The ionization equations and pKa value in magnesium ammonium phosphate solution at 25° [30, 31].
\r\n\t
",isbn:"978-1-83968-460-9",printIsbn:"978-1-83968-459-3",pdfIsbn:"978-1-83969-232-1",doi:null,price:0,priceEur:0,priceUsd:0,slug:null,numberOfPages:0,isOpenForSubmission:!0,hash:"babca2dea1c80719111734cc57a21a4c",bookSignature:"Dr. Amin Talei",publishedDate:null,coverURL:"https://cdn.intechopen.com/books/images_new/10404.jpg",keywords:"Water Budget, Ground Measurement, Satellite Data, Empirical Models, Physical Models, Data-Driven Models, Artificial Neural Network, Neuro-Fuzzy Systems, Genetic Programming, Irrigation Management, Drought, Aquifer Management",numberOfDownloads:null,numberOfWosCitations:0,numberOfCrossrefCitations:null,numberOfDimensionsCitations:null,numberOfTotalCitations:null,isAvailableForWebshopOrdering:!0,dateEndFirstStepPublish:"October 29th 2020",dateEndSecondStepPublish:"November 26th 2020",dateEndThirdStepPublish:"January 25th 2021",dateEndFourthStepPublish:"April 15th 2021",dateEndFifthStepPublish:"June 14th 2021",remainingDaysToSecondStep:"2 months",secondStepPassed:!0,currentStepOfPublishingProcess:3,editedByType:null,kuFlag:!1,biosketch:"A pioneering researcher in developing hydrological models using adaptive neuro-fuzzy systems, a pioneering researcher in tropical biofiltration systems, appointed head of the Civil Engineering Discipline in Monash University Malaysia.",coeditorOneBiosketch:null,coeditorTwoBiosketch:null,coeditorThreeBiosketch:null,coeditorFourBiosketch:null,coeditorFiveBiosketch:null,editors:[{id:"335732",title:"Dr.",name:"Amin",middleName:null,surname:"Talei",slug:"amin-talei",fullName:"Amin Talei",profilePictureURL:"https://mts.intechopen.com/storage/users/335732/images/system/335732.jpg",biography:"Associate Professor Amin Talei joined Monash University Malaysia in January 2013 and currently is the head of Civil Engineering discipline. His previous appointment was as researcher in School of Civil & Environmental Engineering of Nanyang Technological University of Singapore where he studied for his PhD during 2008-2011. His research is predominantly focused on hydrological modeling and flood forecasting using artificial intelligence techniques. Most recently, he has been also involved in research projects dealing with sustainable urban water management. To date, he has published over 50 articles in reputable journals and international conference proceedings. He has supervised several PhD and Master students and won the Supervisor of the Year Award in Monash University Malaysia in 2017. He has absorbed over AUD370,000 research funding from industry and international/national funding agencies since 2014 and is a chartered professional engineer of the Engineers Australia.",institutionString:"Monash University Malaysia",position:null,outsideEditionCount:0,totalCites:0,totalAuthoredChapters:"0",totalChapterViews:"0",totalEditedBooks:"0",institution:{name:"Monash University Malaysia",institutionURL:null,country:{name:"Malaysia"}}}],coeditorOne:null,coeditorTwo:null,coeditorThree:null,coeditorFour:null,coeditorFive:null,topics:[{id:"10",title:"Earth and Planetary Sciences",slug:"earth-and-planetary-sciences"}],chapters:null,productType:{id:"1",title:"Edited Volume",chapterContentType:"chapter",authoredCaption:"Edited by"},personalPublishingAssistant:{id:"297737",firstName:"Mateo",lastName:"Pulko",middleName:null,title:"Mr.",imageUrl:"https://mts.intechopen.com/storage/users/297737/images/8492_n.png",email:"mateo.p@intechopen.com",biography:"As an Author Service Manager my responsibilities include monitoring and facilitating all publishing activities for authors and editors. From chapter submission and review, to approval and revision, copyediting and design, until final publication, I work closely with authors and editors to ensure a simple and easy publishing process. I maintain constant and effective communication with authors, editors and reviewers, which allows for a level of personal support that enables contributors to fully commit and concentrate on the chapters they are writing, editing, or reviewing. I assist authors in the preparation of their full chapter submissions and track important deadlines and ensure they are met. I help to coordinate internal processes such as linguistic review, and monitor the technical aspects of the process. As an ASM I am also involved in the acquisition of editors. 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Venkateswarlu",coverURL:"https://cdn.intechopen.com/books/images_new/371.jpg",editedByType:"Edited by",editors:[{id:"58592",title:"Dr.",name:"Arun",surname:"Shanker",slug:"arun-shanker",fullName:"Arun Shanker"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"878",title:"Phytochemicals",subtitle:"A Global Perspective of Their Role in Nutrition and Health",isOpenForSubmission:!1,hash:"ec77671f63975ef2d16192897deb6835",slug:"phytochemicals-a-global-perspective-of-their-role-in-nutrition-and-health",bookSignature:"Venketeshwer Rao",coverURL:"https://cdn.intechopen.com/books/images_new/878.jpg",editedByType:"Edited by",editors:[{id:"82663",title:"Dr.",name:"Venketeshwer",surname:"Rao",slug:"venketeshwer-rao",fullName:"Venketeshwer Rao"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"4816",title:"Face Recognition",subtitle:null,isOpenForSubmission:!1,hash:"146063b5359146b7718ea86bad47c8eb",slug:"face_recognition",bookSignature:"Kresimir Delac and Mislav Grgic",coverURL:"https://cdn.intechopen.com/books/images_new/4816.jpg",editedByType:"Edited by",editors:[{id:"528",title:"Dr.",name:"Kresimir",surname:"Delac",slug:"kresimir-delac",fullName:"Kresimir Delac"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}}]},chapter:{item:{type:"chapter",id:"54320",title:"Phosphorus Recovery by Struvite Crystallization from Livestock Wastewater and Reuse as Fertilizer: A Review",doi:"10.5772/65692",slug:"phosphorus-recovery-by-struvite-crystallization-from-livestock-wastewater-and-reuse-as-fertilizer-a-",body:'\nPhosphorus is a key factor causing water eutrophication, on the other hand, it is also a nonrecyclable, nonrenewable, and quite valuable resource. According to the Mineral Commodity Summaries 2015 [1] from the United States Geological Survey (USGS), the reserve of phosphate rock in China is 3.7 billion tons in 2014, which is in second place in the world. However, with a total of 43–48% of the world’s phosphate rock production over the last 3 years [2], the phosphate rock might run out in less than 40 years. So phosphate rock has been one of the 20 minerals that could not meet the demand of the national economy development after 2010 as reported by the Ministry of Land and Resources in China.
\nOn the other side, the intensive livestock farming is a pillar industry in agricultural economy and an important way to increase rural incomes in China [3]. However, it usually produces large amount of livestock wastewater containing high concentration of phosphorus [4]. If this wastewater was not treated reasonably, it would not only lead to the pollution of water eutrophication, but also waste nonrenewable resources and would become one of the major contributors to phosphorus loss [5]. According to the first national sources of pollution survey [6] in China in 2008, nonpoint source pollution in agriculture is a major cause of eutrophication. It accounts for 34.24% of the total phosphorus emission amount, including the livestock and poultry industry. Therefore, it is quite valuable to combine nutrient recycling with environmental pollution control to recover losing phosphorus from livestock wastewater [7].
\nNumerous phosphorus recovery technologies have been developed, such as biological phosphorus removal, chemical precipitation, electrolysis, adsorption, and crystallization. Biological phosphorus removal utilizes polyphosphate-accumulating organisms to capture phosphorus in their cells. However, this method is limited by the lack of carbon sources and the difficulty of culturing pure bacteria [8]. Chemical precipitation process may consume expensive chemicals and produce large amounts of chemical sludge [9]. Electrolysis is restricted by the small capacity of handling wastewater and the frequent renewal of electrodes [10, 11]. Recovering phosphorus from wastewater using chemical adsorbents is expensive, so cheaper and more efficient adsorbents are necessary for research [12].
\nRecovering phosphorus by crystallization, by contrast, is a more economical and efficient way. As long as the crystallization conditions are suitable, the struvite crystal would be generated just by adding magnesium (Mg2+) in the raw wastewater which has high concentrations of HnPO4n−3 and NH4+-N. This technology can remove nitrogen at the same time and its production can be used as fertilizer. So it had been studied in many kinds of wastewater, such as multiple wastewater [13], industrial wastewater [14, 15], municipal landfill leachate [16], biogas slurry [17], and effluent of sewage sludge [18], and livestock wastewater is no exception.
Magnesium ammonium phosphate, also known as struvite, is a white crystal generated in neural or mild alkali condition, for which the chemical formula is Mg(NH4)PO4⋅6H2O. Struvite consists of one molecule of magnesium(Mg2+), one molecule of ammonium (NH4+), one molecule of phosphate (PO43−), and six molecules of water (H2O), whose relative molar mass is 245.43 g/mol. It is only slightly soluble in water but soluble in acid solution [19]. Struvite is a light crystal with low relative density of 1.65–1.7. It is not easy to be rush off by rainfall [20]. Pure struvite belongs to orthorhombic crystals which consists of regular PO43− octahedron, distorted Mg(H2O)62+ octahedron, and groups of NH4+ connected by hydrogen bonding [21], but shows rod-like structure [22] or irregular structure [23] sometimes (Figure 1). And struvite of rod-like structure is of low purity, because of the coprecipitation with foreign ions.
The SEM figure of magnesium ammonium phosphate crystal.
Actually, struvite had been widely studied as early as 1937 for the congestion in the pipes of the sludge anaerobic digester [24]. The general struvite forming reaction equation is shown below:
\nWhen Mg2+, NH4+, and HnPO4n−3 (n = 0, 1, or 2) exist in the solution and the product of their concentrations are bigger than the solubility product constant (Ksp) of struvite, the crystal would be generated spontaneously. And the calculation formula of struvite\'s Kspis shown below:
\nwhere [Mg2+], [NH4+], and [PO43−] are concentrations of Mg2+, NH4+, and PO43− in the solution, respectively. As the molar ratio of Mg2+, NH4+, and PO43− is 1:1:1 in struvite, so C* is used to present the same concentration of these three ions, which means C* = [Mg2+] = [NH4+] = [PO43−]. So the calculation formula of struvite’s Kspalso can be shown as:
\nSnoeyink et al. [25] got the Ksp of struvite is 10−12.6 as early as 1980. Ohlinger et al. [26] corrected it to 10−13.26 in 1999. And then Bhuiyan et al. [27] corrected it again to 10−13.36 in 2007, which is widely used now. However, Ksp of struvite is hard to get in the real wastewater for the negative impact of the soluble coexisting ions. Therefore, in the estimation of the saturability of the real wastewater, ionic activity coefficient (Kso) is more widely useful than Ksp. Considering the impact of ionic strength (I) and the ionic activity (Ai) in estimating the Kso, the value of Kso is bigger than Ksp. And the calculation formula of struvite’s Ksois shown below:
\nwhere αi presents the ionic activity (Ai), γi presents the activity coefficient of the ionic strength (I), and [Ci] presents the concentration of the ion. Only when the value of γi is 1, Ksp is able to represent Kso. Therefore, it is necessary to eliminate the interruptions of the soluble coexisting ions (like Ca2+, CO32−, and SO42−) and clear of the ionic activities of Mg2+, NH4+, and PO43− in the specific pH condition. Table 1 shows the ionization equations and pKa value in magnesium ammonium phosphate solution at 25°C, which is helpful to estimate the distribution of these ions and predict the probability to generate struvite under such environment of solution.
No. | Ionization equation | pKa |
---|---|---|
1 | NH4+ ⇌ NH3 (aq) + H+ | 9.26 |
2 | H3PO4 ⇌ H2PO4− + H+ | 2.12 |
3 | H2PO4− ⇌ HPO42− + H+ | 7.20 |
4 | HPO42− ⇌ PO43− + H+ | 12.36 |
5 | MgNH4PO4⋅6H2O ⇌ Mg2+ + NH4++ PO43− + 6H2O | 12.70 |
6 | MgOH+ ⇌ Mg2+ + OH− | 2.56 |
7 | MgH2PO4+ ⇌ H2PO4− + Mg2+ | 0.45 |
8 | MgHPO4 ⇌ HPO42− + Mg2+ | 2.91 |
9 | MgPO4− ⇌ PO43− + Mg2+ | 4.80 |
Nucleation and crystal growth are two classical steps in the process of struvite crystallization from generation to development. As shown in Figure 2, nucleation is the first step of the struvite crystallization. When Mg2+, NH4+, and PO43− meet under the proper pH value, nucleation occurs. And the nucleation time is the time required to form a saturated solution to the beginning of the nucleation. It is mainly influenced by the pH of solution, mixing energy, coexisting ions, and saturation index (SI). The ion activity affected by the value of pH significantly leads to differentiation of combine speed of free ions [28]. Weak ion activity means slow combine speed and longer nucleation time indirectly. When the rate of struvite nucleation and growth is greater than or equal to the rate of mixing magnesium to the solution, there needs additional mixing energy. Kim et al. [15] emphasized that mixing energy could influence the quantity and size of struvite strongly. However, the greatest impaction of struvite nucleation is saturation index (SI) of solution which decides the development of crystal to homogeneous or heterogeneous directly [26]. SI is used to describe the saturation state of the reaction system of struvite. And the SI calculation of struvite is shown as follows:
The crystal nucleation, growth and aggregation mechanism of magnesium ammonium phosphate.
where IAP and Ksp represent ionic activity product and the thermodynamic solubility product of struvite, respectively [29]. The homogeneous crystallization that we want happens on metastable region in the solution. In this region, nucleation is not spontaneous, which differentiated between the process of crystallization and precipitation, and avoids the occurrence of undesirable spontaneous nucleation to a great extent [28]. However, mestastable state of solution is very difficult to control. Therefore, SI, as the indicator for metastable state, is very important. Bonurophoulos et al. [30] found that the threshold between homogeneous and heterogeneous precipitation is the condition where SI ≈ 2.0 and the nucleation rate of 1 nucleus/(cm3⋅s). When the SI is less than 1.716, the struvite crystals are in heterogeneous precipitation and vice versa. Bhuiyan et al. [31] and Mehta et al. [32] also got the threshold at SI = 1.83 and SI = 1.7 at the special nucleation rate, respectively. In addition, Durrant et al. [33] emphasized the great influence of SI on the shape of struvite as early as 1999. And it also has a SI threshold between rhombic structure and rod-like structure of struvite.
\nAfter the crystal nucleus generates, the ions in the solution used to form the crystal begin to deposit on the crystal nucleus and the nucleus grow to the settling particles. During that time, there are two trends for the development of particles. One is orientation growth, which means the ions sequence in the crystal is arranged according to a certain lattice. The other one is nonorientation growth, which means these ions are too late to arrange in order. It is the fast growth rate that causes disorder. And two types of the crystal growth mechanisms lead to different trends. One is the integration mechanism, and the other is the mass transfer mechanism. The former is the integration of solute molecules into the surface; the latter is the transfer (by diffusion or convection) of solute molecules from the bulk solution to the crystal surface. When the effect of mass transfer is greater than the effect of integration, the crystal growth mainly depends on the diffusion effect and the growth of crystal would be orientable. However, if the effect of integration is greater, the integration on the surface of solute decides the crystal growth. And the relative sizes of the nucleation rate, aggregation rate, and directional array rate also decide the trend of crystal growth, which can be changed by precipitation conditions [31]. Abe et al. [34] showed that the growth rate of struvite was very slow. In the high concentration of phosphate (greater than 200 mg/L), the daily growth rate of struvite was 0.173 mm. In the low concentration of phosphate (30–100 mg/L), the daily growth rate of struvite was 0.061 mm. Therefore, increasing crystal growth rate and crystal size of struvite is not only beneficial to further removing phosphorus from livestock wastewater, but also to recycling phosphorus with a bigger size struvite. There is a metastable zone in industrial crystallization to make the crystal bigger and more even. The metastable zone is defined as a region bounded by the solubility curve in which the solution is supersaturated but the spontaneous nucleation cannot occur in such a short time [35]. In the metastable zone, the solute condenses on the nucleus as constantly as possible. As we known, the process of struvite constant growth is also the further recovery of phosphorus from livestock wastewater. So it is meaningful to study the metastable zone of struvite for the industrialized application.
Generally speaking, livestock wastewater is rich in ammonium and phosphorus. So it is needed to add extra magnesium to form struvite. Therefore, the addition amount of magnesium affects the solubility product constant (Ksp) directly, which further affects the quantity of struvite crystal and the recovery rate of phosphorus in livestock wastewater. So the molar ratio of phosphate and magnesium is the key factor to control the yield of phosphorus recovery. The molar ratio of phosphate and magnesium is 1:1 in theory. However, the real molar of the added magnesium is larger than the total amount of phosphorus in the real livestock wastewater. As shown in Table 2, for a higher phosphorus removal rate, the molar ratio of phosphate and magnesium is about 1:1–1.2 from livestock wastewater, 1:1.4 from synthetic livestock wastewater, and 1:1–1.4 from anaerobic digesters of livestock wastewater. It is mainly based on the effect of coexisting ions in the livestock wastewater. The coexisting ions, such as OH− and CO32−, are apt to coprecipitate with Mg2+, which prevent the Mg2+ from touching with the NH4+ and PO43−, so more magnesium is needed. Marit et al. [36] indicated that there would be many other kinds of magnesium phosphate precipitates except for struvite at different value of pH, such as Mg3(PO4)2, MgHPO4, and Mg(H2PO4)2. So it does not mean that more magnesium means more struvite. Excessive amounts of magnesium would increase the pH value of the solution as well as the degree of saturation of the magnesium salts, resulting in the formation of other kinds of magnesium phosphate precipitates mentioned.
Samples | Initial concentration of phosphate (mg/L) | Molar ratio of N, P, and Mg | pH | Reaction time | Removal rate of phosphate (%) | References |
---|---|---|---|---|---|---|
Animal manure wastewater | 145 | 16.4:1:1.05 | 8 | 30 min | 67 | [40] |
Animal manure wastewater | 189.9 | 1:1:0.8–1 | 8.35 | 4 h | 96 | [41] |
Animal manure wastewater | 60.01 | 63.5:1:1 | 8.09 | 4 h | 92.82 | [42] |
Animal manure wastewater | 128 ± 13 | 1:1:1.2 | 9 | 1 h | 98 | [43] |
Synthetic animal manure wastewater | 80 | 8:1:1.4 | 9.5–10.5 | 2 h | 97 | [44] |
Synthetic animal manure wastewater | 130.2 | 1:1:5 | 7.9 | – | 92 | [45] |
Anaerobic digesters of manure wastewater | 51.1 | 30.7:1:1.4 | 8.0–10.0 | 1 h | 74–95 | [46] |
Anaerobic digesters of manure wastewater | 55.4 | 9.6:1:1.2 | 9.0 | 20 min | 85 | [47] |
Anaerobic digesters of manure wastewater | 64.2 | 1:1.2:1.2 | 9.0 | 15 h | 97.2 | [48] |
The summary of parameters on magnesium ammonium phosphate crystallization.
The value of pH of livestock wastewater is an important parameter to the formation of struvite. It affects the quality and the purity of struvite at the same time. As shown in Table 2, the best value of pH to form struvite is between 8 and 10, while 8.0–9.0 is the best for livestock wastewater. However, Hao et al. [37] indicated that struvite could get the highest purity at pH = 7.0, and the purity seemed to have fallen with the increasing of the pH value of wastewater. When the value of pH is higher than 10, the formed precipitate mainly consists of Mg3(PO4)2 (Ksp= 9.8 × 10−25). Song et al. [38] also found that the precipitate of Mg(OH)2 would form at the pH of 11. It does not mean that it is better to form struvite at a lower value of pH. However, considering the phosphorous recovery, as long as the productions of phosphorus salts are harmless and nontoxic, the aim of recovering phosphorus from livestock wastewater is reached. Anyway, the pH value of livestock wastewater is generally between 7.5 and 8.5, which is more convenient to recover phosphorus without the need for adjusting the pH value. It is helpful to simplify the technology and reduce the cost of livestock wastewater treatment.
There are many kinds of coexisting ions interfering with the crystallization of struvite in livestock wastewater, such as calcium ion (Ca2+), carbonate ion (CO32−), suspended solids (SS), and heavy metal ions (HMI). Moerman et al. [39] found that Ca2+ could enhance the phosphorus removal with forming the precipitate of Ca3(PO4)2. However, it reduces the size of struvite. Meanwhile, lots of Ca3(PO4)2 powder flows out with effluent easily, declining the effluent water quality. Le Corre et al. [40] also declared that Ca2+ would compete with Mg2+ and form the precipitates of Ca3(PO4)2 (Ksp = 2.1 × 10−33) and CaHPO4 (Ksp = 1.8 × 10−7) at the pH value of 9. By performing batch experiments, Zhang et al. [41] found that the degree of the supersaturation would decrease with the increase of the concentration of CO32−. The CO32−, easily combining with Mg2+, increases the ion saturation in the solution and decreases the concentration of Mg2+ forming struvite. Suzuki et al. [42] showed that negatively charged SS adsorbed NH4+ and Mg2+ easily in the alkaline environment, which retarded the struvite crystalline rate. And Muryanto et al. [43] studied on the influence of copper ions (Cu2+) and zinc ions (Zn2+) in struvite crystallization and showed that the existence of Cu2+ and Zn2+ would delay the nucleation rate and the growth rate of struvite. Although they had little impact on the crystal shape, the crystal would have some cracks on the surface.
\nAll in all, in the process of recovering phosphorus from livestock wastewater, some pretreatments are necessary to implement for removing these coexisting ions before forming the struvite. Laridi et al. [44] tried to reduce the negative impacts of organics and SS by adding ferric chloride and flocculants into the livestock wastewater, and it worked with a higher phosphorus removal rate at the same time. Suzuki et al. [42] tried to separate the struvite from suspended solids containing heavy metals by the differences of their settlement characteristics. It improved the purity of struvite and reduced the negative impact of SS and heavy metal ions.
Seed crystals have positive influence in the struvite growth. Adding seed crystals can reduce the saturation of struvite crystallization in need, shorten the nucleation time, and increase the rate of crystal growth. What is more, struvite crystallizes on the surface of seed crystals, which enhances the separation of crystals and water, prevents the tiny crystals from flowing out with the effluent, and improves the phosphorus removal efficiency. Ariyanto et al. [45] showed that the smaller the added crystal nucleus is, the faster is the rate of crystal growth. Kim et al. [18] emphasized that the excessive amount of seed crystals added could not improve the phosphorus removal efficiency, and the pH value of wastewater also influenced the efficiency at the same dosage of seed crystals. The phosphorus removal efficiency is more significant at the pH value of 9. So only adding proper amount of seed crystals with a proper average size can the phosphorus removal efficiency be higher.
It is important to realize the phosphorus recycling in crystallizer, as the struvite crystallization equipment. The pros and cons of its design decide the shape and size of the struvite and the phosphorus removal efficiency from livestock wastewater. A series of struvite crystallizers had been developed and put into production successfully abroad previously, which had obtained environmental and economic benefits simultaneously. According to the mode of agitation, these crystallizers can be divided into air agitation type, water agitation type, and mechanical agitation type.
\nThe air agitation type crystallizer is a kind of crystallizer that is studied widely. The special aerate system can not only mix the solution more efficiently, improving the collision chance of crystal forming ions, but also vent the gas carbon dioxide and insoluble ammonium from the solution, increasing the pH value of the solution, the ammonium removal efficiency, and the effluent water quality at the same time. The crystallizer used by the British slough sewage treatment plant (Figure 3a) reached the soluble phosphorus removal rate of 94% and the total phosphorus removal rate of 87.5% with drumming into air under the inner reaction zone [46]. Le Corre et al. designed two concentric meshes made of stainless steel as a substrate to grow struvite in the crystallizer, which can trap and then accumulate the struvite in the reactor as an adhesive (Figure 3b). With the help of crystallizers, the phosphorus removal rate can increase from 81 to 86%. However, because of the limitations of volume and growth time, the struvite crystal cannot grow large enough in the air agitation type crystallizer, which causes the loss of phosphorus recovery. Moreover, some kinds of air agitation type crystallizer have the problem of replacing padding or membranes frequently. What is more, the congestion problem becomes serious once the crystallizer broke down for some reasons, and it is hard to restart.
Different kinds of crystallizers forming struvite. (a) The air agitation crystallizer from the British slough sewage treatment plant. (b) The air agitation crystallizer from Le Corre et al. (c) The water agitation crystallizer from Guadia et al. (d) The water agitation crystallizer from Rahaman et al. (e) The MSMPR type crystallizer with 1—internal circulation of suspension, 2—thermostat, 3—computer, 4—rural wastewater (including aqueous solution of MgCl2), 5—pump, 6—alkalinity agent tank: aqueous solution of NaOH, 7 and 8—pump, 9—storage tank of a product crystal suspension, 10, 11, and 12—electronic balances, M—stirrer speed control, T—temperature control, and pH—acid/alkaline reaction control.
The water agitation type crystallizer realizes uniform mixing by changing the solution flow direction, speed, or gravity changed the flow rate by increasing the diameters of the equipment from the bottom to the top, inserted cone-shape structures at an angle of 45° between every diameter-changed parts to reduce unwanted crystal loss at each junction, and recycled finer particles with the effluent through the external recycler (Figure 3c). This crystallizer can remove 92% phosphate, and the purity of struvite goes up to 99%. Rahaman et al. [47] designed four distinct zones at the same principle, added a settling zone (also called seed hopper) at the top, getting the phosphate removal rate of up to 90% and the size of particles up to 3.5 mm. Seed crystals are added into the crystallizer from the seed hopper and allowed the finer crystals to continue to grow up in the upper supersaturated solution.
\nThe mechanical agitation type crystallizer, mixing solution by impellers, is simple in design and easy to operate. However, it causes greater energy consumption and uneven size of crystals distribution. Recently, a new crystallizer called mixed suspension, mixed product removal crystallizer (MSMPR for short) can solve the problem of uneven crystal size distribution (Figure 3e). With the mechanical agitation centered and the water agitation assisted, MSMPR can uniform the suspension density and particle size of the crystals, and remove productions evenly by controlling the speed and time of mixing. Hutnik et al. [48] and Kozik et al. [49] both got the phosphate removal rate up to 99% from industrial wastewater and wastewater with low concentration of phosphorus. And both of them confirmed that MSMPR could increase the size of crystals, improve the crystallization rate of the struvite, and enhance the phosphorus recovery rate.
It is reckoned that 100 m3 wastewater could form 1 kg of struvite. If all the wastewater in the world is treated by struvite crystallization, 63,000 tons of P2O5 could be recovered, equaling to 16% of the phosphate rock production of the world [50]. And 171 g struvite can be recovered from livestock wastewater per square meter at most and the purity as high as 95% without washing. Therefore, recovery of struvite returning to the farmland is a developmental trend of struvite crystallization technology. Struvite, as a slightly soluble crystal, for containing the equal molar concentrations of magnesium (Mg), ammonium, and phosphate, has been successfully used on herbages [51], vegetables [14, 52], and grain crops [53] as a fertilizer, especially on the magnesium-fond crops, like sugar beet [54]. Especially, the presence of Mg in struvite makes it more attractive as an alternative to contemporary fertilizers for a few crops, which require magnesium [55]. Ryu et al. [52] found that the struvite source provided the essential crop nutrients of N, P, K, Ca, and Mg for Chinese cabbage as much as other commercial fertilizers. Moreover, it has a lasting positive function to roots and does not burn the seeding or roots due to its slow release characteristics. Besides, compared with other highly soluble fertilizers, struvite is more suitable for use in the vast areas of forest. Since the area of forest is too large to fertilize frequently, the use of struvite can decrease the frequency of fertilization and reduce the loss of nutrients [54]. However, as livestock wastewater is full of impurities, especially the heavy metal ions, the struvite recovered from livestock wastewater still contain more or less heavy metal ions. From livestock-based struvite, toxic substances may diffuse into the aquatic environment or accumulate in soils and have an adverse effect on the human health and environment [56, 57]. Although currently no specific threshold values are available for micropollutants in fertilizers, the introduction of potential hazardous substances into the environment should be avoided. The accumulation of heavy metal ions will be a serious concern for sustainability [58]. Ryu et al. [52] made a security evaluation for struvite as a fertilizer used in the soil. They affirmed the fertilizer efficiency of struvite and emphasized the negative effect of higher concentrations of copper and cadmium in struvite at the same time. Because copper and cadmium were tested in the cabbage fertilized by the struvite used as fertilizer, the struvite, especially recovered from livestock wastewater, needs to tested for the amount of toxic or harmful substances, followed by the security evaluation as a fertilizer.
Struvite crystallization represents a promising tool for recovering phosphorus from livestock wastewater. Based on this study, the conclusions are as follows.
\nStruvite is a white crystal which is formed in neural or mild alkali conditions. Nucleation and crystal growth are two steps for struvite crystallization from generation to growth. The molar ratio of magnesium and phosphate, and solution pH are the key factors to control. The coexisting substances, such as calcium, carbonate, suspended solids, and heavy metals, interfere the crystallization of struvite. Seed crystals have positive influence on struvite growth. Adding seed crystals can reduce the saturation of struvite crystallization, shorten the nucleation time, and improve the rate of crystal growth.
\nCrystallizer, its design decides the shape and size of struvite, is important to realize the phosphorus recycling. According to the agitation mode, it can be divided into air agitation, water agitation, and mechanical agitation.
\nThe recovered struvite can be used on herbages, vegetables, and grain crops as a fertilizer, especially on the magnesium-fond crops, like sugar beet.
\nHowever, there are still some problems. Livestock wastewater belongs to the organic wastewater with high concentrations of ammonium, phosphorus, organics, and suspend solids. And the existing forms are complex, such as simple monoester phosphorus, phytate-like phosphorus, and polynucleotide-like phosphoric. So it is necessary to use some physical or chemical measures to transform different kinds of phosphorus to phosphate, as many as possible, before removing phosphorus from livestock wastewater.
\nThe design for struvite crystallizer is still a key to struvite crystallization technology. Although enhancing the phosphorus removal rate has got a big breakthrough by the current crystallizer, the crystals are still too small to recover and block the crystallizer easily. It is the influence of negative zeta potential on the surface of crystals that makes further aggregating hard for small crystals. So finding a way to change the zeta potential on the surface of the crystals, enhancing the aggregation capability, and increasing the size of the crystals is required.
\nStruvite, a fertilizer with high concentrations of nutrients, might be difficult in application for the influence of other toxic or harmful impurities. Therefore, to reduce the environmental risk at source, it is necessary that estimating the potential effects of struvite on the ecosystem before use.
The work was supported by a grant from the National Natural Science Foundation of China (No. 31401944), the National key Research and Development Program of China (No. 2016YFD0501404), the Beijing Municipal Natural Science Foundation (No. 6144026), China Agricultural University Education Foundation “Da Bei Nong Group Education Foundation” (No. 1031-2415005), and the Specialized Research Fund for the Doctoral Program of Higher Education of China (No. 20120008120013).
Macrophages represent up to 50% of the cells infiltrating into the tumor microenvironment (TME) and modulation of macrophage polarization is an interesting and novel therapeutic approach in preclinical or clinical cancer research.
An increasing number of studies have also shown that tumor-associated macrophages (TAMs) can antagonize, augment or mediate the antitumor effects of cytotoxic agents, tumor irradiation, anti-angiogenic/vascular damaging agents and checkpoint inhibitors [1].
In the tumor microenvironment, TAMs are one of the major contributors in angiogenesis by secreting pro-angiogenic factors, such as vascular endothelial growth factor (VEGF), adrenomedullin (ADM), platelet-derived growth factor (PDGF), tumor growth factor-beta (TGF-β) and matrix metalloproteinases (MMPs). Also, TAMs promote tumor cell invasion and metastasis by modifying the composition of extracellular matrix and cell-cell junctions and promoting basal membrane disruption. It was demonstrated that macrophages facilitate the metastasis by enhancing the ability of cancer cells to enter a local blood vessel and also are involved in immunosuppression by inhibiting the T-cell response or by secreting immunosuppressive cytokines and proteases such as IL-10, TGF-β, arginase-1 and prostaglandins, which inhibit T-cell activation and proliferation [2].
TAMs often exhibit an array of activation states. In general, they are skewed away from the “classically” activated, tumoricidal phenotype (sometimes referred to as M1) toward an “alternatively” activated tumor-promoting one (M2) [1]. The classically activated M1 macrophages are stimulated by microbial substrates such as lipopolysaccharide, Toll-like receptor ligands and cytokines such as IFN-γ. They are characterized by secretion of pro-inflammatory cytokines such as interleukins IL-6, IL-12, IL-23 and TNF-α and express high levels of major histocompatibility complex class II (MHC-II), CD68, and CD80 and CD86 costimulatory molecules. The alternatively activated M2 macrophages are stimulated by IL-4 and IL-13, secrete IL-10 and TGF-β and express low levels of MHC-II and feature expression of CD163 and CD206 [3].
Unfortunately, M2 cells are the most representative cells of the TAM population within the tumor promoting genetic instability, local immunosuppression and stem cell nurturing [4] and providing essential support for a malignant phenotype [5].
In the early stages of cancers of the lung, colon and stomach, the macrophages in the normoxic milieu display an M1 phenotype and are associated with good prognosis, but within avascular areas of the tumor, TAMs alter the gene expression profile, favoring a protumor M2 phenotype, correlated with a bad prognosis [6]. In Table 1 are showed recent conclusions concerning the correlation between TAMs and clinical prognostics in several tumor types. In human breast carcinomas, high TAM density is also associated with poor prognosis [7]. TAMs in renal cell carcinoma show a mixed M1/M2 phenotype. CD68 alone has a poor predictive value, while low CD11+ and high CD206+ as single variables correlated with reduced survival [8]. There is strong evidence for an inverse relationship between TAM density and clinical prognosis in solid tumors of the breast, prostate, ovary and cervix. Type I and II endometrial carcinomas had significantly higher macrophage density in both epithelial and stromal compartments than benign endometrium [9]. Type II cancers have nearly twice the TAM density of type 1 cancers and this difference may be due to M1 macrophage predominance in the stroma of type II cancers [10].
Cancer type | TAMs as prognostic factors | Reference |
---|---|---|
Breast | CD68 as a biomarker for TAMs to evaluate the risk is better than CD163 or CD206 alone; high infiltration of TAMs was significantly associated with negative hormone receptor status and malignant phenotype | [14] |
Gastric | The amount of TAMs in tumor stroma predicts the size, stage and metastasis of the gastric tumor Invasive front-/stroma-dominant pattern having worse outcomes Although CD68+ TAMs infiltration has the neutral prognostic effects on OS, the M1/M2 polarization of TAMs are predicative factors of prognosis in gastric cancer patients | [11, 12, 15] |
Lung | The prognostic value of tumor-infiltrating TAMs in lung cancer is still controversial. M2 subset and TAMs in tumor stroma were associated with worse survival, while M1 subset and TAMs in tumor islet were associated with favorable survival of lung cancer. CD204-positive TAMs are the preferable marker for prognostic prediction in NSCLC Although the density of total CD68+ TAMs is not associated with overall survival, the localization and M1/M2 polarization of TAMs are potential prognostic predictors of NSCLC | [13, 16, 17] |
Cervix | Tumor-infiltrating CD204+ M2 macrophages may predict poor prognosis in patients with cervical adenocarcinoma | [18] |
Ovarian | CD163+ TAM infiltration was associated with poor prognosis of ovarian cancer and high M1/M2 macrophage ratio in tumor tissues predicted better prognosis | [19] |
Pancreatic | Although TAM populations in tumor stroma are high, marking them as a probable prognostic factor, the multiple roles that TAMs play in pancreatic cancer progression have not yet been delineated. Additional mechanistic insight into the pathways that regulate the differentiation of TAMs from monocytes is required The density of TAMs has an impact on the overall survival of pancreatic cancer patients. M2-TAMs can be recognized as a prognostic indicator in pancreatic cancer | [20, 21] |
Renal | CD68 alone has a poor predictive value, while low CD11+ and high CD206+ as single variables correlated with reduced survival | [8] |
Glioblastoma | TAM, accounting for approximately 30% of the GBM bulk cell population, may explain, at least in part, the immunosuppressive features of GBMs | [22] |
Hepatocellular carcinoma | The prognostic value of TAMs in patients with hepatocellular carcinoma (HCC) is still controversial. TAMs could serve as independent predictive indicators and therapeutic targets for HCC. Further trials are needed to elucidate the exact relationship and the underlying mechanism | [23] |
Melanoma | Independent of their intratumoral distribution, the prevalent accumulation of M2 TAMs in MM is statistically confirmed to be a poor indicator of patients’ outcome | [24] |
Non-Hodgkin’s lymphoma | High-density CD68+ and CD163+ TAMs, and also high CD163+/CD68+ TAMs ratio is significantly correlated with poor overall survival | [25] |
Hodgkin’s lymphoma | High density of either CD68+ or CD163+ TAMs is a robust predictor of adverse outcomes in adult cHL | [26] |
Colorectal (CRC) | The role of tumor-associated macrophages (TAMs) in predicting the prognosis of CRC remains controversial. Still, high-density CD68+ macrophage infiltration can be a good prognostic marker | [27] |
Squamous cell carcinoma of the head and neck (SCCHN) | CD68+ marker has no prognostic utility in patients with SCCHN; the M2-like marker CD163+ predicts poor prognosis | [28] |
TAMs as potential predictive indicators in several tumor types.
TAMs’ distribution pattern could be an independent prognostic factor for the overall survival of gastric cancer patients, invasive front-/stroma-dominant pattern having worse outcomes [11]. Studies have shown that the amount of TAMs in tumor stroma predicts the size, stage and metastasis of the gastric tumor [12]. In lung cancer, M2 subset and TAMs in tumor stroma were associated with worse survival, while M1 subset and TAMs in tumor islet were associated with favorable survival of lung cancer [13].
While most cancer research has focused upon these changes and most therapeutics are directed against these tumor cells, it is now apparent that the non-malignant cells in the microenvironment evolve along with the tumor and provide essential support for their malignant phenotype [5]. The knowledge of TAM activation status may allow the therapeutic targeting of TAMs, once TAMs’ targeting/modulating agents pass clinical trials and become widely available [6, 29]. The role of macrophages in tumor progression remains to be fully elucidated, in part due to the contrasting roles they play depending on their polarization [30]. Both the systemic and local environments play a tumor-initiating role through the generation of persistent inflammatory responses to a variety of stimuli [31]. To support this correlative data between macrophage-mediated inflammation and cancer induction, genetic ablation of the anti-inflammatory transcription factor STAT3 in macrophages results in a chronic inflammatory response in the colon that is sufficient to induce invasive adenocarcinoma. However, it is unclear whether macrophages in some inflammatory situations can kill aberrant cells before they become tumorigenic and thus be antitumoral [32].
Targeting a single signaling axis that promotes the immunosuppressive and protumoral functions of macrophages is inadequate as there are multiple signals involved in the communication between tumor cells and TAMs. Identifying and inhibiting key driver pathways, which are critical for both cancer cell survival and TAM activation, may offer therapeutic advantages as they disrupt the vicious positive feedback loop between tumor and TAMs [33]. Prevention of TAM accumulation and reduction of TAM presence by depleting existing TAMs represent novel strategies for an indirect cancer therapy specifically aimed at tumor-promoting cells within the microenvironment, but the challenge with this approach is to find ways for local administration of such drugs to the tumor [30]. Targeting TAM polarity toward an M1 phenotype also became a real immunotherapeutical approach in cancer, recalling responses from both innate and adaptive immune systems, leading to tumor regression [4].
Triple combination of anti-CTLA-4, anti-PD-1 and G47Δ-mIL12 was associated with macrophage influx and M1-like polarization in two glioma models [34]. A combination of a bivalent ganglioside and β-glucan, a yeast-derived polysaccharide, able to differentiate TAMs into an M1 phenotype is currently under investigation in a phase I clinical trial of patients with neuroblastoma [35]. Vadimezan, a fused tricyclic analog of flavone acetic acid, was found to repolarize macrophages in M1 phenotype, and it has been the subject of numerous preclinical studies and clinical trials [36]. Zoledronic acid, a clinical drug for cancer therapy, has been found to inhibit spontaneous mammary carcinogenesis by reverting macrophages from the M2 phenotype to the M1 phenotype [37].
Research to date suggests that, despite the potency of cytotoxic anticancer agents and the high specificity that can be achieved by immunotherapy, neither of these two types of treatment is sufficient to eradicate the disease. Moreover, even in standard chemotherapy, there has been efficiency through the introduction into current practice of treatments with combinations of drugs [38]. In general, literature data show that the combination of conventional treatment with natural compounds exerts an additive effect caused by the alternative activation of signaling pathways that induce cell death or increase the activity of the chemotherapeutic agent. The involvement of these natural compounds (alone or in combination therapy) in the immunobiology of cancer is a branch that has not yet been studied but offers major therapeutic opportunities. Herbal compounds have many regulatory effects on macrophage polarization, but the specific mechanisms, signaling pathways and target genes involved remain incompletely understood [39]. Their effects, according to recent research studies, are summarized in Figure 1.
Herbal compounds and their main actions on TAMs in cancer progression.
Although natural products have historically been a critical source for therapeutic drugs, sometimes natural molecules may suffer from insufficient efficacy, unacceptable pharmacokinetic properties, undesirable toxicity or reduced availability, which impedes their direct therapeutic application. Poor availability of some natural compounds, despite their pharmacological effects, limits their clinical application. In recent years, there has been an increased interest in developing nanoformulations with increased bioavailability and fewer side effects. For instance, TAM-rich tumors, due to their enhanced permeability, demonstrated an elevated retention (>700%) of the nanotherapeutic (poly(
Triterpenic compounds, including corosolic acid, tigogenin, timosaponin AIII, neoaspidistrin and oleanolic acid, suppress the CD163 expression. Corosolic and oleanolic acids change M2 polarization to M1 polarization in human monocyte-derived macrophages (HMDMs) by suppressing STAT3 and NF-kB activation. The effects of these two compounds were exerted not only on macrophages but also on glioblastoma cells, suppressing tumor cell proliferation and sensitizing tumor cells to anticancer drugs [40, 41].
M2 polarization was switched also by astragaloside IV (AS-IV, 3-O-β-
A potential role of celastrol, a pentacyclic triterpenoid in antimetastasis treatment, was suggested by Yang et al. [45], which found that this compound suppresses M2-like polarization by interfering with STAT6 signaling pathway after stimulation with IL-13. An active role in decreasing macrophage recruitment and tumor angiogenesis was showed for lupeol and stigmasterol in an in vivo model [46].
Treatment with 9-hydroxycanthin-6-one, a β-carboline alkaloid isolated from the Ailanthus altissima stem bark, inhibited the levels of M2 phenotype markers and some cancer-promoting factors, such as MMP-2, MMP-9 and VEGF, in macrophages educated in ovarian cancer–conditioned medium. The compound also decreased the expressions of MCP-1 and RANTES, major determinants of macrophage recruitment at tumor sites, in ovarian cancer cells [47].
A regulatory effect on macrophage differentiation during tumor development exerts phlenumdines E, A, hupermine A and 12-epi-lycopodine-N-oxide isolated from the club moss Phlegmariurus nummulariifolius (Blume) Ching, which exhibited an inhibitory effect on IL-10–induced expression of CD163, an M2 phenotype marker, in HMDMs [48].
Sophoridine, a bioactive alkaloid extracted from the seeds of Sophora alopecuroides L, was able to reshape gastric cancer immune microenvironment by shifting TAM polarization to M1 and suppressing M2-TAM polarization through TLR4/IRF3 axis [49].
In a model of azoxymethane (AOM)/dextran sodium sulfate (DSS)-induced colitis-associated tumorigenesis, it was showed that isoliquiritigenin (6′-deoxychalcone) inhibits M2 macrophage polarization depending on the downregulation of the IL-6/STAT3 pathway [50]. The same mechanism was proposed by Sumiyoshi et al. [51], for xanthoangelol and 4-hydroxyderricin, chalcones isolated from Angelica keiskei roots. In the in vivo study, the antitumor action of xanthoangelol was higher than that of 4-hydroxyderricin and it was proposed that the presence of a 4-free phenolic OH and/or the presence of a longer isoprene moiety in C-3 could be the cause of better activity of xanthoangelol. Reducing breast cancer cells’ migration with the aid of M2 macrophages was achieved in vitro by the total flavonoid from Glycyrrhizae Radix et Rhizoma and isoliquiritigenin. These compounds inhibited gene and protein expression of Arg-1, upregulated gene of HO-1 and protein expression of iNOS, and enhanced the expression of microRNA 155 and its target gene SHIP1 [52].
Macrophage infiltration and differentiation of macrophages into tumor-promoting M2 macrophage were decreased by epigallocatechin gallate (EGCG) treatment in murine tumor models and the molecular mechanism proposed was the downregulation of NF-κB pathway [53, 54]. EGCG can be rapidly degraded in vivo limiting its clinical application. A peracetate-protected EGCG (Pro-EGCG) synthesized by modification of the reactive hydroxyl groups with peracetate groups proved six times more stability than EGCG and showed greater efficacy in induction of cell death in leukemic cells. Treatment with Pro-EGCG inhibits differentiation of macrophages toward TAMs through decreasing CXCL12 expression in endometrial stromal cells with no influence on the expression level of CD163 and CD206 [55].
Luteolin, 3 0,4 0,5,7-tetrahydroxyflavone, is a common flavonoid derived from various plants and inhibits IL-4–induced phosphorylation of STAT6 and the TAM phenotype, ameliorating the recruitment of monocytes and the migration of lung cancer cells by the reduction of chemokine CCL2 secretion from macrophages [56]. The antitumor mechanism of luteolin in non-small cell lung carcinoma (NSCLC) was mediated by downregulation of TAM receptor tyrosine kinases (RTKs), and it was found to decrease the protein levels of all three TAM RTKs in the A549 and A549/CisR cells in a dose-dependent manner [57]. In an in vitro tumor model, cobalt chloride (CoCl2) was used to simulate hypoxia and it was showed that luteolin decreased the expression of VEGF and MMP-9, which promote angiogenesis. In addition, luteolin also suppressed the activation of HIF-1 and phosphorylated-signal transducer and activator of STAT3 signaling, particularly within the M2-like TAMs [58].
The regulation of M2 macrophage repolarization through inhibiting PI3K/Akt signal pathway is the mechanism proposed for baicalein (5,6,7-trihydroxyflavone), a widely used Chinese herbal medicine derived from the root of Scutellaria baicalensis. Changing the phenotype of macrophages from M2 to M1 was supported by decreasing of M2-specific marker CD206 correlated to the increased M1-specific marker CD86. Still, the authors of the study suggested that the cytotoxic effect of baicalein on breast cancer cells directly is more pronounced than on TAMs (IC 50 of baicalein for MDA-MB-231 at 24 h, 48 h and 72 h was 79.12/50.10/34.77 μmol/L, for MCF-7 at 24 h, 48 h and 72 h was 49.76/43.73/39.44 μmol/L, for TAM at 24 h, 48 h and 72 h was 191.5/107.1/41.78 μmol/L, respectively) [59].
It has been reported that a novel chrysin (5,7-dihydroxyflavone) analog 8-bromo-7-methoxychrysin has anticancer activities with more potent bioactivity than the lead compound [60]. It also has the capacity to regulate the tumor microenvironment by inhibition of NF-κB activation, suppressing significantly the expression of the M2 macrophage marker CD163 and modulating the secretion profile of TAM cytokines [61].
According to traditional Chinese medicine (TCM) theory, herbs with Qi-tonifying character are involved in improving the defense capacity of immune system. Total flavonoids from Glycyrrhizae Radix et Rhizoma significantly inhibited the expression of Arg-1 (above 90% at 100 μg/mL), one of the phenotype markers of M2 macrophages, and suppressed M2 polarization of macrophages partly by inactivating STAT6 pathway. The regulation of M1 and M2 markers’ expressions was partly due to the enhancement of miR-155 levels [62].
Naringin (4′,5,7 trihydroxyflavanone-7-rhamnoglucoside) exert a potential inhibitory effect on tumor progression by inducing CD169-positive and M1-like macrophages, potentially correlating with cytotoxic T-cell activation [63].
Puerarin [4H-1-benzopyran-4-one, 8-β-
Another isoflavone, genistein, can inhibit the increased M2 polarization of macrophages and stemness of ovarian cancer cells by co-culture of macrophages with ovarian cancer stem-like cells through disrupting IL-8/STAT3 signaling axis [65].
Chlorogenic acid (5-caffeoylquinic acid, CA), the ester of caffeic acid, is a phenolic compound widely found in plants. It was showed that this compound inhibits growth of G422 glioma in vivo, an effect associated with a decrease of M2-like TAMs and recruitment of M1-like TAMs into tumor tissue. Low dose (1 μM) of CA could significantly inhibit the M2 macrophage-induced proliferation of glioma and breast cancer cells, mainly via STAT1 and STAT6 signaling pathways [66]. Oršolić et al. [67] concluded that the antitumor activity of CA is the result of the synergistic activities of different mechanisms by which CA acts on proliferation, angiogenesis, immunomodulation and survival. Mice with Ehrlich ascites tumor (EAT) and treated for 10 days with CA in a dose of 40 and/or 80 mg kg−1 showed an increase of the cytotoxic actions of M1 macrophages and inhibition of the tumor growth, probably mediated through its antioxidative activity.
Deoxyschizandrin, a major dibenzocyclooctadiene lignan present in Schisandra chinensis berries, significantly suppressed CD163 and CD209 expression, inhibiting protumor mediator production as well as M2 polarization in TAM macrophages stimulated by the conditioned medium of A2780 cells [68].
Several studies focused on a stilbene derivative, resveratrol (3,4′,5-trihydroxystilbene), a widely studied compound that exhibits potent preventive effects on lifestyle-related disorders such as hyperlipidemia, obesity, coronary heart disease and cancer, as well as on aging. In lung cancer tumors, resveratrol induced their sluggish growth by decreasing F4/80 positive expressing cells and M2 polarization (lower expression of M2 markers‑IL-10, Arg-1 and CD206), probably by STAT3 suppression [69]. Antitumor and antimetastatic effects of resveratrol (25 and 50 μM) based on the regulation of M2 macrophage activation and differentiation were confirmed by Kimura and Sumiyoshi [70], which also conducted a study for correlation of stilbene structure with biological activity. Among the nine stilbenes examined, 2,3-,3,4-, and 4,4′-dihydroxystilbene inhibited the production of MCP-1 in M2-polarized THP-1 macrophages at a concentration of 50 μM, demonstrating that the inhibitory effects of stilbenes with dihydroxy groups on the production of MCP-1 were greater than those with mono-hydroxyl groups. Dihydroxystilbene at 25 and 50 μM, 3,4-dihydroxystilbene at 50 μM, and 4,4′-dihydroxystilbene at 10, 25 and 50 μM significantly inhibited the production of IL-10 by M2 THP-1 macrophages. The three dihydroxystilbenes, 2,3-, 3,4-, and 4,4′-dihydroxystilbenes, at concentrations of 10–50 μM inhibited p-STAT3 increase during M2 THP-1 macrophage differentiation induced by IL-4 plus IL-13 [71].
The resveratrol analogue, HS-1793 (4-(6-hydroxy-2-naphthyl)-1,3-benzenediol), was also shown to elevate the level of IFN-γ production conducting reprograming of TAMs M2 phenotype [72].
Curcumin ((1E,6E)-1,7-Bis(4-hydroxy-3-methoxyphenyl)hepta-1,6-diene-3,5-dione), a natural phenol and the main active ingredient in turmeric, acts in several ways as a suppressor of macrophage functions. Even though curcumin has previously received considerable attention from researchers as an anti-inflammatory agent, it has a promising future in the area of immunomodulation [73]. Most of the studies on curcumin focused on the anti-inflammatory effect, promoting the conversion of macrophages from M1 to an anti-inflammatory and protective M2 phenotype [73]. Gao et al. [74] demonstrated that curcumin plays a key role in M2 polarization in two ways: (1) via the inhibition of DNA methyltransferase3b (DNMT3b), overexpression of which can promote increased M1 polarization, and (2) via increased phosphorylation of signal transducer and activator of transcription STAT-6, an important transcription factor activated by IL-4 and IL-10. Other studies showed that curcumin also induces TAMs re-polarization from tumor-promoting M2 phenotype toward the more antitumor M1 phenotype in tumor-bearing hosts, mediated by inhibition of STAT3 activity [75]. Curcumin administration and delivery to glioblastoma brain tumors (GBM) caused a dramatic re-polarization of TAMs from an M2 to M1 phenotype and tumor remission in 50–60% of GBM-bearing mice [76]. Hydrazinocurcumin, a synthetic analog of curcumin encapsulated within nanoparticles, reeducates TAMs to an M1-like phenotype IL-10 low IL-12 high TGF-β low [54].
It was showed that TriCurin, a synergistic formulation of curcumin, resveratrol, and epicatechin gallate (molar ratio C:E:R: 4:1:12.5) can shift TAM polarity in HPV-positive HNSCC by silencing the M2 TAM and activating/recruiting a discrete population of M1 TAM while maintaining a constant number of overall intra-tumor Iba1+ TAM, along with expression of activated STAT3 and induction of activated STAT1 and NF-kB (p65) [77]. Moreover, a liposomal formulation of TriCurin with increased bioavailability (TrLp) was able to cause repolarization of M2-like tumor (GBM)-associated microglia/macrophages to the tumoricidal M1-like phenotype and intra-GBM recruitment of activated natural killer cells [78].
In a urethane-induced lung carcinogenic model, lung carcinogenesis was ameliorated with increased M1 macrophages and decreased M2 macrophages in the lung interstitial by administration of 6-gingerol ((S)-5-hydroxy-1-(4-hydroxy-3-methoxyphenyl)-3-decanone), the main bioactive component in ginger (Zingiber officinale Roscoe). M2 macrophage-resetting efficacy of 6-gingerol was confirmed in a Lewis lung cancer allograft model and the mechanism proposed was the reduction of Arg-1 and ROS levels and elevation of L-arginine and NO levels [79].
Also, it was showed that paeoniflorin, one of the major active constituents of Paeonia lactiflora Pallas, inhibits the alternative activation of macrophages in subcutaneous xenograft tumors of the C57BL/6 J mice at doses of 40 and 20 mg·kg−1 [80].
It was suggested that modulation of TAM polarization was implicated in the antitumor immunostimulatory activity of polysaccharides from Panax japonicus (ginseng). The transcription and production of TGF-β and IL-10, two well-known immunosuppressive cytokines secreted by TAMs, were reduced in response to Panax polysaccharides and also the number of infiltrated CD168+ M2 TAMs was substantially declined although the number of CD68+ total macrophages in transplanted tumor tissues remained almost unchanged [81]. A significant inhibition of Arg-1 expression (above 90% at 100 μg/mL), one of the phenotype markers of M2 macrophages, was also observed for the ethanol extract of Ginseng Radix et Rhizoma [62]. Recently, Chen et al. [82], showed that water extract of Ginseng and Astragalus could be a novel option for integrative cancer therapies due mainly to their ability to regulate macrophage polarization.
In a murine model of sarcoma, immunotherapy with IAPS-2 (acidic polysaccharide, namely IAPS-2, from the root of Ilex asprella) demonstrated that it could significantly inhibit the growth of tumors via modulating the function of TAMs and increase the animal survival rate [83]. Similar results were obtained with an aqueous extract of Trametes robiniophila Murr (Huaier), a sandy beige mushroom found on the truck of trees and has been widely used in TCM for approximately 1600 years for its antitumor, antiangiogenic and immunomodulatory effects. Huaier not only modulates the macrophage polarization but also could inhibit the macrophage-induced angiogenesis by decreasing the expression of VEGF, MMP2 and MMP9, thus inhibiting the formation of new blood vessels in tumor [84].
Esculetin (6,7-dihydroxycoumarin) and fraxetin (6-methoxy-7,8-dihydroxycoumarin) (50, 75 and 100 μM) inhibited the production of IL-10, MCP-1 and TGF-β-1 in macrophages and the phosphorylation of STAT 3 without affecting its expression during the differentiation of M2 macrophages. Esculetin also suppressed the increased production of these cytokines during M2 macrophage differentiation at 10–100 μM. On the other hand, daphentin (7,8-dihydroxycoumarin) had no such effects, revealing that coumarins with two hydroxyl groups at the 6 and 7 positions (esculetin) or coumarins with a methoxy group at the 6 and two hydroxyl groups at the 7 and 8 positions (fraxetin) are more active, exhibiting antitumor and antimetastatic actions in osteosarcoma LM8 cells [85]. The antitumor and antimetastatic actions of esculetin may be due to the dual actions at tumor and TAM sites: inhibition of the expression of cyclin D 1 and CDK4 in osteosarcoma LM8 cells, and also decreasing the STAT 3 phosphorylation in macrophages. In the case of fraxetin, the effects are partly attributed to the inhibition of M2 macrophage differentiation [85].
A classical formula of traditional Chinese medicine (TCM) to alleviate lung cancer–related symptoms is Bu-Fei decoction (BFD), consisting of six herbal Chinese medicines‑Codonopsis pilosula, Schisandra chinensis, Rehmannia glutinosa, Astragalus sp., Aster sp. and Morus sp.‑but it has not been established whether it induces an antitumor effect or it modulates the tumor microenvironment. The result of an in vivo study revealed that BFD successfully interrupted the interaction between tumor cells and TAMs by inhibiting the expression of two important markers: IL-10 (correlated with late stage (stage II, III and IV), lymph node metastases, pleural invasion, lymphovascular invasion and poor differentiation in NSCLC patients) and PD-L1 (correlated with poor prognosis in a number of human cancers, including breast cancer, kidney cancer and NSCLCs) [86].
It has been shown that emodin (6-methyl-1,3,8-trihydroxyanthraquinone), the active ingredient of several Chinese herbs including Rhubarb (Rheum palmatum), inhibits the growth of a variety of tumors and enhances the responsiveness of tumors to chemotherapy agents. In breast cancer, emodin directly inhibited macrophage infiltration and M2 polarization in the tumors, independent of tumor size [87]. Previously, Jia et al. [88], showed that emodin is not cytotoxic to breast cancer cells at concentration achieved in vivo (up to 30 μM) and it failed to affect macrophage infiltration in primary tumors. In contrast to its lack of effects on primary tumors, emodin dramatically suppressed lung metastasis by diminishing phosphorylation of STAT6 and C/EBPβ signaling upon IL-4 stimulation [88]. Further, it was showed that emodin suppresses the activation of multiple signaling pathways, including NF-kB, IRF5, MAPK, STAT1 or STAT6, and IRF4, depending on the environmental settings. It acts mostly on M2 polarization, suggesting that emodin could be most beneficial for patients with M2 macrophage-driven diseases [89].
In oral squamous cell carcinoma (OSCC) animal models, highly pure super critical CO2 leaf extract of Azadirachta indica (Neem) induces an M1 phenotype in TAMs in vivo, and the primary active component, nimbolide (a limonoid tetranortriterpenoid with an α,β-unsaturated ketone system and a δ-lactone ring) has significant anticancer activity in established OSCC xenografts [90]. β-Elemene, a widely known sesquiterpene, regulated the polarization of macrophages from M2 to M1, inhibiting the proliferation, migration and invasion of lung cancer cells and enhancing its radiosensitivity [91].
Onionin A (ONA), a natural low molecular weight compound containing sulfur isolated from onions, inhibited the EOC cell-induced M2 polarization of HMDMs, and STAT3 activation was significantly inhibited by ONA treatment in all cell lines [92].
Adjunctive treatment with Withaferin A, the most abundant constituent of Withania somnifera (Ashwagandha) root extract, reduced myeloid cell-mediated immune suppression and polarized immunity toward a tumor-rejecting type 1 phenotype, facilitating the development of antitumor immunity [93].
Traditional Chinese medicine provides pharmacologically efficient preparates such as KSG-002, a hydroalcoholic extract of radices Astragalus membranaceus and Angelica gigas at 3: 1 ratio that suppresses breast cancer growth and metastasis through targeting NF-κB–mediated TNF α production in macrophages [94] and SH003, mixed extract from Astragalus membranaceus, Angelica gigas and Trichosanthes kirilowii Maximowicz that suppresses highly metastatic breast cancer growth and metastasis by inhibiting STAT3-IL-6 signaling path [95].
Traditional Chinese medicine Jianpi Yangzheng Decoction (JPYZ) used for improving the quality of life and prolonging the survival of gastric cancer patients was more effective compared with Jianpi Yangzheng Xiaozheng Decoction (JPYZXZ) for inducing the phenotypic change in macrophages from M2 to M1. JPYZXZ inhibits the gastric cancer EMT more effectively than JPYZ, but JPYZ primarily works to regulate the phenotypic change in macrophages from M2 to M1 [96].
CXCL-1 was also found to be a cytokine secreted by tumor-associated macrophage, which recruits myeloid-derived suppressor cells to form pre-metastatic niche and led to liver metastasis from colorectal cancer. The current study demonstrated that after administration of XIAOPI formula (consisting of 10 herbs including Epimedium brevicornum, Cistanche deserticola, Leonurus heterophyllus, Salvia miltiorrhiza, Curcuma aromatica, Rhizoma Curcumae, Ligustrum lucidum, Radix Polygoni Multiflori preparata, Crassostrea gigas and Carapax trionycis), the density of TAMs decreased significantly and the level of CXCL-1 was also inhibited in both mouse plasma and cellular supernatants. When CXCL-1 cytokine was co-administrated with XIAOPI formula, the antimetastatic property of XIAOPI formula was blocked, indicating that CXCL-1 might be the principal gene involved in the network regulating the action of XIAOPI formula [97].
Macrophages, as key players in the tumor microenvironment, play essential roles in maintenance and progression of malignant state. Due to their plasticity, these cells balance between pro- and antitumoral effects in close correlation to specific factors. Recent immunotherapeutic strategies focus on tumor-associated macrophages in two main directions: to inhibit protumor macrophages and their suppressive effects (CCL2 inhibitors, trabectedin, zoledronic acid, JAK/STAT inhibitors, etc.) and to activate TAMs to an antitumor phenotype (TLR and CD40 agonists, PI3kδ inhibitor, VEGF and Ang2 inhibitors, etc.).
Several natural compounds/herbal extracts were studied as therapeutic/supportive agents for macrophage modulation in different types of cancers, most of them being able to change M2 polarization (protumoral) to M1 polarization (antitumoral). They belong to various classes of herbal compounds: saponins (corosolic and oleanolic acids, astragaloside, ginsenosides, celastrol, etc.), alkaloids (9-hydroxycanthin-6-one, phlenumdines E, A, hupermine A and 12-epi-lycopodine-N-oxide, sophoridine, etc.), flavonoids and polyphenolcarboxylic acids (isoliquiritigenin, xanthoangelol and 4-hydroxyderricin, baicalein, naringin, genistein, deoxyschizandrin, chlorogenic acid, curcumin, 6-gingerol and paeoniflorin), polysaccharides (isolated from various vegetal sources), coumarins (esculetin, fraxetin, etc.), and anthraquinones (emodin). This action is most probably achieved by downregulation of the STAT3, STAT 6 and NF-kB pathways with consecutive modulation of the secretory profile of TAM cytokines.
TCM supports the dual approach of cancer therapy, to destroy cancer cells on one hand and to improve patients’ immunological status on the other hand. For several preparations such as Jianpi Yangzheng Decoction, Bu-Fei decoction and XIAOPI formula, research studies proved the correlation between cancer cells and tumor microenvironment and the effective intervention of these herbal products in delaying/breaking the tumorigenic process.
Low solubility of some herbal compounds limits their clinical application and it conducted to designing of new analogs with improved bioavailability‑ginseng-derived nanoparticles, peracetate-protected EGCG, chrysin and resveratrol analogs.
By now, many herbal compounds have been shown to exhibit antitumor effects in various cancer types. Further, more researches need to be focused on the influence of these valuable compounds/preparations on modulation of the tumor microenvironment, as key element in the relation of tumor-host.
This research was financially supported by the Ministry of Research and Innovation in the frame of the project PN.16.41.01.01/2018, CORE Program.
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\n\nPolicy last updated: 2018-09-11
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