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In vitro antibacterial, non-cytotoxic and antioxidant activities of Boscia Senegalensis and Tapinanthus dodoneifolius, plants used by pastoralists in Cameroon

In vitro antibacterial, non-cytotoxic and antioxidant activities of Boscia Senegalensis and... In the Far North Region of Cameroon, pastoralists use the leaves of Boscia senegalensis and the stem of Tapinanthus dodoneifolius to treat common animal diseases. This study aimed to evaluate the in vitro antibacterial, non-cytotoxic and antioxidant potentials of these plants. To achieve this, four extracts (water, methanol, chloroform and hexane) of both plants obtained by successive fractionation were used. Antibacterial activities of the different extracts were evaluated against three bacterial reference strains including Gram-positive (Staphylococcus aureus) and Gram- negative bacteria (Escherichia coli and Salmonella typhi) using agar disc diffusion and broth dilution methods. Human colon cancer cells were used to screen their toxicity. 2,2-Ddiphenyl-1-picrylhydrazyl (DPPH) radical scavenging and ferrous ion chelating assays have been used to investigate the antioxidant activities of the best extract of each plant after antibacterial assay. A sensitive inhibitory effect was observed against S. aureus with hexane extract of B. senegalensis and methanolic extract of T. dodoneifolius. In addition, the results showed that both plant extracts are not toxic. The hexane and methanolic extracts of B. senegalensis and T. dodoneifolius, respectively, showed higher antioxidant activities, but the hexane extract demonstrate a strong hydrogen donating ability or the electron transfer reaction in comparison with vitamin C used as standard. This finding may support the traditional use of both plants for managing animal diseases in the Far North of Cameroon. Keywords: Antibacterial, Cytotoxic, Antioxidant, Boscia senegalensis, Tapinanthus dodoneifolius, Extract, Cameroon Introduction sales of their products or of the animals themselves in In many African countries where the livestock sector times of crisis, to raise funds needed to purchase food plays a prominent role in the economy especially for the and meet other family needs. rural population, animal diseases constitute one of the In some areas of those countries (i.e. South Africa, Far main hindrances (Mthi et al. 2018; Bolajoko et al. 2020). North of Cameroon), because of the lack of access to Animal diseases limit livestock production and product- veterinary drugs, and their mobility, many pastoralists ivity with significant impacts on animal health, public use traditional medicines for preventing and managing health and economies (McElwain and Thumbi 2017; animal diseases (Chitura et al. 2018). In fact, this trad- Chakale et al. 2021). Indeed, in these regions, livestock itional practice is continuing because pastoralists believe act as a “bank” for the provision of cash derived from that medicinal plants are efficient, available and easily accessible and animal health is a prerequisite for higher productivity (FAO (Food and Agriculture Organization * Correspondence: romsonbey@yahoo.fr 1 of the United Nations), 2013; Vougat et al. 2015). Re- Department of Animal Production, School of Veterinary Medicine and Science, University of Ngaoundere, Ngaoundere, Cameroon searchers are working on this subject matter to actually Full list of author information is available at the end of the article © The Author(s). 2022 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. Vougat Ngom and Foyet Pastoralism: Research, Policy and Practice (2022) 12:13 Page 2 of 8 confirm the potential of the plants used by livestock and Far North regions) (Kelly et al. 2016; Motta et al. farmers (Mostafa et al. 2018; Nordin et al. 2019). The in- 2018) where more than 80% of the national cattle, sheep creasing focus on natural products might be due to their and goat population are found (MINEPIA, 2009 Not reduced or non-cytotoxicity or low side effects compared published). However, due to its climate conditions, the with chemically synthesized drugs (Hyun et al. 2013). In Far North region has the majority of pastoralists of the addition, plant extract usage represents an important al- country. This region is characterized by a Sudano- ternative for the reduction of the use of drugs like anti- Sahelian climate. The average annual rainfall in this re- biotics, known to be the main trigger of the gion is about 700 mm. The temperatures are generally development and spread of antimicrobial resistance, a low in the rainy season and the nights in the dry season major global threat to human health (Dadgostar, 2019; between December and January (Dassou et al. 2015). Varona et al. 2020). That is especially important for de- veloping countries like Cameroon where stringent pol- Methods icies on antibiotic use are not fully in place (Mouiche Preparation of plant extracts et al. 2018). T. dodoneifolius was collected from the host plant Aca- Unfortunately, in Cameroon where livestock contrib- cia albida as a study has shown that the properties of T. utes significantly to the gross national product (MINE- dodoneifolius depended on its host plant (Idu et al. PIA 2009), no sufficient attention is focused on 2016). These plants were then identified and authenti- ethnoveterinary medicine. It is common knowledge that cated in the National Herbarium in Yaoundé in the Far North region of Cameroon, the region that (Cameroon) where the voucher specimens already has the second highest cattle population in the country, existed under the reference numbers 23137 SRF/Cam many cattle farmers and specially pastoralists treat their and 50271 HNC respectively for B. senegalensis and T. animals with plant extracts (Vougat et al. 2015; MINE- dodoneifolius. The extraction of both plant samples was PIA, 2019 unpublished). Due to the increasing import- done according to the scheme below (Fig. 1). Each parti- ance of such medicine to cattle farmers, our research tion was obtained after washing three times with the team seeks to analyse the plants used to control and solvent. Each dried fraction was kept in a freezer before treat animal diseases. Our previous study in the Far biological tests. North region of Cameroon consisted of investigating the plants used against one of the most common, frequent Antibacterial assay and recognizable infectious diseases (Foot and Mouth The antibacterial activity of both plants was evaluated by Disease or FMD) and evaluating the phytochemical com- using both qualitative and quantitative methods. position and antioxidant potentials of the two mostly used (Boscia senegalensis and Tapinanthus dodoneifo- Selected test bacteria lius) (Vougat et al. 2015). Thus, this study aims to Three bacterial strains were used for the study: Escheri- deepen the scope of analysis on these two plants which chia coli (ATCC 25922), Staphylococcus aureus (ATCC have a good phytochemical profile (Vougat et al. 2015; 29213) and an in house fully characterized Salmonella Idu et al. 2016). Both plants are also used in many coun- typhimurium. These bacteria are among the most com- tries to treat animal and human diseases (FMD, respira- mon foodborne bacteria in animal source food that tory tract infections, stomach ache, diarrhoea, dysentery, cause a variety of diseases in humans and animals (Ror- diabetes, epilepsy, hepatitis in humans) (Vougat et al. tana et al. 2021). Bacterial strains were grown and main- 2015; Mamman et al. 2019; Mohamed et al. 2020a). tained on Trypticase Soy Agar with 5% Sheep Blood Therefore, with due knowledge of their profile and im- plates (BD BBM™ Becton, Dickinson and Company, mense importance, this study was designed to evaluate Sparks, USA). Bacterial suspensions of 0.5 McFarland the antibacterial, non-cytotoxic and antioxidant poten- tials of B. senegalensis and T. dodoneifolius. Antimicro- bial activity is first screened because antibiotic drugs are the main veterinary medicine used by pastoralists in the study area (Vougat Ngom et al. 2017). The cytotoxic ac- tivity was evaluated to verify the safety of these plants. Study area The plants analyzed in this study were collected in the Far North region of Cameroon as previously described (Vougat et al. 2015). In Cameroon, pastoralists are Fig. 1 Scheme of the extraction mainly located in three regions (North West, Adamawa Vougat Ngom and Foyet Pastoralism: Research, Policy and Practice (2022) 12:13 Page 3 of 8 were prepared with sterile saline solution to inoculate inoculum (for bacteria 1 × 10 CFU/ml) was added to plates during the antibacterial assay. each tube. A tube containing 300 μl of TSB, 200 μlof solvent used for extract dilution and 20 μl inoculum was Extracts re-suspension and paper disc preparation used as a negative control. Each concentration was Sterile saline solution was used to dissolve extracts of B. assayed in duplicate. All the tubes were then incubated senegalensis obtained with methanol and water. For the at 37 °C for 24 h. After incubation, the tubes were then other extracts (hexane and chloroform extracts of B. examined for microbial growth by observing for turbid- senegalensis and all the T. dodoneifolius extracts), 15% ity. The MIC values were taken as the lowest extract dimethyl sulfoxide (DMSO) (Thermo Fisher Scientific concentration that showed no turbidity after incubation. Inc., Pittsburgh, USA) was used (Kawo et al. 2011; Kpadonou-Kpoviessi et al. 2013). Each extract was pre- Cytotoxicity activity pared to yield a stock concentration of 100 mg/ml. After Human colon cancer cells (HT-29) were obtained from dilution of the stock solution, seven final concentrations the American Type Culture Collection (ATCC catalogue (0.001, 0.01, 0.1, 1, 5, 10 and 20 mg/ml) of each sample no. HTB-38). Colon cancer cells were cultured in RPMI were used to be tested against a bacterial suspension. 1640 medium (Hyclone) containing 100 μg/ml strepto- Sterile filter paper discs of 6 mm in diameter (BD BBM™ mycin, 100 units/ml penicillin, 0.25 μg/ml amphotericin Becton, Dickinson and Company, Sparks, USA) were im- B (Fungizone) and 10% fetal bovine serum (FBS). The pregnated with 50 μl of each concentration to give a re- cell line was cultured at 37 °C in a humidified incubator −5 −4 −3 spective final amount of 5 × 10 ,5× 10 ,5× 10 ,5× of an atmosphere of 95% air and 5% CO . Cells were −2 10 , 0.25, 0.5 and 1 mg/disc. A sterile paper disc pre- trypsinized and split for subculture when they reached pared in the same condition with 50 μl of only solvent near-confluent state (5 days). Cells are typically grown used for the corresponding extract was used as a nega- to 60–70% confluence, the medium was then changed tive control. Discs were allowed to dry at 37 °C for 24 h and the cells were used for test procedure 1 day later ac- (so as to remove residual solvent, which might interfere cording to the method described by Skehan et al. (1990) with the determination). and Pan et al. (2010). Agar disk diffusion assay Antioxidative assay Antimicrobial activities of the different extracts were The antioxidant assay was evaluated for the extracts that screened for their inhibitory zone by the agar disc diffu- showed good results during antimicrobial and cytotox- sion method as described elsewhere (Gautam et al. icity analyses. The experiments were conducted in 2013). Briefly, Mueller Hinton Agar medium plates (BD triplicate. Difco™ Becton, Dickinson and Company, Sparks, USA) were inoculated with a bacterial suspension at 0.5 DPPH radical scavenging activity McFarland, and discs with extract were placed on the The antioxidant activities of the samples were measured surface of the agar. Plates were incubated at 37 °C for 24 by determining the radical scavenging ability using the h. The results were recorded by measuring the zone of stable 2,2-diphenyl-1-picrylhydrazyl (DPPH) radical as growth inhibition (mm) surrounding the discs. Each described by Tepe et al. (2005). The activity of each ex- concentration was tested in duplicate. The results of the tract was represented by the IC parameter (substrate diameters of the zones of inhibitions of extracts were concentration required to cause the loss of 50% of the interpreted as sensitive (> 18 mm), intermediate (14–17 initial concentration of DPPH), and vitamin C was used mm), and resistant (< 14 mm) (Mohamed et al. 2020b). as standard. Broth dilution method Ferrous ion chelating capacity The minimum inhibitory concentration (MIC), which is The chelation of iron ions (II) was studied as described considered as the lowest concentration of the sample by Suter and Richter (2000) with minor modifications. which inhibits the visible growth of a microbe, was de- The reaction solution containing 100 μl (2 mM) ferrous termined by the broth dilution method. A dilution chloride and 400 μl (5 mM) potassium ferricyanide as re- method (Elof 2004) was followed for the determination agent was prepared. A 200-μL test sample of the extract of MIC values with few modifications. Briefly, for each at various concentrations ranging from 2 to 10 mg/mL extract, different volumes of the stock solution were was prepared in different test tubes. Double distilled added to tubes containing different volumes of Trypti- water was added to each test tube to a 1-ml level and case Soy Broth (BD BBM™ Becton, Dickinson and Com- mixed. The above reagent was then added, and the reac- pany, Sparks, USA) to obtain the concentrations of tion mixture was incubated at 20 °C for 10 min. The for- 0.001, 0.01, 0.1, 1, 5, 10 and 20 mg/ml. Thereafter, 20 μl mation of the potassium hexacyanoferrate complex was Vougat Ngom and Foyet Pastoralism: Research, Policy and Practice (2022) 12:13 Page 4 of 8 measured at 700 nm using a spectrophotometer. The turbid. Therefore, this was not easy to know if they were 2+ assay was carried out at 20 °C to prevent Fe oxidation. the growth of bacteria or not. This was also observed in Lower absorbance indicated a higher iron chelating cap- the tubes containing S. aureus and water or methanol acity. The negative control was without any chelating extracts of T. dodoneifolius at 20, 10 and 5 mg/ml. The compound or test sample of extract. Ethylenediaminetet- same results were found in the tubes containing S. aur- raacetic acid (EDTA) used as a control was prepared in eus and hexane or chloroform extract of the same plant the same way as the test samples and treated with the at 20 and 10 mg/ml. same reagent. The per cent of ferrous ion chelating cap- The summarized results of the antibacterial suscepti- acity was calculated accordingly by comparing the ab- bility test of B. senegalensis and T. dodoneifolius against sorbance of the test samples with that of the negative the test bacteria are presented in Tables 3 and 4, re- control. spectively. Hexane extract of B. senegalensis was the most effective, and the highest activity was demonstrated Ferrous ion chelating capacity = [(A − A )/A ] at 20 mg/ml (16 mm zone of inhibition), followed by 10 control extract control × 100 mg/ml (14.75 mm) and 5 mg/ml (13.25 mm) against A is the absorbance of the negative control, and Gram-positive bacteria. The methanol extract of T. control A is the absorbance of the extract solution. dodoneifolius shows the highest activity against the same extract microorganism at 20 mg/ml (10 mm). Statistical analysis For the antioxidant activity of the plant extracts, data Cytotoxicity assay of the plant extracts were presented as mean ± standard deviation. One-way Four extracts of each plant sample were evaluated for analysis of variance followed by Duncan’s multiple range their cytotoxicity against human colon cancer cells (HT- test was performed using Statgraphics 5.0. (Windows, 29) in vitro, and the results are presented in Table 5. All www.statgraphics.com) to compare these data. But for the extracts showed an IC significantly higher than the antimicrobial assay where a comparison was not 40 μg/ml. needed, MIC are presented as mean. The IC (median growth inhibitory concentration) values of test samples Antioxidant analysis for the cytotoxicity assay in serial dilutions were calcu- The antioxidant capacity of the extracts studied is shown lated using non-linear regression analysis (Table cur- in Table 6. From this table, it appears that the scaven- ve2Dv4; AISN Software, Inc., Mapleton, OR). The ging activity extract of B. senegalensis (28.80 ± 1.18 μg/ significance level was fixed at 0.05 for all the statistical ml) is significantly higher than that of vitamin C (107.65 analyses. ± 3.72 μg/ml) and T. dodoneifolius (767.28 ± 2.78 μg/ml). 2+ The chelating of Fe by extracts was estimated, and Results the extent to which an extract can form complexes with Antibacterial activity of plant extracts the ferrous ion reflects its antioxidant activity. The IC Tables 1 and 2 show the results of MIC determination of EDTA (0.50 ± 0.12 μg/ml) was significantly lower than of the test bacteria. At all the concentrations, chloro- that of the hexane extract of B. senegalensis (3.36 ± form, methanol and water extracts of B. senegalensis did 0.10 μg/ml). not inhibit the growth of the bacteria studied. The same result was observed for all the extracts of T. dodoneifo- Discussion lius at 1, 0.1, 0.01 and 0.001 mg/ml. A conclusion of the The determination of the MIC of B. senegalensis showed bacterial growth in the tubes containing the hexane ex- that the chloroform, methanol and water extracts at all tract of B. senegalensis at 20, 10 and 5 mg/ml was not concentrations have no activity against the bacteria stud- clear because before adding inoculum, the tubes were ied. The same result was found by Aliyu et al. (2008). Table 1 Minimum inhibitory concentration (MIC) of B. senegalensis on the test bacteria Microorganism Concentrations of the extract (mg/ml)/MIC (mm) 20 10 5 ≤ 1 MH C W MHC W MHC W MHC W S. aureus (ATCC 29213) + / + + + / + + + / + + + + + + E. coli (ATCC 25922) + / + + + / + + + / + + + + + + S. typhi (14028) + / + + + / + + + / + + + + + + M methanol, H hexane, C chloroform, W water “+” = growth of bacteria; “/” = turbidity of the tube was difficult to read because of the presence of two phases, the upper phase was very clear and the second dense as before the introduction of the inoculum Vougat Ngom and Foyet Pastoralism: Research, Policy and Practice (2022) 12:13 Page 5 of 8 Table 2 Minimum inhibitory concentration (MIC) of T. dodoneifolius on the test bacteria Microorganism Concentrations of the extract (mg/ml)/MIC (mm) 20 10 5 ≤ 1 MHC W MHC W MHC W MHC W S. aureus (ATCC 29213) / / / / / / / / / + + / + + + + E. coli (ATCC 25922) + + + + + + + + + + + + + + + + S. typhi (14028) + + + + + + + + + + + + + + + + M methanol, H hexane, C chloroform, W water “+” = growth of bacteria; “/” = turbidity of the tube was difficult to read because of the presence of two phases, the upper phase was very clear and the second dense as before the introduction of the inoculum However, this is in contradiction with Prashant et al.’s extracts used during the study of Aliyu et al. (2008)is (2011) review. Indeed, according to them, these tree sol- their compositions in tannins, saponins and alkaloids, vents are used for the extraction of antibacterial com- compounds known to have antibacterial properties (Pra- pounds in plant materials. However, the results of the shant et al. 2011). Taking into consideration the antioxi- hexane extract at 20, 10 and 5 mg/ml were difficult to be dant properties found and the properties of the organic appreciated. solvent used for the extraction, the antibacterial activity The results of the antibacterial activity of both plants observed can be the result of those compounds. showed that only one extract of each plant (hexane ex- The antibacterial activity of the methanol extract of T. tract of B. senegalensis and methanol extract of T. dodo- dodoneifolius against S. aureus is similar with the finding neifolius) has a significant activity against the strain of of Deeni and Sadiq during the study they conducted in Gram-positive bacteria S. aureus. As this plant is com- Northern Nigeria (Deeni and Sadiq 2002). This similarity monly used again FMD in Far North of Cameroon, this could be justified by its high content of phenolic com- result could suggest that the opportunistic bacterial dis- pounds and other compounds known for their antibac- eases that affect animals infected by FMD could be due terial activities (Tavassoli and Djomeh 2011). Contrary to Gram-positive bacteria. This is in correlation with the to our results, the work of Ndamitso et al. (2013) fact that the main veterinary drugs used by the pastoral- showed that this methanol extract has a low activity. ists in this study area to manage cattle infected by the This difference could be referred to the different parts of said disease consist of penicillin G (Vougat Ngom et al. the plants studied and their host plants. Indeed it has 2017), an antibiotic belonging to the class with the ac- already been shown that the properties of this hemipara- tion spectrum encompasses mainly Gram-positive bac- sitic plant depend on its host (Deeni and Sadiq 2002). teria (Lobanovska and Pilla 2017). The non-cytotoxic effect of the methanol, hexane, B. senegalensis activity against S. aureus demonstrated water and chloroform extract of B. senegalensis and T. in this work is similar with the results found by Aliyu dodoneifolius was evaluated in vitro to assure their et al. (2008) who showed its activity against S. aureus re- safety. This potential has been demonstrated using the sistant to methicillin, an antibiotic belonging to the class colon cancer cells (HT-29) and four concentrations of of penicillins M. This coherence of results could support each extract. The results clearly showed that all the ex- the hypothesis that the hexane extract of B. senegalensis tracts have a very significantly higher IC in comparison contain molecules which have the same mechanism of with 40 μg/ml. Taking into consideration the classifica- action like penicillins. This argument could be supported tion criteria of the extracts according to their cytotoxic by the proximity between the diameter of the inhibition potential as defined by the National Cancer Institute, we zone (16 mm) of B. senegalensis found in this work and can say that apart from the hexane extracts of both those obtained by the authors cited above (19 mm). The plants and the aqueous extract of T. dodoneifolius con- similarity in the phytochemical composition of the sidered moderately toxic, all the other extracts are not Table 3 Antibacterial activity of T. dodoneifolius on the test bacteria Microorganism Concentrations of the extract (mg/ml)/zone of inhibition (mm) 20 10 5 ≤ 1 M H CW MHCW MHC W MH CW S. aureus (ATCC 29213) 10 0 7 7.25 8 0 0 0 7 0 0 0 0 0 0 0 E. coli (ATCC 25922) 6 0 6 0 0 0 0 0 0 0 0 0 0 0 0 0 S. typhi (14028) 6 0 6 0 0 0 0 0 0 0 0 0 0 0 0 0 M methanol, H hexane, C chloroform, W water Vougat Ngom and Foyet Pastoralism: Research, Policy and Practice (2022) 12:13 Page 6 of 8 Table 4 Antibacterial activity of B. senegalensis on the test bacteria Microorganism Concentrations of the extract (mg/ml)/zone of inhibition (mm) 20 10 5 ≤ 1 MH C W MH CWMH CWMHCW S. aureus (ATCC 29213) 0 16 0 0 0 14.75 0 0 0 13.25 0 0 0 0 0 0 E. coli (ATCC 25922) 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 S. typhi (14028) 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 Values are the means of two assays M methanol, H hexane, C chloroform, W water cytotoxic. Indeed, according to this institute, an extract accepts an electron or hydrogen radical to become a that inhibits the proliferation of cells with an IC ≤ stable diamagnetic molecule (Soares et al. 1997). 20 μg/ml is considered as an active anticancer extract, One of the assays of antioxidative action is chelation and an extract with 20 μg/ml < IC <100 μg/ml is indi- of transition metal, thus preventing catalysis of hydro- cated as moderately. The extracts with an IC > 100 μg/ peroxide decomposition and fenotype reactions (Soares ml are inactive compounds (Tanamatayarat et al. 2003; et al. 1997). The hexane extract of B. senegalensis Mutee et al. 2012). The non-toxic effect of different ex- showed a significantly high chelating effect than T. dodo- tracts of the plants studied may be due to their antioxi- neifolius. This finding is not due to the solvent used be- dant activity as already highlighted by Kilani et al. cause generally extracts of solvents of low polarity show (2008). This can justify the usage of these plants by lower chelating capacity while those of higher polarity people of various countries in Africa (Inuwa et al. 2012; show higher chelating capacity (Talla et al. 2014). It is Ndamitso et al. 2013; Bekoe et al. 2020). certainly the result of the phytochemical composition of The stable DPPH radical is widely used to evaluate both extracts as also observed by Ho et al. (2012). In- the free radical scavenging activity of hydrogen donat- deed, it is well known that chelating capacity is attrib- ing antioxidants in many plant extracts (Talla et al. uted to flavonoids and phenolic compounds which use 2014). This scavenging activity was revealed to be their redox properties to chelate transition metals (Gül- higher for B. senegalensis than that of vitamin C and çinIlhami et al. 2004). However, the fact that the extract T. dodoneifolius. However, the activity of hexane ex- of B. senegalensis demonstrated a less chelating effect tract of B. senegalensis found here is less than that of than EDTA suggest that this plant is a moderate metal the methanolic and water extract of the same plant chelating agent as compared to this standard. obtained in our previous study (Vougat et al. 2015). This difference can be explained by the polarity of Conclusions the solvents used for the extraction (Ncube et al. In this study, several in vitro assays were applied to 2008). Indeed, the non-polar solvent (hexane) used evaluate some properties of different extracts of B. sene- showed less activity than the polar protic solvent galensis and of T. dodoneifolius, two plants most used by (water and methanol). Putting together this result and pastoralists in the Far North Region of Cameroon. The our previous finding (Vougat et al. 2015), it could be findings showed that the plant extracts are no toxic. suggested that the antioxidant activity of B. senegalen- Some bacteria tested were highly sensitive to these ex- sis involved its hydrogen donating ability or the elec- tracts. The observed bioactivities of B. senegalensis and tron transfer reaction (Foti et al. 2004; Friaa et al. T. dodoneifolius may support the traditional use of both 2008). Indeed,DPPH is astablefreeradical and plants for managing animal diseases in the Far North of Table 6 IC (μg/ml) value of different extracts Table 5 IC of T. dodoneifolius and B. senegalensis on human Antiradical activity on Ferrous ions chelating colon cancer cells (HT-29) α β DPPH capacity Extract Plant samples b c Standard 107.65 ± 3.72 0.50 ± 0.12 T. dodoneifolius B. senegalensis c b B. 28.80 ± 1.18 3.36 ± 0.10 Methanol 121.74 176,330.92 senegalensis a a Hexane 66.13 44.37 T. 767.28 ± 2.78 431.48 ± 1.11 dodoneifolius Chloroform 713,879.28 66,565.78 Values are the mean ± E.S.M; n = 3; values with different letters in the same Water 68.02 103.48 column are significantly different (p < 0.05). α: standard used is vitamin C (R = Each value represents the IC of the extract of the plant 50 0.9629); β: standard used is ethylenediamineacetic acid (R = 0.9007) Vougat Ngom and Foyet Pastoralism: Research, Policy and Practice (2022) 12:13 Page 7 of 8 Cameroon. The therapeutic properties of these plants Bolajoko, M.B.F., A.R. Van Gool, J.S. Peters, C.J. Martinez, and V.B. Dungu. 2020. Field survey of major infectious and reproductive diseases responsible for could be due to their antioxidant and antibacterial ef- mortality and productivity losses of ruminants amongst Nigerian Fulani fects of their secondary metabolilities. However, further pastoralists [version 1; peer review: awaiting peer review]. Gates Open studies are necessary to examine the in vivo effect of Research 4: 162. https://doi.org/10.12688/gatesopenres.13164.1. Chakale, M.V., M. Mulunda, and O.A. Adeyemi. 2021. Ethnoveterinary knowledge those extracts and to isolate the active compounds re- and biological evaluation of plants used for mitigating cattle diseases: a sponsible for these pharmacological activities. critical insight into the trends and patterns in South Africa. Frontiers in Veterinary Science 8: 891. https://doi.org/10.3389/fvets.2021.710884. Abbreviations Chitura, T., P.T. Muvhali, K. Shai, B. Mushonga, and E. Kandiwa. 2018. Use of IC : Median growth inhibitory concentration; DPPH: 2,2-Diphenyl-1- medicinal plants by livestock farmers in a local municipality in Vhembe picrylhydrazyl; MIC: Minimum inhibitory concentration; District, South Africa. Applied Ecology and Environmental Research 16 (5): EDTA: Ethylenediaminetetraacetic acid 6589–6605. https://doi.org/10.15666/aeer/1605_65896605. Dadgostar, P. 2019. Antimicrobial resistance: implications and costs. Infection and Acknowledgements drug resistance 12: 3903–3910. https://doi.org/10.2147/IDR.S234610. Cytotoxicity activity of plants studied was performed at the Division of Dassou, E.F., A. Ombolo, G.E. Mboudou, S. Chouto, E.B. Ambomo, and J.M.A. Essi. Medicinal Chemistry and Pharmacognosy of the College of Pharmacy, Ohio 2015. Caractérisation de la variabilité spatio-temporelle des précipitations State University (OSU). The antimicrobial assay was conducted at the dans la zone soudano-sahélienne du Cameroun au cours des cinq dernières Department of Veterinary Preventive Medicine of the same university. But décennies. Afrique Science 11 (4): 331–348. antioxidant activity was performed at the University of Ngaoundere. Deeni, Y.Y., and N.M. Sadiq. 2002. Antimicrobial properties and phytochemical We acknowledge Dr. Rebecca Garabed from OSU and Dr. Ziebe from the constituents of the leaves of African mistletoe (Tapinanthus dodoneifolius University of Maroua for the advice and Pr. Douglas Kinghorn, Dr. Jie Li, and (DC) Danser) (Loranthaceae): an ethnomedicinal plant of Hausa land, Dr. Hee-Byung Chai from the College of Pharmacy at OSU (OH, USA) for the Northern Nigeria. Journal of Ethnopharmacology 83 (3): 235–240. https://doi. assistance during extraction and non-cytotoxic essay. The authors thank Drs. org/10.1016/S0378-8741(02)00244-1. Armando Hoet and Joany C. Van Valen from the College of Veterinary Medi- ElofEloff, J.N. 2004. Quantifying the bioactivity of the plant extracts during cine at OSU for giving us the opportunity to work with them. screening and bioassay-guided fractionation. Phytomedicine 11 (4): 370–371. https://doi.org/10.1078/0944711041495218. Authors’ contributions FAO (Food and Agriculture Organization of the United Nations). 2013. World VN and FH designed the study. VN collected the sample in the field under livestock 2013: changing disease landscapes, 130. Rome: FAO Available at: the supervision of FH. VN performed the laboratory work, analyzed and https://www.fao.org/docrep/019/i3440e/i3440e.pdf. Accessed 30 Sept 2014. interpreted the data and drafted the manuscript. All authors read and Foti, M.C., C. Daquino, and C. Geraci. 2004. Electron-transfer reaction of cinnamic approved the final manuscript. acids and their methyl esters with the DPPH radical in alcoholic solutions. The Journal of Organic Chemistry 69 (7): 2309–2314. https://doi.org/10.1021/ Funding jo035758q. This research was supported by the US National Science Foundation under Friaa, O., V. Chaleix, M. Lecouvey, and D. Brault. 2008. Reaction between the Grant DEB-1015908 via a fellowship from the Disease Ecology and Computer anesthetic agent propofol and the free radical DPPH in semiaqueous media: Modeling Laboratory (DECML) of the Ohio State University (Columbus, OH, kinetics and characterization of the products. Free Radical Biology and USA). Medicine 45 (7): 1011–1018. https://doi.org/10.1016/j.freeradbiomed.2008.07. Availability of data and materials Gautam, K., P. Kumar, and A. Jindal. 2013. Evaluation of antimicrobial efficacy of The datasets used/or analyzed during the current study are available from flavonoids and alkaloids of Andrographis paniculatanees. International Journal the corresponding author on reasonable request. of Green Pharmacy 7 (1): 5757–5761. https://doi.org/10.4103/0973-8258.11161 Declarations GülçinIlhami, Ö., K. Irfan, O. Münir, and E.B. Mehmet. 2004. Antioxidant, antimicrobial, antiulcer and analgesic activities of nettle (Urticadioica L.). Ethics approval and consent to participate Journal of Ethnopharmacology 90 (2-3): 205–215. https://doi.org/10.1016/j. Not applicable. jep.2003.09.028. Ho, S., Y. Tung, Y. Chen, Y. Zhao, M. Chung, and J. Wu. 2012. Antioxidant activities Consent for publication and phytochemical study of leaf extracts from 18 indigenous tree species in Not applicable. Taiwan. Evidence-Based Complementary and Alternative Medicine 8: 1–8. https://doi.org/10.1155/2012/215959. Hyun, T.K., K. Myeong-ok, L. Hyunkyoung, K. Younjoo, K. Ju-Sung, and K. Euikyung. Competing interests 2013. Evaluation of anti-oxidant and anti-cancer properties of Dendropanax The authors declare that they have no competing interests. morbifera Léveille. Food Chemistry 141 (3): 1947–1955. https://doi.org/10.101 6/j.foodchem.2013.05.021. Author details Idu, M.M., O. Ovuakporie-Uvo, and M.J. Nwaokolo. 2016. Phytochemistry and Department of Animal Production, School of Veterinary Medicine and microscopy of Tapinanthus dodoneifolius (DC) (Danser) (Santalales: Science, University of Ngaoundere, Ngaoundere, Cameroon. Department of Loranthaceae) (African mistletoes) from guava, rubber and orange host trees. Biological Sciences, University of Maroua, Maroua, Cameroon. Brazilian Journal of Biological Sciences 3 (5): 27–35. https://doi.org/10.21472/ bjbs.030503. Received: 24 November 2020 Accepted: 29 November 2021 Inuwa, H.M., V.O. Aina, S. Ibrahim, and D.A. Ameh. 2012. Phytochemical screening and antibacterial activity of Globimetulla browni extracts during dry season. 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In vitro antibacterial, non-cytotoxic and antioxidant activities of Boscia Senegalensis and Tapinanthus dodoneifolius, plants used by pastoralists in Cameroon

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Abstract

In the Far North Region of Cameroon, pastoralists use the leaves of Boscia senegalensis and the stem of Tapinanthus dodoneifolius to treat common animal diseases. This study aimed to evaluate the in vitro antibacterial, non-cytotoxic and antioxidant potentials of these plants. To achieve this, four extracts (water, methanol, chloroform and hexane) of both plants obtained by successive fractionation were used. Antibacterial activities of the different extracts were evaluated against three bacterial reference strains including Gram-positive (Staphylococcus aureus) and Gram- negative bacteria (Escherichia coli and Salmonella typhi) using agar disc diffusion and broth dilution methods. Human colon cancer cells were used to screen their toxicity. 2,2-Ddiphenyl-1-picrylhydrazyl (DPPH) radical scavenging and ferrous ion chelating assays have been used to investigate the antioxidant activities of the best extract of each plant after antibacterial assay. A sensitive inhibitory effect was observed against S. aureus with hexane extract of B. senegalensis and methanolic extract of T. dodoneifolius. In addition, the results showed that both plant extracts are not toxic. The hexane and methanolic extracts of B. senegalensis and T. dodoneifolius, respectively, showed higher antioxidant activities, but the hexane extract demonstrate a strong hydrogen donating ability or the electron transfer reaction in comparison with vitamin C used as standard. This finding may support the traditional use of both plants for managing animal diseases in the Far North of Cameroon. Keywords: Antibacterial, Cytotoxic, Antioxidant, Boscia senegalensis, Tapinanthus dodoneifolius, Extract, Cameroon Introduction sales of their products or of the animals themselves in In many African countries where the livestock sector times of crisis, to raise funds needed to purchase food plays a prominent role in the economy especially for the and meet other family needs. rural population, animal diseases constitute one of the In some areas of those countries (i.e. South Africa, Far main hindrances (Mthi et al. 2018; Bolajoko et al. 2020). North of Cameroon), because of the lack of access to Animal diseases limit livestock production and product- veterinary drugs, and their mobility, many pastoralists ivity with significant impacts on animal health, public use traditional medicines for preventing and managing health and economies (McElwain and Thumbi 2017; animal diseases (Chitura et al. 2018). In fact, this trad- Chakale et al. 2021). Indeed, in these regions, livestock itional practice is continuing because pastoralists believe act as a “bank” for the provision of cash derived from that medicinal plants are efficient, available and easily accessible and animal health is a prerequisite for higher productivity (FAO (Food and Agriculture Organization * Correspondence: romsonbey@yahoo.fr 1 of the United Nations), 2013; Vougat et al. 2015). Re- Department of Animal Production, School of Veterinary Medicine and Science, University of Ngaoundere, Ngaoundere, Cameroon searchers are working on this subject matter to actually Full list of author information is available at the end of the article © The Author(s). 2022 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. Vougat Ngom and Foyet Pastoralism: Research, Policy and Practice (2022) 12:13 Page 2 of 8 confirm the potential of the plants used by livestock and Far North regions) (Kelly et al. 2016; Motta et al. farmers (Mostafa et al. 2018; Nordin et al. 2019). The in- 2018) where more than 80% of the national cattle, sheep creasing focus on natural products might be due to their and goat population are found (MINEPIA, 2009 Not reduced or non-cytotoxicity or low side effects compared published). However, due to its climate conditions, the with chemically synthesized drugs (Hyun et al. 2013). In Far North region has the majority of pastoralists of the addition, plant extract usage represents an important al- country. This region is characterized by a Sudano- ternative for the reduction of the use of drugs like anti- Sahelian climate. The average annual rainfall in this re- biotics, known to be the main trigger of the gion is about 700 mm. The temperatures are generally development and spread of antimicrobial resistance, a low in the rainy season and the nights in the dry season major global threat to human health (Dadgostar, 2019; between December and January (Dassou et al. 2015). Varona et al. 2020). That is especially important for de- veloping countries like Cameroon where stringent pol- Methods icies on antibiotic use are not fully in place (Mouiche Preparation of plant extracts et al. 2018). T. dodoneifolius was collected from the host plant Aca- Unfortunately, in Cameroon where livestock contrib- cia albida as a study has shown that the properties of T. utes significantly to the gross national product (MINE- dodoneifolius depended on its host plant (Idu et al. PIA 2009), no sufficient attention is focused on 2016). These plants were then identified and authenti- ethnoveterinary medicine. It is common knowledge that cated in the National Herbarium in Yaoundé in the Far North region of Cameroon, the region that (Cameroon) where the voucher specimens already has the second highest cattle population in the country, existed under the reference numbers 23137 SRF/Cam many cattle farmers and specially pastoralists treat their and 50271 HNC respectively for B. senegalensis and T. animals with plant extracts (Vougat et al. 2015; MINE- dodoneifolius. The extraction of both plant samples was PIA, 2019 unpublished). Due to the increasing import- done according to the scheme below (Fig. 1). Each parti- ance of such medicine to cattle farmers, our research tion was obtained after washing three times with the team seeks to analyse the plants used to control and solvent. Each dried fraction was kept in a freezer before treat animal diseases. Our previous study in the Far biological tests. North region of Cameroon consisted of investigating the plants used against one of the most common, frequent Antibacterial assay and recognizable infectious diseases (Foot and Mouth The antibacterial activity of both plants was evaluated by Disease or FMD) and evaluating the phytochemical com- using both qualitative and quantitative methods. position and antioxidant potentials of the two mostly used (Boscia senegalensis and Tapinanthus dodoneifo- Selected test bacteria lius) (Vougat et al. 2015). Thus, this study aims to Three bacterial strains were used for the study: Escheri- deepen the scope of analysis on these two plants which chia coli (ATCC 25922), Staphylococcus aureus (ATCC have a good phytochemical profile (Vougat et al. 2015; 29213) and an in house fully characterized Salmonella Idu et al. 2016). Both plants are also used in many coun- typhimurium. These bacteria are among the most com- tries to treat animal and human diseases (FMD, respira- mon foodborne bacteria in animal source food that tory tract infections, stomach ache, diarrhoea, dysentery, cause a variety of diseases in humans and animals (Ror- diabetes, epilepsy, hepatitis in humans) (Vougat et al. tana et al. 2021). Bacterial strains were grown and main- 2015; Mamman et al. 2019; Mohamed et al. 2020a). tained on Trypticase Soy Agar with 5% Sheep Blood Therefore, with due knowledge of their profile and im- plates (BD BBM™ Becton, Dickinson and Company, mense importance, this study was designed to evaluate Sparks, USA). Bacterial suspensions of 0.5 McFarland the antibacterial, non-cytotoxic and antioxidant poten- tials of B. senegalensis and T. dodoneifolius. Antimicro- bial activity is first screened because antibiotic drugs are the main veterinary medicine used by pastoralists in the study area (Vougat Ngom et al. 2017). The cytotoxic ac- tivity was evaluated to verify the safety of these plants. Study area The plants analyzed in this study were collected in the Far North region of Cameroon as previously described (Vougat et al. 2015). In Cameroon, pastoralists are Fig. 1 Scheme of the extraction mainly located in three regions (North West, Adamawa Vougat Ngom and Foyet Pastoralism: Research, Policy and Practice (2022) 12:13 Page 3 of 8 were prepared with sterile saline solution to inoculate inoculum (for bacteria 1 × 10 CFU/ml) was added to plates during the antibacterial assay. each tube. A tube containing 300 μl of TSB, 200 μlof solvent used for extract dilution and 20 μl inoculum was Extracts re-suspension and paper disc preparation used as a negative control. Each concentration was Sterile saline solution was used to dissolve extracts of B. assayed in duplicate. All the tubes were then incubated senegalensis obtained with methanol and water. For the at 37 °C for 24 h. After incubation, the tubes were then other extracts (hexane and chloroform extracts of B. examined for microbial growth by observing for turbid- senegalensis and all the T. dodoneifolius extracts), 15% ity. The MIC values were taken as the lowest extract dimethyl sulfoxide (DMSO) (Thermo Fisher Scientific concentration that showed no turbidity after incubation. Inc., Pittsburgh, USA) was used (Kawo et al. 2011; Kpadonou-Kpoviessi et al. 2013). Each extract was pre- Cytotoxicity activity pared to yield a stock concentration of 100 mg/ml. After Human colon cancer cells (HT-29) were obtained from dilution of the stock solution, seven final concentrations the American Type Culture Collection (ATCC catalogue (0.001, 0.01, 0.1, 1, 5, 10 and 20 mg/ml) of each sample no. HTB-38). Colon cancer cells were cultured in RPMI were used to be tested against a bacterial suspension. 1640 medium (Hyclone) containing 100 μg/ml strepto- Sterile filter paper discs of 6 mm in diameter (BD BBM™ mycin, 100 units/ml penicillin, 0.25 μg/ml amphotericin Becton, Dickinson and Company, Sparks, USA) were im- B (Fungizone) and 10% fetal bovine serum (FBS). The pregnated with 50 μl of each concentration to give a re- cell line was cultured at 37 °C in a humidified incubator −5 −4 −3 spective final amount of 5 × 10 ,5× 10 ,5× 10 ,5× of an atmosphere of 95% air and 5% CO . Cells were −2 10 , 0.25, 0.5 and 1 mg/disc. A sterile paper disc pre- trypsinized and split for subculture when they reached pared in the same condition with 50 μl of only solvent near-confluent state (5 days). Cells are typically grown used for the corresponding extract was used as a nega- to 60–70% confluence, the medium was then changed tive control. Discs were allowed to dry at 37 °C for 24 h and the cells were used for test procedure 1 day later ac- (so as to remove residual solvent, which might interfere cording to the method described by Skehan et al. (1990) with the determination). and Pan et al. (2010). Agar disk diffusion assay Antioxidative assay Antimicrobial activities of the different extracts were The antioxidant assay was evaluated for the extracts that screened for their inhibitory zone by the agar disc diffu- showed good results during antimicrobial and cytotox- sion method as described elsewhere (Gautam et al. icity analyses. The experiments were conducted in 2013). Briefly, Mueller Hinton Agar medium plates (BD triplicate. Difco™ Becton, Dickinson and Company, Sparks, USA) were inoculated with a bacterial suspension at 0.5 DPPH radical scavenging activity McFarland, and discs with extract were placed on the The antioxidant activities of the samples were measured surface of the agar. Plates were incubated at 37 °C for 24 by determining the radical scavenging ability using the h. The results were recorded by measuring the zone of stable 2,2-diphenyl-1-picrylhydrazyl (DPPH) radical as growth inhibition (mm) surrounding the discs. Each described by Tepe et al. (2005). The activity of each ex- concentration was tested in duplicate. The results of the tract was represented by the IC parameter (substrate diameters of the zones of inhibitions of extracts were concentration required to cause the loss of 50% of the interpreted as sensitive (> 18 mm), intermediate (14–17 initial concentration of DPPH), and vitamin C was used mm), and resistant (< 14 mm) (Mohamed et al. 2020b). as standard. Broth dilution method Ferrous ion chelating capacity The minimum inhibitory concentration (MIC), which is The chelation of iron ions (II) was studied as described considered as the lowest concentration of the sample by Suter and Richter (2000) with minor modifications. which inhibits the visible growth of a microbe, was de- The reaction solution containing 100 μl (2 mM) ferrous termined by the broth dilution method. A dilution chloride and 400 μl (5 mM) potassium ferricyanide as re- method (Elof 2004) was followed for the determination agent was prepared. A 200-μL test sample of the extract of MIC values with few modifications. Briefly, for each at various concentrations ranging from 2 to 10 mg/mL extract, different volumes of the stock solution were was prepared in different test tubes. Double distilled added to tubes containing different volumes of Trypti- water was added to each test tube to a 1-ml level and case Soy Broth (BD BBM™ Becton, Dickinson and Com- mixed. The above reagent was then added, and the reac- pany, Sparks, USA) to obtain the concentrations of tion mixture was incubated at 20 °C for 10 min. The for- 0.001, 0.01, 0.1, 1, 5, 10 and 20 mg/ml. Thereafter, 20 μl mation of the potassium hexacyanoferrate complex was Vougat Ngom and Foyet Pastoralism: Research, Policy and Practice (2022) 12:13 Page 4 of 8 measured at 700 nm using a spectrophotometer. The turbid. Therefore, this was not easy to know if they were 2+ assay was carried out at 20 °C to prevent Fe oxidation. the growth of bacteria or not. This was also observed in Lower absorbance indicated a higher iron chelating cap- the tubes containing S. aureus and water or methanol acity. The negative control was without any chelating extracts of T. dodoneifolius at 20, 10 and 5 mg/ml. The compound or test sample of extract. Ethylenediaminetet- same results were found in the tubes containing S. aur- raacetic acid (EDTA) used as a control was prepared in eus and hexane or chloroform extract of the same plant the same way as the test samples and treated with the at 20 and 10 mg/ml. same reagent. The per cent of ferrous ion chelating cap- The summarized results of the antibacterial suscepti- acity was calculated accordingly by comparing the ab- bility test of B. senegalensis and T. dodoneifolius against sorbance of the test samples with that of the negative the test bacteria are presented in Tables 3 and 4, re- control. spectively. Hexane extract of B. senegalensis was the most effective, and the highest activity was demonstrated Ferrous ion chelating capacity = [(A − A )/A ] at 20 mg/ml (16 mm zone of inhibition), followed by 10 control extract control × 100 mg/ml (14.75 mm) and 5 mg/ml (13.25 mm) against A is the absorbance of the negative control, and Gram-positive bacteria. The methanol extract of T. control A is the absorbance of the extract solution. dodoneifolius shows the highest activity against the same extract microorganism at 20 mg/ml (10 mm). Statistical analysis For the antioxidant activity of the plant extracts, data Cytotoxicity assay of the plant extracts were presented as mean ± standard deviation. One-way Four extracts of each plant sample were evaluated for analysis of variance followed by Duncan’s multiple range their cytotoxicity against human colon cancer cells (HT- test was performed using Statgraphics 5.0. (Windows, 29) in vitro, and the results are presented in Table 5. All www.statgraphics.com) to compare these data. But for the extracts showed an IC significantly higher than the antimicrobial assay where a comparison was not 40 μg/ml. needed, MIC are presented as mean. The IC (median growth inhibitory concentration) values of test samples Antioxidant analysis for the cytotoxicity assay in serial dilutions were calcu- The antioxidant capacity of the extracts studied is shown lated using non-linear regression analysis (Table cur- in Table 6. From this table, it appears that the scaven- ve2Dv4; AISN Software, Inc., Mapleton, OR). The ging activity extract of B. senegalensis (28.80 ± 1.18 μg/ significance level was fixed at 0.05 for all the statistical ml) is significantly higher than that of vitamin C (107.65 analyses. ± 3.72 μg/ml) and T. dodoneifolius (767.28 ± 2.78 μg/ml). 2+ The chelating of Fe by extracts was estimated, and Results the extent to which an extract can form complexes with Antibacterial activity of plant extracts the ferrous ion reflects its antioxidant activity. The IC Tables 1 and 2 show the results of MIC determination of EDTA (0.50 ± 0.12 μg/ml) was significantly lower than of the test bacteria. At all the concentrations, chloro- that of the hexane extract of B. senegalensis (3.36 ± form, methanol and water extracts of B. senegalensis did 0.10 μg/ml). not inhibit the growth of the bacteria studied. The same result was observed for all the extracts of T. dodoneifo- Discussion lius at 1, 0.1, 0.01 and 0.001 mg/ml. A conclusion of the The determination of the MIC of B. senegalensis showed bacterial growth in the tubes containing the hexane ex- that the chloroform, methanol and water extracts at all tract of B. senegalensis at 20, 10 and 5 mg/ml was not concentrations have no activity against the bacteria stud- clear because before adding inoculum, the tubes were ied. The same result was found by Aliyu et al. (2008). Table 1 Minimum inhibitory concentration (MIC) of B. senegalensis on the test bacteria Microorganism Concentrations of the extract (mg/ml)/MIC (mm) 20 10 5 ≤ 1 MH C W MHC W MHC W MHC W S. aureus (ATCC 29213) + / + + + / + + + / + + + + + + E. coli (ATCC 25922) + / + + + / + + + / + + + + + + S. typhi (14028) + / + + + / + + + / + + + + + + M methanol, H hexane, C chloroform, W water “+” = growth of bacteria; “/” = turbidity of the tube was difficult to read because of the presence of two phases, the upper phase was very clear and the second dense as before the introduction of the inoculum Vougat Ngom and Foyet Pastoralism: Research, Policy and Practice (2022) 12:13 Page 5 of 8 Table 2 Minimum inhibitory concentration (MIC) of T. dodoneifolius on the test bacteria Microorganism Concentrations of the extract (mg/ml)/MIC (mm) 20 10 5 ≤ 1 MHC W MHC W MHC W MHC W S. aureus (ATCC 29213) / / / / / / / / / + + / + + + + E. coli (ATCC 25922) + + + + + + + + + + + + + + + + S. typhi (14028) + + + + + + + + + + + + + + + + M methanol, H hexane, C chloroform, W water “+” = growth of bacteria; “/” = turbidity of the tube was difficult to read because of the presence of two phases, the upper phase was very clear and the second dense as before the introduction of the inoculum However, this is in contradiction with Prashant et al.’s extracts used during the study of Aliyu et al. (2008)is (2011) review. Indeed, according to them, these tree sol- their compositions in tannins, saponins and alkaloids, vents are used for the extraction of antibacterial com- compounds known to have antibacterial properties (Pra- pounds in plant materials. However, the results of the shant et al. 2011). Taking into consideration the antioxi- hexane extract at 20, 10 and 5 mg/ml were difficult to be dant properties found and the properties of the organic appreciated. solvent used for the extraction, the antibacterial activity The results of the antibacterial activity of both plants observed can be the result of those compounds. showed that only one extract of each plant (hexane ex- The antibacterial activity of the methanol extract of T. tract of B. senegalensis and methanol extract of T. dodo- dodoneifolius against S. aureus is similar with the finding neifolius) has a significant activity against the strain of of Deeni and Sadiq during the study they conducted in Gram-positive bacteria S. aureus. As this plant is com- Northern Nigeria (Deeni and Sadiq 2002). This similarity monly used again FMD in Far North of Cameroon, this could be justified by its high content of phenolic com- result could suggest that the opportunistic bacterial dis- pounds and other compounds known for their antibac- eases that affect animals infected by FMD could be due terial activities (Tavassoli and Djomeh 2011). Contrary to Gram-positive bacteria. This is in correlation with the to our results, the work of Ndamitso et al. (2013) fact that the main veterinary drugs used by the pastoral- showed that this methanol extract has a low activity. ists in this study area to manage cattle infected by the This difference could be referred to the different parts of said disease consist of penicillin G (Vougat Ngom et al. the plants studied and their host plants. Indeed it has 2017), an antibiotic belonging to the class with the ac- already been shown that the properties of this hemipara- tion spectrum encompasses mainly Gram-positive bac- sitic plant depend on its host (Deeni and Sadiq 2002). teria (Lobanovska and Pilla 2017). The non-cytotoxic effect of the methanol, hexane, B. senegalensis activity against S. aureus demonstrated water and chloroform extract of B. senegalensis and T. in this work is similar with the results found by Aliyu dodoneifolius was evaluated in vitro to assure their et al. (2008) who showed its activity against S. aureus re- safety. This potential has been demonstrated using the sistant to methicillin, an antibiotic belonging to the class colon cancer cells (HT-29) and four concentrations of of penicillins M. This coherence of results could support each extract. The results clearly showed that all the ex- the hypothesis that the hexane extract of B. senegalensis tracts have a very significantly higher IC in comparison contain molecules which have the same mechanism of with 40 μg/ml. Taking into consideration the classifica- action like penicillins. This argument could be supported tion criteria of the extracts according to their cytotoxic by the proximity between the diameter of the inhibition potential as defined by the National Cancer Institute, we zone (16 mm) of B. senegalensis found in this work and can say that apart from the hexane extracts of both those obtained by the authors cited above (19 mm). The plants and the aqueous extract of T. dodoneifolius con- similarity in the phytochemical composition of the sidered moderately toxic, all the other extracts are not Table 3 Antibacterial activity of T. dodoneifolius on the test bacteria Microorganism Concentrations of the extract (mg/ml)/zone of inhibition (mm) 20 10 5 ≤ 1 M H CW MHCW MHC W MH CW S. aureus (ATCC 29213) 10 0 7 7.25 8 0 0 0 7 0 0 0 0 0 0 0 E. coli (ATCC 25922) 6 0 6 0 0 0 0 0 0 0 0 0 0 0 0 0 S. typhi (14028) 6 0 6 0 0 0 0 0 0 0 0 0 0 0 0 0 M methanol, H hexane, C chloroform, W water Vougat Ngom and Foyet Pastoralism: Research, Policy and Practice (2022) 12:13 Page 6 of 8 Table 4 Antibacterial activity of B. senegalensis on the test bacteria Microorganism Concentrations of the extract (mg/ml)/zone of inhibition (mm) 20 10 5 ≤ 1 MH C W MH CWMH CWMHCW S. aureus (ATCC 29213) 0 16 0 0 0 14.75 0 0 0 13.25 0 0 0 0 0 0 E. coli (ATCC 25922) 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 S. typhi (14028) 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 Values are the means of two assays M methanol, H hexane, C chloroform, W water cytotoxic. Indeed, according to this institute, an extract accepts an electron or hydrogen radical to become a that inhibits the proliferation of cells with an IC ≤ stable diamagnetic molecule (Soares et al. 1997). 20 μg/ml is considered as an active anticancer extract, One of the assays of antioxidative action is chelation and an extract with 20 μg/ml < IC <100 μg/ml is indi- of transition metal, thus preventing catalysis of hydro- cated as moderately. The extracts with an IC > 100 μg/ peroxide decomposition and fenotype reactions (Soares ml are inactive compounds (Tanamatayarat et al. 2003; et al. 1997). The hexane extract of B. senegalensis Mutee et al. 2012). The non-toxic effect of different ex- showed a significantly high chelating effect than T. dodo- tracts of the plants studied may be due to their antioxi- neifolius. This finding is not due to the solvent used be- dant activity as already highlighted by Kilani et al. cause generally extracts of solvents of low polarity show (2008). This can justify the usage of these plants by lower chelating capacity while those of higher polarity people of various countries in Africa (Inuwa et al. 2012; show higher chelating capacity (Talla et al. 2014). It is Ndamitso et al. 2013; Bekoe et al. 2020). certainly the result of the phytochemical composition of The stable DPPH radical is widely used to evaluate both extracts as also observed by Ho et al. (2012). In- the free radical scavenging activity of hydrogen donat- deed, it is well known that chelating capacity is attrib- ing antioxidants in many plant extracts (Talla et al. uted to flavonoids and phenolic compounds which use 2014). This scavenging activity was revealed to be their redox properties to chelate transition metals (Gül- higher for B. senegalensis than that of vitamin C and çinIlhami et al. 2004). However, the fact that the extract T. dodoneifolius. However, the activity of hexane ex- of B. senegalensis demonstrated a less chelating effect tract of B. senegalensis found here is less than that of than EDTA suggest that this plant is a moderate metal the methanolic and water extract of the same plant chelating agent as compared to this standard. obtained in our previous study (Vougat et al. 2015). This difference can be explained by the polarity of Conclusions the solvents used for the extraction (Ncube et al. In this study, several in vitro assays were applied to 2008). Indeed, the non-polar solvent (hexane) used evaluate some properties of different extracts of B. sene- showed less activity than the polar protic solvent galensis and of T. dodoneifolius, two plants most used by (water and methanol). Putting together this result and pastoralists in the Far North Region of Cameroon. The our previous finding (Vougat et al. 2015), it could be findings showed that the plant extracts are no toxic. suggested that the antioxidant activity of B. senegalen- Some bacteria tested were highly sensitive to these ex- sis involved its hydrogen donating ability or the elec- tracts. The observed bioactivities of B. senegalensis and tron transfer reaction (Foti et al. 2004; Friaa et al. T. dodoneifolius may support the traditional use of both 2008). Indeed,DPPH is astablefreeradical and plants for managing animal diseases in the Far North of Table 6 IC (μg/ml) value of different extracts Table 5 IC of T. dodoneifolius and B. senegalensis on human Antiradical activity on Ferrous ions chelating colon cancer cells (HT-29) α β DPPH capacity Extract Plant samples b c Standard 107.65 ± 3.72 0.50 ± 0.12 T. dodoneifolius B. senegalensis c b B. 28.80 ± 1.18 3.36 ± 0.10 Methanol 121.74 176,330.92 senegalensis a a Hexane 66.13 44.37 T. 767.28 ± 2.78 431.48 ± 1.11 dodoneifolius Chloroform 713,879.28 66,565.78 Values are the mean ± E.S.M; n = 3; values with different letters in the same Water 68.02 103.48 column are significantly different (p < 0.05). α: standard used is vitamin C (R = Each value represents the IC of the extract of the plant 50 0.9629); β: standard used is ethylenediamineacetic acid (R = 0.9007) Vougat Ngom and Foyet Pastoralism: Research, Policy and Practice (2022) 12:13 Page 7 of 8 Cameroon. The therapeutic properties of these plants Bolajoko, M.B.F., A.R. Van Gool, J.S. Peters, C.J. Martinez, and V.B. Dungu. 2020. Field survey of major infectious and reproductive diseases responsible for could be due to their antioxidant and antibacterial ef- mortality and productivity losses of ruminants amongst Nigerian Fulani fects of their secondary metabolilities. However, further pastoralists [version 1; peer review: awaiting peer review]. Gates Open studies are necessary to examine the in vivo effect of Research 4: 162. https://doi.org/10.12688/gatesopenres.13164.1. Chakale, M.V., M. Mulunda, and O.A. Adeyemi. 2021. Ethnoveterinary knowledge those extracts and to isolate the active compounds re- and biological evaluation of plants used for mitigating cattle diseases: a sponsible for these pharmacological activities. critical insight into the trends and patterns in South Africa. Frontiers in Veterinary Science 8: 891. https://doi.org/10.3389/fvets.2021.710884. Abbreviations Chitura, T., P.T. Muvhali, K. Shai, B. Mushonga, and E. Kandiwa. 2018. Use of IC : Median growth inhibitory concentration; DPPH: 2,2-Diphenyl-1- medicinal plants by livestock farmers in a local municipality in Vhembe picrylhydrazyl; MIC: Minimum inhibitory concentration; District, South Africa. Applied Ecology and Environmental Research 16 (5): EDTA: Ethylenediaminetetraacetic acid 6589–6605. https://doi.org/10.15666/aeer/1605_65896605. Dadgostar, P. 2019. Antimicrobial resistance: implications and costs. Infection and Acknowledgements drug resistance 12: 3903–3910. https://doi.org/10.2147/IDR.S234610. Cytotoxicity activity of plants studied was performed at the Division of Dassou, E.F., A. Ombolo, G.E. Mboudou, S. Chouto, E.B. Ambomo, and J.M.A. Essi. Medicinal Chemistry and Pharmacognosy of the College of Pharmacy, Ohio 2015. Caractérisation de la variabilité spatio-temporelle des précipitations State University (OSU). The antimicrobial assay was conducted at the dans la zone soudano-sahélienne du Cameroun au cours des cinq dernières Department of Veterinary Preventive Medicine of the same university. But décennies. Afrique Science 11 (4): 331–348. antioxidant activity was performed at the University of Ngaoundere. Deeni, Y.Y., and N.M. Sadiq. 2002. Antimicrobial properties and phytochemical We acknowledge Dr. Rebecca Garabed from OSU and Dr. Ziebe from the constituents of the leaves of African mistletoe (Tapinanthus dodoneifolius University of Maroua for the advice and Pr. Douglas Kinghorn, Dr. Jie Li, and (DC) Danser) (Loranthaceae): an ethnomedicinal plant of Hausa land, Dr. Hee-Byung Chai from the College of Pharmacy at OSU (OH, USA) for the Northern Nigeria. Journal of Ethnopharmacology 83 (3): 235–240. https://doi. assistance during extraction and non-cytotoxic essay. The authors thank Drs. org/10.1016/S0378-8741(02)00244-1. Armando Hoet and Joany C. Van Valen from the College of Veterinary Medi- ElofEloff, J.N. 2004. Quantifying the bioactivity of the plant extracts during cine at OSU for giving us the opportunity to work with them. screening and bioassay-guided fractionation. Phytomedicine 11 (4): 370–371. https://doi.org/10.1078/0944711041495218. Authors’ contributions FAO (Food and Agriculture Organization of the United Nations). 2013. World VN and FH designed the study. VN collected the sample in the field under livestock 2013: changing disease landscapes, 130. Rome: FAO Available at: the supervision of FH. VN performed the laboratory work, analyzed and https://www.fao.org/docrep/019/i3440e/i3440e.pdf. Accessed 30 Sept 2014. interpreted the data and drafted the manuscript. All authors read and Foti, M.C., C. Daquino, and C. Geraci. 2004. Electron-transfer reaction of cinnamic approved the final manuscript. acids and their methyl esters with the DPPH radical in alcoholic solutions. The Journal of Organic Chemistry 69 (7): 2309–2314. https://doi.org/10.1021/ Funding jo035758q. This research was supported by the US National Science Foundation under Friaa, O., V. Chaleix, M. Lecouvey, and D. Brault. 2008. Reaction between the Grant DEB-1015908 via a fellowship from the Disease Ecology and Computer anesthetic agent propofol and the free radical DPPH in semiaqueous media: Modeling Laboratory (DECML) of the Ohio State University (Columbus, OH, kinetics and characterization of the products. Free Radical Biology and USA). Medicine 45 (7): 1011–1018. https://doi.org/10.1016/j.freeradbiomed.2008.07. Availability of data and materials Gautam, K., P. Kumar, and A. Jindal. 2013. Evaluation of antimicrobial efficacy of The datasets used/or analyzed during the current study are available from flavonoids and alkaloids of Andrographis paniculatanees. International Journal the corresponding author on reasonable request. of Green Pharmacy 7 (1): 5757–5761. https://doi.org/10.4103/0973-8258.11161 Declarations GülçinIlhami, Ö., K. Irfan, O. Münir, and E.B. Mehmet. 2004. Antioxidant, antimicrobial, antiulcer and analgesic activities of nettle (Urticadioica L.). Ethics approval and consent to participate Journal of Ethnopharmacology 90 (2-3): 205–215. https://doi.org/10.1016/j. Not applicable. jep.2003.09.028. Ho, S., Y. Tung, Y. Chen, Y. Zhao, M. Chung, and J. Wu. 2012. Antioxidant activities Consent for publication and phytochemical study of leaf extracts from 18 indigenous tree species in Not applicable. Taiwan. Evidence-Based Complementary and Alternative Medicine 8: 1–8. https://doi.org/10.1155/2012/215959. Hyun, T.K., K. Myeong-ok, L. Hyunkyoung, K. Younjoo, K. Ju-Sung, and K. Euikyung. Competing interests 2013. Evaluation of anti-oxidant and anti-cancer properties of Dendropanax The authors declare that they have no competing interests. morbifera Léveille. Food Chemistry 141 (3): 1947–1955. https://doi.org/10.101 6/j.foodchem.2013.05.021. Author details Idu, M.M., O. Ovuakporie-Uvo, and M.J. Nwaokolo. 2016. Phytochemistry and Department of Animal Production, School of Veterinary Medicine and microscopy of Tapinanthus dodoneifolius (DC) (Danser) (Santalales: Science, University of Ngaoundere, Ngaoundere, Cameroon. Department of Loranthaceae) (African mistletoes) from guava, rubber and orange host trees. Biological Sciences, University of Maroua, Maroua, Cameroon. Brazilian Journal of Biological Sciences 3 (5): 27–35. https://doi.org/10.21472/ bjbs.030503. Received: 24 November 2020 Accepted: 29 November 2021 Inuwa, H.M., V.O. Aina, S. Ibrahim, and D.A. Ameh. 2012. Phytochemical screening and antibacterial activity of Globimetulla browni extracts during dry season. 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Journal

Pastoralism – Springer Journals

Published: Mar 15, 2022

Keywords: Antibacterial; Cytotoxic; Antioxidant; Boscia senegalensis; Tapinanthus dodoneifolius; Extract; Cameroon

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