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Argentinian plant extracts with relaxant effect on the smooth muscle of the corpus cavernosum of Guinea pig.

Summary

Extracts of different polarity from Baccharis trimera, Haplopappus rigidus Huperzia saururus, Maytenus ilicifolia, Satureja parvifolia and Senecio eriophyton were tested for their relaxant activity on smooth muscle using L-phenylephrine precontracted strips of corpus cavernosum obtained from Guinea pigs. Highly significant and dose dependent results were obtained with the dichloromethane extracts of H. saururus (87% of relaxation at the dose of 10 mg/ml), S. parvifolia (95% of relaxation at 2.5 mg/ml) and S. eriophyton (94 % of relaxation at 5 mg/ml). Similar effects were observed with the methanol extracts of H. saururus (88% of relaxation at 10 mg/ml) and S.parvifolia (84% of relaxation at 10 mg/ml). These results were comparable to those obtained with the dichloromethane and methanol extracts of the well known Mexican species Turnera diffusa. Moreover, the aqueous extract of H. rigidus and the aqueous and methanol extracts of S. eriophyton were highly effective in a dose dependent manner (more than 90% of relaxation at the dose of 10 mg/ml). Significant results, but with a lower overall relaxant activity (about 70% of relaxation at 10 mg/ml), could also be obtained with the aqueous extract of S. parvifolia and with the dichlormethane and methanol extracts of B. trimera and M. ilicifolia. The positive controls with Sildenafil citrate at doses ranging from 0.35 to 35 [micro]g/ml yielded moderate effects (up to 46% of relaxation at 35 [micro]g/ml). The effects observed in the present study seem to validate the folk medicinal use of the tested plants and open new ways in the search for natural products with vasodilatory effects.

Key words: Plant extracts, corpus cavernosum relaxation, Baccharis trimera, Haplopappus rigidus, Huperzia saururus, Maytenus ilicifolia, Satureja parvifolia, Senecio eriophyton

* Introduction

Erectile disfunction is a serious clinical problem in adult men. The failure of penile erection could be due to impaired relaxation of the smooth muscle related to the increase in blood flow into the spaces of the corpus cavernosum. Although the mechanism its not fully understood, there is increasing evidence that nitric oxide is a mediator of the relaxation in the corpus cavernosum (Anderson et al. 1998).

Since several synthetic drugs commonly used in erectile disfunction are associated with uncomfortable side effects, there is an increasing interest in finding new effective drugs. Various reports on natural products with vasodilatory effects on smooth muscle appeared recently (Slish et al. 1999; Ko et al. 1999; Chiou et al. 2001).

Many pharmacologically active substances came from plants that have been used in traditional medicine and a review of the Argentine medicinal flora shows the existence of 27 species used in popular medicine as aphrodisiacs (Bandoni et al. 1996). Six of these species (see Table 1) were selected for the present study. Extracts of different polarity were tested for their relaxing effect on the smooth muscle of Guinea pig corpus cavernosum and the effects were compared to those of Turnera diffusa, a well studied Mexican species sold in Argentina as an aphrodisiac, and Sildenafil citrate, which was used as a positive control.

* Materials and Methods

Plant material

Plant materials were collected from different places in North, Northwestern and Northeastern regions of Argentina according to the habitat of each species. Baccharis trimera was collected in Villa Zorroaquin, Entre Rios Province; Haplopappus rigidus in Antofagasta de la Sierra, Catamarca Province; Huperzia saururus in Sierras Altas, Cordoba Province; Maytenus ilicifolia in Camp Roca, Misiones Province; Satureja parvifolia in Dep. Belen, Laguna Blanca, Catamarca Province and Senecio eriophyton in Cordoba Province. The botanical identity was confirmed by Prof. Dr. M. Wagner by comparison with authentic samples.Voucher specimens are deposited in the Museo de Farmacobotanica, Facultad de Farmacia y Bioquimica, Universidad de Buenos Aires, Argentina: B. trimera 6662 BAF; H. rigidus 513 BACP-M; H. saururus without number J. Dominguez; M. ilicifolia 5500 BAF; S. parvifolia Galafassi 3215 BACP and S. eriophyton 10251 BAF.

Preparation of the extracts

Aqueous extracts: The aqueous (A) extracts were prepared by macerating 5 g of dried and powdered plant material for 20 min with 100 ml of boiling water. After filtering, the solution was frozen and lyophilized.

Dichloromethane and methanol extracts: The dried and powdered plant material (50 g) was extracted twice by maceration with dichloromethane (100 ml each) for 24 h at room temperature. The resulting dichloromethane (D) extract was filtered. The dried marc of the dichloromethane extraction was macerated twice with methanol (100 ml each), as described above, and the resulting methanol (M) extract was filtered. Both extracts (D and M) were taken to dryness under reduced pressure (Paya et al. 1996).

Testing solutions

200 mg of each extract were dissolved with 25% ethanol in water and added to Krebs' solution (KS) to obtain final concentrations of 0.625; 1.25; 2.50; 5.00 and 10.00 mg/ml. These solutions were used for the respective relaxation analysis. Sildenafil citrate (1-[[3-(6,7-dihydro-1-methyl-7-oxo-3-propyl-1H-pyrazo-lo [4,3-d]pyrimidin-5-yl)-4-ethoxyphenyl]sulphonyl]4-methylpiperazine citrate; Pfizer S.A.C.I.V., Buenos Aires, Argentina) was dissolved in KS and used at final concentrations ranging from 0.35 to 35 [micro]g/ml.

Tissue preparation and experimental procedure

Male albino Guinea pigs from the breeding laboratories of the Instituto Nacional de Tecnologia Agropecuaria (INTA, Buenos Aires, Argentina) weighing 450-650 g, were used for each experimental group throughout all experiments. They were housed in a temperature and humidity controlled environment with automatic light/dark cycle of 12/12 hours and fed with standard rabbit chow from Nutrimentos Purina (Buenos Aires, Argentina) supplemented with green vegetables and tap water ad libitum. The animals were used in compliance with the international guidelines for research animals.

The animals were killed by cervical dislocation and then exsanguinated. The penis was immediately removed and placed in KS gassed with 95% 02 and 5% CO2 mixture (pH = 7.4) and the temperature was held thermostatically at 37 [degrees]C. Then, the urethra was isolated and the remaining corpus cavernosum tissues cut into helical strips and mounted in an organ-bath chamber. After a 60 min stabilization period, the strip was precontracted by adding L-phenylephrine (PE) to obtain a concentration of [10.sup.-5] M in the bath, in order to adjust the maximum of contractile tension (Ballard et al. 1998). Once the measured tension reached a plateau, extracts were added in different doses (0.625; 1.25; 2.50; 5.00 and 10.00 mg/ml), one at a time. The effect was measured as change in isometric force and recorded during 5-7 min with a force-displacement transducer model FT 03 connected to a polygraph (Grass Instrument Model 79, Quincy, MASS, USA). Tissue tones were tested by adding acetylcholine ([10.sup.-4] M) before and after each experience.

Statistical analysis

The relaxation induced by each extract was expressed as a percentual reduction of the contractile tension induced by PE. The statistical analysis was performed by using one way analysis of variance. A value of p < 0.05 was considered significant. All data were expressed as mean [+ or -] S.E.M.

* Results and Discussion

The yield of each extract is shown in Table 2. According to the polarity of the extracts, different relaxation effects were obtained with the tested species (see Table 3).

Highly significant and dose dependent results were obtained with the D extracts of H. saururus (87% of relaxation at the dose of 10 mg/ml), S. parvifolia (95% of relaxation at 2.5 mg/ml) and S. eriophyton (94% of relaxation at 5 mg/ml). Similar effects were observed with the M extracts of H. saururus (88% of relaxation at 10 mg/ml) and S. parvifolia (84% of relaxation at 10 mg/ml). For comparison, the D and M extracts of the Mexican species T. diffusa yielded at the dose of 10 mg/ml 89% and 86% of relaxation, respectively, and at the dose of 5 mg/ml the values obtained were 58% and 62% of relaxation, respectively. Moreover, the A extract of H. rigidus and the A and M extracts of S. eriophyton were highly effective in a dose dependent manner (more than 90% of relaxation at the dose of 10 mg/ml). Significant dose dependent results, but with a lower overall relaxant activity, could also be obtained with the A extract of S. parvifolia (71% of relaxation at 10 mg/ml) and with the D and M extracts of B. trimera and M. ilicifolia (50-74% of relaxation at 10 mg/ml). Evaluating the results it is noteworthy that some extracts of the selected Argentinian species are even more effective than those of T. diffusa, which is a well studied species sold in Argentina as an aphrodisiac.

The experimental procedure applied in the present study was also implemented by other authors, but using rabbits (Chiou et al. 2001). These authors have suggested that nitric oxide (NO) is involved in the relaxation they observed. In our study several extracts show highly significant relaxant effects in Guinea pig and it is tempting to propose a similar hypothesis. We used Sildenafil citrate as a positive control and the results are summarized in Table 4. The effect of Sildenafil is mainly attributed to its inhibitory activity on cGMPspecific phosphodiesterase type 5 (Ballard et al. 1998; Moreland et al. 1998) and significant synergistic effects of Sildenafil combined with sodium nitroprusside, forscolin, VIP and phentolamine have been described (Seo et al. 2001). However, it has been shown that the distribution of phosphodiesterase isoforms in corpus cavernosum tissue obtained from animals may significantly differ from human tissue (Qiu et al. 2000; see also Stief et al. 1998) and nothing is known about this distribution in Guinea pig. Additionally, Sildenafil has been reported to be poorly effective on phenylephrine precontracted tissue in the absence of a NO donor (Chuang et al. 1998; Aydin et al. 2001), a fact which may account for the low relaxation values obtained with Sildenafil in our experiments. Taken together, the observations indicate that the extracts with high relaxation values seem to be acting by a different mechanism than Sildenafil and that their effectiveness is not dependent on the presence of an additional NO donor. Further studies are needed to determine the occurrence of the NO-cGMP pathway and to examine the mechanisms by which the extracts induce relaxation in the experimental conditions described here.

Preliminary TLC studies indicate that the tested plant extracts contain phenolic compounds, which may be responsible (at least in part) for the observed effects. The best results were obtained mainly with the less polar extracts (D and M extracts) and this fact points to the possible involvement of flavonoids, coumarins, terpenes, and other related substances, which were reported to have relaxant activities (Duarte et al. 1993; Torres et al. 2000; Chiou et al. 2001; Ko et al. 2001). The most promising extract in this group seems to be the D extract of Satureja parvifolia, which is highly effective at a low dose (2.5 mg/ml). But also the A extracts should be considered in view of the notable results obtained with Haplopappus rigidus, Senecio eriophyton and, to a lesser extent, with S. parvifolia, which indicate the presence of some polar active substances in these plants and thus may explain the effects observed in the folk medicinal applications of the infusions.

In conclusion, our results show that extracts of different polarity of the selected plants are highly effective in relaxing the smooth muscle of the corpus cavernosum obtained from Guinea pig and suggest that these extracts could be worthy of further phytochemical and pharmacological investigation in the search for new compounds with relaxant properties.
Table 1. List of the selected Argentinian plants.

Species and Popular name Traditional uses Phytochemistry
 Family

Baccharis Carqueja Digestive, tonic, Diterpenes (6);
 trimera (Less.) Yaguarete caa febrifuge, saponins and
 De Candolle antidiarrheal, flavonoids (7)
 (Asteraceae) hepatoprotective,
 contraceptive,
 against woman
 sterility and
 aphrodisiac (1-5)

Haplopappus Bailabuena Treatment of Essential oils
 rigidus Phil. grip, pneumonia, and resins (8);
 (Asteaceae) cold and urinary diterpenes (9)
 deseases;
 aphrodisiac (8)

Huperzia saururus Cola de Purgative, Alkaloids
 (Lam.) Trevis quirquincho emmenagogue, (12-15)
 (Lycopodiaceae) Pillijan abortifacient,
 stimulant and
 aphrodisiac;
 treatment of
 impotence in old
 men (8, 10, 11)

Maytenus Cangorosa Sialagogue, Alkaloids and
 ilicofolia Mart. Congorosa emmenagogue, terpenes (16)
 ex Reisseck Sombra de abortifacient,
 (Celasteraceae) toro contraceptive,
 Molle antispasmodic,
 espinoso digestive and
 aphrodisiac;
 treatment of
 whooping cough,
 asthma and
 menstrual pains
 (1-3, 8, 11)

Satureja parvifolia Muna-muna Digestive, Essential oils
 (Phil.) Epling Oreganillo laxative, (19, 20);
 (Lamiaceae) purgative, flavonoids (21)
 emmenagogue,
 stimulant,
 against women
 sterility and
 aphrodisiac
 (8, 10, 17, 18)

Senecio Chachacoma Digestive, Essential oils;
 eriophyton emmenagogue, resins and
 J. Remy stimulant and sesquiterpenes
 (Asteracea) aphrodisiac (2) (8)

References: (1) Arenas and Moreno-Azorero, 1976; (2) Toursarkissian,
1980; (3) Bandoni et al., 1996; (4) Marzocca, 1997; (5) Freire and
Urtubey, 1999; (6) Torres et al., 2000; (7) Gene et al., 1996;
(8) Ratera and Ratera,1980; (9) Morales et al., 2000; (10) Hieronymus,
1882; (11) Martinez Crovetto, 1981; (12) Deulofeu and De Langhe, 1942;
(13) Ayer et al., 1965; (14) Oberti and Juliani, 1967; (15) Braekham
et al., 1974; (16) Alonso, 1998; (17) Fargione de pelissero, 1982;
(18) Bustos et al., 1996; (19) Fester et al., 1956; (20) Muschietti
et al., 1996; (21) Hernandez et al., 2000.

Table 2. Yield of different extracts.

Plant Part used Extraction yield (% w/w)

 Aqueous Methanol Dichloromethane
 extract extract extract
 (A) (M) (D)

Baccharis aerial parts 13.9 12.0 4.5
 trimera
Haplopappus aerial parts 16.9 11.5 10.6
 rigidus
Huperzia leaves 9.2 15.9 7.4
 saururus
Maytenus aerial parts 10.0 7.9 2.0
 ilicifolia
Satureja leaves 11.8 8.2 2.8
 parvifolia
Senecio aerial parts 10.6 4.1 6.2
 eriophyton

Table 3. Effects (%, of relaxation) of the aqueous (A), methanol (M)
and dichloromethane (D) extracts on L-phenylephrine precontracted
corpus caveruosum strips.

Plant Extract 0.625 mg/ml 1.25 mg/ml

B. trimera A -- --
 M -- --
 D -- --
H. rigidus A -- --
 M -- --
 D -- --
H. saururus A -- --
 M -- --
 D -- --
M. ilicifolia A -- --
 M -- --
 D -- --
S. parvifolia A -- --
 M -- --
 D 67.7 [+ or -] 3.8 82.2 [+ or -] 4.1 (a)
S. eriophyton A -- --
 M -- --
 D 19.0 [+ or -] 4.2 65.7 [+ or -] 3.3 (a)

Plant Extract 2.50 mg/ml

B. trimera A 0.0
 M 22.0 [+ or -] 8.3
 D 32.2 [+ or -] 9.0
H. rigidus A 0.0
 M 12.5 [+ or -] 2.5
 D 35.3 [+ or -] 2.7
H. saururus A 1.3 [+ or -] 1.2
 M 25.0 [+ or -] 9.4
 D 26.8 [+ or -] 12.6
M. ilicifolia A 14.5 [+ or -] 7.5
 M 30.0 [+ or -] 3.1
 D 29.9 [+ or -] 10.0
S. parvifolia A 29.8 [+ or -] 4.4
 M 21.3 [+ or -] 6.2
 D 95.4 [+ or -] 3.7 (b)
S. eriophyton A 30.8 [+ or -] 4.2
 M 19.2 [+ or -] 3.1
 D 77.1 [+ or -] 6.0 (b)

Plant Extract 5.00 mg/ml

B. trimera A 14.0 [+ or -] 1.0 (+)
 M 39.0 [+ or -] 5.9 (+)
 D 35.2 [+ or -] 9.5 (+)
H. rigidus A 62.4 [+ or -] 14.4 (+)
 M 52.5 [+ or -] 2.1 (+)
 D 57.0 [+ or -] 11.8 (+)
H. saururus A 7.3 [+ or -] 6.9
 M 46.3 [+ or -] 1.7 (+)
 D 60.9 [+ or -] 9.8 (+)
M. ilicifolia A 3.1 [+ or -] 2.7
 M 39.5 [+ or -] 16.4 (+)
 D 50.3 [+ or -] 8.6 (+)
S. parvifolia A 58.1 [+ or -] 8.3 (+)
 M 47.4 [+ or -] 9.1 (+)
 D --
S. eriophyton A 70.2 [+ or -] 6.7 (+)
 M 81.8 [+ or -] 5.6 (+)
 D 94.2 [+ or -] 7.7 (+)

Plant Extract 10.00 mg/ml

B. trimera A 30.2 [+ or -] 6.0 *
 M 74.0 [+ or -] 1.4 *
 D 49.8 [+ or -] 3.5 *
H. rigidus A 90.1 [+ or -] 8.8 *
 M 77.6 [+ or -] 3.6 *
 D 79.2 [+ or -] 1.4 *
H. saururus A 14.3 [+ or -] 12.4
 M 88.1 [+ or -] 2.0 *
 D 87.4 [+ or -] 11.7 *
M. ilicifolia A 19.5 [+ or -] 2.5 *
 M 64.6 [+ or -] 8.5 *
 D 69.0 [+ or -] 3.9 *
S. parvifolia A 70.7 [+ or -] 3.0 *
 M 84.2 [+ or -] 8.6 *
 D --
S. eriophyton A 97.4 [+ or -] 3.2 *
 M 96.8 [+ or -] 3.6 *
 D --

Values are mean [+ or -] SEM (n = 4). (a) p < 0.05 vs 0.62 mg/ml,
(b) p < 0.05 vs 1.25 mg/ml, (+) p < 0.05 vs 2.5 mg/ml, * p < 0.05
vs 5.0 mg/ml.

Table 4. Effect (% of relaxation) of Sildenafil citrate on
L-phenylephrine precontracted corpus covernosum strips.

Sildenafil concentration ([micro]g/ml % of relaxation

0.35 15.8 [+ or -] 6.2
3.50 17.0 [+ or -] 7.1
10.0 25.4 [+ or -] 4.8
20.00 33.6 [+ or -] 4.9
35.00 43.3 [+ or -] 6.6

Values are mean [+ or -]


Acknowledgements

The authors are indebted to NAPRALERT for providing bibliographical data and to Prof. Dr. M. Wagner for the botanical identification of plant material. This work was supported by IQUIMEFA-CONICET.

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* Address

O. Hnatyszyn. Catedra de Farmacognosia, IQUIMEFA (UBA-CONICET), Facultad de Farmacia y Bioquimica, Universidad de Buenos Aires. Junin 956, (1113) Buenos Aires, Argentina Fax: ++54-11-4508-3642; e-mail: ohnatys@ffyb.uba.ar
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Author:Hnatyszyn, O.; Moscatelli, V.; Garcia, J.; Rondina, R.; Costa, M.; Arranz, C.; Balaszczuk, A.; Ferra
Publication:Phytomedicine: International Journal of Phytotherapy & Phytopharmacology
Geographic Code:3ARGE
Date:Nov 1, 2003
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