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Raphanus Sativus L. Var Niger As a Source of Phytochemicals for the Prevention of Cholesterol Gallstones

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Raphanus Sativus L. Var Niger As a Source of Phytochemicals for the Prevention of Cholesterol Gallstones PHYTOTHERAPY RESEARCH Phytother. Res. (2013) Published online in Wiley Online Library (wileyonlinelibrary.com) DOI: 10.1002/ptr.4964 Raphanus sativus L. var niger as a source of Phytochemicals for the Prevention of Cholesterol Gallstones Ibrahim Guillermo Castro-Torres,1* Minarda De la O-Arciniega,2 Janeth Gallegos-Estudillo,3 Elia Brosla Naranjo-Rodríguez4 and Miguel Ángel Domínguez-Ortíz3 1Instituto de Química, Universidad Nacional Autónoma de México, México, D.F., México, 2Área Académica de Farmacia, Instituto de Ciencias de la Salud, Universidad Autónoma del Estado de Hidalgo, Pachuca de Soto, Hidalgo, México 3Laboratorio de Productos Naturales, Instituto de Ciencias Básicas, Universidad Veracruzana, XalapadeEnríquez,Veracruz,México 4Laboratorio de Neurofarmacología, Departamento de Farmacia, Facultad de Química, Universidad Nacional Autónoma de México, México, D.F., México, Raphanus sativus L. var niger (black radish) is a plant of the cruciferous family with important ethnobotanical uses for the treatment of gallstones in Mexican traditional medicine. It has been established that the juice of black radish decreases cholesterol levels in plasma and dissolves gallstones in mice. Glucosinolates, the main secondary metabolites of black radish, can hydrolyze into its respective isothiocyanates and have already demonstrated antioxidant properties as well as their ability to diminish hepatic cholesterol levels; such therapeutic effects can prevent the formation of cholesterol gallstones. This disease is considered a current problem of public health. In the present review, we analyze and discuss the therapeutic effects of the main glucosinolates of black radish, as well as the effects that this plant has on cholesterol gallstones disease. Copyright © 2013 John Wiley & Sons, Ltd. Keywords: Raphanus sativus L. var niger; gallstones; glucosinolates; cholesterol. levels, important effects that not only serve for treating the INTRODUCTION disease, but also to prevent it (Castro-Torres et al., 2012). The secondary metabolites of the black radish are mainly Cholesterol gallstones are a highly prevalent affection glucosinolates, of which glucoraphasatin represents more in Western countries such as the United States; in Latin than 65% of them (Hanlon et al., 2007); this component America, it is prevalent in countries such as Chile, and its hydrolysis product, called raphasatin, have Mexico and Argentina (Portincasa et al., 2006). As this demonstrated to possess antioxidant properties in disease produces a high number of medical consultations different biological models and that these effects can and hospital admissions, it is thought to be a public prevent the appearance of oxygen reactive species, health problem; its pharmacological treatment is very which can appear in conditions that are also suitable for limited (Di Ciaula et al., 2010), and the invasive prophylactic the appearance of gallstones, due to the high concentration therapy for symptomatic gallstones is cholecystectomy, of hepatic cholesterol. Oxygen reactive species damage the or the removal of the gallbladder (Portincasa et al., gallbladder epithelium and, due to the constant secretion 2012). Because of this, research focuses on the search of biliary cholesterol, produce a pathophysiological for preventive treatments; the possible preventive effects imbalance which ends with the formation of a gallstone of numerous proteins that participate in the transport (Koppisetti et al., 2008); therefore, glucoraphasatin and and metabolism of biliary lipids have been investigated, raphasatin could be two natural agents that prevent both such as ATP or ABC-binding cassette: ABCB11, ABCB4, the formation of oxygen reactive species and cholesterol ABCG5 and ABCG8 (Castro-Torres, 2012; Stokes gallstones. Another glucosinolate present in black radish and Lammert, 2011). Treatments based on traditional is glucoraphanin, which yields sulforaphane as a product medicine are highly relevant, and researching them is of its immediate hydrolysis; in addition to the antioxidant a complex matter. In Mexican traditional medicine, the properties of these metabolites, they also diminish hepatic black radish has been used since ancient times for treating cholesterol levels by inhibiting the expression of enzymes gallstones (Castro-Torres and Naranjo-Rodríguez, 2012), and transcription factors associated with cholesterol stimulating the biliary function and to treat some digestive metabolism (Rodríguez-Cantú et al., 2011). Black radish problems caused by the high intake of fats (Lugasi et al., contains important metabolites for the prevention of 2005). It is now known that black radish juice can be used gallstones; in this review, we discuss the reports that for treating gallstones in mice fed with a lithogenic diet support this therapeutic mechanism. (rich in cholesterol and cholic acid) and that it has the property of diminishing serum triglycerides and cholesterol Raphanus sativus L. var niger * Correspondence to: Ibrahim Guillermo Castro-Torres, Prof. Instituto de Química, Universidad Nacional Autónoma de México, Circuito Exterior s/n, Ciudad Universitaria, C.P. 04510, Delegación Coyoacán, México, D.F., México. This plant, popularly known as black radish, belongs to the E-mail: [email protected] cruciferous family, which includes cabbage, cauliflower, red Received 16 March 2012 Revised 27 January 2013 Copyright © 2013 John Wiley & Sons, Ltd. Accepted 01 February 2013 I. G. CASTRO-TORRES ET AL. radishes, spinach and broccoli (Sipos et al., 2002). The medicine, called ezetimibe, which inhibits the expression origin of black radish is not known exactly; nevertheless, of the Niemann-Pick type C1 type 1 (NPC1L1) protein in many Asian and African regions, it is used for treating and thereby diminishing the rate of intestinal absorption different problems associated with the gastrointestinal, of cholesterol (de Bari et al., 2012). Ezetimibe inhibits hepatic and biliary systems (Vargas et al., 1999). Its effects the formation of cholesterol gallstones in experimental have not been scientifically demonstrated; they are only models (Wang et al., 2008; Zúñiga et al., 2008); regrettably, known from ethnobotanical information. In Mexico, the there are no specific clinical studies that can evaluate plant is used to treat pigmented and cholesterol gallstones the effect of NPC1L1 expression in the prevention (Castro-Torres et al., 2012). We know that treatment is of gallstones. The pharmacological treatment has its a different concept from prevention; in the search limitations; the medications used as prophylactics are: for curative and preventive treatments for cholesterol ursodeoxycholic acid, ezetimibe and statins (Di Ciaula gallstones, the essential thing is to diminish the concen- et al., 2010); it is important to mention that when tration of intestinal, hepatic and biliary cholesterol, and gallstones are already formed, these therapeutic also, although less importantly, of plasmatic cholesterol. agents present a low capacity to dissolve them, Black radish is capable of diminishing serum lipids ursodeoxycholic acid being the most used medicine for in C57BL/6 mice, an important species that develops it, but, in order to work, gallstones should be strictly of gallstones (Castro-Torres and Naranjo-Rodríguez, cholesterol, and they must be within a gallbladder with 2012); the decrease of serological cholesterol can be a adequate motility. The search for a therapeutic target is factor associated with the development of gallstones, but focused on biliary secretion and the intestinal absorption it does not necessarily indicate that there is a constant of cholesterol, but it is very important to consider biliary lipid secretion; nevertheless, black radish can also the production of reactivate oxygen species, which dissolve cholesterol gallstones in mice (Castro-Torres are produced by cholesterol loading and that cause et al., 2012), which demonstrates the strong effect it secretion rates to exceed normal levels. Considering has on cholesterol that is already crystallized and inside these species to be target molecules and knowing a matrix of glycoproteins. Moreover, if it can disintegrate that they can be produced in both hepatocytes and in gallstones, it is probable that it can diminish biliary the vesicular epithelium, the glucosinolates and their cholesterol concentration; these factors are indeed essential degradation products (with antioxidant capacity) that for avoiding the formation of lithiasis. No toxicity related are present in black radish might impede the formation to the different therapeutic effects of black radish has of gallstones in the gallbladder and at the same time been reported, but, with respect to cholesterol gallstones diminish biliary cholesterol secretion by reducing treatment, we have reported that the DL50 of black radish hepatic cholesterol. juice is over 5000 mg/kg (Castro-Torres et al., 2012), which allow us to think that the natural product is not toxic, that it is effective and that it is not necessary to look for a lethal Glucosinolates dose at higher values than the one we analyzed because therapeutic effects produced with minimal doses are Glucosinolates are biologically active secondary metabolites preferred. In Mexico, there are also ethnobotanical uses that play an interspecific and intraspecific role in the of the plant for the treatment of pigment gallstones, which Brassicaceae family of plants (Sønderby et al., 2010). have a pathophysiology different from that of cholesterol
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