S. aureus; S. epidermidis; S.mutans; C. albicans; C. tropicalis; C. glabrata
Hydroalcoholic bark extract
Ethyl acetate fraction
S. aureus; Bacillus subtilis
Ethyl acetate fraction
C. albicans; C. tropicalis, Cryptococcus neoformans
[42, 114, 115]
Hexanic leaf extract
Methanolic extract and tannin fraction from the bark
SA: S. adstringens. SP: S. polyphyllum. SR: S. rotundifolium.
Interestingly, the hydroalcoholic extract (containing tannin pyrogallates, flavones, flavonols, xanthones, chalcones, aurones, flavononols, and flavonones) showed synergistic activity with the antibiotics gentamicin, kanamycin, amikacin, and neomycin against Escherichia coli and S. aureus . In contrast, a saline extract of the seeds of S. rotundifolium did not inhibit S. aureus, E. coli, and Pseudomonas aeruginosa . Hence, the antibacterial activity of gallic acid and different proanthocyanidins [120, 121] could justify the use of the stem bark of Stryphnodendron spp in disorders as sore throat and dental and urinary infections.
On the other hand, the antifungal activity of the “barbatimão” species is more significant and different studies have attempt to elucidate the mechanism involved in the Candida spp virulence, biofilm inhibition, as well as the main active compound [42, 114, 122]. The propylene glycol extract of S. adstringens inhibited the formation of C. albicans biofilm on acrylic resins . To elucidate the main active compound, Ishida et al.  performed bioguided extract fractionation according to the growth inhibition of C. albicans, which yielded a group of subfractions from the aqueous partition and the ethyl acetate fraction contained the polymer of 2114 Da with six units of flavan-3-ol and one galloyl group. This subfraction had similar inhibitory activity to that of nystatin, but showed fungistatic effect. Moreover, it decreased the Candida spp. virulence effect of adherence and filamentous formation in C. albicans, and enhanced the yeast phagocytosis by macrophage. A similar activity was reported for the polymer-rich subfraction against C. tropicalis, and biofilm reduction was also observed following pretreatment of planktonic cells with the subfraction or treatment during the adherence and matrix formation . Further, the subfraction decreased the metabolic activity of sessile and dispersed cells during biofilm formation and maturation, indicating that the subfraction penetrated the biofilm matrix . These findings are very important to developing strategies for avoiding the contamination of implanted medical devices and dissemination of the infection by dispersion cells .
Genitourinary disorders, especially in women, are among the most ethnopharmacological uses of “barbatimão”, since the widespread and recurrent vulvoginal candidiasis infection  can be treated with the stem bark of Stryphnodendron spp. Furthermore, the proven activity of the stem bark against Candida could contribute to the standardization of the extract and pharmaceutical formulations to effectively combat the pathogen.
In addition, the polymer-rich fraction inhibited the growth of Cryptococcus neoformans despite its fungistatic effect  and the hexanic leaf extract of S. adstringens inhibited the growth of different clinical isolates of the dermatophyte Trychophyton rubrum . These findings could explain the folkloric use of this fraction for itching, chilblain, and dermatitis and is extremely important since both fungi present concerns of resistance to antifungals [127, 128].
The antimicrobial activities of “barbatimão” could be related to the activity of the tannin content. Scalbert  proposed three different tannin antimicrobial mechanisms of action. These are inhibition of enzymes of the microorganism (correlating with protein interaction); microorganism deprivation of nutrients such as metals (explained by the complexation with tannin hydroxyl groups), and inhibition of oxidative phosphorylation (due to the antioxidant property). In addition, it is noteworthy that the compound epigallocatechin 3-O-gallate also exhibits antimicrobial activity. It has shown antibacterial (mainly against gram-positive bacteria), antibiofilm, and anticandidal activities, which enhances the understanding of the Stryphnodendron species antimicrobial activity .
7.5. Effect on diabetes, blood pressure, and diuresis
This revision found only one study on the use of Stryphnodendron spp in diabetes. Low concentrations (1.86 and 0.61 µg/mL) of the ethanolic extract of the bark of S. adstringens inhibited the enzymes α-amylase and α-glucosidase, which indicates its blood glucose-lowering effects . Moreover, the enzymatic inhibition likely corresponds to the general interaction of tannins with proteins, but a more specific interaction with the active site could also be possible [73, 131]. Further studies on diabetes would be important since epigallocatechin 3-O-gallate also improved the insulin sensitivity of rats and myocytes . Another study  reported the reduction of blood pressure in dogs with normal arterial pressure following treatment with 8.2–12.3 mg/kg of acetone:water extract of the bark of S. adstringens and the fractions obtained with ethyl acetate, butanol, and water.
Analysis of the bark of S. adstringens and S. rotundifolium as dry powder on water renal excretion in mice revealed an antidiuretic effect, whereas the dry powder of the seeds of S. rotundifolium induced the claimed diuretic effect with no electrolyte excretion changes [133, 134].
However, the data of the activities described in this section are currently inconclusive and further detailed analysis must be performed to ensure the proper use of extracts in the phytotherapy of diabetes, hypertension, and for diuresis. The evaluation of the toxicity of these extracts is an important topic that needs to be summarized, particularly with the allegedabortive effects of the seeds, which are described later.
7.6. Anthelmintic activity and other promising activities
The claimed folkloric anthelmintic activity of the bark was tested against Schistosoma mansoni using the acetone:water extracts of S. adstringens and S. polyphyllum, which both showed a faster larvicidal activity against miracidia and cercariae forms than the control treatment did . This finding supports the validity of this reported application of the extracts. In addition, extracts of the barks and leaves of S. adstringens and S. polyphyllum showed molluscicidal activity against Biomphalaria glabrata, the snail intermediate host of S. mansoni [136-138].
Studies of the Stryphnodendron spp commenced against protozoans when the acetonic extract of the bark of S. adstringens was shown to inhibit the cell growth of Herpetomonas samuelpessoai. It is a non-pathogenic trypanosomatid used as an experimental model because it shares antigens with Trypanosoma cruzi, causing immune response and is susceptible to the same drugs used to treat T. cruzi. Subsequently, inhibitory concentrations of the acetonic extract as well as the aqueous and ethyl acetate fractions were determined and ultrastructural alterations in cells were observed using transmission electron microscopy, in addition to decreased activity of the mitochondrial enzyme succinate cytochrome c reductase . The extract of S adstringens (100 µg/mL) showed weak growth inhibition of the pathogenic protozoan Leishmania amazonensis in the promastigote and amastigote form and moderate inhibition of T. cruzi in the epimastigote form . In an in vivo study, the ethanolic extract decreased the number of f T. cruzi parasites in the blood of inoculated mice . The ethanolic extracts of the barks of S. adstringens and S. polyphyllum also exhibited trypanocidal activity, reducing the number of parasites in infected mice faster than the control group mice .
Then, an ethanolic extract of the bark of S. rotundifolium and its aqueous and organic fractions were tested against promastigote forms of L. amazonensis, which they highly inhibited and this effect was potent with the tannins isolated from the organic phase. Gallic acid exhibited the best inhibition (50% of promastigote inhibition at 1.7 µg/mL), followed by the epigallocatechin 3-O-gallate . The hydroalcoholic extract of S. rotundifolium was also tested against L. brasiliensis and L. infantum promastigotes and T. cruzi epimastigotes and the mortality rates at 1000 µg/mL were of 56, 45, and 82%, respectively . This observation indicates that the best activity of S. rotundifolium was achieved with the organic fraction and gallic acid was the most active compound against L. amazonensis. These results show the promising antiprotozoal activity of Stryphnodendron species, especially their tannin content, and further analysis should be carried out to determine the inhibitory agents, appropriate concentrations, and in vivo activity.
Ethnopharmacology data indicates the use of the stem bark of S. rotundifolium against influenza and the antiviral activity of S. adstringens bark was assayed using the aqueous and ethyl acetate fractions against poliovirus 1 (P-1) and bovine herpesvirus 1 (BHV-1) in HEp-2 cells. Both extracts inhibited the viral replication and the prodelphinidins catechin, epicatechin, gallocatechin, and epigallocatechin were identified in the ethyl acetate fraction .
Taking together, these results indicate the antiviral activity of the extract and its effective wound healing activity and, therefore, it was formulated and patented as an ointment with different “barbatimão” species for used against the human papillomavirus (HPV), particularly in the prevention of cervical cancer .
Another ointment was formulated using the aqueous extract of S. adstringens, and was found to reduce the hemorrhagic and myotoxic effects in mice caused by the venom of Bothrops pauloensis, and these effects were claimed to be mediated by an interaction between the tannins and the toxic proteins of the venom .
The bark and leaf extracts of S. rotundifolium and S. adstringens had little or no inhibitory effects on Rhipicephalus microplus (tick) , Rhopalosiphummaidis (corn aphid)  and Diabrotica speciose (the larva of this insect perforates potatoes) .
Therefore, the anthelmintic folkloric uses of this species has also been confirmed, but requires further detailed investigation. Among the activities not mentioned in ethnopharmacological surveys, the molluscicidal, antiviral, and antiprotozoal activity should receive more attention to confirm the promising results reported here to facilitate the standardization process for the use of the bark for these applications.
8. Cytotoxicity and toxicology
As seen, stem bark of “barbatimão” from Stryphnodendron spp has diverse use in folk medicine and some of them were confirmed by scientific studies. Therefore, it is very important to ensure the safety of the active extracts and products obtained of the species in this genus.
In that sense, cytotoxic effects against mammalian cell lines is a recurrent property analyzed. The acetonic extract of the barks of S. adstringens did not cause hemolysis of sheep erythrocytes  neither did the aqueous and ethyl acetate fractions and subfractions. The same samples were not cytotoxic at 50% (50% cytotoxic concentration, CC50) of Vero and macrophages J774G8 cells up to 100 µg/mL and showed hemagglutinant effect above 500 µg/mL . Likewise, the ethanolic extract, aqueous, and organic fractions of S. rotundifolium and the isolated compounds gallic acid, gallocatechin, epigallocatechin, catechin, and epigallocatechin 3-O-gallate showed CC50 against macrophages at 100-300 µg/mL and did not cause lysis of human red blood cells ; the hydroalcoholic extract of S. rotundifolium showed CC50 against fibroblast cells at 190.24 µg/mL . According to all these reports, it is important to pay attention to the active concentration of samples to each biological activity and evaluate whether the cytotoxic concentration is smaller to indicate safe use. For example, ethyl acetate subfraction polymer-rich has anti-Candida activity bellow 10 µg/mL, whereas antibacterial and anti-protozoal activities are achieved close to 1000 µg/mL.
Cytotoxicity by genotoxic effects of ethanolic extracts of S. adstringens was evaluated but no DNA damage was observed, for instance, no mutagenicity activity was observed with the Ames test using Salmonella typhimurium strains , or by somatic mutation and recombination test or by chromosome damage in germ cells of Drosophila melanogaster, or even by mutation in larvae or in adult male of the same insect . Otherwise, it was shown that aqueous extract and fraction and hydroalcoholic extract of the leaves of S. adstringens exhibited antigenotoxic effects by reducing DNA damage and micronuclei formation in bone marrow cells from rats treated with the genotoxic cyclophosphamide .
Acute toxicity and 50% lethal dose (LD50) are somewhat different among the extracts of S. adstringens. The LD50 of hydroalcoholic bark extract was considered high, at the concentration of 250 µg/mL, when administrated intraperitoneally in mice for 14 days . An alcoholic extract of S. adstringens showed LD50 of 250 mg/kg also intraperitoneally in mice, did not show skin primary irritation or ocular alterations in rabbits . No behavioral change was observed in rats receiving acetonic extract, and it did not show high LD50 (2699 mg/kg) though daily oral dose of 800 mg/kg for 30 days decreased the animals weight, promoted thymic involution and increased glucose and aspartate aminotransferase levels in their plasma . Those effects could reflect alterations in cell metabolism and it was observed that the extract impaired mitochondrial oxidative phosphorylation and liver metabolism by increasing oxygen consumption . In opposition, a methanolic extract did not show acute toxicity or histological alterations in liver and kidney of treated rats, neither showed hepatic or renal dysfunctions in rabbits .
However, when evaluating genotoxicity and acute toxicity of the polymer-rich subfraction obtained from the ethyl acetate fraction of the barks of S. adstringens, a safer sample was detected. In fact, it is possible to see a cytoprotective effect against mutagenicity, low cytotoxicity against Artemia salina , a LD50 higher than 3000 mg/kg in mice and chronic toxicity evaluation for 90 days with 200 mg/kg of the subfraction did not show biochemical, hematological, and histopathological effects . Meanwhile, epigallocatechin 3-O-gallate caused hepatocyte disfunction and damage to mitochondria at high doses  and embryonic cytotoxicity .
Although broad beans of Stryphnodendron spp are not ethnopharmacologically used, it is worthy to point their abortive effect in animals. To confirm the information of farmers about cow abortion after consuming the beans from S. rotundifolium, a study administered 5 g/kg/day for 9 to 26 days. In fact, four out of seven cows had abortion and the behavior of others was abnormal, with decrease in activity and appetite, salivation, difficulty in getting up, unstable gait, muscular tremors, and loss of weight . Evaluation of toxic dose showed death of bovines with 60 g/kg of broad beans administered once and death from 10 g/kg for repeated days. Other diverse poisoning symptoms were also observed as well as diverse histopathological alterations [161, 162]. Seed extracts of S. adstringens and S. polyphyllum showed abortive effect on female rats, corroborating to the attention needed for trees in farms with animals .
A congruent evaluation of cytotoxic and toxic effects and doses correlated with the different biological activities is still required for ensuring the safe use of the barks of “barbatimão” as well as the use of isolated compounds. No teratogenic or neurotoxicity have been reported for the extracts in animals or humans.
Ethnoknowledge is still one of the most important tools for drug discovery, and phytotherapeutic treatments are easily accessible to the majority of the population. Ethnopharmacological uses of “barbatimão” from the genus Stryphnodendron genus were confirmed for different purposes, which would help guide the best approach for handling the stem bark extracts by the general population and would stimulate the development of pharmaceutical formulations. Topical use of the bark extract as a wound-healing agent, in order to take advantage of its antimicrobial action, is a well-established application of Stryphnodendron spp. Unfortunately, there is still insufficient scientific data about the correlation between dosage and pharmacological and toxicological parameters with regard to other activities, which can be explored as long as the mechanism of action of the bioactive compounds. A better understanding of those parameters could also motivate further studies on tannin from “barbatimão” aid the development of a drug that may be made available worldwide. It is also important to bear in mind the need to conserve these plants by adopting appropriate harvesting of the barks.
Acknowledgments:This study was supported by PADC-UNESP.
Author Contributions:All authors contributed substantially to this research. Tatiana M. Souza-Moreira and Geisiany M. Queiroz-Fernandes were responsible for the bibliographic search, analysis, and manuscript writing; Rosemeire C.L.R. Pietro was mainly responsible for conceiving the manuscript and critical revision.
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Sample Availability: Samples of the compounds ...... are available from the authors.