Abstract
Objective
To evaluate the antioxidant activity, hydrogen peroxide radicals scavenging activity, reducing power, the total phenolic and flavonoids contents, and antimicrobial and antifungal activities of methanol, ethanol and water extracts of leaves of Lantana camara (L. camara).
Methods
Methanol, ethanol and water extracts were evaluated against four Gram positive and Gram negative bacterial isolates (Staphylococcus aureus, Pseudomonas aeruginosa, Klebsiella pneumoniae, Bacillus subtilis) and two fungal strains (Aspergillus fumigatus and Aspergillus flavus). Methanol extract at different concentrations was tested for antioxidant potential and phytochemicals were determined by using spectrophotometric method.
Results
The total phenolic content was (40.859±0.017) mg gallic acid/g in the leaves of L. camara, while the total flavonoids was (53.112±0.199) mg/g dry weight. Methanol leaf extract of L. camara showed maximum antibacterial activity against Staphylococcus aureus and Pseudomonas aeruginosa and was also effective against other bacterial strains as compared to ethanol and aqueous extracts of leaves. The methanol leaf extract of L. camara exhibited significant inhibition (71%) and (66%) against Aspergillus fumigatus and Aspergillus flavus respectively.
Conclusions
The methanol extract of the L. camara leaves is effective against selected bacterial and fungal strains. Its phytochemical contents have broad antimicrobial properties and the plant might be a novel source of antimicrobial drug.
Keywords: MIC, Antioxidants, Phytochemicals, Antimicrobial, Lantana camara
1. Introduction
Resistance to antimicrobial agents is a major global public health problem[1]. Infectious diseases account for approximately one-half of all death in tropics. Despite the progress made in the understanding of microorganisms and their control in industrialized nations, incidents due to drug resistant microorganisms and the emergence of unknown disease causing microbes, posed enormous public health concern[2]. Streptococcus pyogenes, Stephylococcus aureus and Streptococcus pneumoniae, the organisms that causes respiratory and cutaneous infection, as well as Pseudomonas and members of Enterobacteriaceae, causing diarrhea and urinary tract infections and sepsis, are now resistant to virtually all of the known antibiotics[3]. This resistance is largely due to indiscriminate use of antimicrobial drugs commonly used for the treatment of infectious diseases[4]. Furthermore some antibiotics have serious undesirable side effect which limit their application, so there is serious need to develop new antimicrobial agents that are very effective with minimal unwanted side effect. Plants represent a potential source of novel antibiotic prototypes[5].
Lantana camara (L. camara) is mainly used as a herbal medicine and in some areas as firewood and mulch[6]. It is also used for the treatment of cancers, chicken pox, measles, asthma, ulcers, swellings, eczema, tumors, high blood pressure, bilious fevers, catarrhal infections, tetanus, rheumatism, malaria and atoxy of abdominal viscera[7]. Extracts from the leaves exhibit antimicrobial, insecticidal and nematicidal activity and also contain verbascoside, which possesses antimicrobial, immunosuppressive and antitumor activities[8]. Several previous reports have described antifungal, anti proliferative and antimicrobial activities of L. camara[9]–[13]. The present study aims to investigate the phytochemicals, free radical scavanging activities and antimicrobial potential of leaves extract of the commonly used medicinal plant L. camara.
2. Materials and methods
2.1. Plant materials
Fresh leaves of L. camara were collected from Margalla Hills of Quaid-i-Azam University Islamabad, Pakistan. The plants were identified by the National Herbarium, Department of Plant Sciences, Quaid-i-Azam University Islamabad.
2.2. Processing of the plant material
Plant leaves were washed thoroughly with distilled water. The leaves were dried under shade at room temperature. The dried leaves of L. camara were finely grinded using electrical grinder and stored in air tight containers for further use. A total of 250 g of the pulverized plant material was extracted for 4 d in methanol, ethanol and sterile water[14]. The separated extracts were then filtered through Whatman's No. 1 filter paper and the methanol and ethanol filtrate were then separately condensed to dryness using rotary evaporator. The thick extracted mass was then dried at room temperature. Dried extract was collected in an air tight container and stored at 4 °C for further analysis.
2.3. Chemicals
1,1-diphenyl-2-picryl-hydrazyl (DPPH), methanol, ferric chloride, chloroform, H2SO4, HCl, benzene, NH4OH, potassium ferro-cyanide, sodium chloride, ethanol, Folin-Ciocalteau, Na2CO3, gallic acid, hydrogen peroxide and ascorbic acid were obtained from Sigma Chemical Co. (St. Louis, MO, USA).
2.4. DPPH radical scavenging activity
The antioxidant activity was assessed in DPPH radical scavenging system using gallic acid and ascorbic acid as a positive control, and the decrease in absorbance was determined at 517 nm in a spectrophotometer (HITACHI Model: U-1100 573×415)[15]–[17].
 |
Where A0 was the absorbance of the control reaction and A1 was the absorbance in the presence of the sample[18].
2.5. Hydrogen peroxide-scavenging activity
The ability of the extracts to scavenge hydrogen peroxide was determined according to the method of Ruch et al[19]. Absorbance of the hydrogen peroxide activity was recorded at 230 nm in a spectrophotometer (HITACHI Model: U-1100 573×415). Hydrogen per oxide scavenging ability (in triplicate) was calculated by following equation:
Hydrogen peroxide scavenging activity (%) = 1-A1/A0×100
A0 was the absorbance of the control and A1 was the absorbance of the sample.
2.6. Reducing power assay
The reducing powers of the extracts were determined according to the method described by Chung et al[20]. The extract which have reduction potential, react with potassium ferricyanide (Fe3+) to form potassium ferrocyanide (Fe2+), which then reacts with ferric chloride to form ferric ferrous complex that has an absorption maximum at 700 nm in a spectrophotometer (HITACHI Model: U-1100 573×415).
 |
2.7. Preliminary phytochemical screening
Phytochemical screening of the L. camara was performed to detect the presence of different classes of constituents, such as alkaloids, phenolics, flavonoids, tannin, saponins, terpenes, phlobatannins and coumarins[21],[22].
2.8. Quantitative analysis of phytochemicals
2.8.1. Total phenolic contents (TPC)
TPC of L. camara were determined by the Folin-Ciocalteu colorimetric method using gallic acid as a standard, and the absorbance was measured at 765 nm in a spectrophotometer (HITACHI. Model: U-1100 573×415). Results were expressed as gallic acid equivalent (GAE) mg/g of dried extract. Data for plant extract was recorded in triplicate[15],[23].
2.8.2. Determination of the total flavonoids content
Total flavonoids content was determined according to the protocol of Sakanaka et al[24]. The absorbance was measured immediately at 510 nm in a spectrophotometer (HITACHI Model: U-1100 573×415). Flavonoids were estimated as mg/g of dried fraction. All samples were run in triplicate.
2.8.3. Determination of total tannins
Tannin content was determined by using Van-Burden and Robinson WC method[25]. Absorbance at 120 nm was recorded in a spectrophotometer (HITACHI Model: U-1100 573×415) within 10 min and tannins contents were expressed as mg/g of the dried fraction.
2.9. Test microorganism
The test microorganisms used in this investigation included bacteria Staphylococcus aureus ATCC 6538 (S. aureus), Pseudomonas aeruginosa ATCC 7221 (P. aeruginosa), Klebsiella pneumoniae (K. pneumoniae) and Bacillus subtilis ATCC 6059 (B. subtilis); and fungi Aspergillus fumigatus (A. fumigatus) and Aspergillus flavus (A. flavus). The bacterial isolates were first sub cultured in a nutrient broth (SIGMA) and incubated at 37 °C for 18 h, while the fungal isolates were sub cultured on a Sabouraud dextrose agar (MERCK) for 72 h at 25 °C.
2.10. Positive and negative control
Penicillin (1 mg/mL) was used as positive control for the test bacterial strains. Sterilized distilled water and dimethyl sulfoxide were used as negative control.
2.11. Antibacterial activity
Antibacterial activity of the methanol, ethanol and aqueous extract of L. camara leaf extract was determined by using the agar-well diffusion method[26]. The bacterial strains were first cultured in a nutrient broth for 18 h prior to use and standardized to 0.5 McFarland standards (106 CFU/mL).
Nutrient agar medium was prepared by adding nutrient agar 2.3 g in 100 mL of distilled water; pH was adjusted at 7.0 and was autoclaved. It was allowed to cool up to 45 °C. Petri plates were prepared by pouring 75 mL of seeded nutrient agar and allowed to solidify. Wells were bored into the agar using a sterile 6 mm diameter cork borer. Approximately 100 µL of the crude extract at 12 mg/mL were added into the wells, allowed to stand at room temperature for about 2 h and incubated at 37 °C. Controls were set in parallel in which case the respective solvents were used to fill the well. The plates were observed for zones of inhibition after 24 h. The effects were compared with those of penicillin at a concentration of 1 mg/mL.
2.12. Determination of relative percentage inhibition
The relative percentage inhibition of the test plant extract with respect to positive control was calculated by using the following formula[27].
 |
Where, X is total area of inhibition of the test extract, Y is total area of inhibition of the solvent, and Z represents total area of inhibition of the standard drug. The total area of the inhibition was calculated by using area = πr2; where, r=radius of zone of inhibition.
2.13. Assay for antifungal activity
The agar tube dilution method was used for the determination of antifungal activity of L. camara leaves extract in different solvents[28]. The samples were prepared by dissolving 12 mg extract in 1 mL of dimethyl sulfoxide. Culture media was prepared by dissolving 6.5 g of Sabouraud dextrose agar (MERCK) per 100 mL distilled water (pH 5.6). The 10 mL of Sabouraud dextrose agar was dispensed in screw capped tubes or cotton plugged test tubes and was autoclaved at 121 °C for 21 min. Tubes were allowed to cool at 50 °C and Sabouraud dextrose agar was loaded with 67 µL of extract pipetted from the stock solution. The tubes containing the media were then allowed to solidify in slanting position at room temperature. Three slants of the extract sample were prepared for fungus species. The tubes containing solidified media and plant extract were inoculated with 4 mm diameter piece of inoculum, taken from seven days old culture of fungus. One test tube of each extract was prepared, used as positive control. Slants without extract were used as negative control. The test tubes were incubated at 28 °C for 7 d. Cultures were examined twice weekly during the incubation. Reading was taken by measuring the linear length (mm) of fungus in slant and growth inhibition was calculated with reference to negative control.
Percentage inhibition of fungal growth for each concentration of compound was determined as
 |
3. Results
3.1. DPPH radical-scavanging activity
Results shown in Table 1 indicates the relative activities against ascorbic acid and butylated hydroxytoluene (BHT). The activity of 0.8 mg/mL BHT was the highest followed by ascorbic acid and L. camara leaf extracts respectively. Leaves extracts of the plant quenched DPPH in a dose dependent manner: [R2=0.983 7] for L. camara against the control (ascorbic acid and BHT).
Table 1. Analysis of DPPH radical scavanging activity of leaf extracts of L. camara.
| Plant and drugs (mg/mL) | % inhibition±SD | Logarithm equation | IC50 (mg/mL) | |
| L. camara | 0.2 | 45.00±0.47 | y=19.871ln(x)+43.994 R2=0.983 7 |
≥0.2 |
| 0.4 | 56.17±0.41 | |||
| 0.6 | 64.83±0.44 | |||
| 0.8 | 73.13±0.42 | |||
| Ascorbic acid | 0.2 | 61.40±0.57 | y=15.853ln(x)+61.372 R2=0.999 9 |
≤0.2 |
| 0.4 | 72.37±0.30 | |||
| 0.6 | 78.63±0.40 | |||
| 0.8 | 83.47±0.46 | |||
| Gallic acid | 0.2 | 70.43±0.50 | y=14.029ln(x)+69.801 R2=0.979 5 |
≤0.2 |
| 0.4 | 78.80±0.40 | |||
| 0.6 | 83.93±0.38 | |||
| 0.8 | 90.63±0.55 | |||
3.2. Hydroxyl radical-scavanging activity
The scavenging abilities of selected plant leaves fraction extracts on hydroxyl radical inhibition by the 2-deoxyribose oxidation method are shown in Table 2. The results are indicated as the inhibition rate. Leaf extract of L. camara showed good hydroxyl radical scavenging activities (45%–73%) at a concentration of 0.2–0.8 mg/mL in the reaction mixture. Leaf extract showing hydroxyl radical-scavenging activity was increased with increasing concentration of the extract sample. Leaf fraction of L. camara had higher activity but lower than that of ascorbic acid and BHT (Table 2).
Table 2. Analysis of hydroxyl radical scavanging activity of leaf extracts of L. camara.
| Plant and drugs (mg/mL) | % inhibition±SD | Logarithm equation | IC50 (mg/mL) | |
| L. camara | 0.2 | 55.00±0.47 | y=16.365ln(x)+54.281 R2=0.987 4 |
≤ 0.2 |
| 0.4 | 64.50±0.47 | |||
| 0.6 | 71.50±1.44 | |||
| 0.8 | 78.13±0.24 | |||
| Ascorbic acid | 0.2 | 67.40±0.47 | y=18.224ln(x)+67.989 R2=0.985 3 |
≤0.2 |
| 0.4 | 82.37±0.20 | |||
| 0.6 | 86.63±0.75 | |||
| 0.8 | 93.47±0.46 | |||
| 0.2 | 79.77±0.42 | y=12.587ln(x)+78.234 R2=0.870 9 |
≤0.2 | |
| Gallic acid | 0.4 | 85.13±0.33 | ||
| 0.6 | 89.07±0.23 | |||
| 0.8 | 98.97±0.37 | |||
3.3. Reducing power
The reducing power of the selected plant leaf extract increased with increase in concentration. At 0.8 mg/mL concentration, the leaves extracts of L. camara showed absorbance of 0.888 (Table 3). Thus, the plant leaves extracts exhibited a lower reducing ability than the standard. Also, the reducing ability was found to be the concentration dependent. With increasing concentration, the reducing ability of all the leaves extracts was found to increase. In this case, at 0.8 mg/mL, the reducing power was found to be at maximum value.
Table 3. Analysis of reducing power ability of leaf extracts of L. camara.
| Plant and drugs (mg/mL) | % inhibition± SD | Logarithm equation | IC50 (mg/mL) | |
| L. camara | 0.2 | 0.721±0.001 | y=0.1055ln(x)+0.701 4 R2=0.757 8 |
≤0.2 |
| 0.4 | 0.750±0.001 | |||
| 0.6 | 0.782±0.002 | |||
| 0.8 | 0.888±0.006 | |||
| Ascorbic acid | 0.2 | 0.815±0.006 | y=0.1485ln(x)+0.7812 R2=0.668 2 |
≤0.2 |
| 0.4 | 0.843±0.004 | |||
| 0.6 | 0.881±0.003 | |||
| 0.8 | 1.058±0.06 | |||
| Gallic acid | 0.2 | 0.856±0.006 | y=0.3147ln(x)+0.772 2 R2=0.628 7 |
≤0.2 |
| 0.4 | 0.878±0.002 | |||
| 0.6 | 0.985±0.002 | |||
| 0.8 | 1.370±0.006 | |||
3.4. Qualitative analysis of phytochemicals
Results of phytochemical screening presented in Table 4 reveales moderate concentration of alkaloids, phenolics, flavonoids, tannin, saponin, terpenoids, phlobetanin and coumarine.
Table 4. Qualitative phytochemical analysis of leaf extracts of L. camara.
| Constituents | Presence | |
| Alkaloids | Dragondorff's test | - |
| Mayer's test | +++ | |
| Phenolic | +++ | |
| Flavonoids | +++ | |
| Tannin | ++ | |
| Saponin | ++ | |
| Terpenoids | - | |
| Phlobetanin | - | |
| Coumarin | - | |
+++: Strongly positive, ++: Moderately positive, +: Weakly positive, -: Negative.
3.5. Quantitative analysis of phytochemicals
3.5.1. TPC
TPC was determined in comparison with standard gallic acid and the results were expressed in terms of mg GAE/g dry sample of plant. TPC values for L. camara was (40.859±0.017) as mg GAE/g dry sample.
3.5.2. Total flavonoid content
Total flavonoid content was determined in comparison with standard rutin and the results expressed in terms of mg RU/g of dry sample of plant. Total flavonoid content values for L. camara (53.112±0.199) was mg RU/g dry sample.
3.5.3. Estimation of tannin
The results of total tannin were presented in Table 5. The amount of tannin for L. camara (0.860±0.038) mg/g of the dried fraction in dry sample.
Table 5. MIC values of methanol, ethanol and water extracts from leaves tissue of L. camara.
| Test bacteria | MIC (mg/mL) |
|||
| Methanol mg/mL |
Ethanol mg/mL |
Water mg/mL |
Penicillin mg/mL |
|
| S. aureus | 5.0 | 6.5 | 8.0 | 0.05 |
| B. subtilis | 8.0 | 10.0 | nd | 0.20 |
| P. aeruginosa | 5.0 | 8.0 | 10.0 | 0.05 |
| K. pneumoneae | 8.0 | 12.0 | nd | 0.25 |
PC: Penicillin, nd: Not determined.
3.6. Antibacterial activity
The antibacterial activity of methanol, ethanol crude extracts and water extracts of leaves of L. camara was investigated against two gram positive (B. subtilis and S. aureus) and two gram negative (P. aeruginosa and K. pneumoniae) bacterial strains (Figure 1). The methanol and ethanol extracts of L. camara exhibited the maximum zone of inhibition 21.7 mm and 19.7 mm against gram positive strain S. aureus and 20 mm and 17.7 mm zone of inhibition against gram negative strain P. aurignosa and showed minimum antibacterial activity against B. subtilis and K. pneumoniae. The results revealed that aqueous leaf extracts of L. camara has minimum antibacterial activity against four bacterial strains as compared to methanol and ethanol solvents.
Figure 1. Antibacterial activities profile of methanol, ethanol and water extracts from leaves tissue of L. camara.
3.7. Relative percentage inhibition
The standard drug (Penicillin) was used to determine the relative percentage inhibition of antibacterial activity of L. camara leaves extract in different solvents.
Methanol leaf extract of L. camara exhibited maximum relative percentage inhibition (74.9% and 74.8% respectively) against P. aeruginosa and S. aureus, while minimum percentage inhibition was recorded against B. subtilis. Ethanol leaf extract of L. camara showed maximum relative percentage inhibition (67.9%) against S. aureus, while water leaf extract showed maximum inhibition of 63% against S. aureus (Figure 2).
Figure 2. Determination of relative percentage inhibition of methanol, ethanol and water extracts from leaves tissue of L. camara compared to standard antibiotics.
3.8. Minimum inhibitory concentration (MIC)
Results showed in Table 5 revealed the MIC of methanol, ethanol and water extracts of L. camara. MIC values of methanol extract of L. camara ranged between 5–8 mg/mL, ethanol 6.5–12 mg/mL and MIC of water leaf extract was recorded 8 mg/mL and 10 mg/mL against S. aureus and P. aeruginosa, while MIC was not determined against B. subtilis and K. pneumoniae. MIC range of penicillin (standard drug) was recorded between 0.05–0.25 against four bacterial strains.
3.9. Antifungal activity
Antifungal activity of methanol and water leaf extracts of L. camara was investigated against two fungal strains viz. A. fumigatus and A. flavus (Table 6). Methanol leaf extract of L. camara showed 71.4% and 66.4%, while water extract showed 61.5% and 57.8% inhibition against A. fumigatus and A. flavus respectively (Table 6).
Table 6. Antifungal activity of methanol and aqueous extracts from leaves tissue of L. camara.
| Test fungi | Linear growth (cm) |
Percentage inhibition (%) |
|||
| Methanol | Water | Methanol | Water | ||
| A. fumigatus | 2.8 | 4.0 | 71.4 | 61.5 | |
| Control | 9.8 | 10.3 | - | - | |
| A. flavus | 3.33 | 4.3 | 66.4 | 57.8 | |
| Control | 9.9 | 10.2 | - | - | |
4. Discussion
From the present study the maximum radical scavanging and antimicrobial activities of methanol extract of leaves of L. camara was investigated.
The phytochemical compositions of L. camara reported previously[29]. With regards to reducing power, higher reducing activities can be attributed to higher amounts of polyphenolics and the reducing capacity of a compound may reflect its antioxidant potential[30]. It has been reported that the reducing properties are generally associated with the presence of reductones, which have been shown to exert antioxidant action by breaking the free radical chain by donating a hydrogen atom[31].
L. camara has been studied extensively for their antibacterial properties. L. camara possess many important biological activities viz., antipyretic, antimicrobial, antimutagenic, antimicrobial, fungicidal, insecticidal, nematicidal and others[29]. Lantadenes which present in all L. camara is believed to be responsible for almost all the biological activities. In addition, other secondary metabolites such as alkaloids, terpenoids, and phenolics could be held partially responsible for some of these biological activities[32].
Therefore, antibacterial activities of L. camara leaf and flower extracts might be due to the presence of some of these chemical constituents particularly lantadenes and theveside in the extracts. The presence of phenolics, anthocyanins and proanthocyanidins in L. camara leaves which could also be responsible for the antibacterial properties of the L. camara have been documented[33].
Antimicrobial activity of different plant extracts on phytopathogenic bacteria was studied and reported by other workers[34]. The methanol leaf extracts of various medicinal plants showed significant antibacterial and antifungal activity against A. flavus, Dreschlera turcica and Fusarium verticillioides have been reported[35]. Methanolic extracts of root and shoots of the herb Heracleum candicans wall (Apiaceae), showed antifungal effect against Pythium and Aspergillus species[36].
The value of medicinal plants lies in phytochemical constituents that cause definite pharmacological action on the human body[37]. The plants are the vital source of innumerable number of antimicrobial compounds. Several phytoconstituents like flavonoids, phenolics and polyphenols, tannins, terpenoids, sesquiterpenes etc., are effective antimicrobial substances against a wide range of microorganisms[37].
The study showed that the methanol leaf extract of L. camara had more antimicrobial potential than ethanol and water extract. The antimicrobial activity of L. camara may be attributed to the various phytochemical constituents present in the crude extract. The purified compounds may have even more effectiveness with respect to inhibition of bacterial and fungal strains. The work carried was a basic approach to find out the antimicrobial activity of L. camara in different solvents. We therefore suggest more work should be required to isolate, identify and characterized the active components and also possibly their mechanism of biological action and thus, find its way into the arsenal of antimicrobial drugs.
Acknowledgments
The authors would like to thank the Higher Education Commission (HEC) of Pakistan for providing the necessary financial support for the study. The personal identification number (PIN) for getting this financial support/scholarship from HEC is 0 74-0998-Av4-036.
Comments
Background
Plants have been used to treat a variety of ailments and the introduction of orthodox medicine did not affect their use. L. camara belongs to Verbenaceae family and is reported to be used in traditional medicine system for the treatment of itches, ulcers, cuts, swellings, eczema, bilious fever and cataract. The literature reported that different parts of the plants are used in the treatment of cold, whooping cough, bronchitis, chicken pox and eye injuries.
Research frontiers
Research was performed on leaves of L. camara in different solvents to determine the most efficient solvent system against microbial infections. The leaf extract in three different solvents have been studied against both Gram negative and Gram positive bacterial strains and also against two fungal species (A. fumigatus and A. flavus). Antioxidants and phytochemical screening of L. camara leaves have also been studied.
Related reports
Our results of efficient methanol extract are in agreement with the previous work which showed that in plants most of the compounds having antimicrobial potential (Verma et al., 2006). Methanol leaf extract is more effective against pathogenic bacterial strains than ethanol or water extracts (Naz et al., 2011). Previous studies using extracts from Lantana species showed that they were able to inhibit the growth of Gram-positive bacteria strains (Júnior et al., 2005).
Innovations & breakthroughs
Data regarding potential of leaf extract of L. camara against Gram positive and Gram negative bacterial strains, against fungal Aspergillus species in different solvents and also about antioxidants and phytochemicals is scarce. This study has shown that methanol leaf extract had a significant higher antimicrobial potential than ethanol and water leaf extracts.
Applications
The present study indicated that the antibacterial and antifungal activities vary with the different solvents of plant leaf material used. L. camara was effective even at low concentration against bacterial and fungal pathogens. The solvent extracted leaves extracts of L. camara contains some highly potential phytochemicals, which could be characterized and effective against bacterial and fungal infections.
Peer review
This is a good study in which the authors evaluated the antimicrobial potential of L. camara leaf extracts in different solvents and also analyzed the antioxidant and phytochemicals in leaves. The results are interesting and suggest the presence of potential phytochemicals, antioxidants and active compounds which could be identified and thus, find its way into the arsenal of antimicrobial drugs.
Footnotes
Foundation Project: Supported by the Higher Education Commission (HEC) of Pakistan. The personal identification number (PIN) for this financial support/scholarship is 0 74-0998-Av4-036.
Conflict of interest statement: We declare that we have no conflict of interest.
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