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Medicinal Plants in the Treatment of Colitis: Evidence from Preclinical Studies

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Medicinal Plants in the Treatment of Colitis: Evidence from Preclinical Studies Reviews Medicinal Plants in the Treatment of Colitis: Evidence from Preclinical Studies Authors ABSTRACT Marília T. Santana, Luana M. Cercato, Janaíne P. Oliveira, Ulcerative colitis is a chronic inflammatory condition whose Enilton A. Camargo treatment includes aminosalicylates, corticosteroids, and im- munomodulators. Medicinal plants seem to be an important Affiliation alternative treatment for this condition. They have been the Department of Physiology, Federal University of Sergipe, subject of a great number of studies in recent years. This São Cristóvão, SE, Brazil study was conducted to systematically review the medicinal plants tested in experimental models of ulcerative colitis. We Key words conducted a systematic literature search through specialized ulcerative colitis, medicinal plant, phytotherapy, flavonoid, databases (PUBMED, SCOPUS, EMBASE, MEDLINE, LILACS, terpene SCIELO, and SCISEARCH) and selected articles published be- tween January 2000 and June 21, 2016 by using “medicinal received November 11, 2016 plants” and “ulcerative colitis” as key words. Sixty-eight stud- revised January 17, 2017 ies were included, and the families Asteraceae and Lamiaceae accepted February 20, 2017 presented the largest number of studies, but plants from sev- Bibliography eral other families were cited; many of them have shown DOI http://dx.doi.org/10.1055/s-0043-104933 good results in experimental animals. However, only a few Published online March 14, 2017 | Planta Med 2017; 83: 588– species (such as Andrographis paniculata and Punica granatum) 614 © Georg Thieme Verlag KG Stuttgart · New York | have undergone clinical tests against ulcerative colitis, and ISSN 0032‑0943 the observation that many preclinical studies reviewed are purely descriptive has certainly contributed to this fact. Correspondence Chemical constituents (mainly flavonoids and terpenes) seem Prof. Dr. Enilton A. Camargo to play a role in the effects of the plants. Thus, the data herein Department of Physiology, Federal University of Sergipe (UFS) reviewed reinforce the potential of medicinal plants as a Marechal Rondon Avenue, 49100–000 São Cristóvão, SE, source of alternative approaches to the treatment of ulcera- Brazil tive colitis. Phone: + 557931946351, Fax: + 557921051787 [email protected] The symptoms of UC emerge from gastrointestinal tract in- Introduction flammation that leads to chronic tissue damage in susceptible individuals exposed to environmental risk factors. The etiology IBDs mainly comprise two different clinical conditions, UC and remains unknown, although alterations in innate and adaptive Crohnʼs disease, that bear distinct characteristics, since UC is re- immune pathways seem to be involved in this process [3]. stricted to the colon and rectum and Crohnʼs disease may affect In addition, an imbalance in proinflammatory cytokines, such any region of the gastrointestinal tract [1]. The main symptoms as TNF-α, IFN-γ, IL-1, IL-6, and IL-12, and anti-inflammatory cyto- of UC include diarrhea, abdominal cramps, and rectal bleeding, kines, including IL-4, IL-10, and IL-11, is suggested to be crucial in while Crohnʼs disease causes abdominal pain, diarrhea, fatigue, the modulation of the inflammatory process [4]. A significant weight loss, and occasional bleeding as common symptoms. number of studies support this hypothesis in experimental mod- Although there are few epidemiologic data from developing els of intestinal inflammation that have been generated [5]. countries, the incidence and prevalence of UC has been increasing The ideal therapeutic strategies for patients with UC should over the decades and in different regions worldwide, indicating its not only induce remission, but also maintain long-term remission emergence as a global disease. In Brazil, Parente et al. [2] demon- as well as reduce abnormal colon inflammation, diarrhea, rectal strated a predominance of UC in people who are under 40 years bleeding, and abdominal pain. Generally, anti-inflammatory old, mixed-race, or low-income in the geographic area of North- drugs, such as 5-aminosalicylic acid, corticosteroids (dexametha- eastern Brazil. sone), immunosuppressive drugs, 6-mercaptopurine, and aza- 588 Santana MT et al. Medicinal Plants in … Planta Med 2017; 83: 588–614 ABBREVIATIONS Search Strategy CAT catalase COX cyclooxygenase A systematic review was carried out through a literature search DAI disease activity index performed in June 2016 and included articles published over a pe- DSS dextran sulfate sodium riod of 16 years (from January 2000 to June 21, 2016). This litera- GPx glutathione peroxidase ture search was performed through specialized databases GSH glutathione (PUBMED, SCOPUS, EMBASE, MEDLINE, LILACS, SCIELO and IBDs inflammatory bowel diseases SCISEARCH) using different combinations of the following MeSH IFN-γ interferon gamma terms: medicinal plants and ulcerative colitis. The inclusion crite- IL interleukin ria used for manuscript selection considered original articles pub- iNOS inducible nitric oxide synthase lished in English, Spanish, and Portuguese, articles with the key JNK c-Jun N-terminal kinase words in the title, abstract, or full text, and studies that used LDH lactate dehydrogenase plants for treating UC. Studies targeting only isolated secondary MAPK mitogen-activated protein kinases metabolites, combinations of two or more plants, or other associ- MDA malondialdehyde ated types of pathology (like colon carcinogenesis) were excluded MPO myeloperoxidase from the search. NF-κB nuclear factor-κB For the selection of the manuscripts, two independent investi- NO nitric oxide gators (M. T. S. S. and L. M. C.) first selected the articles by analyz- PGE2 prostaglandin E2 ing the titles. The abstracts of the selected articles were then an- PI3K phosphatidylinositol 3-kinases alyzed, and finally the full texts of the articles were evaluated. Any p-JNK phosphorylated c-Jun N-terminal kinase disagreement was resolved through a consensus between the in- p-p38 phosphorylated p38 kinase vestigators. The resulting articles were manually reviewed with SOD superoxide dismutase the goal of identifying and excluding the studies that did not fit STAT signal transducer and activator of transcription the criteria described above. The selected studies were submitted TNBS 2,4,6-Trinitrobenzenesulfonic acid to a hand search, and the cited references that met the inclusion TNF-α tumor necrosis factor-α criteria were also included. UC ulcerative colitis All the selected studies were submitted to data extraction by two collaborators (L. M. C. and M. T. S. S.) using a standardized form and were verified for their quality and accuracy by a third collaborator (E. A. C.). The information extracted included the spe- cies and family of the plants, the part of the plant used, the dose thioprine, are used [6]. Another alternative for the treatment of and route used, the animal model of colitis, a summary of the re- UC is the use of biological agents, such as anti-TNF-α agents, sults, the bioactive compounds found, the study selected, and the which were the first biological agents applied to treat UC. Other reference. examples include infliximab and adalimumab, which are currently To guide the discussion of data, the selected articles were di- in use for treating UC. Recently, golimumab, another anti-TNF-α vided according to the families of plants and were also submitted agent, and vedolizumab, an anti-adhesion therapy, have been ap- to additional analysis that considered the following: i) whether the proved for UC treatment [7]. effect of the medicinal plant on colitis was not purely descriptive Because of potential adverse events and the lack of effective- and was accompanied by any evidence about the mechanism ness of standard therapies, a widespread search has been underlying the effect and ii) whether any isolated compound was launched to identify new therapies from natural sources to re- described for such plants and was related to the beneficial effect place or complement actual drug options for UC treatment. In this on colitis by the selected study itself or other studies presented in way, medicinal plants are considered a potential resource to con- the literature. trol various diseases, including UC. Many articles have reported the importance of medicinal plants in the treatment of UC [8–10]. Some systematic reviews have been conducted in order to Data evaluation and outcomes evaluate the efficacy of herbal therapy in the treatment of pa- tients with IBDs, including UC [11,12]. These studies have shown This review searched for plants with anti-inflammatory activity on a great need for randomized, controlled trials with less limitation UC over the past 16 years. The primary search identified 379 and heterogeneity in spite of the promising effects found in pre- articles (93 from PUBMED, 180 from SCOPUS, 31 from EMBASE, clinical studies on medicinal plants in UC. Thus, the aim of the 56 from MEDLINE, 17 from SCISEARCH, 1 from SCIELO, and 1 from present study was to develop a systematic review to analyze LILACS). whether medicinal plants have efficacy in the treatment of UC in After the initial screening of titles, abstracts, and full text and experimental studies, which represents an important step for the exclusion of repetitions, 43 articles were selected. The hand making decisions on translational advances. search in the references of the selected articles allowed for the identification of 25 additional articles that met the inclusion crite- Santana MT et al.
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