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Bryophyllum Pinnatum and Related Species Used in Anthroposophic Medicine: Constituents, Pharmacological Activities, and Clinical Efficacy*

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Bryophyllum Pinnatum and Related Species Used in Anthroposophic Medicine: Constituents, Pharmacological Activities, and Clinical Efficacy* 930 Reviews Bryophyllum pinnatum and Related Species Used in Anthroposophic Medicine: Constituents, Pharmacological Activities, and Clinical Efficacy* Authors Karin Fürer 1, 2, Ana Paula Simões-Wüst 2, Ursula von Mandach2, Matthias Hamburger1, Olivier Potterat 1 Affiliations 1 Division of Pharmaceutical Biology, Department of Pharmaceutical Sciences, University of Basel, Basel, Switzerland 2 Department of Obstetrics, University Hospital Zurich, Zurich, Switzerland Key words Abstract phyllum daigremontianum and Bryophyllum dela- l" Bryophyllum pinnatum ! goense, have also been included. Taken together, l" Bryophyllum daigremon- Bryophyllum pinnatum (syn. Kalanchoe pinnata)is current data support the use of B. pinnatum for tianum a succulent perennial plant native to Madagascar the mentioned indications, but further studies l" Bryophyllum delagoense that was introduced in anthroposophic medicine are needed to fully understand the modes of ac- l" Crassulaceae l" constituents in the early 20th century. In recent years, we con- tion, and to identify the pharmacologically active l" anthroposophic medicine ducted a large collaborative project to provide re- constituents. l" pharmacological activities liable data on the chemical composition, pharma- l" clinical studies cological properties, and clinical efficacy of Bryo- phyllum. Here, we comprehensively review the Abbreviations phytochemistry, as well as the pharmacological ! and clinical data. As to the pharmacology, special AM: anthroposophic medicine emphasis is given to properties related to the use AUC: area under the curve in anthroposophic medicine as a treatment for GABA: γ-aminobutyric acid “hyperactivity diseases”, such as preterm labor, i.v.: intravenous restlessness, and sleep disorders. Studies suggest- i.p.: intraperitoneal ing that B. pinnatum may become a new treat- NO: nitric oxide ment option for overactive bladder syndrome are OAB: overactive bladder also reviewed. Tolerability is addressed, and toxi- p.o.: per os (oral administration) cological data are discussed in conjunction with the presence of potentially toxic bufadienolides Supporting information available online at in Bryophyllum species. The few data available on http://www.thieme-connect.de/products received February 29, 2016 two related species with medicinal uses, Bryo- revised March 23, 2016 accepted April 6, 2016 Bibliography Introduction B. pinnatum from the perspective of rational phy- DOI http://dx.doi.org/ ! totherapy. Some years ago we therefore embarked 10.1055/s-0042-106727 Published online May 24, 2016 Bryophyllum pinnatum (Crassulaceae) is a peren- within the Bryophyllum Study Group (see ac- Planta Med 2016; 82: 930–941 nial succulent herb originating from Madagascar knowledgments) in a large collaborative project © Georg Thieme Verlag KG with a long tradition of use in tropical countries. on B. pinnatum with the aim to provide reliable Stuttgart · New York · In Europe, its utilization is more recent and al- clinical, pharmacological, and chemical data on ISSN 0032‑0943 most exclusively restricted to anthroposophic this plant. We review here the current state of Correspondence medicine (AM). Introduced in 1921 by Rudolf knowledge on the phytochemistry, pharmacolog- PD Dr. Olivier Potterat Steiner initially for the treatment of what at that ical properties, and clinical data of B. pinnatum. Division of Pharmaceutical “ ” Biology time was called hysteria , Bryophyllum is now With respect to pharmacology, an emphasis is Department of Pharmaceutical used for a variety of hyperactivity disorders. Until put on properties related to the use in AM, but Sciences very recently, only a few experimental and clini- other bioactivities are also briefly reviewed. University of Basel Klingelbergstraße 50 cal data were available to support the use of Some reviews have been previously published on CH-4056 Basel the constituents and pharmacological activities of Switzerland B. pinnatum [1–3] or, very recently, on the entire Phone: + 41612671534 * Dedicated to Professor Dr. Dr. h.c. mult. Kurt Hostett- Fax: + 416 12671474 mann in recognition of his outstanding contribution to genus Kalanchoe, which includes, according to [email protected] natural product research. some botanical authors, species of the genus Fürer K et al. Bryophyllum pinnatum and… Planta Med 2016; 82: 930–941 Reviews 931 Bryophyllum (see below) [4]. While these reviews describe vari- steroids, phenanthrenes, and some ubiquitous compounds. Data ous compounds and bioactivities, none of them addresses the on the composition of B. daigremontianum and B. delagoense are pharmacological and clinical data that support the therapeutic almost exclusively limited to bufadienolides. use of Bryophyllum preparations in European countries. The present review focuses on B. pinnatum, but the few data Bufadienolides available on Bryophyllum daigremontianum, Bryophyllum dela- Thirteen bufadienolides (1–13), including three glycosides, have goense, and the hybrid Bryophyllum daigremontianum x tubiflo- been reported from B. pinnatum, B. delagoense, B. daigremontia- rum have also been included. The German homeopathic pharma- num, and the hybrid B. daigremontianum x tubiflorum copeia (HAB) 2014 [5] lists the two species B. pinnatum and (l" Table 1, Fig. 1), mostly in conjunction with various bioactiv- B. daigremontianum as officinal in its monography “Bryophyllum ities such as insecticidal and cytotoxic properties [11–23]. A char- Rh”, and both have been used in AM. B. delagoense was intro- acteristic structural feature is the 1,3,5-orthoacetate function, duced in the 1980s as an anthroposophic medicinal product in which is present in about half of these compounds. Bersaldege- Germany, primarily for sedative purposes (Personal communica- nin-1-acetate (1), bersaldegenin-1,3,5-orthoacetate (3), the gly- tion, Dr. med. Siegward-M. Elsas, see Acknowledgments). coside bryotoxin A (7), and bryotoxin C (= bryophyllin A, 4)have been found in all species. In contrast, bryophyllins B (5)andC(6) have been reported only in B. pinnatum, the glycosides kalantu- Botany bosides A (11)andB(12)onlyinB. delagoense, and daigremontia- ! nin (9), daigredorigenin-3-acetate (10), and methyl daigremo- The genus Bryophyllum comprises approximately 25 perennial nate (13) only in B. daigremontianum and/or B. daigremontianum succulent species that are native to Madagascar [6]. Meanwhile, x tubiflorum. The latter compound is listed here on the basis of many of them have been introduced in other tropical areas biogenetic considerations even though it is not a bufadienolide where they have sometimes become invasive plants. The genus but rather a congener with an opened lactone ring. Bufadieno- has an intricate taxonomy, with a variable number of species lides were recently quantified in different batches of leaves and and numerous synonyms, and is regarded by some authors as press juices of B. pinnatum with the aid of UHPLC‑MS/MS. Bryo- one of three sections (Kitchingia, Bryophyllum, and Eukalanchoe) phyllin A (4), bersaldegenin-1-acetate (1), bersaldegenin-3-ace- of the genus Kalanchoe [6–8]. Bryophyllum species have a unique tate (2), and bersaldegenin 1,3,5-orthoacetate (3) were found to mode of vegetative reproduction whereby young plantlets devel- be the main bufadienolides in the analyzed plants, with the total op on the edges of leaves before being shed for propagation. contents in the leaves ranging from 3.78 to 40.50 mg/100 g dry Bryophyllum pinnatum (Lam.) Oken, originally described by La- weight. Interestingly, when single leaves from individual plants marck as Cotyledon pinnata Lam. according to The Plant List [9], were analyzed, the content was found to be significantly higher possesses approx. 20 synonyms including Bryophyllum calycinum in younger leaves. In the same study, the four compounds were Salisb. and Kalanchoe pinnata (Lam.) Pers., a name that is very also quantified in leaves of B. daigremontianum and B. delagoense frequently used in the literature (For the full list of synonyms, [24]. see Table 1 S, Supporting Information). B. pinnatum grows up to 1.5 m in height and is known by numerous vernacular names, Flavonoids such as life plant, air plant, love plant, miracle leaf, cathedral A number of flavonoids have been identified in B. pinnatum.They bells, and Goethe plant. The latter refers to the detailed observa- include numerous flavonol derivatives (14–35), mainly quercetin tions written down by Wolfgang von Goethe (1749–1832) about and kaempferol glycosides, as well as a few flavone glycosides, this plant. Bryophyllum daigremontianum (Raym.-Hamet & such as acacetin, luteolin, and diosmetin glycosides (36–40) Perrier) A.Berger (syn. Kalanchoe daigremontiana Raym.-Hamet (l" Table 2, Fig. 2)[13,25–36]. In addition, epigallocatechin-3-O- & H. Perrier) is somewhat smaller (up to 1 m) and commonly syringate (41) [36] and an ethenylamino-substituted anthocyani- known as mother of millions, or devilʼs backbone. Bryophyllum din with a biogenetically unlikely structure [37] have been re- delagoense (Eckl. & Zeyh.) Druce (syn. Bryophyllum tubiflorum ported. Harv., Bryophyllum verticillatum (Eliott) A. Berger, Kalanchoe de- To our knowledge, no flavonoids have been reported from B. dai- lagoensis Eckl. & Zeyh., Kalanchoe tubiflora (Harv.) Raym.-Hamet, gremontianum, but quercetin (27), 4′-O-methylherbacetin (42), Kalanchoe tuberosa H. Perrier, and Kalanchoe verticillata Scott- and 3,5,7,8,4′-pentahydroxy-3′-methoxyflavone (43) have been Eliot [9]) grows up to 1.5 m
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