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Heliopsis Longipes: Anti-Arthritic Activity Evaluated in a Freund’S Revista Brasileira de Farmacognosia 27 (2017) 214–219 ww w.elsevier.com/locate/bjp Original Article Heliopsis longipes: anti-arthritic activity evaluated in a Freund’s adjuvant-induced model in rodents a,∗ b Carolina Escobedo-Martínez , Silvia Laura Guzmán-Gutiérrez , a c a María de los Milagros Hernández-Méndez , Julia Cassani , Alfonso Trujillo-Valdivia , a d Luis Manuel Orozco-Castellanos , Raúl G. Enríquez a Departamento de Farmacia, División de Ciencias Naturales y Exactas, Universidad de Guanajuato, Guanajuato, Mexico b Catedrática CONACyT, Departamento de Inmunología, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, México, DF, Mexico c Departamento de Sistemas Biológicos, Universidad Autónoma Metropolitana Unidad Xochimilco, México, DF, Mexico d Instituto de Química, Universidad Nacional Autónoma de México, México, DF, Mexico a b s t r a c t a r t i c l e i n f o Article history: This study assesses the anti-arthritic effect of the affinin-enriched (spilanthol, main alkamide) hexane Received 26 June 2016 extract from the roots of Heliopsis longipes (A. Gray) S.F. Blake, Asteraceae, on a Freund adjuvant-induced Accepted 5 September 2016 arthritis model in rodents. The extract was orally administered at a dose of 2, 6.6, or 20 mg/kg; a significant Available online 19 October 2016 edema-inhibitory activity in the acute and chronic phases was observed with a dose of 2 and 20 mg/kg, respectively. The extract showed higher anti-inflammatory and anti-arthritic effects than the reference Keywords: drug phenylbutazone (80 mg/kg). Moreover, the extract prevented the occurrence of secondary lesions Heliopsis longipes associated to this pharmacological model. Affinin Anti-arthritic © 2016 Sociedade Brasileira de Farmacognosia. Published by Elsevier Editora Ltda. This is an open Complete Freund adjuvant access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). Spilanthol Introduction ideal, Freund’s adjuvant-induced rat arthritis shares several traits with human arthritis, and its sensitivity to evaluate anti-arthritic Rheumatoid arthritis (RA) is an idiopathic auto-immune dis- agents was the basis for its choice as the model to assess the activ- ease, characterized by symmetrical synovitis in large and small ity of the Heliopsis longipes (A. Gray) S.F. Blake, Asteraceae, hexane joints that may lead to progressive articular damage and disability extract (Ekambaram et al., 2010; Tanushree and Saikat, 2013). (Mendoza-Vázquez et al., 2013). Analgesic and anti-inflammatory RA prevalence in developed countries is 0.5–2%, with an annual drugs, including steroids, are used to suppress the symptoms. New incidence of 12–1200 per 100,000 inhabitants. The female:male therapies, like those targeting the tumor necrosis factor alpha ratio is 2–3:1, and the peak age range of onset is 30–55 years (infliximab) or the anti-CD20 therapy (rituximab), which inhibit old, but it could occur at any age. In Mexico, RA affects 1.6% of the underlying immune process, have been proposed. However, all general population, being the main reason for consultation at the these drugs have several undesired effects. Recent research aims to Rheumatology Service (Mendoza-Vázquez et al., 2013; Guía de discover long-acting anti-inflammatory drugs with minimal side Práctica Clínica, Diagnóstico y Tratamiento de Artritis Reumatoide effects (Ekambaram et al., 2010). A number of animal models are del Adulto, México: Secretaría de Salud, 2009). used to evaluate potentially useful compounds against RA, and the H. longipes is a perennial herb, endemic in a region comprising choice of a particular model depends on the immunological prop- parts of Sierra de Alvarez and Sierra Gorda, near the triple border of erties being observed in the model and their relation with the San Luis Potosi, Guanajuato and Queretaro, in Central Mexico. The human disease. Among the available models is collagen-induced common names for this plant are chilcuague, pelitre, golden root, or adjuvant-induced (e.g., Freund’s adjuvant) arthritis in rodents, and Aztec root (Cilia-López et al., 2008). The paralyzing and toxic spontaneous arthritis induced by TNF-␣ or genetic models, like the action against flies and other insects of H. longipes root extracts transgenic animal model. While no RA model can be considered was discovered as similar as that of pyrethrins during World War II (Acree et al., 1945). Fortunately, chilcuague did not become extinct after the expor- ∗ tation boom, even though its wild population was severely reduced. Corresponding author. E-mail: [email protected] (C. Escobedo-Martínez). To date, land plots solely dedicated to the cultivation of this species, http://dx.doi.org/10.1016/j.bjp.2016.09.003 0102-695X/© 2016 Sociedade Brasileira de Farmacognosia. Published by Elsevier Editora Ltda. This is an open access article under the CC BY-NC-ND license (http:// creativecommons.org/licenses/by-nc-nd/4.0/). C. Escobedo-Martínez et al. / Revista Brasileira de Farmacognosia 27 (2017) 214–219 215 disseminated either by seed or by cutting, can be found between Materials and methods Guanajuato and Queretaro; the root is fully developed after 2–3 years (García-Chávez et al., 2004). It is the most economically Plant material important species in its genus; its root is used in the region as a cooking condiment, and it is added to alcoholic beverages to Heliopsis longipes (A. Gray). S.F. Blake, Asteraceae, roots were col- improve taste. In traditional medicine, chilcuague root is used to lected on February 16, 2014, 2:14:59 pm, within the boundaries of ◦ ◦ treat respiratory diseases, as an anesthetic to treat tooth and mus- a land plot in Beltran community (N 21 16.427 , W 100 0.2672 ) at cular aches, to treat buccal lesions, and as an anti-parasitic (Cilia 1780 m above sea level, Xichu municipality, in Guanajuato, Mexico. López, 2007). Several alkamides have been isolated from H. longipes, After proper identification, five plant specimens were deposited in but affinin, also known as spilanthol ((2E,6Z,8E)-N-isobutyl-2,6,8- the Isidro Palacios herbarium (SLPM), at the Universidad Autónoma decatrienamide), was identified as the main alkamide in the plant de San Luis (No. 048150). (Molina-Torres et al., 1996; García-Chávez et al., 2004; Hernández et al., 2009). The oily substance causes intense lip numbness and Extraction tingling within a few minutes after placed in the mouth, and it also stimulates salivation (Correa et al., 1971). H. longipes is also Dry, ground H. longipes roots (1285 g) were macerated for three reported to produce analgesia and anti-inflammation in human consecutive times: First component extraction was performed dental and oral pathologies (Colvard et al., 2006). Additionally, it with 2.5 l of hexane for 2 h; then, the recovered extract solu- has been reported that H. longipes dichloromethane extract showed tion (1750 ml) was evaporated, yielding a dark yellow, viscous oil analgesic activity, as demonstrated in vitro by releasing of gamma- (26.386 g, labeled as Hl-A). A second maceration was performed on aminobutyric acid (GABA) in mouse brain slices; the increase in the same plant material after the first extraction, adding 1.250 l of GABA release in a region of cerebral cortex leads to sustained hexane and left for 24 h; extract solution (1 l) was recovered, and analgesia, favoring a descendent inhibition of nociceptive spinal after evaporation it yielded 12.29 g of viscous oil, labeled as Hl-B. A neurons (Ríos et al., 2007). third and last maceration was performed as described above, using With regard to anti-inflammatory activity, Hernández et al. 1.5 l of hexane for 4 h, recovering an extract solution (900 ml) and (2009) evaluated H. longipes ethanolic extract and purified affinin yielding 3.469 g of viscous oil, labeled as Hl-C. Each maceration was on mouse ear edema induced by either arachidonic acid (AA) monitored by thin-layer chromatography. The Hl-A sample yielded or phorbol 12-myristate 13-acetate (PMA), demonstrating a sig- 26.386 g of affinin (1), with a 95% purity. nificant anti-inflammatory effect. DE50 values of 0.8 mg/ear and 1.2 mg/ear were obtained, respectively, in the AA-induced edema model; nimesulide (1 mg/ear) was used as reference drug. In the PMA-induced edema model, the ethanolic extract and affinin showed a dose-dependent anti-inflammatory effect with DE50 val- ues of 2 mg/ear and 1.3 mg/ear, respectively, using indometacin (3 mg/ear) as reference drug. On the other hand, Cilia-López et al. (2010) evaluated the anal- gesic activity of H. longipes ethanolic extract and affinin and their HPLC and NMR analysis effect on the central nervous system on a mouse model; both affinin (1 mg/kg) and H. longipes root ethanolic extract (10 mg/kg) showed High performance liquid chromatography (HPLC) analysis of the an analgesic action similar to ketorolac (6 mg/kg), as assessed by Hl-A sample was performed in a Waters 1525 Binary HPLC pump pain induction with acetic acid and thermal stimulation (hot plate); equipment, controlled by Breeze software. A 15 cm × 4.6 mm, C18 also, H. longipes extract and affinin showed a stimulant effect on Kromasil 100-5 column was used, coupled to a diode array detector the central nervous system comparable to caffeine, as measured by (maximum absorbance was set to 230 nm). A water-acetonitrile the Irwin test. Carino-Cortés˜ et al. (2010) evaluated the cytotoxic gradient from 60:40 to 30:70 in 25 min was used for elution, at a potential of H. longipes ethanolic extract by recording the vari- flow rate of 1 ml/min (Fig. 1). ability in the count of micronucleated polychromatic erythrocytes Magnetic nuclear resonance (NMR) measurements for the Hl- induced by the extract and the ratio of polychromatic erythro- A sample were acquired in an Agilent 600 MHz, DD2, Oneprobe cytes with respect to normochromatic erythrocytes; no significant 1 13 equipment for H y C in CDCl solution, using tetramethylsilane cytotoxic effect was observed.
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