was handled at a time in order to avoid cross ment of skin eruptions and rheumatic pains and in treatment contamination. Using a Yanhe Analytical Electronic Balance, of syphilis, gastritis, cough, fever, ringworm, leprosy, epilepsy, the dry samples each were weighed into a separate clean, dysentery, and mouth ulcers, as a vermicide and contra- marked plastic container of known weight and the sample ceptive . Communities in South Africa and Ethiopia weight was recorded. The menstruum used was ethanol traditionally utilize Acacia sieberiana for the treatment of var- (Sigma-Aldrich) of analytical grade which was added till all ious ailments including inflammation, tiredness, joint pains, the sample was fully soaked and macerated for 3 days with bilharzia, and fever and as an enema [28, 29]. The stem and constant shaking. The samples were then strained and filtered root bark extract, both rich in tannins, are used in treating using 110 mm Whatman lfi ter paper and excess menstruum schistosomiasis, fever, stomach ache, jaundice, cough, sexual was evaporated using a rotary evaporator and then finally impotence, erectile dysfunction, haemorrhoids, syphilis, and transferred to dry in an oven (Shel Lab) till constant weight. International Journal of Zoology 3 Table 1: Codes of the extracts used during this study. Name of plant Code of plant Plant part (p p) Code of pp Leaves A.L Acacia sieberiana A Stem bark A.S Root bark A.R Leaves B.L Cassia abbreviata ssp. abbreviata B Stem bark B.S Root bark B.R Stem bark C.S Sterculia africana C Root bark C.R Figure 1: A map of Tanzania showing the location of Mikumi National Park and Morogoro region. The marc was resoaked in fresh ethanol for 3 days and Bacterial strains used in this study were standardized treated as the previous samples and then dried before being by the American Type Cell Collection (ATCC/Manassas, added to the corresponding samples. The crude plant extracts VA/USA) and constituted of Gram negative and Gram were then codedas shown in Table 1 andstored at room positive bacteria. The Gram negative bacteria tested were temperature before use for subsequent analysis. Salmonella paratyphi (ATCC 9150), Klebsiella pneumoniae (ATCC 13883), Shigella sonnei (ATCC 25931),Enterobacter 2.3. Antibacterial Screening cloacae (ATCC 23355), Pseudomonas aeruginosa (ATCC 27853), and Escherichia coli (ATCC 25922). Gram positive 2.3.1. Test Microorganisms. Agar well diffusion method was bacteria tested were Enterococcus faecalis (ATCC 51299) and used for preliminary analysis to screen for samples with Staphylococcus aureus (ATCC 25923). Bacterial culture cells antibacterial activity and thereafter MIC was used for anal- ysis. were maintained at 37 C on Muller-Hinton (MH) agar on 4 International Journal of Zoology Table 2: Minimum Inhibitory Concentration (mg/ml) of plant extracts. Code of plant part Test organism C.R C.S A.R A.S A.L B.R B.S B.L E. coli (ATCC 25922) 1.25 1.25 1.25 0.63 0.31 0.63 0.63 0.31 S. paratyphi (ATCC 9150) 0.63 0.63 0.16 0.16 0.31 0.31 0.63 0.31 K. pneumoniae (ATCC 13883) 0.63 1.25 2.50 0.63 2.50 1.25 1.25 2.50 S. sonnei (ATCC 25931) 2.50 2.50 2.50 2.50 0.31 1.25 1.25 0.63 E. cloacae (ATCC 23355) 2.50 0.63 1.25 1.25 1.25 1.25 1.25 0.63 P. aeruginosa (ATCC 27853) 0.63 0.63 0.16 0.16 0.31 0.31 0.63 0.31 S. aureus (ATCC 25923) 0.63 0.63 0.63 0.63 0.63 0.31 0.63 0.31 E. faecalis (ATCC 51299) 0.63 1.25 2.50 0.63 2.50 1.25 1.25 2.50 slants until required. All microbial species used were supplied to 2.5 mg/ml with 0.16 mg/ml being the lowest value denoting by the Department of Microbiology, Muhimbili University of the greatest antibacterial efficacy as presented by A.R and A.S Health and Allied Sciences, Dar es Salaam, Tanzania. plant parts. Gram negative bacteria in the ethanol extracts had higher MIC values as opposed to the Gram positive 2.3.2. Minimum Inhibitory Concentration (MIC). The Min- bacteria. A.R and A.S demonstrated the lowest MIC values of imum Inhibitory Concentration (MIC) is the lowest con- 0.16 mg/ml and 0.31 mg/ml for both Pseudomonas aeruginosa centration of crude plant extract that inhibits growth of test and Klebsiella pneumoniae strains. The lowest MIC value for microorganisms. A modified method by  was employed Gram positive strains was 0.31 mg/ml demonstrated by B.R in determining the MIC of the different sample extracts. and B.L against Staphylococcus aureus. Overall, plants A and Sterile 100𝜇 l of Muller-Hinton broth was measured in each B presented lower MIC values as opposed to plant C. The well of a 96-well microtiter plate . 100𝜇 lof 10mg/ml of experiments were performed in duplicate and the average extract prepared in dimethyl sulfoxide (DMSO) was added to value was tabulated in Table 2. row 1 and mixed using a micropipette. This was followed by serial dilution to row 8 with the additional 100𝜇 ltherein dis- carded. One column was used for sterility control (no culture 4. Discussion was added), another column was used as a negative control Cassia abbreviata ssp. abbreviata, Acacia sieberiana, and Ster- (100𝜇 l of DMSO without extract), and another column was culia africana extracts possess antibacterial activity against used as the positive control with Gentamicin (0.01 mg/ml) the test strains as shown from the results of the in vitro making a total of 12 rows. 0.5 McFarland standard suspension experiment in Table 2. Cassia abbreviata ssp. abbreviata of test bacteria was made in nutrient broth from which and Acacia sieberiana exhibited better activity against the 100𝜇 l of the final inoculums containing approximately 1 × test microorganisms as compared to Sterculia africana with 10 cfu/ml was added to each well except the sterility control Cassia abbreviata ssp. abbreviata showing the lowest MIC to make a final volume of 200 𝜇 l. The experiments were value of 0.16 mg/ml of the three plants. The positive control performed in duplicate. The microtiter plates were sealed in was a standard drug, Gentamicin (0.01 mg/ml), an amino- a plastic film and then incubated at 37 Cinahumidiefi d glycoside targeting the bacterial ribosome. Interestingly, the incubator for 18 hrs. After incubation, 40 𝜇 l of 0.2 mg/ml lowest crude plant extract MIC of 0.16 mg/ml was only 16- iodonitrotetrazolium (INT) was added to each well and the fold weaker than Gentamicin. The crude plant extracts per- microtiter plates were incubated for another 2 hours before formed better than the negative control to a concentration of removal for observation. The development of a purple colour 0.313 mg/ml of extract. Other studies that reported on Cassia resulting from the formation of the red/purple formazan was abbreviata ssp. abbreviata and Acacia sieberiana concur with an indication of growth (positive indicator of cell viability). these findings [16, 17, 30]. A viable challenge in interpreting Decrease in the intensity of the red/purple formazan colour self-medication is differentiating between plants that are was indicative of inhibition of growth of test microorganisms. ingested for their nutritional value but are medicinal foods and therefore oer ff passive prevention and plants ingested 3. Results solely for their therapeutic medicinal use, medicinal plants. The MIC results tabulated in Table 2 showed that the crude This challenge exists in traditional human societies where plant extracts were active against all the test microorganisms. medicine and food are oeft n of the same origin [2, 3, 28, The lowest MIC value was 0.16 mg/ml as compared with 34]. For instance, traditional spices and condiments of daily 0.01 mg/ml of the standard, Gentamicin. The negative control Asian cuisine such as marine algae, ginger root, turmeric and herbs also play an important role in suppressing viral and showed development of a purple colour resulting from for- mation of the purple formazan which is a positive indicator parasite infections [2, 34, 35]. Results showed that different of cell viability whereas the sterility control showed no colour concentrations of the plant extracts were required to inhibit change, an indication of absence of test microorganisms. the growth of different microbes due to the difference in Minimum Inhibitory Concentration ranged from 0.16 mg/ml potency of the plant extracts attributed to the phytochemicals International Journal of Zoology 5 present, environment of growth, or extraction method used. Acknowledgments The variation in the susceptibility of microorganisms could The authors acknowledge INTRA-ACP mobility scholarship also be attributed to their intrinsic properties that are related and RISE-AFNNET for partially funding this research and to the permeability of their cell surface to the plants extracts. the Faculty of Veterinary Medicine, Sokoine University of Their pharmacological eeff ct could therefore be experienced Agriculture, for facilitating this study. They thank in a special with repeated ingestion or work together in synergy. way Mr. Mwesongo James, Mr. Frank Mbago, and Ms. Anna This study provides evidence that the yellow baboon Mpanyakavili for their invaluable help. Safari Bookings is also forages for similar plants also used in ethno medicine as acknowledged for the map of Mikumi National Park. seen from previous literature reviewed [16, 17, 22, 23]. 27.5% of microbes that aec ff t nonhuman primates aeff ct humans as well, Staphylococcus aureus, Salmonella,and Escherichia References coli being only a few examples of such microbes, a factor  V. Carrai, S. M. Borgognini-Tarli, M. A. Huffman, and M. attributed to our phylogenetic closeness [4, 12, 36, 37]. 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