Technological Aptitudes and Pharmaceutical Applications of Schinus terebinthifolius Raddi Leaf and Seed Oil and Fruit Powders of Ziziphus jujuba Mill
- By A. Benahmed Djilali,
- C. Besombes,
- K. Allaf
- and M. Nabiev
Pages 305 to 313
Cite this article
- DJILALI, A. Benahmed,
- BESOMBES, C.,
- ALLAF, K.
- and NABIEV, M.,
- Djilali, A. Benahmed.,
- et al.
- Djilali, A.-B.,
- Besombes, C.,
- Allaf, K.
- and Nabiev, M.
https://doi.org/10.3166/phyto-2018-0083
Cite this article
- Djilali, A.-B.,
- Besombes, C.,
- Allaf, K.
- and Nabiev, M.
- Djilali, A. Benahmed.,
- et al.
- DJILALI, A. Benahmed,
- BESOMBES, C.,
- ALLAF, K.
- and NABIEV, M.,
https://doi.org/10.3166/phyto-2018-0083
Abbreviations
DIC: Instant controlled pressure-drop
FT-IR: Fourier transform infrared spectroscopy
TPC: Total phenolic compounds
SEM: Scanning electron microscope
EP: European Pharmacopoeia
Introduction
1 The species Schinus terebinthifolius Raddi is a medicinal plant, native to the coast of Brazil. It grows in subtropical areas, in many countries such as South America, parts of Central America, Bermuda, Bahamas, West Indies, China, Florida, Southern Arizona, California, Hawaii, South Asia, Mediterranean Europe, North Africa, South Africa [1,2].
2 The biological applications of this plant have been known for many years, and its properties have been described in the first edition of the Brazilian Pharmacopoeia, published in 1926 [3].
3 Many medicinal properties have been attributed to this plant, such as antitumor activity [4], antimicrobial [5,6], antioxidant [7,8], and healing [7] properties. It has also been used in the treatment of gastric ulcers [9].
4 In addition, this species has been used to treat sexually transmitted diseases, uterine inflammation, urinary tract infections, skin ulcers, and peptic disorders [10].
5 In 1996, a US patent was awarded to a researcher who used its essential oil as a topical bactericide to control the development of Pseudomonas and Staphylococci in humans and animals. A year later, another patent was awarded to another researcher who found a similar preparation used as a topical wound cleanser [11].
6 Most of the previous studies performed on these species were devoted to the chemical characterization of the fruits whereas the leaves have been little studied. Schinus terebinthifolius Raddi leaf powder is rich in minerals and tannins. Moreover, it has less sugar and the substances responsible for water retention. Unfortunately, because of its slightly bitter flavor, it is not preferred by consumers.
7 Numerous research works have been conducted on the bioactive compounds derived from Ziziphus jujuba Mill fruits, such as antioxidant peptides [12] and phenolic compounds (flavonoids, carotenoids, exopolysaccharides); the fruits have received much attention, since they might help in the prevention or control of human diseases. These fruits are known for their richness in sugars, minerals, and the high fatty acids composition of their seed oil. Swell-driedZiziphus jujuba Mill flavonoid extracts showed the highest antimicrobial activity [13]. Ziziphus jujuba Mill extract has been used as a prebiotic to improve milk clotting and to develop new functional yoghurt with ideal viscosity [14]. As far as we know, no scientific work has been devoted to the formulation of a healing gel. The aim of this work is to prepare a possible gel formulation in order to valorize the two medicinal species and evaluate some of their physical and chemical, rheological, and organoleptic properties.
Material and methods
Plant material
8 The plant species used in the present study is Schinus terebinthifolius Raddi. It was harvested in northern Algeria (Boumerdes) from February to April, 2016. Just after harvesting, the Schinus terebinthifolius Raddi leaves were dried in open hot air (65 °C and 75 °C); the drying kinetics are not presented here. Then, the obtained powders containing 0.02–0.04 g H2O/g d.b. (dry basis) were kept in bags at ambient temperature.
9 DIC swell-driedZiziphus jujuba Mill fruit powders were used as a source of sucrose, of bioactive substances (flavonoids, carotenoids), specific ingredients responsible for viscosity (contains mucilage), and aroma [13].
10 Ziziphus jujuba Mill fruit powders were achieved through DIC swell-drying. This high temperature–high pressure/short time treatment is usually used for texturing fruits and vegetables without causing thermal degradation. The DIC equipment unit was provided by ABCAR-DIC Process (La Rochelle, France). This part of the work was carried out at the Laboratory of Engineering Science for Environment, LaSIE-UMR-CNRS 7356, (University of La Rochelle), France. The Ziziphus jujuba Mill seed oil used was high in fatty acids (C18:1 [47.76%] and C18:2 [42.60%]) [13]. Carrageenan was used as a texturing agent. The powder was provided by a yoghurt manufacturer located in Algiers.
Methods
Ethno-botanic study and traditional pharmacopeia of Schinus terebinthifolius Raddi
11 This survey was carried out in Tizi-Ouzou city, situated on a 270-m high pass. It is located 100 km east of Algiers, 125 km west of Bejaia, and 30 km south of the Mediterranean coast. This survey was conducted in March/April 2016.
12 The main objective of this study was to collect information related to the traditional usages of the plant, specifying the organs and parts used, directions for use, routes of administration, and diseases this plant can treat. The required criteria were given on a card issued to each individual in the surveyed population. The designed population consisted of 100 persons of different intellectual levels, from both sexes (50 women and 50 men) and of different ages.
Physical and chemical properties of powders
13 The Schinus terebinthifolius Raddi leaf powders underwent the following characterization assessments.
- Phytochemical analyses, which were performed according to standard phytochemical screening methods [15]: These preliminary tests were related to the intensity of the precipitate and the turbidity or coloring which is proportional to the quantity of the desired substance;
- moisture content measurement, which was carried out using appropriate desiccators (OHAUS MB45, Switzerland): This allows determining the dry weight at 105 °C in less than 5 min [16];
- swelling index evaluation: This is the volume in ml occupied by 1 g of powder, including the mucilage adhering thereto, which was swelled in an aqueous liquid for 4 h [17];
- salt quantification, which was achieved through atomic absorption spectroscopy, using an Atomizer (Varian AA 240, Australia): This method relies on the dissolution of 1 g of ashes with 5 mL of HCl acid (0.5 N) [18];
- lipid content estimation: This was determined on the basis of the hexane extraction method [19]. The fatty acids were determined by gas chromatography (GC) using Chrompack CP 9002. Methyl esters were formed by transesterification in a methanolic solution of potassium hydroxide as an intermediate phase prior to saponification following the method laid out in ISO 5509:2000 [20].
Total phenolic compounds (TPC) extraction
14 The polyphenol extraction method adopted was suggested by Owen and Johns [21]. 2 g of Schinus terebinthifolius Raddi leaves powders were macerated in 20 mL of ethanol: water solvent (ranged between 0% and 100% ethanol and pure distilled water) for 72 h in a dark refrigerator. Further, all the sample extracts obtained were filtered through a filter paper (Whatman N°4) followed by evaporation at 45 °C using a rotavapor (Laborota 4000 Heidolph, Germany). The dry extracts were then kept at 4 °C until use [22]. The obtained extracts were used for the determination of TPC and to evaluate the antimicrobial activity. The TPC contents were determined spectrophotometrically according to the Folin–Ciocalteu method described by Juntachote et al. [23].
15 The microstructure of differently dried Schinus terebinthifolius Raddi leaves was studied through an environmental scanning electron microscope, SEM (Philips ESEM XL.30; Heindoven, Netherlands).
Antimicrobial activity of powders
16 The antimicrobial activities of phenolic compound extracts (ethanol and water extracts) of Schinus terebinthifolius Raddi leaf powders were carried out according to the method described by Rahal [24]. The sensitivity of three strains Staphylococcus aureus ATCC 25923, Escherichia coli ATCC 25322, and Aspergillus niger versus the obtained phenolic compound extracts were assessed on the basis of the inhibition zone diameter. The strains were provided by the microbiology laboratory of the Mouloud Mammeri University of Tizi-Ouzou. 20 μL of each extract were tested with the Mueller–Hinton agar diffusion method as recommended by Rahal [24], the concentration of each stock being 107 UFC/mL.
Gel formulations
17 In order to properly conduct this study, different gels were made using the practical guide of Galenic technology of drugs preparation [25]. Several formulations were devised by applying the mixed mixture plan. The composition of the four gels retained is displayed in table 1.
Formulas for gel manufacturing
| Ingredients | F1 | F2 | F3 | F4 |
|---|---|---|---|---|
| Carragenan powder (%) | 4 | 4 | 4 | 4 |
| Open-air dried Schinus terebinthifolius Raddi leaf powder (%) | 0.5 | 0 | 1 | 0.5 |
| DIC dried Ziziphus jujuba Mill fruit powder (%) | 0.5 | 1 | 0 | 0.5 |
| Schinus terebinthifolius Raddi lipid matter (%) | 0.5 | 0.5 | 0.5 | 0.75 |
| Ziziphus jujuba mill seed oil (%) | 0.5 | 0.5 | 0.5 | 0.25 |
Formulas for gel manufacturing
Properties of Gels
18 With the aim of studying some properties (sensory, physical, chemical, and rheological) of the formulated gels, different tests were conducted using the following methods:
- The sensory assessment of gels was carried out by a fifty-member panel (both males and females) of University Mouloud Mammeri of Tizi-Ouzou. The informants were selected on the basis of experience and familiarity with sensory evaluation. The overall sensory quality was assessed by means of a 4-hedonic scale (1–4 points), where 4 was the best score and 1 was the lowest score for color, taste, odor, and flavor [10];
- pH measurement: the pH was obtained by putting an electrode in an aqueous solution with 10% of gel, preheated for 30 min [26];
- the degree of acidity was determined by titrating a sample of 5% using a hydroxide of sodium solution (0.1 N) [27];
- acid index was determined by titrating a mixture of 5:5 W/W gel and ethanol using a potassium hydroxide solution (0.1 mol/L) [28];
- ester index was determined by titrating the surplus of KOH using a hydrochloric acid solution (0.5 mol/L) [29];
- gel viscosity measurement was carried out at 20 °C using a rheometer (AR 2000). The method is based on the measurement of the shear forces; the method makes it possible to measure the dynamic viscosity expressed in Pascal/second [30].
Results and discussion
Ethnobotanic study
19 Schinus terebinthifolius Raddi species is used in traditional medicine and cosmetics. Specifically, 28% of women aged between 15 and 25 years, and 13% of men in the age group of 25 to 35 years use the plant in traditional medicine. The results of this study showed that no cases of toxicity were reported in the surveyed population, although different organs of the plant were used. The leaves have been the most used by women in the age group 15–25 years, with the use rate of 24%, as opposed to 13% in males aged between 25 and 35 years.
20 Overall, the plant fruit represents low utilization rates for both sexes (11.5%).
21 On the other hand, in cosmetology, the plant is somewhat developed with low utilization rates (< 5%). 12% of women in the age range 15–25 years use the powder of this plant. The other modes of use (infusion and decoction) are recommended by the population surveyed with low application frequencies (< 10%).
22 The ways of administration vary by gender. Women of the age class 15–25 years prefer both oral and local ways of administration with varying frequencies of 11–8% respectively. In contrast, men of the age group 25–35 recommend only the oral way, with a frequency of use of 12%.
23 According to this survey, the plant is not used as a bath by the whole population. The plant studied has various traditional uses; according to men of the age class 25–35, it is used to treat gastric disorders. As for women, they use it to treat wounds and rheumatic pains. Besides, 10% of women aged 25–35 years use this species as an antiseptic agent and to fight against worms.
Properties of powders
24 The phytochemical analysis of Schinus terebinthifolius Raddi leaves shows the presence of secondary metabolites (tannins, flavonoids, combined quinones, alkaloids, triterpenic, saponins, coumarins, glucosides, and sennosides) at miscellaneous amounts. Our results coincide with those of other researchers who studied the same species [31,32].
25 The presence of the peaks at 2917.98/cm and 2849.46/cm corresponded to the aldehyde (O=C–H) and acid (O–H) bonds, respectively.
26 The spectrum FT-IR (Fourier transform infrared spectroscopy) of Schinus terebinthifolius Raddi leaf powder (not presented here) showed the presence of peaks at (1) 1616.72/cm, which corresponds to the deformation type vibration in the δ planes of the primary amine (NH) groups and to the (C=C) bonds of the alkenes; (2) 1541.75/cm as the absorption band of elongation type of the aromatic groups (C=C), which corresponds to the aromatic groups of the polyphenols.
27 The presence of a peak at 1447.12/cm denotes the presence of alcohol and phenol (O–H) groups and nitro derivatives (NO2).
28 On the other hand, absorption bands at 1320.08/cm,1206.06/cm, and 1031.97/cm were also observed. The bands indicate the presence of the groups (OH), (CN), and (CO) respectively.
29 These results confirm that the studied species constitutes a reservoir of bioactive substances endowed with several biological activities such as the anti-inflammatory activity of flavonoids and the antioxidant activity of tannins [33,34]. These substances offer promising ways of extraction and use in various fields of application.
30 Furthermore, Schinus terebinthifolius Raddi leaf powder did not have mucilage (swelling index = 5). The latter was determined in order to show the rheological behavior of the constituents of this powder in water (lower water holding capacity (WHC)). According to Paris and Moyse [17], plants with a swelling index greater than 10 contain mucilage. This result is crucial from the point of view of storage of powders, as the water retaining ability of the plant powder is less.
31 Moreover, hot-air dried powders compared to open air-dried powder had a higher percentage of big grain sizes (Ø > 400 μm) against 239.883 μm. SEM (scanning electron microscope) observation of the different Schinus terebinthifolius Raddi leaf powders (Fig. 1) showed that drying at 75 °C improves the powder integrity with the presence of multi-particulate pores, and constitutes a reactivity indication of good pharmacodynamic properties as recommended by the European Pharmacopeia [16].
SEM structure of Schinus terebinthifolius Raddi leaf powders: 1) dried at 65 °C; 2) dried at 75 °C and; 3) dried at open air
SEM structure of Schinus terebinthifolius Raddi leaf powders: 1) dried at 65 °C; 2) dried at 75 °C and; 3) dried at open air
32 The analysis of the chemical composition of the Schinus terebinthifolius Raddi leaves revealed the presence of high Na, Mg, Fe, and K contents in excess of 2.6 mg/gd.b. The richness in minerals can be explained by the growing conditions (moist climate and soil type). With regard to the toxicity of heavy metals, the analyzed powder did not contain any f toxic metals (Cr and Pb) at high doses; the obtained contents complied with the standards recommended by FAO and WHO [35].
33 Therefore, it would be productive to educate people and motivate them to develop this plant in wet regions, especially in the coastal regions.
34 Schinus terebinthifolius Raddi can be used to remedy mineral deficiencies, especially in populations that suffer from iron deficiency (anemia) in underdeveloped countries. Since the leaves are not edible, it would be expedient to use them in decoction or in the form of syrups to cure rheumatism as used in traditional medicine; they can also serve as excipients in the pharmaceutical industry.
35 The leaf revealed the presence of eight fatty acids with different percentages, namely linolenic acid (18.17%), palmitic acid (15.50%), arachedic acid (13.59%), hypogenic acid (10.49%), oleic acid (10.40%), linoleic acid (9.83%), capric acid, and lauric acid (< 3%). These acids can play an important role in the health of humans and animals, particularly in the prevention of a large number of pathologies (metabolic, neurodegenerative, cardiovascular, and inflammatory diseases [36].
Results of anti-microbial activity
36 The results obtained show that the ethanolic extracts of Schinus terebinthifolius Raddi powders dried at free air temperature and with hot air (65 and 75 °C) had a broad spectrum of activity, because they acted on positive and negative Gram bacteria, but the different degrees of sensitivity depended on strains (Table 2). However, the extracts did not exert any antifungal activity against Aspergillus niger. They were more effective against Staphylococcus aureus ATCC 25923 and Escherichia coli ATCC 25322 with diameters up to 28 mm, while aqueous extracts were less effective with diameters that did not exceed 18 mm.
Inhibition diameters (mm) observed under the effect of different polyphenols extracted from powders (N = 3)
| Staphylococcus aureus ATCC 25923 | Escherichia coli ATCC 25322 | Aspergillus niger | |||||||
|---|---|---|---|---|---|---|---|---|---|
| Powders | P1 | P2 | P3 | P1 | P2 | P3 | P1 | P2 | P3 |
| Water extract | 16 ± 0.15 | 17 ± 0.4 | 21.2 ± 0.21 | R | R | R | R | R | R |
| Ethanol extract | 17 ± 0.004 | 20 ±0.001 | 11 ± 0.004 | 14.7 ± 0.13 | 17.1 ± 0.38 | 18.3 ± 0.09 | R | R | R |
Inhibition diameters (mm) observed under the effect of different polyphenols extracted from powders (N = 3)
Where P1: open-air dried Schinus terebinthifolius Raddi leaf powder; P2: hot-air dried Schinus terebinthifolius Raddi leaf powder (65 °C):hot-air dried Schinus terebinthifolius Raddi leaf powder (75 °C), R: Resistant37 This can be explained by the fact that the ethanol extract was higher in polyphenols (Table 3). Thus, a higher extraction concentration was obtained from ethanol than from water with 649.473 as against 484.210 mg EAG/g d.b, respectively.
Total phenolic content of different extracts issued from Schinus terebinthifolius Raddi leaf powders (N = 3)
| Total phenolic compounds (mg EAG/g db) | |||
|---|---|---|---|
| Powders | P1 | P2 | P3 |
| Water extract | 175.759 ± 9.15 | 222.105 ± 11.71 | 484.210 ± 19.64 |
| Ethanol extract | 246.315 ± 13.85 | 260 ± 14.01 | 649.473 ± 22.34 |
Total phenolic content of different extracts issued from Schinus terebinthifolius Raddi leaf powders (N = 3)
P1: open air dried Schinus terebinthifolius Raddi leaf powder; P2: hot air dried Schinus terebinthifolius Raddi leaf powder (65 °C): hot air dried Schinus terebinthifolius Raddi leaf powder (75 °C)38 The absence of inhibition zone for Aspergillus niger should be linked to both the resistance of this strain and the less quantity of the extract amount. Moreover, the type of phenolic extracts may have positive effects on the growth of such fungi strains.
39 This content was relatively higher than the content reported by Fedel-Miyasato et al. [37], which was demonstrated by the value of 544.14 mg EAG/g d.b obtained in the methanol extract of Schinus terebinthifolius Raddi leaves. Similarly, D'Sousa Costa et al. [38] have reported a low value of 73.90 mg EAG/g db of the ethanol extract (80%) prepared from the leaf powder of the same plant dried at 105 °C. Indeed, the two drying temperatures tested positively influence the availability of polyphenols in terms of the bacteriostatic effects.
40 These results are in agreement with other researchers’ results, which confirmed the antimicrobial effect of this plant against a large number of microorganisms. This plant was particularly effective at low concentrations against positive Gram Candida albicans, Streptococcus mutans, Staphylococcus aureus, and Actinobacillus actinomycetemcomitans [39], as well as against certain negative Gram bacteria including Pseudomonas aeruginosa and Escherichia coli [12]. Our results are also similar to those reported by Degaspari et al. [40] — no inhibitory effect were exerted by the same types of extracts on the growth of Aspergillus niger and Escherichia coli.
Physical and chemical characteristics of gels
41 Rheological analysis results show that the gelling phenomenon was the most important parameter through the firmer gel texture (Fig. 2) and the amount of the Schinus terebinthifolius Raddi leaf powder when added to the gel. In our case, formulation F3 was characterized by higher viscosity, and an increase in the total solid content due to the addition of fiber; hence, the gel was very firm.
Aspect of the different gels
Aspect of the different gels
42 Nevertheless, the combination of DIC Ziziphus jujuba Mill and Schinus terebinthifolius Raddi powders favored the formation of a less firm gel (formulation F4). We can conclude that the gel firmness is due to the higher availability of tannins in the Schinus terebinthifolius Raddi leaf powder.
43 Indeed, different biological activities have been attributed to tannins, mainly the ability to complex with metal ions as well as macromolecules such as proteins and polysaccharides [33].
44 On the other hand, it is worth noting that Ziziphus jujuba Mill fruit powder contains a considerable quantity of polymeric catechins known as anthocyanidin, which easily releases aglycon [12]. The study conducted by Arts and Hollman [41] demonstrated that the dimeric and trimeric forms of catechins may be absorbed through the intestinal wall after their degradation, while high-polymerization-degree polymers cannot be absorbed.
45 The viscosity of the four formulations of our manufactured gels and the reference gel (anti-inflammatory gel marketed) (Fig. 3) shows a “rheofluidifying” type because their viscosities decrease when the shear rate increases.
Variation of viscosity with the shear rate of the formulated gels
Variation of viscosity with the shear rate of the formulated gels
46 Indeed, this characteristic justifies the fact that the gels possess the viscous properties of a liquid and the elastic properties of a solid (Fig. 4).
Scheme of treatment
Scheme of treatment
47 The results of spreading the gels on paper sheets show that the formulations F1, F2, and F3 were very compact except the formulation F3, which was viscous. The spreading power is related to the availability of water in the sample (higher reconstitution capacity).
48 There were no lumps in the gels (Fig. 2); they were perfectly homogeneous.
49 The comparison between various gels analyzed in terms of their total polyphenol contents (Table 2), allowed us to note that the gelling mode had the best preservation.
50 The increasing availability of ester index in Schinus terebinthifolius Raddi leaf powder would have been due to the highest lipid matter (formulas F2 and F3). The various gels had the same acid index with lower value than those of olive oils; the obtained value was in conformity with the recommended standards [42,43].
51 From the results of table 4, we could select gels F2 and F4 as those having the best physical, chemical (slightly acidic gels), organoleptic, and rheological properties (viscous gel).
Results of some physical and chemical parameters of the elaborated gels
| Parameters | F1 | F2 | F3 | F4 |
|---|---|---|---|---|
| pH at 20 oC | 6.13 ± 0.06 | 5.95 ± 0.046 | 6.35 ± 0.034 | 5.86 ± 0.075 |
| Assayable acidity (%) | 1.89 | 2.8 | 0.7 | 1.19 |
| Total phenolic compounds (mg EAG/g d.b) | 777.8 ± 0.28 | 230.5 ± 0.01 | 804.2 ± 0.19 | 748.0 ± 0.07 |
| Ester index | 18.12 | 55.98 | 41.96 | 27.94 |
| Acid index | 0.1 | 0.1 | 0.1 | 0.1 |
Results of some physical and chemical parameters of the elaborated gels
Conclusion
52 This first approach to formulating a gel greatly encourages the use of powders of Schinus terebinthifolius Raddi leaves and Ziziphus jujuba Mill fruits to prepare a natural gel as a very efficient and economical plant-based drug to fight certain health problems.
53 It would be of use to evaluate the anti-inflammatory properties of these formulations. However, it is clear that the physico-chemical, rheological, and biological properties of these powders greatly depend on the drying process. High-temperature air dried Schinus terebinthifolius Raddi leaves and DIC swell-driedZiziphus jujuba Mill fruits have allowed us to obtain the most adequate powders to manufacture relevant gels, with higher chemical constituents (Na, Mg, Fe, and K), higher availability of phenolic compounds, better rheological (viscous gel) behavior, and better organoleptic properties. In other words, more available bioactive substances (polyphenols, tannins, and fatty acids) result in better biological activities.
Acknowledgments
This research work was supported by grants from: Laboratory of Engineering Science for Environment LaSIE-UMR-CNRS 7356 France; Laboratory of Chemistry and Microbiology of University Mouloud Mammeri of Tizi-Ouzou (Algeria) and Laboratory of Petrochemical Synthesis FHC, University M'Hamed Bougara of Boumerdes, 35000, Algeria.This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors
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Publisher keywords: DIC (Instant controlled pressure drop), Drying, Gel formulation, Mill, Raddi, Schinus terebinthifolius, Texturing, Traditional pharmacopoeia, Ziziphus jujuba
Uploaded: 09/27/2024
https://doi.org/10.3166/phyto-2018-0083