The 2013 ISHLT working formulation for pathologic diagnosis of cardiac antibody-mediated rejection.
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More than half of the publishers listed alongside IntechOpen (18 out of 30) are Social Science and Humanities publishers. IntechOpen is an exception to this as a leader in not only Open Access content but Open Access content across all scientific disciplines, including Physical Sciences, Engineering and Technology, Health Sciences, Life Science, and Social Sciences and Humanities.
\\n\\nOur breakdown of titles published demonstrates this with 47% PET, 31% HS, 18% LS, and 4% SSH books published.
\\n\\n“Even though ItechOpen has shown the potential of sci-tech books using an OA approach,” other publishers “have shown little interest in OA books.”
\\n\\nAdditionally, each book published by IntechOpen contains original content and research findings.
\\n\\nWe are honored to be among such prestigious publishers and we hope to continue to spearhead that growth in our quest to promote Open Access as a true pioneer in OA book publishing.
\\n\\n\\n\\n
\\n"}]',published:!0,mainMedia:null},components:[{type:"htmlEditorComponent",content:'
Simba Information has released its Open Access Book Publishing 2020 - 2024 report and has again identified IntechOpen as the world’s largest Open Access book publisher by title count.
\n\nSimba Information is a leading provider for market intelligence and forecasts in the media and publishing industry. The report, published every year, provides an overview and financial outlook for the global professional e-book publishing market.
\n\nIntechOpen, De Gruyter, and Frontiers are the largest OA book publishers by title count, with IntechOpen coming in at first place with 5,101 OA books published, a good 1,782 titles ahead of the nearest competitor.
\n\nSince the first Open Access Book Publishing report published in 2016, IntechOpen has held the top stop each year.
\n\n\n\nMore than half of the publishers listed alongside IntechOpen (18 out of 30) are Social Science and Humanities publishers. IntechOpen is an exception to this as a leader in not only Open Access content but Open Access content across all scientific disciplines, including Physical Sciences, Engineering and Technology, Health Sciences, Life Science, and Social Sciences and Humanities.
\n\nOur breakdown of titles published demonstrates this with 47% PET, 31% HS, 18% LS, and 4% SSH books published.
\n\n“Even though ItechOpen has shown the potential of sci-tech books using an OA approach,” other publishers “have shown little interest in OA books.”
\n\nAdditionally, each book published by IntechOpen contains original content and research findings.
\n\nWe are honored to be among such prestigious publishers and we hope to continue to spearhead that growth in our quest to promote Open Access as a true pioneer in OA book publishing.
\n\n\n\n
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\r\n\tThe advent of next-generation sequencing along with the development of bioinformatics tools has opened avenues to explore this technology in numerous fields of biomedical research. This book evaluates and comprehensively summarizes the scientific findings which have been achieved through RNA-Seq technology. RNA-Seq allows us to accurately capture all subtypes of RNA molecules, in any sequenced organism or single-cell type, under different experimental conditions. RNA-Seq transcriptome profiling of healthy and diseased tissues allows understanding the alterations in cellular phenotypes through the expression of differentially spliced RNA isoforms. Assessment of gene expression by RNA-Seq provides new insight into host response to pathogens, drugs, allergens, and other environmental triggers.
\r\n\r\n\tRNA-sequencing becomes even more powerful when combined with other assays. Merging genomics and transcriptomic profiling provides novel information underlying causative DNA mutations and the cellular effects of genetic variants caused by SNPs, indels, etc. Combining RNA-Seq with immunoprecipitation and cross-linking techniques is a clever multi-Omics strategy assessing transcriptional, posttranscriptional and posttranslational levels of gene expression regulation. The optimization of RNA-Seq technology will allow countless opportunities in our pursuit of achieving the goals of individualized medicine.
",isbn:"978-1-83962-815-3",printIsbn:"978-1-83962-686-9",pdfIsbn:"978-1-83962-816-0",doi:null,price:0,priceEur:0,priceUsd:0,slug:null,numberOfPages:0,isOpenForSubmission:!1,hash:"62399ea4ed0544b946dcbd1853b2d1b8",bookSignature:"Prof. Irina Vlasova-St. Louis",publishedDate:null,coverURL:"https://cdn.intechopen.com/books/images_new/10369.jpg",keywords:"RNA-Seq, Genomics, Transcriptomics, Gene Expression, Transcriptome Profiling, Genetic Variation, Single-Cell Genomics, Single-Cell Genome, Data Mining, Bioinformatics, Transcriptomic Biomarkers, Inherited and Somatic Diseases",numberOfDownloads:null,numberOfWosCitations:0,numberOfCrossrefCitations:null,numberOfDimensionsCitations:null,numberOfTotalCitations:null,isAvailableForWebshopOrdering:!0,dateEndFirstStepPublish:"September 25th 2020",dateEndSecondStepPublish:"October 23rd 2020",dateEndThirdStepPublish:"December 22nd 2020",dateEndFourthStepPublish:"March 12th 2021",dateEndFifthStepPublish:"May 11th 2021",remainingDaysToSecondStep:"3 months",secondStepPassed:!0,currentStepOfPublishingProcess:4,editedByType:null,kuFlag:!1,biosketch:"Dr. St. Louis conducts discovery research in several key areas including infectious diseases, immunology, and oncology. By integrating specific areas of expertise - genomics, transcriptomics, proteomics, ribonomics, and bioinformatics - Irina’s group is studying normal and pathological conditions at the molecular, cellular, and organismal levels.",coeditorOneBiosketch:null,coeditorTwoBiosketch:null,coeditorThreeBiosketch:null,coeditorFourBiosketch:null,coeditorFiveBiosketch:null,editors:[{id:"211159",title:"Prof.",name:"Irina",middleName:null,surname:"Vlasova-St. Louis",slug:"irina-vlasova-st.-louis",fullName:"Irina Vlasova-St. Louis",profilePictureURL:"https://mts.intechopen.com/storage/users/211159/images/system/211159.png",biography:"Irina St. Louis earned her M.D. and Ph.D. degrees from Ural State Medical Academy, Yekaterinburg, Russia. She completed her residency in lab pathology at Russian Medical Academy for Postgraduate Education, Moscow. She joined the Department of Microbiology at the University of Minnesota, as a postdoctoral trainee, followed by fellowships at the University of Minnesota Supercomputing Institute and Lymphoma Research Foundation.\r\nPresently, Dr. St. Louis is appointed as an Assistant Professor at the Department of Medicine at the University of Minnesota. \r\nDr. St. Louis conducts discovery research in several key areas including infectious diseases, immunology, and oncology. By integrating specific areas of expertise - genomics, transcriptomics, proteomics, ribonomics, and bioinformatics - Irina’s group is studying normal and pathological conditions at the molecular, cellular, and organismal levels.\r\nThe basic research in Dr. St. Louis’ laboratory is centered on post-transcriptional gene expression regulation, specifically, through messenger RNA turnover. Her translational research focuses on immune restoration disorders (IRD). Dr. St. Louis is engaged in a number of clinical studies, within the Global Health & International Medicine Program. These studies involve the stratification of AIDS patients, for optimal treatment regimens. The studies also include searches for biomarkers of immune reconstitution inflammatory syndrome (IRIS). Additionally, Dr. St. Louis’ lab collaborates with the Division of Hematology-Oncology and Transplantation, on virus-specific immune reconstitution after various hematopoietic cell transplantation regimens. This collaborative research aims to define the parameters and conditions for favorable post-transplant immune restoration and functional recovery in adult patients.",institutionString:"University of Minnesota",position:null,outsideEditionCount:0,totalCites:0,totalAuthoredChapters:"1",totalChapterViews:"0",totalEditedBooks:"0",institution:{name:"University of Minnesota",institutionURL:null,country:{name:"United States of America"}}}],coeditorOne:null,coeditorTwo:null,coeditorThree:null,coeditorFour:null,coeditorFive:null,topics:[{id:"6",title:"Biochemistry, Genetics and Molecular Biology",slug:"biochemistry-genetics-and-molecular-biology"}],chapters:null,productType:{id:"1",title:"Edited Volume",chapterContentType:"chapter",authoredCaption:"Edited by"},personalPublishingAssistant:{id:"259492",firstName:"Sara",lastName:"Gojević-Zrnić",middleName:null,title:"Mrs.",imageUrl:"https://mts.intechopen.com/storage/users/259492/images/7469_n.png",email:"sara.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. Whether that be identifying an exceptional author and proposing an editorship collaboration, or contacting researchers who would like the opportunity to work with IntechOpen, I establish and help manage author and editor acquisition and contact."}},relatedBooks:[{type:"book",id:"6694",title:"New Trends in Ion Exchange Studies",subtitle:null,isOpenForSubmission:!1,hash:"3de8c8b090fd8faa7c11ec5b387c486a",slug:"new-trends-in-ion-exchange-studies",bookSignature:"Selcan Karakuş",coverURL:"https://cdn.intechopen.com/books/images_new/6694.jpg",editedByType:"Edited by",editors:[{id:"206110",title:"Dr.",name:"Selcan",surname:"Karakuş",slug:"selcan-karakus",fullName:"Selcan Karakuş"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"1591",title:"Infrared Spectroscopy",subtitle:"Materials Science, Engineering and Technology",isOpenForSubmission:!1,hash:"99b4b7b71a8caeb693ed762b40b017f4",slug:"infrared-spectroscopy-materials-science-engineering-and-technology",bookSignature:"Theophile Theophanides",coverURL:"https://cdn.intechopen.com/books/images_new/1591.jpg",editedByType:"Edited by",editors:[{id:"37194",title:"Dr.",name:"Theophanides",surname:"Theophile",slug:"theophanides-theophile",fullName:"Theophanides Theophile"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"3092",title:"Anopheles mosquitoes",subtitle:"New insights into malaria vectors",isOpenForSubmission:!1,hash:"c9e622485316d5e296288bf24d2b0d64",slug:"anopheles-mosquitoes-new-insights-into-malaria-vectors",bookSignature:"Sylvie Manguin",coverURL:"https://cdn.intechopen.com/books/images_new/3092.jpg",editedByType:"Edited by",editors:[{id:"50017",title:"Prof.",name:"Sylvie",surname:"Manguin",slug:"sylvie-manguin",fullName:"Sylvie Manguin"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"3161",title:"Frontiers in Guided Wave Optics and Optoelectronics",subtitle:null,isOpenForSubmission:!1,hash:"deb44e9c99f82bbce1083abea743146c",slug:"frontiers-in-guided-wave-optics-and-optoelectronics",bookSignature:"Bishnu Pal",coverURL:"https://cdn.intechopen.com/books/images_new/3161.jpg",editedByType:"Edited by",editors:[{id:"4782",title:"Prof.",name:"Bishnu",surname:"Pal",slug:"bishnu-pal",fullName:"Bishnu Pal"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"72",title:"Ionic Liquids",subtitle:"Theory, Properties, New Approaches",isOpenForSubmission:!1,hash:"d94ffa3cfa10505e3b1d676d46fcd3f5",slug:"ionic-liquids-theory-properties-new-approaches",bookSignature:"Alexander Kokorin",coverURL:"https://cdn.intechopen.com/books/images_new/72.jpg",editedByType:"Edited by",editors:[{id:"19816",title:"Prof.",name:"Alexander",surname:"Kokorin",slug:"alexander-kokorin",fullName:"Alexander Kokorin"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"1373",title:"Ionic Liquids",subtitle:"Applications and Perspectives",isOpenForSubmission:!1,hash:"5e9ae5ae9167cde4b344e499a792c41c",slug:"ionic-liquids-applications-and-perspectives",bookSignature:"Alexander Kokorin",coverURL:"https://cdn.intechopen.com/books/images_new/1373.jpg",editedByType:"Edited by",editors:[{id:"19816",title:"Prof.",name:"Alexander",surname:"Kokorin",slug:"alexander-kokorin",fullName:"Alexander Kokorin"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"57",title:"Physics and Applications of Graphene",subtitle:"Experiments",isOpenForSubmission:!1,hash:"0e6622a71cf4f02f45bfdd5691e1189a",slug:"physics-and-applications-of-graphene-experiments",bookSignature:"Sergey Mikhailov",coverURL:"https://cdn.intechopen.com/books/images_new/57.jpg",editedByType:"Edited by",editors:[{id:"16042",title:"Dr.",name:"Sergey",surname:"Mikhailov",slug:"sergey-mikhailov",fullName:"Sergey Mikhailov"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"371",title:"Abiotic Stress in Plants",subtitle:"Mechanisms and Adaptations",isOpenForSubmission:!1,hash:"588466f487e307619849d72389178a74",slug:"abiotic-stress-in-plants-mechanisms-and-adaptations",bookSignature:"Arun Shanker and B. 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:"60658",title:"Humoral Rejection in Cardiac Transplantation: Management of Antibody-Mediated Rejection",doi:"10.5772/intechopen.76143",slug:"humoral-rejection-in-cardiac-transplantation-management-of-antibody-mediated-rejection",body:'Orthotopic heart transplantation (OHT) is still the gold standard of treatment among end-stage heart failure. Worldwide, about 3500 heart transplantations are performed annually [1]. However, shortage of donors and allograft dysfunction are the most common problems cardiac surgeons have to cope with. Rejection is the most common reason for allograft dysfunction and is responsible for 25% of postoperative deaths [2]. Episodes of rejection may emerge at any time after transplantation as acute or chronic cellular rejection (CR), humoral rejection (=antibody-mediated = vascular rejection (AMR)), or mixed rejection. Despite AMR that is known to be rare, it is potentially lethal due to the capillary vasculopathy caused by neutrophil and macrophage infiltration in endothelial cells [3, 4]. Today, treatment of rejection episodes is directed mostly to cellular response. Each center sets the treatment in the light of their experience. In this chapter, we will discuss the effector mechanisms that are used by antibodies to eliminate antigens and clinical experience about AMR and its treatment with discussing the latest articles.
Antibodies are accumulated by the immune system to identify and neutralize foreign objects. They were the first specific product of the adaptive immune response to be identified and are found in the plasma, in the blood, and in extracellular fluids. Immunity mediated by antibodies is known as humoral immunity because of body fluids that were once known as humors [4]. The humoral immune response begins with the recognition of antigens by native B cells. These cells then undergo a process of clonal expansion and differentiation. In this way, the B cell matures into antibody-secreting plasma cells, which secrete antibodies. The activation of B cells and their differentiation into antibody-secreting plasma cells is triggered by antigen and usually requires helper T cells. The term “helper T cell” is often used to mean a cell from the TH2 class of CD4 T cells, but a subset of TH1 cells can also help in B-cell activation [5]. B cells can receive help from helper T cells when antigen bound by surface immunoglobulin is internalized and returned to the cell surface as peptides bound to major histocompatibility complex (MHC) class II molecules. MHC then delivers activating signals to the B cell. Thus, protein antigens binding to B cells both provide a specific signal to the B cell by cross-linking its antigen receptors and allow the B cell to attract antigen-specific T-cell help. These antigens are unable to induce antibody responses in animals or humans who lack T cells, and they are therefore known as thymus-dependent antigens [5]. The first signal required for B-cell activation is delivered through its antigen receptor. For thymus-dependent antigens, the second signal is delivered by a helper T cell that recognizes degraded fragments of the antigen as peptides bound to MHC class II molecules on the B-cell surface; the interaction between CD40 ligand on the T cell and CD40 on the B cell contributes an essential part of this second signal [5]. For thymus-independent antigens, the second signal can be delivered by the antigen itself or by non-thymus-derived accessory cells. The B-cell co-receptor complex of CD19:CD21:CD81 can greatly enhance B-cell responsiveness to antigen. CD21 (=complement receptor 2) is a receptor for the complement fragment C3d. Whether binding of CD21 enhances B-cell responsiveness by increasing B-cell signaling, by inducing co-stimulatory molecules on the B cell, or by increasing the receptor-mediated uptake of antigen is not yet known [5]. Antibodies are the effector products of humoral immunity. Finally, as this response declines, a pool of memory cells remains behind. If the body is reexposed to the antigen, these memory cells will recognize the antigen and respond much more quickly and effectively [6]. There are two purposes of antibodies. The first purpose is to neutralize the target threat, and the second purpose is to recruit other cells or proteins to an antigen so that those cells or proteins can eliminate the antigen [6]. AMR develops when recipient antibody is directed against donor human leukocyte antigens (HLA) on the endothelial layer of the allograft. Antibodies induce fixation and activation of the complement cascade, resulting in tissue injury. Complement and immunoglobulin are deposited within the allograft microvasculature, which results in an inflammatory process that is characterized by endothelial cell activation, upregulation of cytokines, infiltration of macrophages, increased vascular permeability, and microvascular thrombosis. This process ultimately manifests as allograft dysfunction [6].
AMR is mediated by donor-specific antibodies and is histologically defined by linear deposits of immunoglobulin (Ig) and complement in the myocardial capillaries [7]. Herskowitz et al. [8] described AMR for the first time in 1987 as an arteriolar vasculitis with poor outcome. Hammond et al. [9] firstly demonstrated that vascular rejection is associated with deposits of antibodies and complement activation. AMR incidence is reported between 8 and 15% [10, 11, 12], and it has been reported concurrent with CR in up to 24% of cases. Approximately 50% of heart transplant recipients who develop rejection >7 years after transplantation have evidence of AMR [12]. AMR was described as an acute phenomenon seen in weeks to months just after OHT. However, in recent years, studies have been reported that it also occurs in the longer term [9, 13, 14]. Rejection can be hyperacute (occurring within minutes after the vascular anastomosis (0–7 days)) in patients who are sensitized to donor HLA antigens and acute (occurring days to weeks after transplantation) because of the development of de novo donor-specific antibody (DSA) and preexisting DSA. Early AMR tends to be associated with a higher prevalence of allograft dysfunction and hemodynamic compromise. Late (occurring 3 months after transplantation) or chronic rejection most likely because of heightened recognition (occurring months to years after transplantation) [15]. Risk factors include young age, female gender, high levels of pretransplant panel-reactive antibodies (PRAs), positive donor-specific crossmatch, cytomegalovirus infection, prior OKT3 use, and artificial heart devices [10, 13]. Olsen et al. [16] stated that 23% of patients had AMR episodes for the second time resulting in graft loss in two-thirds due to the continuous complement activation and production of donor-reactive antibodies that cause graft dysfunction by sensitized memory B cells. As the definition of AMR has evolved and more sensitive diagnostic modalities have become available, there is increasing evidence that AMR is a spectrum of immunologic injury that ranges from subclinical, histological, immunologic, and/or serological findings without graft dysfunction (i.e., subclinical AMR) to overt AMR with hemodynamic compromise.
The first description of humoral rejection was included in the 1990 International Society of Heart and Lung Transplantation (ISHLT) criteria defined as positive immunofluorescence, vasculitis, or severe edema in the absence of cellular infiltrate [14, 17]. The classification AMR 0 was assigned in the absence of histological or immunopathologic features. Confirmation of AMR or AMR 1 was defined as histological evidence with identification of antibodies (CD68, CD31, C4d) and serum presence of DSA [14]. ISHLT Immunopathology Task Force provided an expanded description of the histological evidence of acute capillary injury, the minimum requirement for immunopathologic evidence of antibody-mediated injury, and an improved definition of serological evidence of circulating antibodies in 2006 [18]. The persistent variations in the diagnosis and treatment of AMR were addressed in the Heart Session of the Tenth Banff Conference on Allograft Pathology (2009) and the ISHLT Consensus Conference on AMR (2010) conferences. The most important issues included the need for a clinical definition of AMR, the significance of asymptomatic patient without cardiac dysfunction biopsy-proven AMR, and the recognition that AMR may be caused by DSA as well as antibodies to non-HLA antigens. Although AMR would be a pathological diagnosis, it was strongly recommended that at the time of suspected AMR, blood can be drawn at biopsy and tested for the presence of donor-specific anti-HLA class I and class II antibodies [14]. On the basis of the initial Banff criteria, a definitive diagnosis of AMR required morphologic evidence (primarily microvascular inflammation), immunohistological (C4d staining), and serologic criteria (presence of circulating DSA). These criteria were modified to address the current evidence of the existence of C4d-negative AMR and lesions of intimal arteritis secondary to the action of the antibodies at the Banff Consensus in 2013 [19]. The myocardial capillaries, arterioles, and venules are readily sampled at biopsy. The vascular endothelium is the point of the first contact for anti-donor antibody in the allograft and the primary locus of activity in AMR. The appearance of vasculitis or leukocytes infiltrating through the endothelium into the vessel wall demonstrates active humoral immunity with antibody-dependent cytotoxicity, cytokine, and circulating monocyte recruitment [20, 21]. Mechanisms of immune complex-mediated neutrophil recruitment and tissue injury. Antibodies induce fixation and activation of the complement cascade, resulting in tissue injury. Complement activation, a key contributor to the pathogenesis of AMR, results in activation of the innate and adaptive immune responses. Complement and immunoglobulin are deposited within the allograft microvasculature, which results in an inflammatory process that is characterized by endothelial cell activation, upregulation of cytokines, infiltration of macrophages, increased vascular permeability, and microvascular thrombosis. Interstitial edema and hemorrhage are also seen. Capillary changes indicative of AMR include endothelial cell swelling and intravascular macrophage accumulation coincident with pericapillary neutrophils. The role of immunoglobulins, complement activation, and coagulation cascade in AMR is under constant study as diagnostic methods increase in sensitivity and specificity [14, 22]. It has been suggested that AMR is a clinical pathological continuum that begins with a latent humoral response of circulating antibodies and then progresses through a silent phase of circulating antibodies with C4d deposition without clinical or histological alterations, to a subclinical stage, to symptomatic AMR [14]. Mauiyyedi et al. described the correlation between DSAs and diffuse C4d deposition (>50%) as diagnostic markers for AMR [23]. C4d deposition may be earlier than 3 months, as may be after 160 months [7, 10, 24]. The complement components C3 and C1q have been demonstrated in kidney AMR; however, their detection is limited by a short half-life in vivo and consequently a short window of detection during a rejection episode [25]. The protein C4d is a complement split product that binds covalently to the endothelium at the site of complement activation and persists longer than C3 or C1q [14]. C4d and C3d detection predicts graft dysfunction and mortality better than C4d alone [14, 26]. Haas et al. reported that biopsies positive for C4d (C4d+) and C3d (C3d+) are strongly associated with DSA and allograft dysfunction, while cases with episodes that are only positive for C4d are mostly subclinical [19]. Berry et al. published working formulation by pathologists to diagnose “pathological AMR (pAMR)” without the requirement of clinical dysfunction or positive DSA (Table 1) [27, 28]. CD59 and CD55 (decay-accelerating factors) are used in conjunction with C4d and C3d to indicate aborted complement activation. Lengthy incubation times and a granular staining pattern render these assays impractical for clinical use [26]. The macrophage antigen CD68 allows identification of subtle accumulations of macrophages within vessels, which helps to differentiate intravascular/perivascular macrophages from lymphocytes, thereby excluding ACR. Because interstitial macrophages are commonly found in allograft myocardium in a variety of settings, including AMR, ACR, and ischemic injury, investigators agree that only macrophages within capillaries and small venules are to be considered [29]. The term “intravascular macrophage” was replaced by “activated mononuclear cells” because it was clear that without immunostaining with CD68, intravascular T lymphocytes and activated endothelial cells could be misinterpreted as macrophages at the 2012 ISHLT workshop [28]. Endothelial cell markers CD34 and CD31 can be used to ascertain the intravascular location of macrophages/mononuclear cells [30]. Immunopathologic features of AMR were summarized in Table 2. Using criteria that included prominent endothelial cell swelling and/or vasculitis and the vascular deposition of immunoglobulin and complement, it was first defined by Hammond and co-workers [9]. The clinic spectrum of AMR ranges from latent AMR to silent AMR, to subclinical AMR, and to clinical AMR. Pathologic evidence of AMR appears in silent AMR as C4d deposition in capillaries of an otherwise normal myocardium and progresses to subclinical AMR showing myocardial alterations in the setting of C4d deposition but the absence of organ dysfunction. The onset of allograft dysfunction is the hallmark of clinical AMR [28, 31].
Category | Description |
---|---|
pAMR 0: negative for pathological AMR | Both histological and immunopathologic studies are negative |
pAMR 1 (H+): histopathologic AMR alone | Histological findings positive and immunopathologic findings negative |
pAMR1 (I+): immunopathologic AMR alone | Histological findings negative and immunopathologic findings positive |
pAMR 2: pathological AMR | Both histological and immunopathologic findings are present |
pAMR 3: severe pathological AMR | Severe AMR with histopathologic findings of interstitial hemorrhage, capillary fragmentation, mixed inflammatory infiltrates, endothelial cell pyknosis and/or karyorrhexis, and marked edema |
The 2013 ISHLT working formulation for pathologic diagnosis of cardiac antibody-mediated rejection.
AMR, antibody-mediated rejection; pAMR, pathological AMR (Source: [28]).
Interpretation | AMR limitations | |
---|---|---|
IgG/IgM | Immunoglobulin binding | + Easily dissociated, short half-life, interobserver variability |
C3, C1q | Complement activation | + Short half-life |
C3d/C4d | Complement activation | + Combination more predictive of AMR than C4d alone, long half-life |
HLA-DR | Endothelial integrity | + Staining always present, but “frayed” pattern indicates capillary injury |
Fibrin | Thrombotic environment | + Interstitial extravasation suggests more severe AMR episode |
CD55, CD59 | Complement inhibitor | − Long incubation and granular staining pattern, difficult to be interpreted |
CD31, CD34, CD68 | Intravascular macrophages | + CD68 confirms macrophage lineage of mononuclear cells, CD31 and CD34 are endothelial markers which differentiate macrophages from endothelial cells and delineate intravascular localization |
Immunopathologic features of antibody-mediated rejection.
AMR, antibody-mediated rejection; HLA, human leukocyte antigens (Source: [14]).
Kfoury et al. recommended that immunostaining for C4d be avoided in the first 2 weeks after transplant because a number of perioperative issues can confound staining and interpretation [32]. Center-specific approaches to the issue of surveillance vary widely, ranging from none to every biopsy. The other question is follow-up of positive immunostaining after therapy of AMR. The ISHLT pathology group recommended that subsequent biopsies should be studied by immunostaining until a negative result is achieved in 2011. However, investigators reported that capillary staining of C3d cleared within 2 weeks to 1 month, while capillary staining of C4d cleared within 1–2 months [26].
Investigators have since reported on its incidence, histopathological features, clinical outcome, and treatment. However, clinical series are few and sparse, and the incidence of HR and the method of choice for its management remain uncertain and may differ among different centers [33]. All transplantation centers often prefer pulse steroid as an initial therapy in combination with plasmapheresis. Otherwise, intravenous cyclophosphamide (0.5 to 1 gm/m2, every 3 weeks for 4–6 months) may be added to treatment regimen according to the clinical experience and preferences. In case of recurrent AMR exacerbations, cyclophosphamide and IVIg (250 mg/kg/day, 4 days, 4–6 months repeated every 3 weeks) followed by plasmapheresis (5–6 sessions, 10–14 days) have been suggested. After 2002, rituximab (375 mg/m2, once a week, four dose infusions) after plasmapheresis is added to treatment regimen [34].
Plasmapheresis is the cornerstone in the treatment of AMR. Exchange method and double-filtration technique are among the most used plasmapheresis methods. Both techniques are nonselective and eliminate immunoglobulins nonspecifically. Immunoadsorption plasmapheresis method using adsorbent membrane is more specific to the removal of antibodies; however, it is expensive. Each type of plasmapheresis involves risks such as hypovolemia and infection [4, 35, 36].
Plasmapheresis has been always reported in combination with other immunosuppressive agents; there is always a possibility of AMR recurrence as a monotherapy. In this context, other therapies are to be combined in order to prevent recurrence.
Another issue which is also controversial regarding plasmapheresis is about the number of sessions of plasmapheresis to be made and at what intervals. General practice is three to five sessions every other day. However, Crespo-Leiro et al. [33] reported that they use plasmapheresis every day until the recovery of the clinical status. The author who reported this period may extend to the nineteenth day. We perform plasmapheresis every other day for three sessions, and if there is no clinical improvement, we extend it up to five sessions in our general practice. Cytolytic therapy would be useful especially for those who need inotropics or mechanical circulatory support [13, 16]. Cytolytic therapy may indirectly suppress B lymphocyte activation, whereas antithymocyte globulin may directly suppress B-cell function [37, 38].
CD20 protein is a molecule present on the surface of B lymphocytes. Rituximab is a chimeric monoclonal antibody raised against the CD20 protein. Combination of rituximab with plasmapheresis, IVIg, or steroids was found to increase the success of treatment [39, 40]. Complement blockade would be an important strategy for prevention and treatment of AMR. Agents targeting C5 and C1 esterase have been evaluated in clinical trials. Eculizumab binds to complement protein C5 and inhibits complement. It prevents the breakdown of C5 and formation of MAC. Since eculizumab cannot decrease the levels of donor-specific antigen, antibody-lowering therapy should be added. Although early studies on the effects of eculizumab are promising, the use of eculizumab is limited due to the cost and lack of coverage by most insurers [41, 42]. Plasma-derived human C1-inhibitor (20UI/kg/twice weekly), an inhibitor which targets the classical complement pathway, was successfully administered for caAMR prevention in highly sensitized patients [43, 44]. Two C1-INH products that are approved for use by the FDA in the treatment of hereditary angioedema have been evaluated in small pilot studies for AMR: Berinert® (CSL Behring, Kankakee, IL, USA) and Cinryze® (Shire ViroPharma Inc., Lexington, MA, USA) [45, 46, 47]. A potential limitation of available therapies for AMR is the lack of direct effect on the major alloantibody-producing plasma cell. In recent years, studies regarding bortezomib, a reversible 26S proteasome inhibitor used in the treatment of multiple myeloma, have been reported [48, 49]. These studies rather relate to the treatment of AMR in kidney transplantation. Woodle et al. reported promising results in this regard [49, 50]. This molecule has been used as a rescue therapy in combination with other immunotherapies for refractory AMR. Everly et al. treated refractory mixed AMR and ACR with kidney transplant recipients. They used a single cycle of bortezomib: 1.3–1.5 mg/m2 × 4 doses over 11 days (days 1, 4, 8, and 11) [51, 52]. Alemtuzumab is a monoclonal antibody that binds to CD52 on the surface of B and T lymphocytes. It depletes mature lymphocytes without myeloablation [53]. Woodside et al. reported reversal of recurrent severe cardiac rejection [54].
A humanized monoclonal antibody against the IL-6R (tocilizumab) has been used in phase I/phase II studies for the treatment of chronic active AMR unresponsive with high-dose IVIg for patients who are difficult to desensitize. Choi et al. reported that AMR patients who had failed high-dose IVIg, rituximab, and plasmapheresis received monthly doses of tocilizumab for 6 to 18 months and they found to have good outcomes [55, 56].
Antithymocyte globulins (ATG) are antibodies directed at T-cell lymphocyte. This class of drugs is used for active treatment of ACR; thus, they are adapted for AMR treatment, but there are few data on their effect. Although there have been patients with AMR treated successfully with ATG in combination with other drugs, ATG requires more analysis as part of a randomized trial [14, 57]. Furthermore, total lymphocyte radiation is used to treat acute rejection but is risky due to its reported effects increasing hematologic malignancies [58]. Our opinion is that pAMR should be considered important due to the long-term survival of patients. If patient has pAMR, we perform plasmapheresis every other day for three sessions.
There are limited studies about treatment of subclinical AMR. Patients with subclinical AMR are not generally treated, because more data regarding the significance of a positive biopsy in the absence of symptoms are needed. Wu et al. reported that 5-year actuarial survival rates for the subclinical AMR (86%), treated AMR (68%), and control groups (79%) were not significantly different; however, patients with subclinical AMR were more likely to develop cardiac allograft vasculopathy than the control group and even tended to do worse than patients with treated symptomatic AMR [59]. The incidence of CAV or death in the patients with AMR was twice that of the control subjects [13].
The authors declare no conflicts of interest and no financial support for the research and/or authorship of this article.
Microalgae are a variety of autotrophic, prokaryotic or eukaryotic organisms, where their single-cell structure allows solar energy to be easily converted into chemical energy. This biochemical conversion is being used commercially to obtain the biomass, consequently, in the insertion in products with commercial application. The most used microalgae cultivation techniques are opens aerated lagoons and closed photobioreactors [1, 2, 3, 4].
Due to the advantages that microalgae offer over many other species, researchers and entrepreneurs have shown great interest in the development of production processes for biofuels, functional foods and bio-products from different species. Compared to terrestrial crops, these microorganisms have photosynthetic efficiency, growth rate and higher biomass production, consequently mass cultivation for commercial microalgae production can be carried out efficiently [5]. In addition, the cultivation of microalgae does not require arable soil, and can be grown in saline, brackish and wastewater and in harsh conditions, not competing with the production of food that is currently a major challenge for the production of first and second biofuels generation [6]. Therefore, competition for arable land with other crops, especially for human consumption, is greatly reduced.
Although most microalgae grow exclusively through photosynthesis, some species are mixotrophic and use extracellular organic carbon when a light source is not available [7]. Microalgae can be a source of several important compounds, including hydrogen and hydrocarbons, pigments and dyes, food and feed, biopolymers, biofertilizers, insecticides, neutraceuticals (foods capable of providing health benefits) and pharmacological compounds, in addition to being a potential biomass for production of biofuels [8].
Although the production of microalgae does not directly compete with food production and can be grown in harsh conditions, economic viability does not yet exist in many of the processes of industrial interest. However, the improvement and mastery of technologies capable of making inserted industrial processes viable become essential. Despite of the microalgae have a wide potential for production and applications, there are many obstacles to the biodiversity of these algae, such as mastery of technologies for production, genetic improvement research of strains more resistant to pathogens and economic viability in large-scale production [9, 10]. According to Georgianna and Mayfield [11], although promising, the success of inserting microalgae in the production of various products depends mainly on two important factors: high productivity and quality of biomass, as well as cost-effective production.
One of the viable solutions to reduce the costs of microalgae biomass production is to explore different forms of energy metabolism, highlighting the photoautotrophic, heterotrophic and mixotrophic for commercial production. Understanding these forms of metabolism allows the application of efficient crop strategies aimed at increasing the production of biomass and bioproducts on a large scale with cost optimization to couple the agroindustry waste treatment [7]. Microalgae are able to eliminate a variety of pollutants in wastewater mainly nitrogenated, phosphates and organic carbons [12].
Mixotrophic cultivation is a preferable microalgae growth mode for biomass production [13]. Compared to photoautotrophic and heterotrophic metabolism, mixotrophic cultures have been demonstrated many advantages, such as less risk of contamination, reduced cost and high biomass productivity. Even susceptible to contaminations, the use of photobioreactors minimizes this risk, but increases the cost of the process, which can be offset by the high biomass yield that can reach 5–15 g/L, being 3–30 times higher than those produced under autotrophic growth conditions [14, 15].
The use of waste for microalgae mixotrophic growth has been researched, mainly with the objective of expanding and diversifying in an alternative way the control and combating the inappropriate disposal of these in the respective industries, combined with the perspective of minimizing the operational costs of producing microalgae in large scale that are still considered high. The waste generated by the agribusiness has a high load of organic matter with high concentrations of Biochemical Oxygen Demand (BOD), Chemical Oxygen Demand (COD), ammonia, phosphates, suspended solids harmful to the environment, in addition to dissolved components such as sugars, fat and proteins originating from food, contributing to environmental pollution [16].
According to Patel et al. [7], research involving the mixotrophic cultivation of microalgae using organic matter as a source of carbon points to the production of high yields of biomass and biocomposites of industrial interest when compared to systems involving photoautotrophic and heterotrophic metabolisms. In this sense, recent studies have been carried out using agroindustrial waste to grow microalgae in a mixotrophic regime in order to minimize the cost of the biomass production process and treat the effluent adding value to the process, suggesting a microalgae biorefinery system [17].
Patel et al. [18] cultivated C. protothecoides UTEX-256 under mixotrophic conditions using dairy waste as source of carbon. The high CO2-emitting dairy industry obligated to treat waste and improve its carbon-footprints. In general, biochemical treatment was effective to remove respectively 99.7 and 91–100% of organic and inorganic pollutants and produce biomass and lipids fractions.
Xio-Bo Tan et al. [19] demonstrated that Chlorella pyrenoidosa (FACHB-9) cultivated under mixotrophic conditions using anaerobic digestate of sludge with an optimal addition of acidified starch wastewater improved biomass and lipids production by 0.5-fold (to 2.59 g·L−1) and 3.2-fold (87.3 mg·L−1 ·d−1), respectively. In addition, 62% of total organic carbon, 99% of ammonium and 95% of orthophosphate in mixed wastewater were effectively removed by microalgae.
Wang et al. [20] utilized glucose recovered from enzymatic hydrolysis of food waste as culture medium in mixotrophic cultivation of Chlorella sp. to obtain high levels of lipid and lutein. The algal biomass was 6.9 g L−1 with 1.8 g L−1 lipid and 63.0 mg L−1 lutein using hydrolysate with an initial glucose concentration of 20 g L − 1. Furthermore, lipid derived from microalgae biomass using food hydrolysate was at high quality in terms of biodiesel properties.
Due to the success of mixotrophic microalgae growth, the use of agro-industrial by-products stands out, adding value to production processes and reducing costs. The nutritional characteristics, availability and low cost of obtaining evidence the possibility of using the by-products in the cultivation of microalgae. This work reviews the mixotrophic cultivation system of microalgae using waste from agribusiness as a source of organic carbon, pointing out the benefits of this strategy as a solution to the environmental problems caused by these effluents, adding value to an industrial process for the production of biomass and biocompounds as biorefinery.
Microalgae is a generic term used to refer a widely diverse group of photosynthetic microorganisms [21]. There are several species of microalgae, which are found in aquatic environments of fresh water, brackish and saline [22]. Microalgae in general, have varying microscopic sizes, perform photosynthesis, use carbon dioxide as a nutrient source for growth, in addition to playing a fundamental role in ecosystems [23, 24, 25]. It is estimated that there are about 800 thousand species of microalgae, of which about 40 to 50 thousand are of scientific knowledge, which makes it an almost unexplored resource, demonstrating the great biodiversity of these algae [26, 27]. In addition, most species are not yet known and very few are used for any purpose.
The basic composition of microalgae is based on carbohydrates, lipids, proteins, ash and nucleic acids, in addition to chlorophyll and other protective pigments and light capture that provide high photosynthetic capacity, allowing conversion of up to 10% of energy in biomass [28]. In conventional plants, this percentage is higher when compared to other conventional plants, whose conversion is limited to a maximum of 5% [29]. The predominant elements in the biomass of microalgae are carbon, nitrogen and phosphorus and some metals such as iron, cobalt, zinc is also found [28].
In recent years, several researches have been carried out seeking to develop technologies for the elaboration and diversification of products based on microalgae. The growing expansion of these products is part of a wide range of utilities inserted in the most different commercial niches, expanding the possibilities of use and adding value to the market. According to Hu et al. [30], the global algae market is expected to be worth of about $ 1.1 billion by 2024.
Microalgae are inserted in a wide variety of species, distinguishing one from the other due to their biological structure. In this sense, these microorganisms offer potential possibilities for CO2 biofixation, remediation, effluent treatment, production of biofuels, high-value products including pharmaceuticals, food and neutraceutics [31].
According to Rizwan et al. [32], microalgae can be a source of antioxidant compounds, carotenoids, enzyme polymer, lipid, natural dye, polyunsaturated fatty acid, peptide, toxin and sterols, which are widely used in industry. In addition, they are used for the synthesis of antiviral, antimicrobial, antiviral, antibacterial and anticancer drugs [33].
Commercial microalgae cultivation systems are operated to produce mainly pigments and metabolites for nutritional supplements [34]. The algae that have technical and economic viability of production are Spirulina (Arthrospira) for supplements with a high protein content, Haematococcus as a source of astaxanthin and Dunaliella salina for the production of pro-vitamin A [31]. Spirulina represents 60% of all biomass produced on a large scale [35]. This species can be easily grown in tropical regions and is well adapted to extreme environments, being relatively less susceptible to contamination than other microalgae, making it the most favorable choice for large-scale production [36].
Spirulina consists mainly of proteins (50–70%), being widely used in human nutrition to combat malnutrition [37]. This species is rich in essential amino acids, beta-carotene, minerals, essential fatty acids, vitamins, polysaccharides, among others. Chlorella accumulate high concentrations of carotenoids (astaxanthin, lutein, β-carotene, violaxanthin and zeaxanthin), antioxidants, vitamins, polysaccharides, proteins, peptides and fatty acids [5, 38]. In addition to all the benefits mentioned, the bioactive compounds of microalgae can have a biological, immune, antiviral and anti-cancer properties, being highly active [39].
Global warming has been worrying environmentalists across the planet. Although there are different ways of capturing CO2, the biological method stands out as a potentially attractive alternative. The requirements for producing and obtaining biomass from microalgae are basically CO2 and a source of light, be it natural or artificial [2]. Carbon dioxide can be converted into organic matter by performing photosynthesis using sunlight as an energy source [40, 41, 42]. Microalgae are more efficient for fixing CO2 and have a higher productivity rate (ton/ha/year) when compared to terrestrial plants. In addition, CO2 biofixation can be combined with other processes, such as the treatment of organic waste, being advantageous in terms of economic viability and environmental sustainability. Microalgae can also be grown in nutrient-rich organic effluents, salt and brackish water, reducing the use of fertile land and fresh drinking water [43].
Studies involving the mixotrophic cultivation of microalgae using industrial residues from agro-industry as a source of organic carbon have been carried out to minimize the cost of biomass production, treat the effluent and promote CO2 biofixation [7]. In this sense, expanding the ways in which these residues are used, avoiding their incorrect disposal, minimizes the effects of environmental pollution and adds value to industrial processes, encouraging a cleaner and more sustainable bioeconomy.
Currently, fossil fuels represent the main source of energy in the world, but unsustainable and directly related to the pollution of air, land, water and climate change. The burning of fossil fuels consolidated to increase the atmospheric concentration of CO2 being directly associated with global warming. Allied to this, the future oil scarcity is a major challenge for scientists, motivating a constant search for technologies capable of producing clean and sustainable fuels [44]. Among many biomasses, microalgae represent a promising source for the production of clean renewable energy, as they are capable of fixing CO2 by performing photosynthesis with efficiency and productivity superior to that of conventional oilseeds and terrestrial plants used in the production of biodiesel and bioethanol. Among the available biomass sources, microalgae have been evaluated and investigated as generation third biomass, being researched to produce different types of biofuels, among which are biodiesel, bioethanol, bio-oil, char, hydrogen and synthesis gas [45]. Recent research involving the production of biofuels has been focused on third generation biomass, since the first and second raw materials are based on terrestrial cultures that compete with food production and can lead to food crises [46]. Algae biofuels are not yet obtained on a large scale due to the high cost of the process justifying the development of new technologies that can bring economic viability [47].
Bioremediation and biofuel production from waste resources by microalgae platform is mainly important to utilize abundantly available solar energy biofixing CO2 and treat effluents through the mixotrophic growth of microalgae [7]. Algal bioremediation is a good strategy to produce biomass for biofuels production while remediating wastes, also improving carbon-footprint through carbon capturing and utilization technology.
A microalgae biorefinery enables to integrate fractionation and conversion processes to transform biomass into bioproducts such as food, feed, chemicals, and bio-energy as optimization of the use of the microalgae for reducing waste production, and maximizes process profit. After lipid transesterification for biodiesel, the residual biomass can be used to produce other biofuels such as methane, bio-oil and ethanol or biocompounds for food and pharmaceutical industry [48].
There are currently four cultivation technologies in use for the production of commercial microalgae including open ponds and raceway ponds (open systems), photobioreactors and fermenters [49]. In open systems, microalgae are grown in open areas, including tanks, lakes, and ponds, deep channels, among others. In closed systems, crops are grown in transparent bioreactors, exposed to sunlight or artificial radiation for photosynthesis and fermenters.
Natural and artificial lakes and ponds, where most of the systems commonly used are large, shallow ponds and tanks, represent open pond systems. The main advantages of these systems are the ease of construction and operation when compared to photobioreactors and the possibility of operating hybrid processes involving the cultivation of algae associated with the treatment of wastewater. However, the disadvantages are inefficient light distribution, losses through evaporation, diffusion of CO2 into the atmosphere, contamination and the requirement for large areas of land [50]. Open ponds are currently in use for wastewater treatment and production of Dunaliella salina, characterized as a hybrid process. These systems are used by Ognis Australia Pty Ltd. to produce β-carotene from Dunaliella salina in Hutt Lagoon and Whyalla. In terms of surface area used, these are among the largest algae production systems in the world.
Closed or artificial ponds (circular ponds and raceway ponds) are more efficient than open systems for producing microalgae, since control over the production environment is much better than open ponds or extensive ponds. The cost of raceway ponds is higher than that of open lagoon systems, but lower than that of photobioreactors. These systems are the most used due to their potential to produce large quantities of biomass for commercial application. Raceway pond ponds are commonly used to grow Chlorella sp., Spirulina platensis, Haematococcus sp. and Dunaliella salina, with a biomass production rate of 60–100 mg of dry biomass/L/day [50]. Raceway ponds are used to produce Spirulina at Earthrise Nutraceuticals in the USA and Cyanotech Corp. in Hawaii [49].
Photobioreactors were designed to overcome the problems associated with open growth systems. It has been shown that cultivation of microalgae in these systems are capable of producing large amounts of biomass as they allow an effective control of process parameters, such as pH, temperature, CO2 concentration, level of contamination, among others. However, photobioreactors are much more expensive than open ponds and raceway ponds. Commercial photobioreactor productions include the production of H. pluvialis in Israel and Hawaii and C. vulgaris in Germany. Production costs are very high, reaching $ 100/kg [49]. As a result, biofuel production based entirely on photobioreactors is generally considered unlikely to be commercially viable [6, 49, 50].
Closed fermenters are used for the production of heterotrophic algae, where sugars or other simple carbon sources are used for growth instead of CO2 and light. Open fermenters similar to the fermenters used in the production of ethanol in industries are not suitable for the growth of algae, since these microorganisms have slow growth when compared to yeasts and bacteria. In the USA, India and China ω-3 fatty acids are produced from Thraustochytrids by heterotrophic fermentation through sugars and O2. As it is a high value-added product, it is sold for 100 $ /kg, which justifies the high cost of the process [49].
Microalgae have different growth metabolisms, which characterizes their versatility. Cultivation conditions define the metabolic route for the production of biocompounds, including proteins, carbohydrates, pigments and fatty acids. Although the production of microalgae has traditionally been photoautotrophic, these microorganisms have different forms of energy metabolism including heterotrophic and mixotrophic, which use an organic carbon source for the growth and production of biomass. The understanding of these metabolisms allows the diversification of current growth systems aiming at increasing the production of biomass and certain specific metabolites.
Photoautotrophic growth is the most common way to cultivate microalgae through photosynthesis. In these systems, high concentrations of CO2 are sequestered, but productivity is low when compared to heterotrophic and mixotrophic systems that provide high yields of biomass and secondary metabolites [51, 52]. Through photobioreactors is possible to obtain the maximum cell density of 40 g/L, while in outdoor open-pond or raceway-pond cultures, the cell concentration is usually lower than 10 g/L. This significantly increases the energy consumption of cell harvesting and the cost of biomass production [53] Usually scale-up of microalgae cultivation in wastewater is fulfilled phototrophically, which may be hindered by inefficient illumination and the low biomass density, leading to poor removal of nutrients [54].
For photosynthesis, light is used as an energy source and CO2 is used as a carbon source [55]. The carbon source is essential for growth and the higher its concentration, the higher the productivity. Nitrogen sources in the culture medium are also essential for the synthesis of proteins, nucleic acids and other biocomposites necessary for cell growth and survival [56] and the concentration must be compatible with the amount of carbon in the medium [6]. The type of cultivation, the nutrients, the carbon source, the salinity of the medium, the irradiance and the temperature vary according to the chosen species and also considerably influence the success of the microalgae production.
Microalgae can grow in the absence of light in culture media assimilating organic carbon. Studies show that some species, including Chlorella, C. protothecoides, C. vulgaris, C. zofingensis, C. minutissima, Tetraselmis and Neochloris [57] are able to grow in both autotrophic and heterotrophic conditions [56]. According to Hosoglu et al. [58], microalgae of the Chlorella Beyerinck genus are those that have the greatest potential for large-scale heterotrophic production, with emphasis on the species C. protothecoides that has been widely studied.
In heterotrophic crops, microalgae acquire carbon and energy from organic sources via oxidative phosphorylation, consuming O2 and releasing CO2. According to Behrens [59], the cost of producing the kg of dry biomass produced in photoautotrophic conditions can be 5.5 times higher than in heterotrophic conditions. In heterotrophic systems there are no light limitation problems, since microalgae grow in the absence of light using organic carbon as a carbon and energy source reaching high concentrations of biomass reaching up to 100 g/L, which considerably facilitates the harvesting process [60]. In heterotrophic processes, 18% of the energy obtained can be converted into adenosine triphosphate (ATP) whereas in photoautotrophic cultures this percentage is only 10% [61]. However, despite the advantages, the cultivation of microalgae under heterotrophic conditions, due to the use of organic carbon, requires reactors and techniques of greater complexity and high cost to avoid contamination caused by other microorganisms.
Under mixotrophic conditions, microalgae grow both photoautotrophically and heterotrophically, being able to assimilate organic compounds as a carbon source and use inorganic carbon as an electron donor [62]. In this metabolism, the energy is captured through the catalysis of external organic compounds through respiration and the light energy is converted into chemical compounds via photosynthesis, being a promising solution in the processes of environmental remediation, being able to treat the effluents of the agribusiness and produce biomass rich in metabolites of industrial interest.
In photoautotrophic crops, self-shade caused by the high density of cells makes light penetration difficult, causing photoinhibition and may be the limiting factor to its propagation leading to low biomass yields. Under heterotrophic conditions, not all microalgae species are able to grow and the strict use of only organic substrates as a source of carbon and energy makes the process more prone to contamination. Thus, an alternative to maximize production can be through mixotrophic cultivation. Therefore, the cells would multiply with autotrophic metabolism until reaching the maximum cell density, at which point a source of organic carbon is added to stimulate, also, heterotrophic growth. Thus, due to the high cell density in the medium, problems with contamination of microorganisms would be less likely to happen. For the success of this technique, the cultivated species must be able to grow in heterotrophic conditions without microbial contamination and the organic compound to be added, as well as its ideal concentration must be known.
Reducing use of light in mixotrophic processes decreases the demand for energy, which minimizes the operational cost in processes with artificial light. According to Perez-Garcia and Bashan [63] in these systems there is a better control capable of regulating the growth rate of the species, which minimizes the risk of contamination by photosynthetic microorganisms. Due to the significant heterotrophic contribution of the organic fraction, the reactor design does not require a maximized area to expose the microalgae to light to perform photosynthesis, decreasing the process cost.
According to Patel et al. [7], mixotrophic cultivation has advantages over photoautotrophic and heterotrophic metabolism. In this process, in addition to the higher growth rates reducing the microalgae growth cycle, there is also growth in the dark phase mediated by respiration, potentiating the production of biomass. There is also a comparatively prolonged exponential growth phase, great flexibility to change the metabolism from heterotrophic to photo-autotrophic and vice versa, prevention of photo-oxidative damage caused by O2 accumulated in closed photobioreactors and reduction in substrate uptake photoinhibition. It has been shown that microalgae cultivated under mixotrophic conditions can present, under controlled conditions, higher biomass productivity when compared to photoautotrophic and heterotrophic cultures [64].
The advancement of agro-industry has generated a large amount and variety of waste causing serious environmental problems and is one of the sectors that generate more waste rich in organic matter. According to Dahiya et al. [65], approximately 1.3 billion tons of foods are wasted each year during its production, handling, storage, processing, distribution or consumption. The composition of food processing residues is extremely varied and depends on both the nature of the raw material and the production technique employed.
Due to the scarcity of available areas close to large urban centers for the disposal of industrial and urban waste, the vast majority of companies do not carry out treatment and/or correct disposal of this material, which contributes to the increase in environmental pollution. Pollution is due to high concentrations of organic matter and heavy metals causing contamination, eutrophication of water bodies, death of aquatic organisms and local vegetation, ecological imbalance and health problems for the population. In this sense, the use of agro-industrial waste as a source of organic carbon for the cultivation of microalgae is presented as an option for the bioremediation of these effluents added to the production of biomass rich in biocompounds with different applications.
A lot of studies have evaluated the mixotrophic growth of microalgae using glucose, glycerol and acetate as a source of organic carbon and observed that the biomass yields were higher, which could decrease the cost of the process. Liang et al. [66] investigated C. vulgaris strain under autotrophic, mixotrophic and heterotrophic growth conditions. Mixotrophic growing on glucose with light produced the highest lipid productivity compared with other growth modes. Garcia et al. [67] studied the mixotrophic growth of tricornutum UTEX-640 using acetate, lactic acid, glycine, glucose and glycerol. The best results were obtained using with urea, which resulted in maximum biomass and eicosapentaenoic acid productivities significantly higher than those obtained for the photoautotrophic control, which suggest the possibility of using mixotrophy for the mass production of microalgae. Cheirsilp & Torpee [68] cultivated Chlorella sp., Chlorella sp., Nannochloropsis sp. and Cheatoceros sp. under mixotrophic condition using glucose as source of organic carbon. They observed that the biomass and lipid production of all tested strains in mixotrophic culture were notably enhanced in comparison with photoautotrophic and heterotrophic cultures.
Due to the success of the microalgae mixotrophic cultivation method, recent studies have been evaluating the possibility of using residues from the agro-industry as source of organic matter as a strategy to treat the effluent, produce biomass and reduce the cost of the process.
Hu et al. [69] evaluated the mixotrophic cultivation of Chlorella sp. UMN271 utilizing swine manure as nutrient supplement for evaluate the nutrient removal efficiencies by alga. The results showed that addition of 0.1% (v/v) acetic, propionic and butyric acids, respectively, could promote algal growth, enhance nutrient removal efficiencies and improve total lipids productivities. They concluded that Chlorella sp. grown on acidogenically-digested manure could be used as a feedstock for high-quality biodiesel production.
Li et al. [70] investigated the effects of autotrophic and mixotrophic growth on cell growth and lipid productivity of green microalgae Chodatella sp and Piggery wastewater served as nutrient sources for mixotrophic growth. The specific growth rate, biomass production, and lipid productivity obtained with mixotrophic growth were until 5.6 times higher than those obtained with autotrophic growth. The mixotrophic cultivation simultaneously assimilated 99.7% ammonia nitrogen and 75.9% total phosphorus from piggery wastewater, which reduced the required nutrient for the culture of microalgae, thereby reducing the cost of biomass for diverse application.
León-Vaz et al. [71] cultivated C. sorokiniana microalgae under mixotrophic conditions utilized Oxidized wine waste lees among other agro-industrial wastes as carbon source. The fed-batch strategy and the medium optimization, with nutrient supplementation, have been found to be very effective in enhancing biomass and neutral lipid productivity, suggesting that this is a promising strategy for production of microalgal biomass. The algal biomass concentration was 11 g L-1 with a lipid content of 38% (w/w).
Bhatnagar et al. [72] evaluated mixotrophic growth of Chlamydomonas globosa, Chlorella minutissima and Scenedesmus bijuga under medium supplemented with different organic carbon substrates and wastewaters. The mixotrophic growth of these microalgae resulted in 3–10 times more biomass production relative to phototrophy. Poultry litter extract as growth medium recorded up to 180% more biomass growth compared to standard growth medium, while treated and untreated carpet industry wastewaters also supported higher biomass, with no significant effect of additional nitrogen supplementation.
Andrade & Coosta [73] determined the effects of molasses concentration and light levels on mixotrophic biomass production by Spirulina platensis. Molasses concentration was the main factor influencing maximum biomass concentration (Xmax) reached 2.94 g L− 1 and μmax 0.147 d − 1. Molasses, suggesting that this industrial by-product could be used as a low-cost supplement for the growth of Spirulina platensis, stimulated the production of biomass.
Melo et al. [74] evaluated the growth, nutrients and toxicity removal of Chlorella vulgaris cultivated under autotrophic and mixotrophic conditions using corn steep liquor, cheese whey and vinasse as source of organic matter. The results demonstrated that corn steep liquor toxicity was totally eliminated and cheese whey and vinasse toxicity were minimized by C. vulgaris. They demonstrated that the mixotrophic cultivation of C. vulgaris is able to increase cellular productivity and could be an alternative to remove the toxicity from agroindustrial by-products.
Hugo et al. [75] studied the growth of forty microalgae strains under mixotrophic conditions using sugarcane vinasse as source of organic matter. Micractinium sp. Embrapa|LBA32 and C. biconvexa Embrapa|LBA40 presented expressive growth in a light-dependent manner even in undiluted vinasse under non-axenic conditions. Microalgae strains presented higher biomass productivity in vinasse-based medium compared to autotrophic medium. This research showed the potential of using residues derived from ethanol plants to cultivate microalgae for the production of energy and bioproducts.
Mitra et al. [76] cultivated Chlorella vulgaris under mixotrophic/heterotrophic conditions using dry-grind ethanol thin stillage and soy whey as nutrient feedstock. The results showed the biomass yields from thin stillage, soy whey and modified basal medium after 4 days of incubation at mixotrophic conditions in the bioreactor were 9.8, 6.3 and 8.0 g.L− 1 with oil content at 43, 11, and 27% (w/w) respectively. This research highlights the potential of these agro-industrial co-products as microalgal growth media with consequent production of high-value microalgal oil and biomass.
Salati et al. [77] cultivated Chlorella vulgaris using cheese whey, white wine lees and glycerol as carbon sources under mixotrophic conditions. The mixotrophic biomass production was1.5–2 times higher than autotrophic growth. Furthermore, it gave much higher energy recovery efficiency, i.e. organic carbon energy efficiency of 32% and total energy efficiency of 8%, suggesting the potential for the culture of algae as a sustainable practice to recover efficiently waste-C and produce biomass.
Piasecka et al. [78] studied the growth of Tetradesmus obliquus by supplementation with beet molasses in photoheterotrophic and mixotrophic culture conditions. The highest protein content was obtained in the mixotrophic growth suggesting this metabolism promising for protein production.
Tsolcha et al. [79] evaluated a mixed cyanobacterial-mixotrophic algal population, dominated by the filamentous cyanobacterium Leptolyngbya sp. and the microalga Ochromonas under non-aseptic conditions for its efficiency to remove organic and inorganic compounds from second cheese whey, poplar sawdust, and grass hydrolysates. Nutrient removal rates, biomass productivity, and the maximum oil production rates were determined. The highest lipid production was achieved using the biologically treated dairy effluent (up to 14.8% oil in dry biomass corresponding to 124 mg L − 1), which also led to high nutrient removal rates (up to 94%). Lipids synthesized by the microbial consortium contained high percentages of saturated and mono-unsaturated fatty acids (up to 75% in total lipids) for all the substrates tested, which implies that the produced biomass may be harnessed as a source of biodiesel.
Grupta et al. [80] cultivated the Chlorella microalgae under mixotrophic conditions using a raw food-processing industrial wastewater. About 90% reduction in TOC and COD were obtained for all dilutions of wastewater. Over 60% of nitrate and 40% of phosphate were consumed by microalgae from concentrated raw wastewater. The degradation kinetics also suggested that the microalgae cultivation on a high COD wastewater is feasible and scalable.
Yeesang et al. [81] evaluated B. braunii, a microalgae rich in oil under mixotrophic cultivation using molasses, a cheap by-product from the sugar cane plant as a carbon source and under photoautotrophic cultivation using nitrate-rich wastewater supplemented with CO2. The mixotrophic cultivation produced a high amount of biomass of 3.05 g L − 1 with a high lipid content of 36.9%. The photoautotrophic cultivation in nitrate-rich wastewater supplemented with 2.0% CO2 produced a biomass of 2.26 g L − 1 and a lipid content of 30.3%. They showed that these strategies could be promising ways for producing cheap lipid-rich microalgal biomass as biofuel feedstock and animal feeds.
Gélinas et al. [82] studied the mixotrophic growth and lipid production of Chlorella consortium using residual corn hydrolysate and corn silage juice as source of organic and compared to heterotrophic conditions. Maximum microalgal biomass of 0.8 g/L was obtained with 1 g/L of residual corn hydrolysate whatever the trophic strategy. Under mixotrophic conditions, the use of residual corn hydrolysate led to an increase of 21% and 22% in comparison with the biomass produced with glucose or silage juice, respectively. This increase varied between 11% and 28% under heterotrophic condition. They observed that at the end of the experiment, algae exposed to silage juice decreased significantly. Residual corn hydrolysate represented an interesting and efficient alternative as an organic carbon source. However, silage juice needs additional treatments to be implemented as a culture medium.
Nur et al. [83] studied palm oil mill effluent (POME), one of the wastewaters generated from palm oil mills, as source of organic carbon for mixotrophic microalgae growth. The aim of this research was to identify the growth of Chlorella vulgaris cultured in POME medium under mixotrophic conditions in relation to a variety of organic carbon sources added to the POME mixture. The research was conducted with 3 different carbon sources (D-glucose, crude glycerol and NaHCO3) in 40% POME. They showed that C. vulgaris using D-glucose as carbon source gained a lipid productivity of 195 mg/l/d.
Manzoor et al. 2020 presented the growth of Scenedesmus dimorphus NT8c cultivated mixotrophically on sugarcane bagasse hydrolysate, a low-value agricultural by-product. Under mixotrophic conditions the S. dimorphus NT8c showed higher growth rates compared to photoautotrophic cultivation and the biomass productivity was 119.5 mg L d − 1, protein contents was 34.82% and fatty acid contents was 15.41%. They concluded that mixotrophically-cultivated microalgae are able to increase the biomass and lipid productivity. However, the concentrations of supplementation need to be studied because higher level of organic carbon can result in unfavorable levels of turbidity and bacterial growth, reducing microalgal biomass productivity.
Microalgal biomass represents a sustainable alternative to fossil consumption and bioproducts for food and pharmaceutical industry. Microalgae can growth under photoautotrophic, heterotrophic or mixotrophic modes where the latter two trophic modes require organic carbon to grow efficiently. Actually, researchers have highlighted the role of low cost-efficient agro-industrial by-products used as supplements in algal culture media. However, supplementation of organic carbon contributes significantly to a higher cost of microalgae production and this can compete with human and animal alimentation. Agro-industrial by-products and wastes are of great interest as cultivation medium for microorganisms because of their low cost, renewable nature, and abundance.
Faced with this scenario, biotechnological technologies are necessary to develop the production of microalgae on a large scale and expand the range of utilities that, in the short or long term, contribute to the improvement of industrial processes. In addition, mixotrophic microalgae growth is a great strategy to reduce environmental pollution generated by residues rich in organic matter and can reduce the cost of the industrial process. However, more investments, development and greater knowledge of the metabolism of these microalgae and their effectiveness in the generation of new bioproducts are increasingly necessary.
The authors gratefully acknowledge the Postgraduation Dean’s Office of the Federal University of Rio Grande do Norte and Dean of Extension of Federal Institute of Rio Grande do Norte. The authors would like to thank Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the financial support.
Ove Odredbe i uvjeti ističu pravila i regulacije u svezi korištenja IntechOpenove stranice www.intechopen.com i svih poddomena u vlasništvu IntechOpena, tvrtke sa sjedištem u 5 Princes Gate Court, London, SW7 2QJ, Ujedinjeno Kraljevstvo.
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\\n\\nOsim ako nije suprotno navedeno, IntechOpen i/ili svi davatelji licence vlasnici su intelektualnog vlasništva nad svim materijalima na www.intechopen.com. Sva prava intelektualnog vlasništva su pridržana. Stranice sa www.intechopen.com možete gledati, preuzimati, dijeliti, dijeliti poveznice i printati za osobnu uporabu, a temeljem pravila sadržanih u ovim Odredbama i uvjetima.
\\n\\nMi koristimo kolačiće. Korištenjem IntechOpenove stranice slažete se s korištenjem kolačića u skladu s IntechOpenovom Politikom privatnosti. Većina modernih, interaktivnih stranica koristi kolačiće kako bi omogućila ponovno pronalaženje korisničkih detalja kod svakog posjeta. Na našoj stranici kolačići se uglavnom koriste kako bi omogućili funkcionalnost i olakšali posjetiteljima korištenje stranice.
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\n\nSljedeća terminologija odnosi se na Odredbe i uvjete, te na sve naše ugovore:
\n\nKlijent, stranka, vi, vaš odnosi se na vas, osobu koja pristupa ovoj stranici i prihvaća IntechOpenove Odredbe i uvjete;
\n\nKompanija, tvrtka, mi, naše odnosi se na tvrtku IntechOpen;
\n\nStranke, strane odnosi se na klijenta i na nas, ili samo na klijenta ili nas.
\n\nSve odredbe koje se odnose na ponudu, prihvat ili razmatranje plaćanja, a za koja mi pružamo asistenciju klijentu, bilo na ugovoreni ili fiksni način, a s ciljem da se ostvare potrebe i želje klijenta u svezi s našim uslugama, su podložne zakonskim odredbama Ujedinjenog Kraljevstva.
\n\nOsim ako nije suprotno navedeno, IntechOpen i/ili svi davatelji licence vlasnici su intelektualnog vlasništva nad svim materijalima na www.intechopen.com. Sva prava intelektualnog vlasništva su pridržana. Stranice sa www.intechopen.com možete gledati, preuzimati, dijeliti, dijeliti poveznice i printati za osobnu uporabu, a temeljem pravila sadržanih u ovim Odredbama i uvjetima.
\n\nMi koristimo kolačiće. Korištenjem IntechOpenove stranice slažete se s korištenjem kolačića u skladu s IntechOpenovom Politikom privatnosti. Većina modernih, interaktivnih stranica koristi kolačiće kako bi omogućila ponovno pronalaženje korisničkih detalja kod svakog posjeta. Na našoj stranici kolačići se uglavnom koriste kako bi omogućili funkcionalnost i olakšali posjetiteljima korištenje stranice.
\n\nIntechOpen ili njegovi suradnici niti u jednom slučaju neće biti odgovorni za štete (štete uključuju gubitak podataka ili profita, druge poslovne prekide, te sve ostale štete) koje nastanu zbog korištenja materijala na IntechOpenovoj stranici ili nemogućnosti da se iste koriste, čak i ako je IntechOpen ili njegov predstavnik o takvoj šteti obaviješten pismenim ili usmenim putem. Neke jurisdikcije ne dozvoljavaju ograničenja garancija ili ograničenja obveza za posljedične ili slučajne štete pa se u tom slučaju ova ograničenja možda ne odnose na vas.
\n\nMaterijali koji se pojavljuju na IntechOpenovoj stranici mogu sadržavati manje greške, tipfelere ili fotografske greške. IntechOpen može napraviti promjene na bilo kojem materijalu koji se nalazi na stranici u bilo koje vrijeme.
\n\nIntechOpen nije formalno povezan niti s jednom vanjskom stranicom čije poveznice vode na www.intechopen.com, osim ako to nije izravno navedeno. Iz tog razloga IntechOpen nije odgovoran za sadržaj koji se pojavljuje na takvim stranicama. Poveznica na IntechOpenovu stranicu ne implicira povezanost sa IntechOpenom. Korištenje takvih poveznica isključiva je odgovornost korisnika.
\n\nZadržavamo pravo vlasništva nad cjelokupnom stranicom www.intechopen.com i nad svim materijalom na toj stranici. Koristeći se našim uslugama, slažete se da maknete sve poveznice na našu stranicu odmah nakon što to od vas zatražimo. Također, zadržavamo pravo da ove Odredbe i uvjete, i politiku o poveznicama izmjenimo u bilo koje vrijeme. Koristeći se poveznicama na naše stranice slažete se s ovim Odredbama i uvjetima.
\n\nAko smatrate da je bilo koja poveznica na našoj stranici sumnjiva iz bilo kojeg razloga, molimo vas da nas kontaktirate. U tom slučaju razmotrit ćemo micanje poveznice s naše stranice, iako nismo obvezni to napraviti.
\n\nBez prethodne privole i izričite pisane dozvole, ne možete stvarati okvire oko naših stranica ili koristiti druge tehnike koje na bilo koji način mogu promijeniti prezentaciju ili izgled naše stranice.
\n\nIntechOpen može ove Odredbe izmijeniti u bilo koje vrijeme i bez prethodne obavijesti. Koristeći ovu stranicu vi se slažete s trenutnim Odredbama i uvjetima koje su na snazi.
\n\nOve Odredbe i uvjeti su sastavljeni u skladu s odredbama prava Ujedinjenog Kraljevstva, a za sve sporove nadležan je sud u Londonu, Ujedinjeno Kraljevstvo.
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