Bioactivity of various plant products containing pentacyclic triterpenes.
\\n\\n
Released this past November, the list is based on data collected from the Web of Science and highlights some of the world’s most influential scientific minds by naming the researchers whose publications over the previous decade have included a high number of Highly Cited Papers placing them among the top 1% most-cited.
\\n\\nWe wish to congratulate all of the researchers named and especially our authors on this amazing accomplishment! We are happy and proud to share in their success!
\\n"}]',published:!0,mainMedia:null},components:[{type:"htmlEditorComponent",content:'IntechOpen is proud to announce that 179 of our authors have made the Clarivate™ Highly Cited Researchers List for 2020, ranking them among the top 1% most-cited.
\n\nThroughout the years, the list has named a total of 252 IntechOpen authors as Highly Cited. Of those researchers, 69 have been featured on the list multiple times.
\n\n\n\nReleased this past November, the list is based on data collected from the Web of Science and highlights some of the world’s most influential scientific minds by naming the researchers whose publications over the previous decade have included a high number of Highly Cited Papers placing them among the top 1% most-cited.
\n\nWe wish to congratulate all of the researchers named and especially our authors on this amazing accomplishment! We are happy and proud to share in their success!
\n'}],latestNews:[{slug:"intechopen-authors-included-in-the-highly-cited-researchers-list-for-2020-20210121",title:"IntechOpen Authors Included in the Highly Cited Researchers List for 2020"},{slug:"intechopen-maintains-position-as-the-world-s-largest-oa-book-publisher-20201218",title:"IntechOpen Maintains Position as the World’s Largest OA Book Publisher"},{slug:"all-intechopen-books-available-on-perlego-20201215",title:"All IntechOpen Books Available on Perlego"},{slug:"oiv-awards-recognizes-intechopen-s-editors-20201127",title:"OIV Awards Recognizes IntechOpen's Editors"},{slug:"intechopen-joins-crossref-s-initiative-for-open-abstracts-i4oa-to-boost-the-discovery-of-research-20201005",title:"IntechOpen joins Crossref's Initiative for Open Abstracts (I4OA) to Boost the Discovery of Research"},{slug:"intechopen-hits-milestone-5-000-open-access-books-published-20200908",title:"IntechOpen hits milestone: 5,000 Open Access books published!"},{slug:"intechopen-books-hosted-on-the-mathworks-book-program-20200819",title:"IntechOpen Books Hosted on the MathWorks Book Program"},{slug:"intechopen-s-chapter-awarded-the-guenther-von-pannewitz-preis-2020-20200715",title:"IntechOpen's Chapter Awarded the Günther-von-Pannewitz-Preis 2020"}]},book:{item:{type:"book",id:"2478",leadTitle:null,fullTitle:"Optical Communication",title:"Optical Communication",subtitle:null,reviewType:"peer-reviewed",abstract:"Optical communication is very much useful in telecommunication systems, data processing and networking. 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Malignant melanoma, squamous cell carcinoma and basal cell carcinoma represent 98% of all skin cancers [2]. Malignant melanoma determines a higher mortality compared to nonmelanoma skin cancers, being responsible of 75% of skin cancer deaths [2, 3]. Sun exposure is one of the major risk factors, but it influences differently the types of skin cancer. Squamous cell carcinoma is more often related to chronic sun exposure, while malignant melanoma is caused by intermittent sun exposure and overexposure in childhood [4].
\nNonmelanoma skin cancer is considered to have the highest incidence of all cancers and occurs more frequently in people with white skin [5]. However, 232,000 new cases of malignant melanoma were diagnosed in 2012, with the highest incidence in Australia. The number of deaths due to this type of skin cancer was 55,000 worldwide in the same year [6]. Malignant melanoma cases tripled in the last 30 years in the United States and Europe [1]. According to World Health Organization [7], each year occur 132,000 cases of melanoma skin cancers worldwide. The increasing incidence is associated with an increase of treatment costs. This aspect underscores the important role of prevention and early detection efforts for this type of cancer [8].
\nEven though numerous efforts were made for finding effective treatments in melanoma, prognosis for these patients remains unsatisfactory. The standard treatment in early stages is represented by surgical excision, followed by an adjuvant therapy or enrollment in a clinical trial [9]. An early detection of melanoma and a proper treatment increase the chances for cure. Surgery, chemotherapy, immunotherapy or radiation therapy can be used for the treatment [10]. Interferon-α (IFN-α) is used as an adjuvant therapy in patients with high-risk cutaneous melanoma, improving mainly disease-free survival but also overall survival, though not without side effects [11]. An improvement of survival in patients with stage III melanoma has been noticed for ipilimumab therapy. This monoclonal antibody increases the immune response and is approved for treatment in advanced melanoma, but also causes gastrointestinal, endocrine and hepatic adverse effects [12]. New drugs have also been used in the treatment of patients with inoperable or stage IV cutaneous malignant melanoma. The BRAF inhibitors vemurafenib and dabrafenib, the anti-PD1 (programmed death 1) antibodies pembrolizumab and nivolumab or the MEK (mitogen-activated protein kinase) inhibitors trametinib and cobimetinib are new agents proposed in melanoma therapy [13]. Associations of BRAF inhibitors (dabrafenib) and MEK inhibitors (trametinib) have also been evaluated in order to improve overall survival and to delay the appearance of drug resistance in patients with metastatic melanoma with BRAF mutations [14].
\nIn nonmelanoma skin cancer, the therapy is different depending on the severity of the tumor. Standard excision or Mohs micrographic surgery (MMS), radiotherapy, photodynamic therapy (PDT), cryosurgery and topical treatment with imiquimod or 5-fluorouracil are employed in the management of this type of skin cancer [15].
\nDespite the numerous studies and the advances in targeted therapy and immunotherapy, the treatment options in melanoma are limited [9]. The main inconveniences of chemotherapeutic agents currently used in skin cancer are the severe side effects and the multi-drug resistance [16].
\nDue to these disadvantages of conventional therapies, new alternatives have been investigated in order to find compounds that can serve for the synthesis of new drugs [16]. Plant-derived compounds are intensively studied as anticancer agents, many studies being performed to evaluate their properties in different types of cancer, including skin cancer [17].
Plants have gained over the time an important place in the prevention and treatment of various medical conditions. Extracts from plants were obtained since ancient times following simple procedures and used as teas, potions and ointments in an attempt to alleviate pain and to cure diseases. Natural sources of drugs remain an important branch in pharmaceutical drug discovery and therapeutic implementation. Combinatorial chemistry as an initial source of information was unable to offer the expected amount of final products, but is considered a tool for preliminary analysis of new drugs even on cancer treatment. Several groups of researchers provided routes to refine and improve the skeleton of natural compound and to prepare novel active agents [18]. Links between natural sources, synthetic chemistry and knowledge about genetic analysis of microbes are new trends in preclinical evaluations [18, 19]. Drugs derived from nature may be fall in one of the following categories: natural product botanical, derived from natural product or made by total synthesis but with the specification that the pharmacophore is in relation with a natural product [18].
\nDuring the last decades, natural remedies are engaged in an unprecedented evolution aimed at an increased efficacy. The development of sophisticated technologies in the fields of phytochemistry, drug formulation and pharmacology, as well as the focus on the mechanism of action on a cellular and molecular level, enables the obtainment of highly efficient drugs from plants.
\nOne of the numerous categories of plant phytochemicals are triterpenes (Figures 1–3). So far, over 20,000 triterpenes have been isolated from the plant kingdom. They include a variety of structural subtypes: squalene, lanostane, dammarane, tetranortriterpenoids, lupane, oleanane, ursane, hopane and other [20, 21]. Pentacyclic triterpenes, their natural sources and biological effects are presented in Table 1.
Substance | Plant (family) | Plant part | Study/effect | Reference |
---|---|---|---|---|
BA | Ziziphus mauritiana Lam. (Rhamnaceae) | Stem bark | In vitro—inhibitory effect on (MEL-1, -2, -3, -4) cells; apoptotic effect on MEL-2 cells In vivo—antitumor effect on athymic mice injected with MEL-2 cells | [22] |
BE, LU | Betula x caerulea Blanch., Betula cordifolia Regel, Betula papyrifera Marsh., Betula populvolia Marsh. (Betulaceae) | Bark | N/A | [23] |
BA, LU, BE, UA, OA | Syzygium formosanum Hay. Mori (Myrtaceae) | Leaves | N/A | [24] |
BE, BA, UA | Diospyros leucomelas Poir. (Ebenaceae) | Leaves | In vivo—anti-inflammatory activity on Swiss mice, for induced ear edema and induced paw edema | [25] |
OA | Rosa canina L. (Rosaceae) | Rose hip, powder | In vitro—immunomodulatory activity on Mono Mac 6, obtained when a mixture of OA, BA and UA was used | [26] |
BA | Rosmarinus officinalis L. (Labiatae) | Stems and leaves | In vivo—antidepressant-like effect in the TST, for Swiss mice; anti-immobility effect | [27] |
BE, BA | Betula pendula Roth, syn. Betula verrucosa (Betulaceae) | Bark | In vitro—cytotoxic effect in EPG85-257 and EPP85-181 cells line | [28] |
A, BA, BE, LU, UA, OA | Ligustrum pricei Hayata, Ligustrum sinense Lour., Ligustrum lucidum W.T.Aiton (Oleaceae) | Leaves | In vivo—analgesic and anti-inflammatory effect on Sprague Dawley rats | [29] |
OA, BA | Viscum album L. (Santalaceae) – harvested from Malus domestica Borkh. | Sprout | In vitro—cytotoxic and apoptotic effect on B16.F10 cells | [30] |
OA, BA | Viscum album L. (Santalaceae) – harvested from Malus domestica Borkh. | Sprout | In vivo—antiapoptotic, antiproliferative effect on C57BL/6NCrL mice injected with B16.F10 | [31] |
BE, UA | Myrica cerifera L. (Myricaceae) | Bark | In vitro—cytotoxic activity against HL60, A549 and SK-BR-3 cell lines | [32] |
LU | Taraxacum sp. Dandelion (Asteraceae) | Root | In vitro—cytostatic, not cytotoxic effect on B16 2F2 cells; inhibition of cells proliferation by differentiation | [33] |
LU | Lactuca indica L. (Asteraceae) | N/A | In vivo—prevents local tumor progression, distant metastasis in dogs with COMM Dogs: two miniature Dachshunds, two Beagles, two miniature Schnauzers, one Golden Retriever, one Labrador Retriever, one American Cocker Spaniel, one Cavalier King Charles Spaniel and 1 mixed-breed dog | [34] |
LU | Lactuca indica L. (Asteraceae) | N/A | In vivo—tumor growth suppression and induced cell cycle arrest in C57BL/6 mice injected with B16 2F2 cells | [35] |
LU | Bombax ceiba L. (Malvaceae) | Stem Bark | In vitro—antiangiogenic effect on SK-MEL-2, A549 and B16-F10 cell lines | [36] |
BA, OA | Paeonia rockii ssp. rockii T.Hong & J.J.Li (Paeoniaceae) | Root | In vitro—antiapoptotic effect induced selectively in the M-14 cell line | [37] |
UA | Salvia officinalis L. (Lamiaceae) | N/A | In vivo—antiprotease and antimetastatic effects on C57BL/6N mice injected with B16 cells | [38] |
BA | Avicennia officinalis L. (Acanthaceae) | Leaves | In vivo—anti-inflammatory effect on rats | [39] |
BA, UA, MA | Bridelia cambodiana Gagnep. (Phyllanthaceae) | Whole plant | In vitro—cytotoxic effect against HL60 and LCC cell lines | [40] |
Bioactivity of various plant products containing pentacyclic triterpenes.
BA (betulinic acid); BE (betulin); LU (lupeol); UA (ursolic acid); OA (oleanolic acid); MA (maslinic acid); N/A (not applicable); MEL-1, -2, -3, -4 (human melanoma cell line); Mono Mac 6 (human monocytic cell line); TST (tail suspension test); EPG85-257 (human gastric carcinoma cell line); EPP85-181 (human pancreatic carcinoma cell line); B16.F10 (murine melanoma cell line); HL60 (human promyelocytic leukemia cell line); A549 (human lung carcinoma cell line); SK-BR-3 (human breast cancer cell line); B16 2F2 (mouse melanoma derived subclone with high differentiation capability); COMM (canine oral malignant melanoma); SK-MEL-2 (human melanoma cell line); M-14 (human melanoma cell line); B16 (mouse melanoma cell line derived from spontaneous skin tumor); LLC (mouse lewis lung carcinoma).
Triterpene structures (a) lupane; (b) oleanane; (c) ursane; (d) hopane; (e) lanostane; (f) dammarane and (g) quassin.
Lupan skeleton triterpenes (a) betulinic acid; (b) betulin and (c) lupeol.
Other triterpenes (a) ursolic acid; (b) oleanolic acid and (c) maslinic acid.
Among plant sources containing lupan-skeleton pentacyclic triterpenes (Figure 2), birch bark has received particular attention due to its high content in these substances, its well-proven application and uses over the time [41]. Currently, it is acknowledged that the outer birch bark is a rich source of pentacyclic triterpenes, which include: betulin (B lup-20 (29)-ene-3β, 28-diol), betulinic acid (BA, 3β acid, hydroxy-lup-20 (29)-en-28-oic) and lupeol (L, Lup-20 (29)-en-3-ol). The development of birch bark extracts, their applications and bioactivity has comprehensively been reviewed [42]. By analyzing birch bark extract, it was shown that betulin is present in the highest amount, while betulinic acid content is lower. However, it is possible that plants from different geographical regions present a variable content in pentacyclic triterpene, which requires a rigorous analysis of the content [43]. Differences between barks of birch species regard the content in: betulin, betulinic acid, betulinic aldehyde, lupeol, oleanolic acid, oleanolic acid 3-acetate, betulin 3-caffeate, erythrodiol and other.
Pentacyclic triterpenes from plants are secondary metabolites with high lipophilicity. Therefore, they are mainly located in hydrophobic histological structures. In the cork of trees, which represents the outer tissue of the secondary bark, triterpenes are associated with suberin; a well-known example is birch bark [44]. Triterpenes are as well components of cuticular and epicuticular waxes covering leaves [45] and fruits [46].
\nBetulin was isolated for the first time in the 1788 by Lowitz [47] from birch cork. The elucidation of its structure was performed by only in 1953 by Guider et al. [48]. Additional plant sources for betulin include hornbeam (Carpinus betulus L) and hazel (Corylus avellana L.), plants which are phylogenetically closely related to birch [49]. Betulinic acid, a triterpene of major therapeutic relevance, was isolated under the name of “graciolon” from Gratiola officinalis [50] and recognized as such only 40 years later [51]. “Platanolic acid,” isolated from Platanus acerifolia bark [52], proved later to be betulinic acid as well [53]. Furthermore, betulinic acid could be obtained from an alcoholic extract of Cornus florida L. bark [54]. Ko and co-workers [55] used mistletoe (Viscum album) to obtain an ethanol extract enriched in triterpenes, including betulinic acid and botulin.
\nThe obtainment of triterpenes from the plant matrices employs as a first step extraction with organic solvents such as methanol or ethanol [56]. Other solvents are chloroform, dichloromethane, ethyl acetate, petroleum ether or various mixtures thereof, in accordance with the low polarity of these phytocompounds. Recovery procedures may include Soxhlet extraction, maceration and ultrasound-assisted processes [57]. In order to progressively enrich/isolate triterpenes, the usual phytochemical approaches are employed: partition among solvents of increasing polarity, column chromatography on silica gel, countercurrent chromatography and preparative chromatography. Triterpene acids are extracted after alkalinization with sodium hydroxide [57] or calcium hydroxyde [58]. Pure betulin was prepared from a crude mixture using a chromatographic column with silica gel as a stationary phase and a mixture of hexane and ethyl acetate as eluent, followed by recrystallization from 75% ethyl alcohol [59]. An effective preparation of crystalline betulin (99% purity) from birch bark is clearly described in a recent work, following the steps to remove betulinic acid and lupeol. Additionally, the authors demonstrate the obvious relationship between the cytotoxic activity of betulin and its purity [58]. The analytic determination of triterpenes in samples is performed by reverse-phase HPTLC and gas chromatography, coupled with the detection using mass spectrometry detection, is a widely used method for analysis of betulin and other triterpenes in samples. High-performance thin-layer chromatography (HPTLC) is a valuable straightforward tool for the visualization of impurities [60].
\nBetulinic acid received high attention due to its properties to inhibit the growth of cancer cell lines, without being cytotoxic to normal cells. In plant materials used as sources of triterpenes such as birch, the content in betulinic acid is much lower than that in betulin. For this reason, various attempts have been made to obtain betulinic acid, using betulin as a starting point. In the study of Melnikova and co-workers [61], the most intense catalytic activity was noticed for aluminum salts, which also have a selective activity. The reaction proceeds via the intermediate betulonic acid, purified by recrystallization. Betulonic acid is reduced with NaBH4 (THF or isopropanol) at room temperature to obtain a mixture of 3α-betulinic acid and betulinic acid-3β [61].
\nEnzymatic transformations, privileged for their simplicity, eco-friendliness and safety, are currently a mainstay in the obtainment of drugs. In an enzymatic approach, the fungus Armillaria luteo-virens Sacc ZJUQH100-6 was employed in the biotransformation of betulin into betulinic acid [62]. Optimization of the obtainment was monitored by variation of parameters like pH, glucose, betulin content, addition of tween 80 and stage of inoculation; the presence of the surfactant had a significant impact on the yield of the biotransformation.
\nWhile betulin is readily available from birch and other plants, its anticancer activity is only moderate. Being an accessible starting point for derivatizations, betulin has been the subject of many researches, aiming to obtain compounds with enhanced anticancer activities [63]. The acetylated derivates were tested for antiproliferative effect on several cell lines: colorectal adenocarcinoma, leukemia and breast cancer. By esterificating betulin with propionic acid in dichloromethane solution in the presence of dicyclohexylcarbodiimide and 4-dimethylaminopyridine, derivatives: 28-O-propynoylbetulin and 3.28-A, IB, dipropynoylbetulin were obtained. Column chromatography was employed in order to obtain the pure components with a yield of 60% in the case of the first derivative and 12% in the second. The reaction of betulin with propargyl chloroformate and 3-butyl-1-yl chloroformate in benzene, in the presence of pyridine, resulted in the formation of a mixture of 28-O-propargyloxycarbonylbetulin monoesters and 28-O- (3-butynyloxycarbonyl) toxin and di-3,28-A sheep-di (pro-pargyloxycarbonyl) 3.28-A toxin and sheep-di (3-butyn-yloxycarbonyl) toxin. The resulting mixture was separated by column chromatography; thus, pure components were obtained in a 64–69% yield for monoesters and 23–27% in the case of diesters [64].
The most challenging aspect of the biomedical use of lupane triterpenes is their low water solubility which subsequently causes poor bioavailability [65]; so far, several delivery systems have been developed in order to achieve superior pharmacokinetic outcomes. The current subchapter aims to review the most recent and promising delivery options for betulin, betulinic acid and lupeol.
\nThe first step in the attempt to modulate the aqueous solubility of an insoluble compound relies in its convenient derivatization with water-soluble partners; such an attempt was conducted by Drag-Zalesinska and co-workers [66], who prepared mono- and diesters of betulin and betulinic acid with amino acids. All esters revealed higher water solubilities and significant cytotoxic activity via apoptosis induction; the type of ester as well as the type of the amino acid side chain strongly influences the biological effect of the respective compounds [66]. C(2)-propargyl-substituted pentacyclic triterpenoids conjugated with 1,2,3-triazole glucopyranosides were synthesized via “click” chemistry in order to achieve optimized water solubility as well as pharmacokinetic and pharmacological properties [67].
\nCyclodextrin (CD) complexation represents an attractive solution to increase the aqueous solubility of numerous compounds; through their hydrophobic interior and hydrophilic surface, cyclodextrins are able to accommodate various lipophilic guest molecules which can thus be water-solubilized. According to molecular studies [68], the bulky structures of betulinic acid and betulin fit best inside the cavity of γ-CD and its semisynthetic derivatives, such as hydroxypropyl-γ-CD (HPGCD). As a result of HPGCD complexation, a 14-fold increased water solubility was reported for BA accompanied by superior biological activity [69], i.e., strong antiangiogenic and antitumor effect [70, 71]. Similar outcomes were achieved in terms of anti-melanoma activity tested on B16 cell line (murine melanoma) [72]. Fontanay et al. conducted a study on the inclusion of hydroxy pentacyclic triterpenoid acids, including BA, inside native γ-CD [73]; the physicochemical analysis revealed the formation of a 1:1 complex with a significantly improved aqueous solubility.
\nβ-CD derivatives also served as complexation partners for BA, and its inclusion in the cyclodextrin hydrophilic matrix led to significantly improved dissolution rate and, subsequently, antiproliferative in vitro activity against MCF7 (breast cancer) cell line [74]. The same tumor cell line was involved in the study of the biological activity of betulinic acid accommodated inside native β-CD [75]; a dose-dependent antiproliferative activity was reported, through mitochondria-mediated apoptosis induction and G2/M cell cycle arrest.
\nAn important parameter in the cyclodextrin inclusion process is the stability constant of the final complex, its value giving the measure of the potential use of the complex as biologically active agent; significantly high stability constants were achieved for both betulin and betulinic acid in complex with newly synthesized hydrophilic γ-CD derivatives [76]. Such a high stability constant characterizes a strong interaction between the host- and the guest molecule, thus enabling the delivery of the active drug at the target site in the absence of systemic adverse effects. Both complexes, with betulin and betulinic acid, respectively, were in vitro and in vivo tested, revealing moderate in vitro antiproliferative activity; however, in vivo results on murine models showed a significant decline in tumor size and volume [77, 78].
\nThe inclusion of betulin inside HPGCD led to optimized outcomes in terms of bioavailability and antiproliferative activity [79, 80]; similar results were reported for betulin complexation with hydrophilic β-CD derivatives that caused stronger inhibitory activity against MCF7 (breast cancer) cell line than pure betulin [74].
\nLupeol was also subjected to inclusion inside γ-CD by kneading in a 1:2 molar ratio; the complex revealed optimized antiproliferative and antiangiogenic activities compared to the pure drug [81].
\nThe use of triterpenes as mixtures such as total extract of birch outer bark may trigger simultaneously various mechanisms of apoptosis induction and therefore result in an additive or synergistic effect. Hertrampf et al. [82] used HPBCD as solubilizer for birch total extract; a series of dilutions were prepared using the main ingredient, betulin, as a reference to calculate concentrations. The study reported the multivalent cytotoxic activity of the birch bark at lower concentrations than previously used presumably due to a higher bioavailability of triterpenes provided by cyclodextrin solubilization; moreover, a synergistic effect was suggested. Triterpene-rich mistletoe extract (6.9% BA) was solubilized by Strüh et al. [30] by using HPBCD and tested against B16F10 melanoma cell line; a dose-dependent reduction of cellular ATP was reported accompanied by high cytotoxicity due to DNA fragmentation. The research was continued by in vivo studies on C57BL/6 mice bearing B16F10 subcutaneous melanoma, revealing an increased antitumor effect and a prolonged mice survival [31].
\nAn alternative research direction was the preparation of cyclodextrin conjugates instead of inclusion complexes; “click chemistry” was involved in the synthesis of triazole-bridged conjugates between β-CD and pentacyclic triterpenes [83]. All bioconjugates showed higher hydrophilicity than the parent compound, and several conjugates displayed significant cytotoxicity on various cancer cell lines; in addition, the cyclodextrin conjugation led to the disappearance of haemolytic toxicity. The authors continued their research by synthesizing α-CD conjugates with several pentacyclic triterpenes including BA [84]; all conjugates exhibited lower hydrophobicity than the parent molecules accompanied by significant anti-HCV (hepatitis C virus) entry activity.
\nAn excellent review was published in 2016 by Lima et al. [85], describing the main attempts to use cyclodextrins as nanocarriers for various terpenes; the authors concluded that cyclodextrins are feasible tools in improving the pharmacological profile of terpenes, limited mainly by the scarce pharmacokinetic and clinical studies.
\nLiposomes are small vesicles displaying one or more phospholipidic layers and an aqueous core [86] that may incorporate both lipophilic and hydrophilic compounds [87, 88]. Betulinic acid was trapped inside large liposomes by Mullauer et al. [89] and administered to mice bearing experimental models of colon (SW480) and lung (A549) cancer; no systemic adverse effects were reported following parenteral (i.v.) and oral administration. Similar studies reported liposomal and proliposomal formulations with BA with 95% yield of the incorporation process [90]. Phospholipidic nanosomes prepared by means of supercritical fluids were used to entrap BA in order to increase its efficacy as antiviral agent [91, 92]. Several betulin derivatives such as 28-acetylenic derivatives [93] and pyrazoles and 1,2,3-triazole derivatives [94] were synthesized and formulated as liposomes; the nanoformulations exhibited strong apoptotic activity due to both higher biological effect of the active compound and optimized delivery. PEG-ylated BA liposomes were obtained by Liu et al. in 2016, entrapping BA in the lipid bilayer of the liposomes by the ethanol injection technique [95]; the hydrophilic outer PEG layer ensured improved sustained release and antitumor effect compared to free BA or BA liposomes.
\nAnother attractive option in drug delivery is the use of micro- and nanoemulsions; a nanoemulsion containing BA was prepared using flax-seed oil as lipophilic phase and the high-pressure homogenization method [96]; the in vivo testing on the chorioallantoic membrane (CAM assay) revealed a significant antiangiogenic activity. The same procedure was applied for betulin nanoemulsion, followed by in vivo testing by CAM assay and experimental murine cancer model; the study reported strong anti-inflammatory, antiproliferative and antiangiogenic activities of the incorporated betulin as well as its potential benefits in inhibiting metastasis [97]. An oil-in-water nanoemulsion with BA was prepared through the use of phospholipase-catalyzed modified phosphatidylcholine as emulsifier in an ultrasound device; various factors such as composition, ultrasound amplitude, temperature and pH significantly influenced nanoparticle size and stability [98].
\nA different approach consists in the administration of betulin via the nasal route; in order to avoid mouth sedimentation of betulin particles, the solvent exchange method was used to limit particle sizes to nanoscale, thus leading to higher bioavailability of betulin in the lower respiratory tract [99].
\nWater solubility may be increased through grinding with hydrophilic polymers (i.e., polyvinylpyrrolidone, polyethylene glycol, arabinogalactan) [100, 101]; solid dispersions of BA with various hydrophilic polymers (i.e., Soluplus, HPMCAS-HF, Kollidon VA64, Kollidon K90, Eudragit RLPO) in 1:4 (w/w) ratio were prepared and analyzed by Yu et al. [102] in 2014, revealing a great potential to increase BA water solubility. Moreover, hydrophilic bioconjugates can be synthesized between active drugs and hydrophilic polymers. BA-monomethoxy polyethylene glycol (mPEG) conjugate was synthesized by covalent bonding of the carboxyl moiety of BA and the amine groups of mPEG [103]; the conjugate exhibited cytotoxicity through cell apoptosis on hepatic cancer cells (Hep3B, Huh7) as well as in vivo antitumor efficacy in Ehrlich ascites tumor (EAT) model while lacking any sign of biochemical and histological toxicity. A step further was represented by the use of multiarm-PEGs as conjugation partner which offer a high density of functional groups; through the formation of an ester bond, BA was linked to eight-arm PEG (8arm-PEG) and then to a targeting molecule (folate) followed by the self-assembly into nanoparticles [104]. A second anticancer drug, hydroxycamptothecin, was added by nanoprecipitation; the ensemble achieved a dramatically increased cytotoxicity, prolonged blood circulation, enhanced tumor targeting and lower systemic toxicity than the free drugs; in addition, a synergistic antitumor efficacy was reported [104]. BA also shows the ability to self-assemble into nano- and microfibers with antileukemic efficacy and cytoprotective activity as well [105].
\nBiodegradable polymeric nanospheres based on poly(lactide-co-glycolide)-poly(ethylene glycol) (PLGA-PEG) were prepared by nanoprecipitation to incorporate 40% BA [106]; the study reported an increased cytotoxicity and lower IC50 value compared to the pure drug. PLGA was used as building material by interfacial deposition for nanocapsules that efficiently entrapped lupeol [107]. Polymer matrixes can be involved in regional chemotherapy, an approach that avoids systemic adverse effects [108] and allows the controlled release of the pure drug; betulin was incorporated as model compound in such a matrix (poly(3,4-ethylenedioxythiophene), its release being conducted by passive or active mode. The novel formulation exhibited efficient cytotoxic activity against KB and MCF7 cancer cell lines.
\nBA conjugates with carboxyl-functionalized single-walled carbon nanotubes were synthesized via π–π stacking interaction, leading to a 20% loading of the active drug [109]; following physicochemical and biological analysis, the authors reported the controlled, prolonged release of the drug, with no sign of toxicity on normal fibroblasts and significant cytotoxicity against A549 (lung cancer) cell line. The research continued by coating the nanotubes with four biopolymers: tween 20, tween 80, polyethylene glycol and chitosan in order to further improve biocompatibility [110]; the procedure induced sustained and prolonged release compared to the uncoated nanotubes, while cytotoxicity depended on the chosen biopolymer.
\nMetallic nanoparticles were also used as nanocarriers for pentacyclic triterpenes; as an example, magnetic nanoparticles coated with chitosan were loaded with BA and exhibited a pseudo-second-order kinetic model release of the active drug [111]; the nanoparticles were cytotoxic on MCF7 cells in a dose-dependent manner while lacking toxicity against normal mouse fibroblast cells. Silver nanoparticles coated with BA were involved in the in vitro testing on a panel of cancer cell lines, including A375 (murine melanoma) [112]; the new formulation revealed strong antiproliferative and antimigratory activity, in particular against melanoma cells.
Preclinical trials are important in the initial evaluation of new drugs, formulations or specific new design of pathology. They are complex processes with an uncertain ending, as just a reduced percent of evaluations lead to a market product. It is estimated that around 90% of tested drugs are not launched to the market [113]. Despite intense of basic research, the actual delivery of accepted drugs is scarce.
\nThe classical route of a tested compound in preclinical trials includes in vitro tests followed by in vivo tests on animals [113]. These tests may be conceived in a variety of ways and are constantly improved and diversified. The mainstay of preclinical tests regarding a potential efficacy against skin cancer types is in vitro tests using different types of cell lines. In this regard, lupane triterpenes were tested on human melanoma (G361, SK-MEL-28, MEL-2, SK-MEL2, A375), mouse melanoma (B16-F1, B16 2F2) and human skin epidermoid carcinoma A431. In case of betulin, the latter showed a particularly high sensitivity (with a IC50 value below 10µM), while various types of human melanoma cell lines may display a high variation range of the sensitivity to betulin, with differences in IC50 values of one order of magnitude, from 12.4 to over 250 µM [114]. For betulinic acid, IC50 was 154 µM when tested on A375 melanoma [115], and 70 µM when tested on B16-F10 murine melanoma [116]. Information of particular relevance for the actual clinical utilization as anticancer agent comes from comparative data on the cytotoxicity against normal cells and cancer cell lines. Betulin, for example, is more cytotoxic against cancerous cells than nontumoral ones [114]. Further steps in preclinical evaluation are the investigation of the mechanism of action; lupeol, betulin, betulinic acid and their semi-synthetic derivatives have so far shown significant effects on apoptosis and cell cycle regulation [117, 118]. As inflammation is an important player in the pathogenesis of cancer, the anti-inflammatory effects and mechanisms are as well explored to give a correct picture of the antitumoral potential [117]. Furthermore, it is important to explore the antimigratory potential of natural products, as it has a seminal importance for malignant melanoma—a cancer type with a high invasiveness [119]. A global approach to relevant preclinical tests regarding triterpenes should thus be multi-component. In this regard, our workgroup has established an efficient battery of tests for aimed at establishing the potential of natural triterpenes with anticancer/anti-inflammatory activity as agents against skin cancer. The module of preclinical evaluations includes as follows:
\nStep 1: in vitro tests on normal cells (e.g., HaCat) comparing with specific pathological tests; evaluation of cytotoxic activity;
Step 2: in vitro evaluations concerning the impact on apoptosis, and observations of specific markers via DAPI/HOPI staining, and evaluation of Annexin V, caspases and other cellular markers [120];
Step 3: in vivo embryonated egg membrane assay for toxicological evaluation (HET CAM assay) and investigations of the potential to affect angiogenesis; future aspects include cultivation of cancer cells on embryonated eggs and direct research of the therapeutic potential;
Step 4: in vivo tests including a large number of experimental protocols: photochemical model, inoculation of murine cells, xenograft of human pathological cells on adequate mouse hosts and correlations with therapeutical surveillance. Furthermore, histopathological evaluations and immuno-histochemical assays are correlated with innovative approaches like RAMAN skin evaluation, noninvasive methods for skin quality and surface damage characterization.
Additional determinations could require selection of cells from a primary experimental tumor, cultivation of cells and evaluation of compounds, PET animal observations and other methods applied for a detailed pathologic surveillance of drugs.
Apoptosis is a programmed cell death consisting in morphological changes including cell shrinkage, nuclear condensation, chromosomal DNA fragmentation, plasma membrane blebbing and caspase activation [121]. In this regard, apoptosis is considered a crucial physiological process in tumor clearance, being a major target for anticancer drugs [122]. The molecular mechanisms of apoptosis can include extrinsic and intrinsic pathways. The extrinsic pathway of apoptosis is initiated by external signals, which can activate TNF/Fas-receptor, which in turn activates procaspase-8 [123]. The activated caspase-8 is involved into the caspase-3, -6 and -7 cascade activation [124]. Caspases are important cellular enzymes synthesized as inactive zymogens, which can be activated into their active tetrameric forms by various apoptotic signals [124]. The activation of caspase-3, -6 and -7 leads to cell death not only by breaking down the cytoskeleton, but also the nucleus.
\nThe intrinsic pathway of apoptosis, known as the mitochondrial pathway, is initiated by internal stimuli which can activate the proapoptotic genes from the outer membrane of mitochondria. Bcl-2 family proteins (Bax, Bak, Bcl-xs) are important proapoptotic genes involved in permeabilization of the mitochondrial membrane in order to release cytochrome c in cytosol, where it binds to the caspase-activating protein apoptotic protease activating factor-1 (A
Previous evidences showed that the pentacyclic triterpens, especially betulin, betulinic acid, lupeol and ursolic acid, have induced apoptosis in different types of cancer cells via activation of the mitochondrial pathway and not to the death receptor pathway (extrinsic way) [125, 126]. These data have been supported by Drag-Zalesinska et al. [118] study in which betulin and betulinic acid proved to induce apoptosis in human metastatic melanoma cells (Me-45) by releasing cytochrome c or the apoptosis inducing factor (AIF) through the mitochondrial membrane. Liu et al. [122] have also demonstrated that betulinic acid, as well as betulin, could kill CNE2 cells through the mitochondrial pathway. Betulinic acid induced the DNA fragmentation, caspase activation and cytochrome c release but independent of Bax proteins [115, 122]. Moreover, betulinic acid has been also involved in activation of nuclear factor kappa B (NF-κB) responsible for apoptosis in various types of cancer cells [127].
\nThe increased production of reactive oxygen species (ROS) caused by betulin and betulinic acid stimulation [128, 129] has been considered a stress factor involved in the depolarization of mitochondrial membrane [130]. Furthermore, both calcium overload and ATP depletion were additional stress factors responsible for increasing the permeability of the inner mitochondrial membrane through formation of nonspecific pores [116]. For instance, the dimethylaminopyridine triterpenoid derivatives have also caused the depolarization of the mitochondrial membrane in situ, in order to increase the permeability transition pore [131].
\nUnlike the previous data, the study of Şoica et al. [77] on B164A5 murine melanoma cells and on a mouse melanoma model showed that BE and its derivatives had no effect on caspase-2 regulation, the apoptotic mechanism of betulin being suggested to be probably through the transformation of BE into betulinic acid inside the cells.
\nAccording to the study of Muceniece et al. [132] in vitro, betulin had a mimetic effect on melanocortin (MC) receptor, especially on MC-1 subtype. This observation has been also supported by Şoica et al. [77] study in which botulin had revealed strong inhibitory effects on B64A5 murine melanoma cells, by binding to the melanocortin receptors. Betulin has been not involved by itself in stimulation of cAMP generation, but it acted as a weak antagonist on alpha-melanocyte-stimulating hormone (alpha-MSH)-induced cAMP accumulation in B16-F1 mouse melanoma cells [132].
\nIn vitro and in vivo studies have also revealed that the birch bark extract and betulin have significantly increased the expression of PARP-1 in melanoma cells [118], exhibiting interferon-inducing activity [133].
\nAccording to Zhang et al. [126] study, betulinic acid induced apoptosis by suppressing the cyclic AMP-dependent transcription factor ATF-3 and NF-κB pathways and decreasing the expression of topoisomerase I, p53 and lamin B1. On one hand, earlier studies indicated that betulinic acid had induced apoptosis of cells due to the p53 pathways [134]. This conclusion has been also supported by Tiwari et al. [135] study, in which BA proved a dose-dependent apoptotic effect on both p53 mutant and wild-type cells probably because of its involvement in p53-independent apoptotic pathway. On the other hand, a recent study has shown that the apoptotic effect of betulinic acid in human metastatic melanoma cells (Me-45) had been independent of p53-apoptotic pathway [118]. The presumable mechanisms of action of betulinic acid and betulin in skin cancer are depicted in Figure 4.
The mechanism of action of betulinic acid and betulin in skin cancer.
Lupeol is a complex multitarget phytochemical, being involved in controlling IL-1 receptor-associated kinase-mediated toll-like receptor 4 (IRAK-TLR4), Bcl-2 family, nuclear factor kappa B (NF-κB), phosphatidylinositol-3-kinase (PI3-K)/Akt and Wnt/β-catenin signaling pathways [136]. According to the Tarapore et al. study, the anticarcinogenic effect of lupeol has been related to the Wnt/β-catenin signaling pathway. That study has revealed that lupeol caused a dose-dependent decrease in Wnt target genes in Mel 1011 cells. Moreover, there has been also observed a decrease of nuclear β-catenin expression, associated with an enhancement of plasmatic β-catenin expression in melanoma cells (Mel 928 and Mel 1241). Consequently, lupeol has been involved in blocking the movement of β-catenin between cytoplasm and nucleus [137].
\nAn in vivo study on Swiss Albino mice showed that lupeol exerted apoptotic effects through the enhancement of bax and caspase-3 genes expression and downregulation of bcl-2 antiapoptotic genes [138].
\nUnlike botulin and betulinic acid, lupeol has also induced apoptosis via extrinsic pathway by enhancing the expression of FADD protein and Fas receptors [127].
\nUrsolic acid has strongly increased the IR-induced apoptotic effect in various types of cancer cells, likely DU145, CT26 and B16F10, playing a major role in DNA fragmentation, mitochondrial dysfunction and apoptotic marker modulation [139]. Moreover, ursolic acid has induced apoptosis in M4Beu cells human melanoma through intrinsic pathway by enhancing the caspase-3 activity in a dose-dependent manner, correlated with a low caspase-9 activity [140]. Ursolic acid has also proved to act as an inhibitor of the endogenous reverse transcriptase (RT) activity in the following tumor cells: melanoma (A375), glioblastoma (U87) and thyroid anaplastic carcinoma (ARO), as well as on nontransformed human fibroblast cell line (WI-38), exhibiting strong antiproliferative effects [141].
\nThe mechanism of apoptosis induced by pentacyclic triterpens is not fully understood, although, according to the previous studies, we can conclude that these triterpens exhibited strong apoptotic effects, especially via intrinsic pathway, being involved in increasing the permeability of inner mitochondrial membrane, activation of caspase-9 and 3, as well as cell death.
Pentacyclic triterpenes represent an important issue in the field of antiskin cancer formulations; nowadays, the researches focus on the development of nanoformulations that provide multiple advantages over the classical pharmaceutical formulations, including the possibility of being decorated with targeting moieties that significantly improve the antiproliferative activity of the loaded active drug. Different mechanisms of action have been identified so far at cellular and molecular level, in particular for betulinic acid; however, future studies are needed in order to fully comprehend the intimate details of the anticancer treatment with pentacyclic triterpenes and formulations thereof.
This work was supported by a grant financed by the University of Medicine and Pharmacy “Victor Babes” Timisoara (Grant PIII-C4-PCFI-2016/2017-03, acronym NANOCEL to C.S. and V.P.).
Globally many aquatic ecosystems have been negatively affected by phosphorus (P) eutrophication [1]. Phosphorus is a primary limiting nutrient in both freshwater and marine systems [2, 3]. Phosphorus eutrophication is defined as the over enrichment of aquatic ecosystems with P leading to accelerated growth of algae blooms or water plants, anoxic events, altering biomass and species composition [4, 5, 6, 7, 8], eutrophication is a persistent condition of surface waters and a widespread environmental problem. Aquatic systems affected by eutrophication often exhibit harmful algal blooms, which foul water intakes and waterways, fuel hypoxia, disrupt food webs and produce secondary metabolites that are toxic to water consumers and users including zooplantkton, shellfish, fish, domestic pets, cattle and humans [9]. Excess phosphorus inputs to lakes usually come from industrial discharges, sewage and runoff from agriculture, construction sites, and urban areas [1, 6]. Many countries have regulated point sources of nutrients for example industrial and municipal discharges, however, nonpoint sources of nutrients such as runoff from urban and agricultural lands have replaced point sources as the driver of eutrophication in many countries [10].
The plant availability of phosphate fertilizer is reduced by sorption and organic complexation in the soil, therefore fertilizer applications greater than the amount required by the crop are used to counteract the strong binding of the phosphate to the soil matrix leading to increased P content of managed soils [11]. Mining phosphorus (P) and applying it on farm for animal feed and crop production is altering the global P cycle, leading to P accumulation in some of the world’s soils [4]. Over application of P fertilizer to soil is in itself wasteful, but the transport of P to aquatic ecosystems by erosion is also causing widespread problems of eutrophication [12, 13]. Using global budget [4] estimated the increase in net P storage in terrestrial and freshwater ecosystems to be at least 75% greater than preindustrial levels of storage. Large portion of P accumulation occurs as a result of increased agriculture intensification, land use change and increased runoff [14, 15, 16].
Excess phosphorus inputs to lakes usually come from industrial discharges, sewage and runoff from agriculture, construction sites, and urban areas [6]. The input of P to soil creates the potential for an increase in transfer to the wider environment. Phosphorus sources can be natural which includes indigenous soil P and atmospheric deposition and/or anthropogenic which includes fertilizers, animal feed input to the farm and manure applied to the soil [17]. In addition ground water can potentially contribute significant amount of P in water bodies driving eutrophication process [18].
As a result of P point source control in many countries the nonpoint P source especially agriculture is the main pollutant of aquatic systems [10]. The major source of nonpoint nutrient input to water bodies is the excessive application of fertilizer or manure on farm which cause P accumulation in soils [4]. Phosphorus retention has been caused by an excess of fertilizer and animal feed inputs over outputs of agricultural products [19]. For example [12] indicated that less than 20% of P input to the Lake Okeechobee watershed in fertilizers was output in agricultural as well as other products.
Most studies on plant nutrition often consider only inorganic P to be biologically available, however organic phosphorus is abundant in soils and its turnover can account for the majority of P taken up by vegetation [20, 21]. Soil phosphorus exists in a range of organic and inorganic compounds that differ significantly in their biological availability in the soil environment [22]. The inorganic P compounds mainly couple with amorphous and crystalline forms of Al, Fe, and Ca [23] which is highly influenced by soil pH [24]. The organic phosphorus in most soils is dominated by a mixture of phosphate monoesters (e.g., mononucleotides, inositol phosphates) and phosphate diesters (mainly nucleic acids and phospholipids), with smaller amounts of phosphonates (compounds with a direct carbon-phosphorus bond) and organic polyphosphates (e.g., adenosine triphosphate) [25]. Plants can manipulate their acquisition of P from organic compounds through various mechanisms, some of the mechanisms allow plants to utilize organic P as efficiently as inorganic phosphate [26, 27]. In lake sediment in China, the heavily polluted sediments contained higher organic P fractions compared to moderately and no polluted sediments [28]. Increased pH can alter the availability of P binding sites on ferric complexes as a result of competition between hydroxyl ions and bound phosphate ions [29]. Anoxic condition leads to release of P as a result of reduction of ferric to ferrous iron [30]. In addition presence of sulfate could lead to reaction of ferric iron with sulfate and sulfide to form ferrous iron and iron sulfide leading to release of P [31]. Increased temperature can reduce adsorption of P by mineral complexes in the sediment [32]. Other physicochemical processes affecting release of P from the sediment include temperature, pH potential, redox, reservoir hydrology and environmental conditions [33]. These physical chemical processes are further complicated by the influence of biological processes for example mineralization, leading to a complex system governing the release of P across sediment water interface [33].
Phosphorus in most cases enters aquatic ecosystems sorbed to soil particles that are eroded into rivers, lakes and streams [34, 35]. Watershed land use and P concentration in watershed soils strongly influence potential P pollution of aquatic ecosystems [4]. In addition any factor accelerating erosion or elevating P concentration in the soil increases the potential P runoff to aquatic systems [34, 35]. Mobilization of P involves biological, chemical and biochemical processes. The processes are grouped into solubilization or detachment mechanisms and are defined by the physical size of the P compounds that are mobilized [17] and it has been indicated that the potential for solubilization increases with increasing concentrations for extractable P. However, organic P has an important but little understood role in determining P solubilization [25]. Detachment of soil particles and associated P is mainly linked to soil erosion, which provides a physical mechanism for mobilizing P from soil into waters bodies [36].
Depending on site conditions diffuse P transport occurs as particulate or dissolved P in overland flow, channelized surface runoff, drainage, or groundwater [18]. In ground water P concentration is considered to be low [37]. This is as a result of orthophosphate P being adsorbed in the soil and sediment in the vadose or the saturated zone [18]. However, wastewater has been reported to cause heavy groundwater contamination leading to P elevation [38, 39].
Consequences of eutrophication include excessive plant production, blooms of harmful algae, increased frequency of anoxic events, and death of fish, leading to economic losses and health implications which include costs of water purification for human and industry use, losses of fish and wildlife production and losses of recreational amenities [10, 40]. Some of the consequences of eutrophication includes:
High level of Lake Eutrophication has led to suffocating of fish population on a massive scale with a very negative repercussions on the economy [41]. The total economic loss incurred from 1998 algal bloom in the Lake Tai China catchment area was estimated at U.S.$6.5 billion. During winter of 2002–2003, a severe oxygen deficit induced a fish kill in the eutrophicated two-basin Lake Aimajarvi in southern Finland, which resulted in cascading effects on the lower trophic levels of the lake [42].
Coastal areas are an important economic source for tourism [43]. The algal bloom have degraded the investment environment and damaged the hospitality and tourism industry [41].
Toxin producing algae can cause mass mortalities of fish marine mammals, birds and human illness through consumption of sea food [44]. It is estimated that 60–80 species of about 400 known phytoplankton are toxin producing and capable of producing harmful algal blooms [8]. In humans, toxins arising from harmful algal blooms have mainly been from shellfish consumption [44], bivalve shellfish have been reported to graze on algae and concentrate toxins effectively. As a result the poisoning can lead to paralytic shellfish poisoning, diarrhetic shellfish poisoning, neurotoxic shellfish poisoning, amnesic shellfish poisoning and azaspiracid shellfish poisoning. In addition there are many respiratory complaints from inhaling contaminated aerosols [45]. A case reported that in July 2002 teenage boys swam in a blue-green algae covered golf course in Dane County, Wisconsin. They all became ill, the most severe symptoms occurred in the boys who swallowed water. Approximately after 48 h one of the boys suffered a seizure and died of heart failure, the coroner identified anatoxin-a as the most likely underlying cause of death [46, 47].
In May and June 1998, over 200 California sea lions died and others displayed signs of neurological dysfunction along the central California coast, this was linked to a harmful algal blooms [48].
Harmful algal blooms is a cause of restriction on drinking water, fisheries and recreation water uses leading to significant economic consequences [49]. The presence of algal bloom and other species have disrupted the normal supply of drinking water in many parts of the world for example China [41]. The presence of algal blooms in Lake Tai severely affected industrial and agricultural production as well as lives of the urban dwellers. Whereby in 1990 algal bloom forced the shutdown of the entire water supply system and triggered a crisis in water security for the urban population. The direct economic loss was estimated at about U.S.$30 million. Harmful algal blooms present significant challenges for achieving water quality protection and restoration goals especially when these toxins confound interpretation of monitoring results and environmental quality standards implementation efforts for other chemicals and stressors [49].
There is need to reduce anthropogenic nutrient inputs to aquatic ecosystems in order to reduce the negative effects of eutrophication [50]. It has been indicated that reducing P input in the water bodies leads to eutrophication mitigation [16, 51] (Table 1) [16]. Derived this conclusion from four methods, all long-term studies at ecosystem scales:
long-term case histories,
multiyear whole lake experiments,
experiments where chemical treatments are used to remove phosphorus from the water column, and
chemical additions to inhibit return of phosphorus from the sediments to the water column.
However, [6, 52] argued that P based nutrient mitigation commonly regarded as the key tool in eutrophication, in many cases has not yet yielded the desired reductions in water quality and nuisance algal growth in water bodies has not reduced in decades of reducing P input. [52, 53] argued that these observations could be as a result of:
legacies of past land-use management;
decoupling of algal growth responses to river P loading in eutrophically impaired aquatic system; and
recovery trajectories, which may be nonlinear and characterized by thresholds and alternative stable states.
Therefore, as a result of these contrasting findings there is need in some cases to consider a combination of different P mitigation strategies for example employing control of nutrient loading, physicochemical and physicomechanical method simultaneously. Control or mitigation of P eutrophication should encompass multiple components which could include; control of pollutant sources, restoration of the damaged ecosystem, and catchment management [41]. The mitigation strategies includes:
Point source P originating from mines, factories and residence form one of the most important sources of P to water bodies [41]. For example Lake Tai in China, its catchment area used to be full of heavy industrial polluters, for example, chemical and dye factories. The township lacked adequate facilities for treating waste water before disposal. Therefore, to mitigate pollution coming from the industry it is important to shut down heavily polluting industries. While as the less polluting plants could be relocated to a designated industrial part to ensure centralization and effectiveness in handling pollution control.
It has been much easier to control point source P, therefore making nutrient discharge from agricultural fields the chief source of pollution [41]. As a result nutrient discharge from agricultural fields could be addressed through farm, field and catchment management or rationalization of land use [41].
In the farm scale environmentally sound fertilizer application and nutrient handing is important this would be achieved through appropriate placement and proper timing of application. This would result in moderate P levels in the soils. In Addition P input could be reduced through increasing digestible P in fodder and reducing total P [51] (Table 2).
Examples of fresh waters in some countries where eutrophication decreased following the control of phosphorus inputs. Latitudes and longitudes are given. Lakes recovered by using chemicals to precipitate phosphorus are not included, modified from [16].
Mitigation strategies for nutrient management at farm scale. Modified from [51].
To avoid transport of particulate P and leaching of P, increase soil storage there is need to change soil management. In addition there is need to change crop management in order to reduce run off and reduce leaching [51] (Table 3).
Mitigation strategies at field scale modified from [51].
In the catchment scale eutrophication mitigation strategy would involve water management, land use management and landscape management [51]. Water management could be achieved through reducing runoff flow and avoiding subsurface leaching. Land use management would involve protecting vulnerable areas and improving sink and sources of P by changing agricultural use patterns. Land scape management would include reducing direct sources of P from farmyard, livestock and reducing surface runoff and erosion from field to field within the catchment [51] (Table 4).
Mitigation strategies at catchment scale modified from [51].
It has been demonstrated that often the nutrient load and algal blooms in water bodies respond slowly to interventions aimed at controlling external nutrient sources because of the nutrients replenished from waterbodies deposits [54]. As a result P could be reduced through physiochemical and physicomechanical methods. Whereby the P is trapped and removed from the system or trapped on farm and its mobility to aquatic system reduced.
Reduction in the external P loading for control of algal biomass in the water reservoirs can be achieved by the use of ferric dosing. Ferric dosing technique is a physiochemical method and involves the addition of ferric sulfate or alternatives to the pumped input, to precipitate dissolved particulate and orthophosphate in the coming water. The system is coupled with filtration to remove the ferric/phosphorus floc [33]. Resulting in a significant reduction of P in the pumped inputs to the aquatic system.
Flushing and dredging of floor deposits is a physicomechanical methods meant to remove the already accumulated P from the aquatic system floor [55]. The limitation with both ferric dosing and flushing and dredging of floor deposits is that they provide temporal solutions and do not address the root cause of the problem. Once the intervention is stopped nutrients levels goes back to the former status. However, the success of these methods are dependent on their being implemented together with control of nutrient load intervention.
Application of P on farm has potential to mitigate P eutrophication though P adsorption leading to reduction in P translocation (Figure 1). The P adsorption to biochar is favored by increased biochar pyrolysis temperature and is biochar biomass species specific [24]. The increase of biochar aromatic C (Figure 2) and pH adjustment with high biochar pyrolysis temperature is important for P retention [24]. Biochar is a byproduct of biofuel production, therefore increased production of biofuel will be consistent with biochar availability in future.
Biochar phosphorus adsorption; from [24].
Biochar carbon functional groups as determined by nuclear magnetic resonance (NMR); from [24].
Ecosystem restoration focus on rehabilitating the functionality of the damaged ecosystem and it relevant physical, chemical and biological properties [41].
Ecological restoration may be accomplished through reduction of algae in the water bodies through aquatic plants. Being primary producers, advanced aquatic plants and micro-organisms compete with each other for ecological resources, such as light, nutrients, and living space. During their growth, advanced aquatic plants release chemical substances that are conducive to inhibiting algal production, as well as directly absorbing nitrogen and phosphorus in water. Storage of these elements in the plants means that they can be effectively extracted from the water through physical removal of these plants from the lake, thus reducing the nutrient level in lake waters [56].
Wetland restoration and constructed wetlands retain nutrient loss from upstream fields protecting the aquatic system (Table 5) [51]. Wetlands play a key role in P removal due processes that include peat accretion (sorption and burial in soil and sediments), uptake by microbes and vegetation and precipitation by iron and aluminum [57, 58, 59].
Mitigation strategies in aquatic ecosystems. From [51].
Although [18] indicated that ground water contained elevated P which was a driver of eutrophication, there was no clear evidence of the location and sources of the pollution, as a result measure to decrease groundwater derived P loads cannot target the contamination at its source in the catchment. Hence the need to implement measures in the riparian area to eliminate groundwater P directly before it enters the water body.
Phosphorus eutrophication is a major environmental problem globally resulting in negative impact on the economy, health and tourism sector. Phosphorus eutrophication is caused by both point and nonpoint sources of P. In many countries point source of P has been better controlled while nonpoint sources of P which is mainly agricultural sources have been an ongoing major challenge. The excessive P in the farm is a result of excessive fertilizer and manure application on farm. Phosphorus has mainly been translocated from the source to aquatic systems through run off and leaching and in some isolated cases through ground water. There is need to implement mitigation strategies. This chapter recommends implementation of measures to control nutrient loads through restructuring industrial layout which is a point sources of P pollution. To address nonpoint source of P there is need to implement catchment management measures and ecosystem restoration measures. The catchment management encompasses farm scale, field scale and catchment scale measures that will either reduce P availability for translocation or retain P in the catchment area. Human intervention is equally important to ensure removal of P from already contaminated aquatic system or prevention of P translocation to the water bodies; human intervention includes ferric dosing, flushing and dredging of floor deposits and biochar application on farm. The human intervention especially ferric dosing and flushing and dredging of floor deposits has limitation because once intervention is abandoned the P status could easily revert to pre-intervention status. Previous studies indicate contrasting finding on the success of the mitigation strategies, whereby some reported success while others indicated no response to P eutrophication mitigation. As a result, it seems there is need in some cases to combine multiple eutrophication mitigation interventions for example control of nutrient loading, physicochemical and physicomechanical interventions in order to take care of legacy P and ensure successful mitigation process.
Special thanks to College of Agriculture and Food Sciences, Florida A&M University for providing a conducive environment for writing this book chapter. This work was supported by USDA/NIFA (1890 Evans-Allen Research Program), Division of Research Florida A&M University and USDA-Forest Service grant number 17-CA-11330140-027.
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