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29/3/2019 Asian Pacific Journal of Tropical Medicine | Vol 10, Issue 11, Pages 1019-1104 (November 2017) | ScienceDirect.com

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Original research https://doi.org/10.1016/j.apjtm.2017.10.007

Antioxidant, anti-inflammatory and antinociceptive potential of Ternstroemia sylvatica Schltdl. &Cham

Claudia V. Moreno-Quiros, Alberto Sanchez-Medina, Maribel Vazquez-Hernandez, Ana G. Hernandez Reyes,Rosa V. García-Rodríguez✉

Unidad de Servicios de Apoyo en Resolucion Analítica, Universidad Veracruzana, Xalapa, Veracruz, Mexico

ARTICLE INFO

Article history:Received 15 Jul 2017Received in revised form 23 Aug2017Accepted 27 Sep 2017Available online 27 Oct 2017

Keywords:Ternstroemia sylvaticaAnti-inflammatoryAnalgesicMedicinal plants

ABSTRACT

Objective: To evaluate the anti-inflammatory, analgesic, antioxidant and acute toxicityof extracts obtained from a successive extraction with solvents of ascending polarity[hexane, hex; chloroform, CHCl3 and ethanol (EtOH)] of Ternstroemia sylvatica Schltdl.& Cham.Methods: The antioxidant potential was evaluated by 2,2 diphenyl-1-picrylhydrazyl, theferric reducing/antioxidant power assays and by determining the total phenolic content.The anti-inflammatory and antinociceptive effects were evaluated using the in vivo crotonoil-induced ear edema, phorbol 12-myristate 13-acetate induced ear edema, carrageenan-induced paw edema, acetic acid-induced writhing and formalin murine models. The acutetoxicity was tested using the Lorke's method in mice.Results: The EtOH extract was the most active for the antioxidant potential testsdiphenyl-1-picrylhydrazyl (68.70% inhibition), ferric reducing/antioxidant power[(2431.30 ± 102.10) mmol Fe2+ and total polyphenols content (215.80 ± 8.50) meqAG/g]. The anti-inflammatory activity was evaluated by topical application of croton oil(2 mg/ear dose) where the EtOH extract showed the strongest activity compared to thecontrol group (45.13% inhibition), whereas in the phorbol 12-myristate 13-acetate model,at the same dose, the CHCl3 extract showed the highest inhibition (42.88%). In thecarrageenan induced edema model, the EtOH extract showed a stronger inhibitioncompared to indomethacin (56.34% and 50.70% at doses of 250 and 500 mg/kg ofextract, respectively) during the first hour. Similarly, the same extract showed the highestanalgesic activity (30.60% inhibition) in the acetic acid contortion assay, and in theformalin test it showed a greater effect with respect to the control group in both phases.Conclusions: Our work confirms the value of Ternstroemia sylvatica as an importantanti-inflammatory and analgesic plant, whose mechanism seems to be associated to itsantioxidant effects, and supports its uses in the Mexican traditional medicine.

1. Introduction

Ternstroemia sylvatica (T. sylvatica) Schltdl. & Cham. (The-aceae), is a tree about 1.5 m–5.0 m high, which is very commonin wooded areas of Mexico. It is commonly known as “flor detila, “hierba del cura” or “trompillo”. This species is used in

traditional Mexican medicine for treating sleep and anxiety dis-orders; in the State of Veracruz, the leaves are used in alcoholiccataplasms for the treatment of inflammatory and rheumaticprocesses [1]. Phytochemical studies on other species of the genusTernstroemia such as Ternstroemia gymnanthera, Ternstroemiajaponica and Ternstroemia pringlie, have reported the presenceof triterpenes, saponins, carotenoids and the identification ofjacaranone [2–6]. Pharmacological studies on T. sylvatica havedemonstrated a sedative activity of the extracts of flowers andfruits in murine models [7,8]. Recently, the toxic effects ofaqueous extracts from flowers and fruits in murine models havealso been reported. This effect has been attributed to thepresence of a triterpenoid glycoside identified as 28-O- [b-L-6-

First author: Claudia V. Moreno-Quiros, Unidad de Servicios de Apoyo enResolucion Analítica (SARA), Universidad Veracruzana, Xalapa, Veracruz, Mexico.

✉Corresponding author: Dr. Rosa V. García-Rodríguez, Unidad de Servicios deApoyo en Resolucion Analítica (SARA), Universidad Veracruzana, Av. Dr. LuisCastelazo Ayala s/n, Col. Industrial Animas, C.P. 91190, Xalapa, Veracruz, Mexico.Tel: +52 228 8418917.

E-mails: [email protected], [email protected] review under responsibility of Hainan Medical University.

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ramnopyranosyl]-R1-barrigenol [9]. However, there are no reportson the inflammatory and analgesic effects of T. sylvatica leaves.

Inflammation is a response of the cellular and humoral innatesystem, triggered against an infectious agent, irritation and otherinjuries in order to restore damaged tissue [10]. The presence ofreactive oxygen species at different stages of the inflammatoryprocess contributes to inducing a state of short-duration oxida-tive stress. They are important mediators that support theinflammation process, either by initiating or amplifying the re-sponses through stimulating the release of cytokines, such astumor necrosis factor alpha (TNF-a) and interleukin 1 (IL-1),and arachidonic acid-derived metabolites. This results in therecruitment of additional inflammatory cells at the injury site andthe production of additional reactive oxygen species [11].

However, a continuous state of oxidative stress is related tomultiple diseases in which the inflammatory process plays animportant role, such as rheumatoid arthritis, asthma, neurode-generative, cardiovascular, autoimmune diseases and cancer[12,13]. Inflammatory processes are part of several diseases and aredirectly or indirectly related to mechanisms of nociceptive stimuligeneration; since inflammatory mediators such as prostaglandins(PG), TNF-a, IL-1 and interleukin-6 (IL-6) are released at thesite of injury and interact with nociceptors, they facilitate thetransmission of pain signals through the nervous system [14]. Painis an uncomfortable sensation that alerts the organism of harmfulsituations to avoid major injuries. More than half of the patientssuffering pain receive inadequate therapeutic managementwhich severely affects their quality of life [15]. Hence, reducingthe inflammatory response is an effective way of decreasing thepain process. Because inflammation involves the generation ofvarious chemical and cellular mediators, it is difficult to identifya main component for its treatment, so there is a growinginterest in the search for alternative medicinal plants that,because of their chemical composition, have a better ability tomitigate these mediators and their multiple mechanisms to treatsymptoms related to a painful inflammatory process moreeffectively [16]; for this reason the present work evaluated theanti-inflammatory, analgesic, antioxidant and acute toxicityproperties of T. sylvatica extracts in murine models.

2. Materials and methods

2.1. Chemicals

All chemicals used in this study were analytical grade.Methanol (MeOH), ferric chloride, acetone, sodium carbonate,sodium acetate, acetic acid, ethanol (EtOH), chloroform(CHCl3), ethyl acetate (EtOAc), sodium picrate, acetic anhy-dride, Grignard reagent, sulfuric acid, potassium hydroxide,potassium iodine, basic bismuth salts and cobalt chloride werepurchased from Merck Co (Germany). Diphenyl-1-picrylhydrazyl (DPPH), Folin–Ciocalteu reagent, 2,4,6-tripyridyl-5-triazine, phorbol 12-myristate 13-acetate (TPA),indomethacin, carrageenan, ascorbic acid, gallic acid and thin-layer chromatography plates were purchased from Sigma–Aldrich Cod. 2193291 (St. Louis, MO, E.U.A.)

2.2. Plant collection

T. sylvatica Schltdl. & Cham (leaves) was collected inAcatlan municipality, Veracruz State, Mexico in March 2009.

Plants were identified by Luis Hermann Bojorquez Galvan and avoucher specimen (CIB-UV-8905) was deposited at the her-barium of the Centro de Investigaciones Biologicas, UniversidadVeracruzana.

2.3. Preparation of plant extracts

The collected plant material was dried at room temperature,and then 853.0 g of dried aerial parts were extracted bymaceration using solvents of ascending polarity at room tem-perature, 25 �C. The extraction was carried out successivelyusing hexane (EHex, 10.0 g), chloroform (ECHCl3, 12.0 g) andethanol (EEtOH, 7.5 g) and kept in darkness at room tempera-ture for further use. Solvents were removed using a rotaryevaporator (Heidolph LABOROTA 4000) and extracts fullydried in a vacuum oven (ShelLab) at 25 �C.

2.4. Phytochemical and chemical analyses

Phytochemical analyses of the plant extracts were carried outby using standard qualitative methods (color test and/or thinlayer chromatography) to detect the presence of sterols, terpe-noids, coumarins, flavonoids, lignans and alkaloids [17,18]. Twomg of the EHex and ECHCl3 extracts were dissolved in 5 mLCHCl3, the systems of elution were Hex/AcOEt (9:1), theEEtOH was dissolved in MeOH and the elution system wasHex/MeOH (4:1).

2.5. Antioxidant activity

2.5.1. DPPH radical-scavenging activityThe radical-scavenging activity was determined according to

the Brand-Williams method modified by Domínguez-Ortíz[19,20]. These determinations are spectrophotometric-basedmethods and are widely accepted for measuring antioxidantactivity in plant extracts in vitro [20]. Briefly, 2.9 mL of freshlyprepared DPPH solution (9 × 10−5) M in MeOH was placed inan amber vial followed by the addition of 100 mL of plant extractsolution dissolved in MeOH, all extracts were tested at threeconcentrations (33, 16.5 and 8.25 mg/mL) (for the blank,100 mL of MeOH were added instead of the sample). Aftermixing, samples were incubated for 30 min at 37 �C in awater bath. Absorbance values of samples (AE) and blank(AB) were measured at 517 nm using a UV–Visspectrophotometer (Varian Model Cary-100). Experimentswere carried out in triplicate and the activity was calculatedusing the following formula:

% inhibition= ½ðAB −AEÞ=AB�× 100

2.5.2. Total phenolic contentThe total phenolic concentration was determined using the

Folin–Ciocalteu reagent according to Cai and Luo [21] with somemodifications. Fifty mL of each sample, 2.5 mL 1/10 dilution ofFolin–Ciocalteu's reagent and 2 mL of Na2CO3 (7.5%, w/v)were mixed and incubated at 45 �C for 15 min. Theabsorbance of all samples was measured at 765 nm using aUV–Vis spectrophotometer (Varian, model Cary 100). Theexperiments were carried out in triplicates. Results wereexpressed as gallic acid equivalent GAE (mg/L) using astandard gallic acid graph (range 10–1000 mg/L, R2 = 0.9965).

Claudia V. Moreno-Quiros et al./Asian Pacific Journal of Tropical Medicine 2017; 10(11): 1047–10531048

Absorbance = 0.001 [GAE (mg/L)] + 0.0754.

2.5.3. Ferric reducing/antioxidant power (FRAP)The reductive power of samples was measured using the

Benzie and Strain method [22]. FRAP reagent was prepared bymixing 100 mL of sodium acetate buffer solution (300 mM,pH 3.6), 10 mL of 2,4,6-tripyridyl-5-triazine (10 mM) in HCl40 mM, 10 mL of FeCl3$6H2O (20 mM); then incubated at37 �C for 4 min. About 2.7 mL of FRAP solution was trans-ferred into an amber vial and added with 150 mL of methanolsolution of plant extract (1 mg/mL) and 150 mL of distilledwater. The absorbance was measured at 593 nm for triplicate.The blank of the experiment was prepared by adding 300 mL ofdistilled water to 2.7 mL of FRAP solution. The results wereexpressed in mmol Fe2+/L, based on a calibration curve obtainedfrom different concentrations of FeSO4 (10–750 mmol/L,R2 = 0.9989).

Absorbance = 0.0010 (mmol Fe2+/L) + 0.1660.

2.6. In vivo assays of animals

Male CD1 mice (20–25 g) were used for the anti-inflammatory and acute toxicity assays. All animals weremaintained under standard laboratory conditions (25 �C, 12 hdark/12 h light, 50% relative humidity) according to the NOM-062-ZOO-1999 [23]. Food and water were provided ad libitum.

2.7. Anti-inflammatory activity

2.7.1. Croton oil (CO) induced ear edema in miceCO, extracts ECHCl3 and EEtOH of T. sylvatica and indo-

methacin were applied topically, and employed for each group(n = 6). The mice, 1 h before the induced edema, were previ-ously treated in the inner and outer surfaces if the right ear with50 mL ECHCl3 and EEtOH of T. sylvatica and indomethacin todoses of 1–2 mg/ear (WT). The ear edema was induced with50 mg of CO 5% (v/v) in ethanol in the right ear and the left earreceived only acetone (WC). Mice were sacrificed by cervicaldislocation 6 h after TPA treatment and 6 mm diameter sectionsof the right and left ears were cut and weighted. Anti-inflammatory inhibition activity was calculated according tothe weight difference between the right and the left ear sectionscompared to the control group [24].

% inh: edema=ðWT × 100Þ

WC− 100

2.7.2. TPA induced ear edema in miceIn this experiment, TPA and indomethacin were applied

topically. In the test group, animals (n = 6) were initially treatedwith 2.5 mg of TPA dissolved in 25 mL of acetone in the rightear. The left ear received only acetone. After 30 min, theECHCl3, EEtOH or indomethacin (2 mg/ear dissolved in 50 mLof acetone) was applied. Mice were sacrificed by cervicaldislocation 6 h after TPA treatment and 6 mm diameter sectionsof the right and left ears were cut and weighted. Anti-inflammatory inhibition activity was calculated according tothe weight difference between the right and the left ear sectionscompared to the control group [25–27].

2.7.3. Carrageenan induced edema in miceIn this assay, edema was induced by subcutaneous injection of

20 mL of 1% carrageenan in saline solution. Following theadministration of carrageenan, the size of the edema was measuredat t = 1, 3, 5 and 7 h using a digitalmicrometer, t = 0 corresponded toameasurement before the administration of carrageenan [28,29]. Thetest groups (n = 6) were injected intraperitoneally indomethacin(4 mg/kg) or plant extract (250 mg/kg and 500 mg/kg) 30 minbefore administration of carrageenan. The control group onlyreceived the vehicle (tween 80-water 1:9). The percentage of in-hibitionwas calculated comparing themeasurement of the edema atdifferent times to the measurement at t = 0. The results wereanalyzed according to Olajide [30].

2.7.4. Acetic acid-induced writhing testThis test was done using the method described by Collier [31].

Muscle contractions were induced in mice (n = 8) by intraperitoneal injection of 0.6% solution of acetic acid (0.1 mL/10 g). Immediately after administration of acetic acid, theanimals were placed in glass cages, and the number of‘stretching’ per animal was recorded during the following20 min. ECHCl3 and EEtOH (500 mg/kg and 1000 mg/kg),ibuprofen (200 mg/kg) were administered by the intragastricroute. The activity was expressed as the inhibition percent.

2.7.5. Formalin testECHCl3 and EEtOH (500 and 1000 mg/kg), ibuprofen

(200 mg/kg) were administered by the intragastric route, 1 hbefore the formalin. Pain was induced with formalin via subcu-taneous administration of 20 mL of 2.5% formalin into the righthind paw of the mouse (n = 8). The time of licking of the injectedpaw was defined as a nociceptive response, which was recordedduring a 30 min period and measured every 5 min after analgesicinjection. The formalin-induced licking behavior was biphasic.The initial acute phase (first phase, 0–10 min) was followed by arelatively short quiescent period that was then followed by aprolonged tonic response (second phase, 15–30 min) [32].

2.7.6. Acute toxicity (LD50)Animals were fasted 12 h before oral administration via a

gastric catheter and intraperitoneal route of the plant extracts(1500–5000 mg/kg) or vehicle (tween 80-water 1:9), n = 3. Thecontrol group only received the vehicle. Animals were observeddaily for 14 d registering deaths and behavioral changes. At theend of the experiment, mice were sacrificed by clavicle disloca-tion, and selected organs (liver, lungs, heart, spleen and kidney)were excised, weighed and macroscopically examined [33,34].

2.8. Statistical analysis

Data are presented as means ± SEM. For statistical evaluation,comparison between experimental and control groups were per-formed by one-way analysis or variance followed by Tukey test.P � 0.05 were accepted as statistically significant difference.

3. Results

3.1. Antioxidant activity

DPPH and FRAP tests were carried out to evaluate theantioxidant activities in extracts of T. sylvatica (Table 1).

Claudia V. Moreno-Quiros et al./Asian Pacific Journal of Tropical Medicine 2017; 10(11): 1047–1053 1049

Additionally, the total polyphenol content was also measured.The EEtOH extract showed both the highest radical scavengingcapacity of DPPH (68.70% at 33 mg/mL; IC50 22.00 mg/mL) andthe highest ferric reducing ability [(2431.30 ± 102.00) mmolFe2+/L]. The same extract showed the highest concentration ofphenolic content [(215.80 ± 8.50) meqAG/g].

3.2. Anti-inflammatory effect

Table 2 showed the anti-inflammatory activity results ofT. sylvatica extracts in the ear edema induced models with COand with TPA. It was observed that EEtOH had a greater anti-edematous effect in the CO-induced model with a 45.13%edema inhibition, a statistically significant result compared to thecontrol group and slightly higher than that obtained with indo-methacin (39.65%). On the other hand, in the model of earedema with TPA, ECHCl3 showed the greatest effect (42.88%).However, in this model both extracts showed a lower effectcompared to indomethacin (51.46% inhibition).

In the carrageenan model (Table 3), the group treated withECHCl3 at 250 mg/kg showed an edema inhibition activity afterthe first hour (57.74%). The best effect was then observed after3 h (75.47%) and maintained nearly until the end of theexperiment, only to decrease after 7 h (38.77%). The groupstreated with EEtOH at doses of 250 mg/kg and 500 mg/kg,showed activity (56.34% and 50.70%, respectively) after the first

hour of the experiments, this effect was maintained throughoutthe study at both doses. However, we observed that the effectwas better at the lowest doses tested. It was important to notethat the effect shown by the extracts was much better than thatshown by our positive control, indomethacin.

3.3. Antinociceptive effect

Table 4 showed the results of the acetic acid-inducedwrithing test, as observed in our previous anti-inflammatoryand antioxidant tests, the EEtOH at both doses (500 and1 000 mg/kg) resulted in a significant decrease (P < 0.05) in thenumber of writhes compared with the control group. On theother hand, the ECHCl3 only showed a significant activity at1000 mg/kg. However, none of the extracts showed a similar orhigher effect in decreasing the number of writhes, comparedwith the control group, ibuprofen (71.70%, decrease).

The results of the formalin test in mice (Table 5) showed thatin the first phase of the analgesic effect measurement, EEtOHwas the most effective in inhibiting the number of licks in thestudy (48.70%) compared to ECHCl3 and our reference com-pound, ibuprofen (24.90% and 37.60%, respectively). In thesecond phase of the experiment, only EEtOH and ibuprofenmaintained an analgesic effect (25.67% and 65.40%,respectively).

Table 1

Antioxidant activity of T. sylvatica extracts.

Extract DPPH FRAP Total phenolics

Inhibition (%) (mmol Fe+2/L) (meqAG/g)

EHex 8.90 ± 0.80 206.90 ± 20.00 2.81 ± 0.40ECHCl3 7.30 ± 0.90 317.90 ± 6.00 27.80 ± 1.60EEtOH 68.70 ± 3.20 2431.30 ± 102.00 215.80 ± 8.50Ascorbic acid 98.00 ± 0.30 3276.50 ± 40.60 ND

ND: No determinated.

Table 2

Anti-inflammatory effect of T. sylvatica on CO and TPA induced ear acute edema in mice (n = 6).

Treatment Doses (mg/ear) 5% CO induced edema TPA induced edema

Weight (mg) Inhibition (%) Weight (mg) Inhibition (%)

Control 0 9.66 ± 0.54 0.00 11.66 ± 0.46 0.00ECHCl3 2 7.16 ± 0.18* 25.88 6.66 ± 0.87* 42.88EEtOH 2 5.33 ± 0.46* 45.13 8.83 ± 1.07* 24.27Indomethacin 2 5.83 ± 0.33* 39.65 5.66 ± 0.61* 51.46

* P < 0.05, difference from the control group.

Table 3

Anti-inflammatory effect of T. sylvatica on carrageenan induced paw edema in mice (n = 6).

Treatment Doses (mg/kg) 1 h 3 h 5 h 7 h

Length (mm) Inhibition (%) Length (mm) Inhibition (%) Length (mm) Inhibition (%) Length (mm) Inhibition (%)

Control 0 0.71 ± 0.08 0.00 1.06 ± 0.13 0.00 0.72 ± 0.19 0.00 0.49 ± 0.14 0.00ECHCl3 250 0.30 ± 0.07* 57.74 0.26 ± 0.03* 75.47 0.19 ± 0.05* 73.61 0.30 ± 0.07* 38.77

500 0.53 ± 0.11* 25.35 0.93 ± 0.15* 12.26 0.71 ± 0.23* 1.38 0.85 ± 0.15* 0.00EEtOH 250 0.31 ± 0.10* 56.34 0.45 ± 0.08* 57.54 0.35 ± 0.11* 51.38 0.12 ± 0.07* 75.51

500 0.35 ± 0.04* 50.70 0.23 ± 0.07* 78.30 0.16 ± 0.08* 77.77 0.26 ± 0.05* 46.93Indomethacin 4 0.66 ± 0.20 7.04 0.73 ± 0.30 31.10 0.31 ± 0.07 56.94 0.39 ± 0.19 20.40


Table 4

Antinociceptive effect of the T. sylvatica extracts on acetic acid-induced

writhing in mice (n = 8).

Treatment Dose (mg/kg) Number of writhing Inhibition (%)

Control 0 79.00 ± 4.10 0.00ECHCl3 500 65.60 ± 3.60 16.90

1000 56.50 ± 4.70* 28.50EEtOH 500 58.00 ± 1.70* 26.60

1000 54.80 ± 1.80* 30.60Ibuprofen 200 22.30 ± 2.30* 71.70



3.4. Acute toxicity

In this study, we initially tested in the first phase of the studythe acute toxicity of the extracts at 10, 100 and 1000 mg/kgdoses of both ECHCl3 and EEtOH, the results showed that noneof the animals administered died. In the second phase of thestudy, the doses 5000 mg/kg/o.r and 3000 mg/kg/ip.r ofECHCl3 caused death of the mice during the first 24 h afteradministration of the extract. Additionally, the behavior of theanimals was different from that of the control group, presentinga decrease in their locomotor activity, lethargy and piloerection.In the group administered with EEtOH, deaths of mice wereobserved when they were administered at doses of 2 000 mg/kg/ip.r and 5 000 mg/kg/o.r. The behavior in the animals admin-istered with EEtOH was the same as that observed in ECHCl3group. LD50 (o.r.) for both the ECHCl3 and EEtOH extracts was3 872.98 mg/kg, when the extracts were administrated viaintraperitoneally route, the LD50 was 2 449.48 mg/kg and1 732.05 mg/kg for the ECHCl3 and the EEtOH extracts,respectively.

4. Discussion

Previous phytochemical reports on other species of the genusTernstroemia have shown the presence of main triterpenes suchas oleanolic acid, primulagenina A, and A1-barrigenol andquinolic-type compounds such as jacaranona [2,5,9]. In ourqualitative phytochemical analysis we were able to observe thepresence of terpenoids compounds in EEtOH. It is known thatterpenes are responsible for multiple ecological andphysiological functions in plants, such as defense againstenvironmental stress, insects and repair of lesions in planttissue [35]. Physiologically, terpenoid compounds are reportedto suppress the expression of nuclear factor kappa B, the mainregulator in the pathogenesis of chronic inflammatory diseasessuch as atherosclerosis and rheumatoid arthritis. Once nuclearfactor kappa B factor is activated, it migrates to the nucleusand stimulates the transcription of mediators of inflammatoryprocesses. Studies on the anti-inflammatory effects of ole-anolic acid have demonstrated the inhibitory effects on theactivation of nuclear factor kappa B signaling, hence decreasingthe expression of T2 cells (Th2) and the production of cytokinessuch as IL-10, IL-13 and TNF-a [36].

The results observed in the antioxidant tests showed thatT. sylvatica EEtOH offers better protection against oxidativestress in an inflammatory process. This extract showed a highcontent of phenolic compounds, which could be contributing tothe antioxidant protection and the reduction of the expression ofinflammatory and nociceptive mediators such as TNF-a and IL-1 [37]. The presence of reactive species and free radicals are

known to result in adverse reactions in the organism such astissue lesions, over stimulation of inflammatory mediators anddamage to biomolecules that further increase the symptoms ofthe inflammation process [38].

Murine ear-induced edema models are widely accepted aspharmacological models for testing novel anti-inflammatorydrugs [25]. CO induces an inflammatory response characterizedby edema and leukocyte infiltration via phospholipase A2

(PLA2) activation. This results in an increase incyclooxygenase-2 expression at the inflammation site [39]. Onthe other hand, in the TPA (a phorbol ester and maincomponent of croton oil) model, an acute inflammatoryresponse is observed, leading to vasodilation, plateletaggregation and leukocyte tissue infiltration [40]. All theseevents result from protein kinase C activation, leading to otherenzymatic events, such as mitogen-activated protein kinases,increased PLA2 activity. Hence an increase of arachidonic acidand its metabolites, such as PG and leukotrienes, thromboxanesand proinflammatory mediators such as NF-kB, TNF-a and IL-6is observed [41,42]. Both extracts (ECHCl3 and EEtOH), whentested in vivo in the two models showed significant edemainhibition effects compared to the control group, so themechanisms of the anti-inflammatory effect of the compoundscontained in these extracts could be associated with their ca-pacity to regulate both PLA2 and cyclooxygenase-2 and themetabolites derived from these enzymes [43].

It is known that an inflammatory reaction is divided into threephases. The initial phase, (0–1.5 h) is attributed to the release ofhistamine and serotonin. In our model this was induced in thesub-plantar edema using carrageenan. This is followed by asecond phase (1.5–2.5 h), mediated by bradykinin and finally, inthe third phase (2.5–6 h) PG, leukotrienes and other arachidonicacid derivatives are overproduced [44]. The results of this studyshowed that ECHCl3 at a dose of 250 mg/kg and EEtOH atdoses of 500 mg/kg significantly inhibited inflammationduring phase three mainly, anti-inflammatory activities couldbe associated with an inhibitory effect of PG biosynthesis.However, EEtOH at 500 mg/kg doses showed a significativeedema inhibition since the first hour (50% inhibition), thissuggests that the extract influences other mediators such ashistamine and serotonin.

The acetic acid-induced writhing test has been widely used asa tool for evaluating analgesic properties of extracts of plantspecies. The nociceptive properties of acetic acid are due to therelease of cytokines, such as TNF-a, IL-1 and interleukin-8 bymacrophages and mast cells [45]. Additionally, mediators such ashistamine, serotonin and eicosanoids lead to increased levels ofPG in peritoneal fluids [46]. In the present study there was aslightly significant reduction in the number of contortions forthe EEtOH treated groups at the two doses used (500 and

Table 5

Antinociceptive effect of T. sylvatica extracts on formalin test in mice (n = 8).

Treatment Dose (mg/kg) Licking (sec) Inhibition (%)

First phase(0–10 min)

Second phase(15–30 min)

First phase(0–10 min)

Second phase(15–30 min)

Control 0 81.00 ± 2.98 59.60 ± 1.63 – –

Ibuprofen 200 50.50 ± 1.12* 20.60 ± 1.87* 37.60 65.40ECHCl3 500 60.83 ± 5.98* 56.00 ± 1.94 24.90 6.10EEtOH 500 41.50 ± 2.52* 44.30 ± 4.49* 48.70 25.67



1 000 mg/k) with a percentage inhibition of 26.50% and 30.60%respectively compared to the control group. In order to confirmthis effect, the formalin test was also carried out. This model isuseful not only for the evaluation of analgesic substances butalso to elucidate the possible mechanism. The first phase(acute pain) begins immediately after the injection of formalinand lasts only a few minutes, and it is believed to be drivenby afferent activity to a primary nociceptor. The second phase(inflammatory pain) lasts about 20–40 min. In this phase theproduction of PG, cyclooxygenase-2 and the release of nitricoxide are elevated [45]. Drugs that act principally on the centralnervous system suppress both phases, whereas peripheral drugsonly suppress the second phase [46]. The results of the formalintest show that ECHCl3 does not have a remarkable inhibitionpercentage in any of the two phases, especially in the second(6.10%). However, EEtOH significantly suppressed theresponse in the first and second phases with percentageinhibition of the number of licks by 48.70% and 25.67%respectively, relative to the control group. Based on the wholeset of experiments carried out in this study, the anti-inflammatory and antinociceptive assays, the pharmacologicaleffects of T. sylvatica can be associated to the inhibition ofcyclo-oxygen-ase and PLA2 by terpenoid and phenolic com-pounds, both of them found in EEtOH, which show the highesteffects in our assays. These pharmacological effects can also beassociated to the antioxidant potential showed by the varioustypes of components found in T. sylvatica extracts. It isimportant to note that this is the first study reporting on theeffects of T. sylvatica leaves, a commonly used medicinal plantin Veracruz, Mexico, for the treatment of inflammatory andrheumatic processes. However, there is a lack of pharmacolog-ical studies that can add evidence to its traditional use. It is clearthat T. sylvatica leaves has a significant anti-inflammatory,antinociceptive activities associated to the inhibition of cyclo-oxygen-ase and PLA2 that seems to be related to the antioxi-dant mechanisms. Additionally, T. sylvatica shows no lethaleffects at a single dose, when given orally. Finally, this studysupports the therapeutic use of this species in the Mexicantraditional medicine.

Conflict of interest statement

The authors declare that there is no conflict of interest.

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http://www.oecd.org/chemicalsafety/risk-assessment/1948370.pdf

http://www.oecd.org/chemicalsafety/risk-assessment/1948370.pdf






















































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