Parasitic diseases affecting transplant recipients
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IntechOpen Book Series will also publish a program of research-driven Thematic Edited Volumes that focus on specific areas and allow for a more in-depth overview of a particular subject.
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\\n\\nLaunching 2021
\\n\\nArtificial Intelligence, ISSN 2633-1403
\\n\\nVeterinary Medicine and Science, ISSN 2632-0517
\\n\\nBiochemistry, ISSN 2632-0983
\\n\\nBiomedical Engineering, ISSN 2631-5343
\\n\\nInfectious Diseases, ISSN 2631-6188
\\n\\nPhysiology (Coming Soon)
\\n\\nDentistry (Coming Soon)
\\n\\nWe invite you to explore our IntechOpen Book Series, find the right publishing program for you and reach your desired audience in record time.
\\n\\nNote: Edited in October 2021
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\n\nDesigned to cover fast-moving research fields in rapidly expanding areas, our Book Series feature a Topic structure allowing us to present the most relevant sub-disciplines. Book Series are headed by Series Editors, and a team of Topic Editors supported by international Editorial Board members. Topics are always open for submissions, with an Annual Volume published each calendar year.
\n\nAfter a robust peer-review process, accepted works are published quickly, thanks to Online First, ensuring research is made available to the scientific community without delay.
\n\nOur innovative Book Series format brings you:
\n\nIntechOpen Book Series will also publish a program of research-driven Thematic Edited Volumes that focus on specific areas and allow for a more in-depth overview of a particular subject.
\n\nIntechOpen Book Series will be launching regularly to offer our authors and editors exciting opportunities to publish their research Open Access. We will begin by relaunching some of our existing Book Series in this innovative book format, and will expand in 2022 into rapidly growing research fields that are driving and advancing society.
\n\nLaunching 2021
\n\nArtificial Intelligence, ISSN 2633-1403
\n\nVeterinary Medicine and Science, ISSN 2632-0517
\n\nBiochemistry, ISSN 2632-0983
\n\nBiomedical Engineering, ISSN 2631-5343
\n\nInfectious Diseases, ISSN 2631-6188
\n\nPhysiology (Coming Soon)
\n\nDentistry (Coming Soon)
\n\nWe invite you to explore our IntechOpen Book Series, find the right publishing program for you and reach your desired audience in record time.
\n\nNote: Edited in October 2021
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During the last 50 years plant breeding has entered a molecular era based on molecular tools to analyse DNA, RNA and proteins and associate such molecular results with plant phenotype. These marker trait associations develop fast to enable more efficient breeding. However, they still leave a major part of breeding to be performed through selection of phenotypes using quantitative genetic tools. 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Vaz-Leal",slug:"francisco-j.-vaz-leal",email:"fjvazleal@gmail.com",position:null,institution:null},{id:"188719",title:"Dr.",name:"María Cristina",middleName:null,surname:"Álvarez Mateos",fullName:"María Cristina Álvarez Mateos",slug:"maria-cristina-alvarez-mateos",email:"cristinaalvarezmateos@gmail.com",position:null,institution:null},{id:"195142",title:"Dr.",name:"Laura",middleName:null,surname:"Rodríguez Santos",fullName:"Laura Rodríguez Santos",slug:"laura-rodriguez-santos",email:"laura@unex.es",position:null,institution:{name:"University of Extremadura",institutionURL:null,country:{name:"Spain"}}},{id:"195143",title:"Dr.",name:"María I",middleName:null,surname:"Ramos Fuentes",fullName:"María I Ramos Fuentes",slug:"maria-i-ramos-fuentes",email:"miramos@unex.es",position:null,institution:{name:"University of Extremadura",institutionURL:null,country:{name:"Spain"}}}]}},chapter:{id:"52200",slug:"eating-disorders-as-new-forms-of-addiction",signatures:"Francisco J. Vaz-Leal, María I. Ramos-Fuentes, Laura Rodríguez-\nSantos and M. Cristina Álvarez-Mateos",dateSubmitted:"June 28th 2016",dateReviewed:"August 12th 2016",datePrePublished:null,datePublished:"February 1st 2017",book:{id:"5372",title:"Eating Disorders",subtitle:"A Paradigm of the Biopsychosocial Model of Illness",fullTitle:"Eating Disorders - A Paradigm of the Biopsychosocial Model of Illness",slug:"eating-disorders-a-paradigm-of-the-biopsychosocial-model-of-illness",publishedDate:"February 1st 2017",bookSignature:"Ignacio Jauregui-Lobera",coverURL:"https://cdn.intechopen.com/books/images_new/5372.jpg",licenceType:"CC BY 3.0",editedByType:"Edited by",editors:[{id:"323887",title:"Prof.",name:"Ignacio",middleName:null,surname:"Jáuregui-Lobera",slug:"ignacio-jauregui-lobera",fullName:"Ignacio Jáuregui-Lobera"}],productType:{id:"1",title:"Edited Volume",chapterContentType:"chapter",authoredCaption:"Edited by"}},authors:[{id:"188555",title:"Prof.",name:"Francisco J.",middleName:null,surname:"Vaz-Leal",fullName:"Francisco J. Vaz-Leal",slug:"francisco-j.-vaz-leal",email:"fjvazleal@gmail.com",position:null,institution:null},{id:"188719",title:"Dr.",name:"María Cristina",middleName:null,surname:"Álvarez Mateos",fullName:"María Cristina Álvarez Mateos",slug:"maria-cristina-alvarez-mateos",email:"cristinaalvarezmateos@gmail.com",position:null,institution:null},{id:"195142",title:"Dr.",name:"Laura",middleName:null,surname:"Rodríguez Santos",fullName:"Laura Rodríguez Santos",slug:"laura-rodriguez-santos",email:"laura@unex.es",position:null,institution:{name:"University of Extremadura",institutionURL:null,country:{name:"Spain"}}},{id:"195143",title:"Dr.",name:"María I",middleName:null,surname:"Ramos Fuentes",fullName:"María I Ramos Fuentes",slug:"maria-i-ramos-fuentes",email:"miramos@unex.es",position:null,institution:{name:"University of Extremadura",institutionURL:null,country:{name:"Spain"}}}]},book:{id:"5372",title:"Eating Disorders",subtitle:"A Paradigm of the Biopsychosocial Model of Illness",fullTitle:"Eating Disorders - A Paradigm of the Biopsychosocial Model of Illness",slug:"eating-disorders-a-paradigm-of-the-biopsychosocial-model-of-illness",publishedDate:"February 1st 2017",bookSignature:"Ignacio Jauregui-Lobera",coverURL:"https://cdn.intechopen.com/books/images_new/5372.jpg",licenceType:"CC BY 3.0",editedByType:"Edited by",editors:[{id:"323887",title:"Prof.",name:"Ignacio",middleName:null,surname:"Jáuregui-Lobera",slug:"ignacio-jauregui-lobera",fullName:"Ignacio Jáuregui-Lobera"}],productType:{id:"1",title:"Edited Volume",chapterContentType:"chapter",authoredCaption:"Edited by"}}},ofsBook:{item:{type:"book",id:"11651",leadTitle:null,title:"Bone Tumors - Recent Updates",subtitle:null,reviewType:"peer-reviewed",abstract:"\r\n\tThis book intends to present the latest information and modern management of bone-related tumours. Not only from Benign to malignant but also tumours conditions are covered in a detailed and succinct way. It will aim to cover an array of areas in particular tumour including pathology, pathogenesis, genetic basis, oncology modern methods of diagnosing, screening for tumours and aetiological causes, and advice on how to prevent and other early diagnosing strategies. The current concept of bone tumours and tumour management has changed rapidly over the past decades. Therefore, a fresh look at this topic is needed and is timely.
\r\n\r\n\tThe book will aim to include the latest information used in current practice and current research areas on which the future practice will be based on. Not only on modern investigation and diagnosing tools biopsy techniques and radiological imaging but also modern concepts for managing these tumours. The three main areas in managing involve radiotherapy chemotherapy and surgical oncology and the latest advances in these fields are intended to be discussed. This book will aim to benefit not only trainees of surgery, oncology medicine, orthopaedics but also medical students, general practitioners, and anybody interested in the field of bone tumour management.
",isbn:"978-1-80356-930-7",printIsbn:"978-1-80356-929-1",pdfIsbn:"978-1-80356-931-4",doi:null,price:0,priceEur:0,priceUsd:0,slug:null,numberOfPages:0,isOpenForSubmission:!0,isSalesforceBook:!1,isNomenclature:!1,hash:"cf7dd688b160a1ba07e3179613684f16",bookSignature:"Dr. Hiran Wimal Amarasekera",publishedDate:null,coverURL:"https://cdn.intechopen.com/books/images_new/11651.jpg",keywords:"Osteosarcoma, Choindro - Sarcoma, Ewing's Sarcoma, Osteoma, Chondroma, Enchondromas, Bone Cysts, Myelo Proliferative Disease, Plasma Cells, Lymphomas, Soft Tissue Sarcomas, Bone",numberOfDownloads:null,numberOfWosCitations:0,numberOfCrossrefCitations:null,numberOfDimensionsCitations:null,numberOfTotalCitations:null,isAvailableForWebshopOrdering:!0,dateEndFirstStepPublish:"April 6th 2022",dateEndSecondStepPublish:"June 15th 2022",dateEndThirdStepPublish:"August 14th 2022",dateEndFourthStepPublish:"November 2nd 2022",dateEndFifthStepPublish:"January 1st 2023",dateConfirmationOfParticipation:null,remainingDaysToSecondStep:"2 months",secondStepPassed:!0,areRegistrationsClosed:!0,currentStepOfPublishingProcess:4,editedByType:null,kuFlag:!1,biosketch:"Works as a clinician, orthopaedic surgeon, Researcher, academic teacher, examiner, and educator in the field of medicine and orthopaedics. Pioneering work on anatomy and blood supply to joints mainly hip joints and causative factors leading to avascular necrosis was done at the University of Warwick, and the University of California Los Angeles.",coeditorOneBiosketch:null,coeditorTwoBiosketch:null,coeditorThreeBiosketch:null,coeditorFourBiosketch:null,coeditorFiveBiosketch:null,editors:[{id:"67634",title:"Dr.",name:"Hiran",middleName:"Wimal",surname:"Amarasekera",slug:"hiran-amarasekera",fullName:"Hiran Amarasekera",profilePictureURL:"https://mts.intechopen.com/storage/users/67634/images/system/67634.png",biography:"Hiran Amarasekera is a Consultant Orthopaedic Surgeon Currently practicing in Sri Lanka. After obtaining the MBBS from Kasturba medical college, Manipal, Inda, he completed the MS in Surgical sciences from the University of Colombo. He obtained the fellowship of the Royal College of Surgeons of Edinburgh (FRCS Ed) and board certification in 2003. \n\nHis special interests are in the areas of young adult hip and knee problems, sports injuries, lower limb arthroplasty, and keyhole joint surgery, and revision arthroplasty. His present research is focused on non-surgical and minimally invasive alternative treatment for osteoarthritis. He worked and trained in many countries for over twenty including India, Sri Lanka, Australia, United States, and the UK.\n\nAs a keen researcher, he has completed an MPhil from the University of Warwick and completed a research fellowship at the University of California Los Angeles, (UCLA). \n\nPresently, he works as a medical educator, as an honorary senior lecturer at the University of Kelaniya and Kothalawela Defense University in Sri Lanka. He is an examiner of medical students both in Sri Lanka and the UK and a course provider for Trauma courses run by the college of surgeons and was elected a fellow of Sri Lanka College of surgeons in 2013.\n\nDr. Amarasekera is the editor of the Journal of Sri Lanka Orthopaedic association and council member. He is a reviewer for the Journal of Bone and Joint Surgery (Br) e and Bone and Joint Journal (BJJ) and a member of the editorial board of the Sri Lanka Journal of Surgery (SLJS). \n\nHe has over 50 international publications, presentations and several book chapters to his credit and has reviewed over 100 papers for journals of BJJ and SLJS.\n\nAfter joining IntechOpen in 2012 he authored three book chapters and edited several open access books with them.",institutionString:"University of Warwick Science Park",position:null,outsideEditionCount:0,totalCites:0,totalAuthoredChapters:"3",totalChapterViews:"0",totalEditedBooks:"2",institution:{name:"University of Warwick Science Park",institutionURL:null,country:{name:"United Kingdom"}}}],coeditorOne:null,coeditorTwo:null,coeditorThree:null,coeditorFour:null,coeditorFive:null,topics:[{id:"16",title:"Medicine",slug:"medicine"}],chapters:null,productType:{id:"1",title:"Edited Volume",chapterContentType:"chapter",authoredCaption:"Edited by"},personalPublishingAssistant:{id:"429341",firstName:"Paula",lastName:"Gavran",middleName:null,title:"Ms.",imageUrl:"//cdnintech.com/web/frontend/www/assets/author.svg",email:"paula@intechopen.com",biography:null}},relatedBooks:[{type:"book",id:"9500",title:"Recent Advances in Bone Tumours and Osteoarthritis",subtitle:null,isOpenForSubmission:!1,hash:"ea4ec0d6ee01b88e264178886e3210ed",slug:"recent-advances-in-bone-tumours-and-osteoarthritis",bookSignature:"Hiran Amarasekera",coverURL:"https://cdn.intechopen.com/books/images_new/9500.jpg",editedByType:"Edited by",editors:[{id:"67634",title:"Dr.",name:"Hiran",surname:"Amarasekera",slug:"hiran-amarasekera",fullName:"Hiran Amarasekera"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"6755",title:"Recent Advances in Arthroscopic Surgery",subtitle:null,isOpenForSubmission:!1,hash:"5c122c5b88bdc03c130d34ad2ac2d722",slug:"recent-advances-in-arthroscopic-surgery",bookSignature:"Hiran Wimal Amarasekera",coverURL:"https://cdn.intechopen.com/books/images_new/6755.jpg",editedByType:"Edited by",editors:[{id:"67634",title:"Dr.",name:"Hiran",surname:"Amarasekera",slug:"hiran-amarasekera",fullName:"Hiran Amarasekera"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"6550",title:"Cohort Studies in Health Sciences",subtitle:null,isOpenForSubmission:!1,hash:"01df5aba4fff1a84b37a2fdafa809660",slug:"cohort-studies-in-health-sciences",bookSignature:"R. Mauricio Barría",coverURL:"https://cdn.intechopen.com/books/images_new/6550.jpg",editedByType:"Edited by",editors:[{id:"88861",title:"Dr.",name:"R. Mauricio",surname:"Barría",slug:"r.-mauricio-barria",fullName:"R. Mauricio Barría"}],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:"Theophile",surname:"Theophanides",slug:"theophile-theophanides",fullName:"Theophile Theophanides"}],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:"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:"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:"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:"2270",title:"Fourier Transform",subtitle:"Materials Analysis",isOpenForSubmission:!1,hash:"5e094b066da527193e878e160b4772af",slug:"fourier-transform-materials-analysis",bookSignature:"Salih Mohammed Salih",coverURL:"https://cdn.intechopen.com/books/images_new/2270.jpg",editedByType:"Edited by",editors:[{id:"111691",title:"Dr.Ing.",name:"Salih",surname:"Salih",slug:"salih-salih",fullName:"Salih Salih"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"117",title:"Artificial Neural Networks",subtitle:"Methodological Advances and Biomedical Applications",isOpenForSubmission:!1,hash:null,slug:"artificial-neural-networks-methodological-advances-and-biomedical-applications",bookSignature:"Kenji Suzuki",coverURL:"https://cdn.intechopen.com/books/images_new/117.jpg",editedByType:"Edited by",editors:[{id:"3095",title:"Prof.",name:"Kenji",surname:"Suzuki",slug:"kenji-suzuki",fullName:"Kenji Suzuki"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}}]},chapter:{item:{type:"chapter",id:"41513",title:"Complications of Kidney Transplantation: Effects of Over-Immunosuppression",doi:"10.5772/53672",slug:"complications-of-kidney-transplantation-effects-of-over-immunosuppression",body:'Kidney transplantation is a relatively young field within medicine which continues to experience rapid advances in several areas. The number of immunosuppressive medications available to prevent and treat immunologic rejection of the transplanted organ has increased significantly since the late 1990’s, however, there continues to be a great need for developing novel, less toxic medications. The fine balance between over- and under-immunosuppression is difficult to achieve in many transplant recipients, particularly as candidacy for kidney transplantation has expanded to include the elderly, patients with HIV and/or Hepatitis C infection, and sensitized transplant candidates. The relationship between infection and rejection remains closely intertwined, and can be a vicious cycle, with reduction of immunosuppression to manage infection potentially triggering rejection, and increased immunosuppression in the setting of rejection potentially leading to infectious complications. This chapter will focus on post-transplant complications resulting from over-immunosuppression, specifically infection and malignancy.
The occurrence of infection after transplantation is a significant determinant of transplant outcome [1]. The incidence of infections after solid-organ transplantation is dependent on several factors, including the degree of immunosuppression, the type of organ transplanted, technical or surgical complications, need for additional antirejection therapy, environmental exposures, and the time frame after transplantation. A comprehensive list of factors contributing the ‘net state of immune deficiency’ can be found in reference [2]. Most recent United States data shows that infectious complications cause 20.9% of kidney transplant recipient death with a functioning allograft [3]. Infection also accounts for a significant proportion of death-censored graft loss, accounting for 7.7% of graft losses in the U.S. between 1990 and 2006 [4]. Using the leading cause of allograft loss, chronic rejection as a reference, risk factors for infection-related graft loss included prior acute rejection and utilization of any induction therapy. Older transplant recipients (> 65 years at transplant) had a higher risk of infection related graft loss (14.1%). In this series, the infections leading to graft loss were caused by infections associated with urological complications and polyomavirus associated nephropathy [4]. Other infections that directly contribute to death-censored graft loss include pyelonephritis and acute kidney injury in the setting of sepsis/critical illness.
The occurrence of infection after transplantation usually falls within 3 general time frames: the first month, the second through the sixth month, and more than 6 months after transplantation [2, 5, 6]. Infections that occur during the first month after transplantation are generally the same nosocomial infections seen in non-immunosuppressed patients after surgery. These infections include bacterial and candidal urinary tract infection (UTI), wound/surgical site infections, catheter-related infections, and pneumonia.
The period from the second to sixth month after transplantation is the time during which opportunistic infections “classically” associated with transplantation occur [1], although the patterns have changed thanks to the availability of antimicrobial prophylaxis against some infections [2]. The most common infections during this period include cytomegalovirus (CMV),
More than 6 months after transplantation, most transplant recipients (80%) are doing well [6], and can be classified into one of three risk groups [5]:
Patients who have done well and immunosuppression is being tapered
Patients who have required increased immunosuppression exposure due to rejection
Patients at risk for late progressive viral reactivation (polyomavirus, CMV, HBV, HCV, HPV)
The most common infections seen during this period mimic those seen in the general community [6]. Such infections include influenza virus, UTIs, and pneumococcal pneumonia. Although opportunistic infections are rarely observed during this time period, reactivation of varicella zoster virus (VZV) or CMV can occur. In addition, transplant recipients who have had multiple rejection episodes requiring additional antirejection may be predisposed to opportunistic infections more commonly seen 2 to 6 months after transplantation. It is recommended that patients being treated for acute rejection be placed back on opportunistic infection prophylaxis [10]. Transplant recipients experiencing chronic infection due to HBV, HCV, CMV, EBV, or HIV, resulting in a greater degree of morbidity, are subsequently at an increased risk for other infections [1, 6]. In patients who undergo repeat transplantation, the typical timetable of infections may be altered. Infections characteristic of 1 of the 3 conventional time periods may occur simultaneously and with an increased severity [11]. In addition, modern immunosuppressive agents, as well as availability of prophylaxis against some infections has led to an altered timeline for many patients.
Although not addressed in this chapter due to space constraints, transplant centers should be aware of the newer emerging infectious diseases that may affect transplant recipients [12]. This is also a great concern due to increasing rates of transplant tourism, where patients travel to foreign countries to receive a transplant and may be exposed to infectious complications not typically seen in their home country, where they will receive their follow-up care. In addition, transplant recipients travelling for leisure should consult with a travel medicine specialist when possible [13].
Some of the most prevalent microbial pathogens observed after organ transplantation are bacteria. The specific bacterial infections that occur after transplantation can be divided into 4 categories [14]:
Infections due to surgical or technical complications,
Infections related to prolonged hospitalization (nosocomial infections),
Infections associated with the degree of immunosuppression (opportunistic infections), and
Infections occurring months after transplantation when the transplant recipient resumes normal activity (community-acquired infections).
Although transplant recipients are susceptible to common bacterial pathogens observed in normal hosts, the immunosuppressed state of the recipient after transplantation predisposes the patient to bacterial pathogens not commonly observed in the normal host. These opportunist pathogens include
The most common infections occurring after kidney transplantation are UTIs, which may include asymptmatic bacteriuria, cystitis, and/or pyelonephritis. The reported incidence of UTI in kidney recipients is 7.3% to to 90% [15-18] with the variation likely due to differences in definitions of infection and prophylactic strategies. Predisposing factors include renal insufficiency, ischemic changes of the graft, decreased urine flow through the urinary epithelium, prolonged urinary catheterization, ureteral stenting, post-transplant diarrhea, and underlying medical conditions such as diabetes mellitus, female gender, urinary tract abnormalities, bladder dysfunction, and bladder outlet obstruction [17-20]. In pediatric kidney transplant recipients, age less than 5 at the time of transplant and lower urinary tract abnormalities may be risk factors for post-transplant UTI [21]. Studies analyzing whether the utilization of double-J ureteral stents during a kidney transplant procedure increases the risk of post-transplant UTI have produced conflicting results [22-24]. It has been suggested that a shorter duration (3 weeks versus 6 weeks) of ureteral stent placement may reduce the incidence of UTI [24].
The most common pathogens implicated in UTIs include
Risk factors for CDAD include older age, antimicrobial exposure, and rabbit anti-thymocyte globulin induction therapy [30, 31]. For patients developing fulminiant CDAD, risk factors identified include peak leukocyte count of 25,000/mm3 or greater and evidence of pancolitis on CT scan. For those developing fulminant CDAD, colectomy has been associated with improved patient and graft survival when compared to patients managed with medical therapy alone [30]. Medications that suppress gastric acid production, commonly used in transplant recipients, may also increase risk of CDAD [31].
The most commonly utilized diagnostic test for CDAD is
Worldwide, the estimated incidence of tuberculosis (TB) (
Identification of high risk patients (those living in endemic areas or those with prior infection or exposure) is essential in order to administer prophylaxis with isoniazid (INH). A meta analysis of INH prophylaxis in kidney transplant recipients found that the relative risk of TB infection was significantly reduced, while risk of toxicity (hepatitis) did not differ between patients that did or did not receive prophylaxis [33]. Current European [34] and U.S. [35] guidelines recommend 9 months of INH prophylaxis for those with latent TB infection, however, the optimal timing of prophylaxis is unclear, particularly for patients awaiting a deceased donor transplant. When treating transplant recipients with active tuberculosis, close monitoring of calcineurin inhibitor levels with concomitant dose increase is needed due to presence of rifampin or related drugs in the anti-tuberculosis regimen [35].
Trimethoprim/sulfamethoxazole (TMP/SMX), traditionally used for prophylaxis against
To prevent surgical wound and abdominal infections, the local perioperative antibacterial prophylaxis should be administered. The prophylactic antibiotic of choice should be determined by the resident flora of the transplanted, the prevalent bacterial flora identified in wound infections and the institutional antibiotic susceptibility pattern [39]. In kidney transplant recipients, the target pathogens include uropathogens and staphylococci; hence either a first-generation cephalosporin or ampicillin/sulbactam is an appropriate prophylactic agent. More recently, it has been suggested that due to the low incidence of surgical site infection observed in the absence of peri-operative antimicrobial prophylaxis, prophylaxis should only be used in higher risk patients (> 65 years of age and/or obese (defined as body mass index > 35)) in order to reduce resistance, adverse events, and cost [40]. Obesity, an established risk factor for wound complications, is often targeted prior to transplant. Interestingly, significant pre-transplant weight loss has also been identified as a risk factor for wound complications, attributed to body contour changes resulting in an unfavorable abdominal panniculus [41].
The antibiotic of choice for the treatment of infection after renal transplantation is largely dependent on the susceptibility of the bacteria identified in the urine, blood, or wound culture, and is very important due to increasing bacterial resisitance to commonly used antimicrobials. Fluoroquinolones, cephalosporins, or penicillins are commonly used to treat UTIs. For infections due to coagulase-negative staphylococci or ampicillin-resistant enterococci, vancomycin is utilized. Critically ill patients require intial broad spectrum antimicrobials, which should then be narrowed as culture results become available. Nephrotoxic agents (such as aminoglycosides) should be avoided whenever possible, relying on effective non-nephrotoxic alternatives instead.
Treatment duration depends on the origin and severity of infection. Wound infections and most UTIs require treatment for 5 to 7days, whereas pyelonephritis usually requires 2 weeks of therapy or longer. Imaging to rule out obstruction or anatomic abnormalities should be considered in cases of recurrent UTIs. In addition, wound infections may require debridement with an adjunctive antibiotic regimen. Patients with neutropenic fever may receive granulocyte colony stimulating growth factors, which have been shown not to increase the risk of acute rejection [5]. Depending on the severity of the infection, reduction in immunosuppression, with close monitoring of graft function, may also play an important role in clearing the infection.
Invasive fungal infections are a significant infectious complication among solid-organ transplant recipients and remain a major cause of morbidity and mortality. Among all solid-organ transplant recipients, kidney transplantation is currently associated with the lowest rate of fungal infections, with a one-year cumulative incidence of 1.3% [46].
The most common pathogen is the
Infections due to endemic fungi typically occur in the mid to late posttransplantation period, although some do occur within 2 months of transplant. Endemic fungal infections are associated with pathogens like
Systemic prophylaxis of fungal infection is generally not required for kidney transplant recipients. Prevention of oral candidiasis is achieved through use of topical nystatin or clotrimazole. Multiple options are available for the treatment of invasive fungal infections in solid-organ transplantation, including amphotericin B (liposomal formulations preferred due to less nephrotoxicity), azole antifungals (fluconazole, itraconazole, voriconazole, posiconazole) and echinocandins (caspofunginm micafungin, anidulafungin). The optimal regimen should be based on antifungal susceptibility testing. Detailed review of these agents is beyond the scope of this chapter, however, a brief discussion of drug-drug interactions between antifungal agents and immunosuppressants is warranted, as well as mention of toxicities of concern in kidney transplant recipients (see Section 2.5).
Many factors affect the development of viral infection after solid-organ transplantation. These factors include recipient and donor serostatus, recipient comorbidities (eg, diabetes mellitus), immunosuppression regimen, organ(s) transplanted, ischemia-reperfusion injury to graft, and community-acquired infection. Viral infection can be particularly devastating to transplant recipients because of the immunosuppressive properties of the viral pathogens themselves, which may increase the patients’ susceptibility to other opportunistic infection (particularly fungal infection), or posttransplant lymphoproliferative disease (PTLD).
Cytomegalovirus (CMV), a herpesvirus, is the most important viral infection in solid-organ transplantation because of its broad effects on immunocompromised patients [6]. Active infection produces not only signs and symptoms associated with the viral syndrome itself, but also has other widespread effects associated with cytokine-mediated inflammatory response and generation of cross-reactive T cells [52]. These effects may lead to allograft injury and/or acute rejection, systemic immunosuppression from the virus, and EBV-associated PTLD [6]. Risk factors for CMV infection/disease include CMV donor-positive/recipient-negative (D+/R-) serostatus pairs, recent treatment for acute rejection, recent completion of prophylactic antiviral therapy, and rabbit anti-thymocyte globulin induction therapy [53, 54]. In CMV D+/R- pairs, there may be an association between the use of CMV prophylaxis and improved graft survival and lower acute rejection rates [55].
Differentiation between CMV infection and CMV disease is important when assessing a patient for CMV. A patient with CMV infection has active viral replication in the blood or other body fluids, but does not necessarily experience systemic signs and symptoms such as malaise, fever, and pancytopenia. Patients with CMV disease, however, most commonly have a viral syndrome with fever or have invasive infection that has affected an organ system, such as colitis, hepatitis, or pneumonitis [56].
CMV serology of the donor and recipient are useful for estimating the recipient’s risk of CMV developing after transplantation, but is not useful for diagnosing CMV infection/disease because seroconversion often does not occur until after symptoms are resolved [10, 53, 57]. Rather, methods that quantify the extent of the CMV infection are necessary to make the diagnosis. Two common methods include CMV antigenemia (stain circulating neutrophils for CMV antigen) and CMV DNA polymerase chain reaction (PCR) (quantitative viral load) [58]. A major limitation of antigenemia is the need for sufficient quantities of neutrophils to perform the test, which is often not possible because of the neutropenia caused by the CMV virus itself. Therefore, the CMV viral load is a key diagnostic tool; trends in viral loads are more valuable than individual levels [57]. Viral load assays vary between laboratories, however, and assay standardization is needed. Another limitation includes the fact that peripheral viral load may be undetectable in patients with invasive CMV disease, particularly when the gastrointestinal tract and lungs are sites of infection. In these cases, biopsy of the infected tissue and/or bronchial alveolar lavage is often necessary to confirm diagnosis [57].
Several strategies have been used to prevent and treat CMV. Some centers routinely provide antiviral prophylaxis (called universal prophylaxis) to patients at risk for CMV (particularly D+/R- pairs), whereas others employ preemptive strategies, in which patients are routinely monitored and receive prophylaxis only if laboratory markers become positive. Each method has benefits and drawbacks. Benefits of universal prophylaxis include preventing both CMV and other herpes viruses and lack of need for intensive monitoring. Drawbacks include the risk of developing ganciclovir-resistant CMV (although a small risk), adverse effects of the medications, the fact that late CMV disease may occur despite early prophylaxis (delayed onset), and the fact that the disease may have atypical features.
For preemptive strategies, benefits include decreasing the use of antivirals and their associated adverse effects and costs. However, the logistically demanding monitoring schedule, requirement for strict compliance to the costly surveillance methods, potential to develop CMV disease before detection, and development of drug resistance are disadvantages of preemptive strategies [57]. CMV-related morbidity is also a significant risk when adherence to monitoring guidelines is poor [59]. Drug resistance can occur if ganciclovir is used in a patient with active viral replication, owing to its poor oral bioavailability. A recent prospective randomized trial of pre-emptive therapy versus valganciclovir prophylaxis in CMV serostatus positive kidney transplant recipients found that both CMV infection and CMV disease were significantly higher in the pre-emptive group, in particular for D+/R+ patients [60]. The general consensus is that the highest risk patients (D+/R-) should receive universal prophylaxis [10, 61].
With the introduction of valganciclovir, a prodrug of ganciclovir with superior oral bioavailability, interest has focused on use of this agent to prevent and treat CMV infection and disease. For outpatients, valganciclovir 900 mg per day or ganciclovir 1000 mg three times per day are commonly used to prevent CMV [10]. Pharmacokinetic studies show that oral valganciclovir administration at 450 mg (given once daily) gives exposure that is equivalent to the standard oral regimen of ganciclovir (1 g administered 3 times a day) [62]. The manufacturer-recommended dose of valganciclovir for CMV prophylaxis is 900 mg/day, and this dose appears to be equivalent in efficacy to oral ganciclovir, with an increased incidence of neutropenia compared with ganciclovir [56]. In several studies, researchers have retrospectively evaluated the efficacy of low-dose valganciclovir (450 mg daily) as prophylaxis for CMV in kidney transplant recipients [63]. An analysis comparing 3 months of standard ganciclovir versus low dose valganciclovir in the prophylaxis of CMV in 129 kidney or pancreas transplant recipients revealed a 14% incidence of CMV disease at 1 year after transplantation (10% noninvasive and 4% invasive) [63]. The incidence was similar between patients receiving ganciclovir and valganciclovir, and risk factors for development of CMV disease included CMV D+/R- serostatus and use of thymoglobulin as part of immunosuppression regimen (incidence 25% in patients receiving thymoglobulin). The same investigators later reported outcomes in 37 kidney or pancreas recipients who received thymoglobulin induction and an extended course (6 months) of CMV prophylaxis with low-dose valganciclovir [64]. The incidence of CMV disease decreased in thymoglobulin-treated patients from 25% to 8% when prophylaxis was extended from 3 months to 6 months.
The duration of CMV prophylaxis also remains controversial; current recommendations suggest a minimum of 3 months of therapy [10]. Several studies have demonstrated a lower incidence of CMV disease after transplantation in patients receiving prophylaxis for 6 months, particularly in patients at highest risk for developing CMV [53, 64-67]. From a pharmacoeconomic perspective, prolonged (200 days vs. 100 days) valganciclovir prophylaxis for high-risk patients (D+/R-) has been shown to be cost-effective [68].
Patients with CMV infection/disease should be treated with IV ganciclovir or oral valganciclovir; IV ganciclovir should be used in severe/life-threatening cases, and when gastrointestinal symptoms (such as diarrhea) may limit absorption of valganciclovir [10]. Ganciclovir (IV) is the gold standard for treatment due to the large body of experience with it and its lack of nephrotoxicity, which limits the use of other antiviral agents such as cidofovir and foscarnet. The treatment dose of 5 mg/kg IV every 12 hours must be adjusted for renal function; this adjustment should be done carefully, as subtherapeutic ganciclovir exposure in the setting of high CMV viral load may promote the development of resistance [57]. Because the bone marrow–suppressive effects of ganciclovir may further compound the neutropenia caused by the CMV virus itself, care should be exercised in adjusting the dose of ganciclovir to avoid these effects. Rather, use of white blood cell growth factors may be preferable in order to avoid the subtherapeutic ganciclovir exposure [57]. At a dose of 900 mg, valganciclovir provides exposure similar to that of 5 mg/kg body weight of IV ganciclovir, and can also be administered twice per day for treatment of active CMV infection [10, 62]. Thus, the cost of treating active CMV infection could be substantially lowered by its potential to treat with oral valganciclovir in the outpatient setting, for mild to moderate cases in patients not experiencing significant gastrointestinal symptoms (ie. diarrhea) [10]. Another key component of managing patients with CMV disease includes careful reduction in immunosuppression, taking into consideration patient and organ-specific factors. CMV immunoglobulin may also have an adjunctive role in treatment of severe CMV disease [10, 57].
Close monitoring of viral load is necessary to assess response to therapy; monitoring should begin 1 week after initiation of therapy and treatment should be continued until the viral load has been undetectable for 1 week [57]. The role of secondary prophylaxis after treatment is not clearly defined. When secondary prophylaxis is employed, viral load should be monitored for potential development of resistance and use of valganciclovir may be preferable owing to its superior bioavailability [57]. CMV disease recurs in approximately 15% to 35% of patients. Recurrence is due to incomplete suppression of CMV rather than the development of resistance. Patients at higher risk for recurrence include D+/R- pairs, multisystem CMV disease, those who receive treatment for acute rejection, patients with high viral loads at the time of initial diagnosis of the infection, and those who had a detectable viral load at the end of therapy for the initial infection [57].
Ganciclovir-resistant strains of CMV have developed in recent years, and are attributed to mutation of the UL97 +/- the UL54 gene(s), with the combined mutations leading to a high-level of ganciclovir resistance [10, 69]. Patients at highest risk for developing ganciclovir-resistant CMV include D+/R- pairs, as well as kidney-pancreas transplant recipients [57]. Utilization of pre-emptive strategies in D+/R- patients has been associated with development of GCV-resistance in more than 10% of patients [70]. Treatment of ganciclovir-resistant strains includes high-dose IV GCV, combination therapy with ganciclovir plus foscarnet, and CMV hyperimmunoglobulin [10, 57]. Increasing the ganciclovir dose (up to 10 mg/kg every 12 hours) with careful monitoring for toxic effects may also be useful in these patients [57]. An algorithm for management of ganciclovir resistance can be found in reference [10].
The adult seroprevalence rate for varicella zoster virus (VZV) in the United States is greater than 90%. Primary varicella infection is a risk for seronegative transplant recipients; adults are more likely to experience severe infection leading to complications such as hepatitis, pneumonitis, and encephalitis. In an analysis of herpes zoster (shingles) infection in the setting of modern immunosuppression, researchers evaluated 869 solid-organ transplants performed between 1994 and 1999, and the incidence of varicella zoster was 7.4% in kidney recipients. Herpes zoster infection occurred at a median of 9.0 months after transplantation and resulted in significant morbidity; 62.7% of cases were within 1 year of transplant. Independent risk factors for infection included induction therapy and antiviral therapy (other than >6 weeks of CMV prophylaxis with acyclovir or ganciclovir) [71].
Cutaneous scarring, defined as skin disfigurement (scarring or hypopigmentation), occurred in 18.7% of patients with herpes zoster, usually following a dermatomal pattern. Postherpetic neuralgia, defined as pain persisting more than 30 days after rash development, occurred in 42.7% of patients [71]. More serious manifestations of VZV infection may include pneumonitis, hepatitis, or encephalitis. This is especially true in primary infections, where morbidity and mortality may be high.
Diagnosis of VZV infection typically involves clinical examination of skin lesions. Viral cultures, direct fluorescent antibody assays, or PCR testing may be used to confirm diagnosis when necessary [72].
CMV prophylaxis with ganciclovir will most likely prevent VZV, although acyclovir is effective for those patients not receiving ganciclovir [72]. Patients who are VZV seronegative before transplantation should be vaccinated against varicella whenever possible, although pre-transplant administration of the herpes zoster vaccine, Zostavax is not recommended at this time due to a higher live-virus content [72]. The varicella vaccine should not be administered to patients receiving immunosuppressants, because the varicella vaccine is a live, attenuated vaccine that may cause infection in immunocompromised patients. After transplantation, seronegative patients exposed to VZV should receive postexposure prophylaxis, although this is not guaranteed to prevent infection. Postexposure prophylaxis consists of varicella zoster immunoglobulin if the patient arrives for treatment within 96 hours of initial exposure (preferred), or antiviral therapy if that 96-hour window has passed. However, the immunoglobulin preparation is no longer widely available to transplant centers, so IVIG may be utilized [72]. Although some centers have reported administration of the varicella vaccine after liver transplantation with minimal adverse effects [73], others have reported development of infection [74]. Therefore, this practice remains controversial and is not supported by existing guidelines [72].
Patients with active, serious VZV infection should be treated with IV acyclovir, whereas less serious infections may be treated with oral acyclovir, valacyclovir, or famciclovir. In rare cases of acyclovir resistance, foscarnet may be used [72].
Adult seroprevalence rates for herpes simplex virus 1 and 2 in the U.S. are 62% and 22%, respectively. Most infections after transplantation are due to reactivation of latent virus.
Infection with herpes simplex virus generally is manifested by orolabial lesions or genital/perianal lesions, although more serious systemic infection can result in esophagitis, hepatitis, or pneumonitis.
Diagnosis of infection with herpes simplex virus 1 or 2 typically involves clinical examination of skin lesions. Culture of scrapings/tissue from lesions may be necessary to confirm diagnosis in some cases, and PCR assays are increasingly being used [75].
CMV prophylaxis with ganciclovir will most likely prevent HSV; acyclovir is effective for those patients not receiving ganciclovir [59]. HSV infections are usually treated with oral acyclovir, valacyclovir, or famciclovir [75]. In more serious infections, IV acyclovir may be employed, although alternative therapy such as foscarnet may be required in cases of acyclovir resistance [75].
Human herpesvirus (HHV) 6 and 7 are viral pathogens that can cause significant morbidity and mortality in transplant recipients. Although HHV 6 infection has been most commonly reported among stem cell transplant recipients, cases have also been reported in solid-organ transplant recipients [76-78]. As with CMV, HHV 6 and 7 appear to have immunomodulatory effects and may predispose patients to secondary infection. Indeed, the mortality associated with HHV 6 appears to be related primarily to the development of secondary fungal infection [77, 78]. HHV 8 is also known as Kaposi sarcoma–associated herpesvirus because development of Kaposi sarcoma is driven by this virus. The seroprevalence of HHV 8 exhibits geographic variation; it is most common in the Mediterranean, Middle East, and some areas of Africa.
Transplant recipients with HHV 6 infection commonly have fever, bone marrow suppression, interstitial pneumonitis, and/or encephalitis. In addition, hepatitis and cutaneous rash have also been found in patients infected with HHV 6. Severe cases may progress to aplastic bone marrow and secondary infection with fungal and/or other viral pathogens. Symptoms associated with HHV 7 are not as well documented. Patients with HHV 8 may have cutaneous lesions, fever, and evidence of bone marrow suppression.
Patients who are HHV 6–negative before transplantation appear to have a higher incidence of infection, although most cases are reactivations because more than 90% of patients are seropositive by adulthood. As with other viral illnesses, quantitative PCR is useful in diagnosis and in monitoring patients with this infection. HHV 8 serostatus of the donor and recipient may be assessed on the basis of geographic location. Patients who are seropositive before transplantation, who are at risk for primary infection, or who have Kaposi sarcoma can then be monitored after transplantation by means of HHV 8 viral loads [79].
Routine prophylaxis for HHV is not recommended [79]. Symptomatic patients may be treated with ganciclovir, foscarnet, or cidofovir, in combination with immunosuppression reduction [79]. For patients with Kaposi sarcoma, reduction and/or withdrawal of immunosuppression is first-line therapy, and conversion from calcineurin inhibitor therapy to sirolimus is also recommended due to regression of KS lesions after conversion [79]. Surgery, irradiation, and chemotherapy may be required in patients who do not respond to the reduction in immunosuppression.
EBV is a herpesvirus that infects most people at a young age and causes infectious mononucleosis. In immunocompromised patients, primary EBV infection or reactivation of latent infection can cause PTLD, a feared consequence of immunosuppressive therapy. Risk factors for the development of early PTLD include EBV seronegativity at the time of transplantation (leaving children at higher risk than adults), type of organ transplanted, type and degree of immunosuppression, CMV donor/recipient mismatch, CMV disease, and lymphocyte depleting antibody induction, while late PTLD may be related to duration of immunosuppression, type of organ transplanted, and older age of the recipient [80]. Kidney transplant recipients are considered low risk for development of PTLD (~1%). PTLD affects the transplant allograft in approximately 30% of cases. Lesions in the central nervous system are the most difficult to treat. In general, early occurrence of PTLD is polyclonal and easier to treat, whereas late PTLD is often monoclonal, and infected B cells may lose CD20 expression, making treatment difficult.
Signs and symptoms of PTLD may include those of a primary EBV infection/infectious mononucleosis, specifically fever, malaise, and swollen lymph nodes in the neck, tonsils, axilla, and/or groin. In addition, patients may have other nonspecific symptoms, depending on the type of organ transplanted.
Diagnosis of PTLD is a combination of clinical assessment, blood tests, EBV-related blood tests, radiographic imaging, histology, and other adjunctive tests [80]. Pathological examination of tissue is the gold standard for the diagnosis of PTLD; excisional biopsies are preferred over needle biopsies. No specific staging system exists for PTLD; however, the current recommendation is to use the Ann Arbor staging classification system with Cotswold’s modifications, which is used to stage non-Hodgkin lymphoma. Diagnosis is based on morphological classification, origin cell type, presence of EBV, and presence of CD20+ cells [80, 81].
Because no definitive methods to prevent PTLD are known, diligent monitoring of high-risk patients is needed; this is done by performing serial EBV PCR. Risk is defined as high in D+/R- pairs, children, and patients receiving high dose and/or intensity immunosuppression [80, 81]. Utilization of ganciclovir/valganciclovir for CMV prophylaxis may give some protection, as ganciclovir has greater in vitro activity against EBV than acyclovir.
Unfortunately, controlled trials in the treatment of PTLD are generally lacking. Key strategies for the management of patients with PTLD include reduction in immunosuppression, surgical resection, and local irradiation [80]. Secondary treatments may include antivirals, immunoglobulin, and monoclonal antibodies against B cells [80]. Anti-CD20 antibody (rituximab) is promising as first-line therapy after immunosuppression reduction because of its high specificity for B cells with a low adverse event profile. Cytotoxic chemotherapy (such as CHOP) is often used when first- and second-line therapies fail. Patients with CNS lesions may be treated with local radiotherapy, intrathecal anti-CD20 antibody, and/or interferon α [80]. EBV-specific cytotoxic T lymphocytes (CTL) may also have a role in the treatment of PTLD [82]. Patients may receive another transplant after successful treatment of PTLD; however, careful examination of patient-specific factors must occur.
A concern mostly in children, adenovirus is a virus with many different serotypes that may cause diverse signs and symptoms during acute illness. Adenovirus is transmitted through respiratory secretions, fecal-oral route, and fomites; donor transmission has also been postulated in several reported cases. Adenovirus infection may occur in transplant recipients of any age; however, complications occur more commonly, and infections may be more severe in children [83].
Symptomatic disease can vary greatly, ranging from self-limiting febrile illness, to hemorrhagic cystitis or gastroenteritis, to severe infection with necrotizing hepatitis or pneumonia.
The gold standard for diagnosis of adenovirus is by culture or antigen detection. In patients with invasive disease, tissue specimens can be examined for histology (“smudge cells” signaling cytopathic inclusions; the gold standard) or adenovirus PCR may be performed on the specimen [83].
No specific preventative measure is available, other than avoiding the spread of the virus via droplet and contact precautions for infected patients [83]. Supportive care, in conjunction with a decrease in immunosuppression is the standard of care for these patients. The use of antiviral agents such as ribavirin, ganciclovir, cidofovir, and respiratory syncytial virus immunoglobulin have been reported [83]. Cidofovir has the best data supporting its use, however its nephrotoxicity is an important concern in renal transplant recipients [83].
By adulthood, 30% to 60% of people are seropositive for parvovirus B19, an infection that usually is asymptomatic or manifests as a mild illness called erythema infectiosum in school-aged children and is commonly acquired through infected respiratory secretions. Parvovirus infects erythroid precursor cells, causing areticulocytic anemia in patients with severe infection.
Parvovirus infection develops in approximately 1% to 2% of transplant recipients, resulting in a pure red cell aplasia with a low or absent reticulocyte count. Other manifestations of the infection may include fever, arthralgia, rash, pancytopenia, and hepatitis.
In transplant recipients, parvovirus B19 immunoglobulin M is a marker for ongoing infection, and parvovirus B19 DNA PCR may also be useful. Both have limitations, however, because transplant recipients may not be able to mount a response, making the serologic findings a less than ideal marker, whereas PCR may remain positive for up to 9 months after the initial infection. Therefore, the best diagnostic tool appears to be a positive PCR in a patient with pure red cell aplasia. Bone marrow biopsy may be considered for patients with signs and symptoms but negative serology and PCR [84].
No strategies are available to prevent parvovirus B19 infection in transplant recipients, although a vaccine is being developed [84]. The treatment of choice for parvovirus B19 infection is IVIG, although the optimal dosing regimen and duration of therapy are not clear. Current guidelines recommend 400 mg/kg/day for 5 days, possibly in conjunction with immunosuppression reduction [84].
Patients with human papillomavirus (HPV) infection have an increased risk of cervical intraepithelial neoplasia (CIN) and cervical cancer, as well as risk for squamous cell cancers (SCC) of the anus, vulva, vagina, and penis [85]. The role of HPV in skin and oropharyngeal SCC is less clear [85]. The virus, in combination with exposure to ultraviolet radiation and the degree and length of immunosuppression are important factors in the development of cutaneous lesions. Viral warts may progress to these cancers in immunocompromised patients, with HPV DNA being found in 70% to 90% of cutaneous tissue in patients with SCC. Many strains of HPV exist, with HPV 5 and HPV 8 appearing to have a higher prevalence in transplant recipients with skin cancers.
Infected patients have cutaneous and anogenital warts (verruca vulgaris). Although less common, HPV may also be manifest as a respiratory tract infection.
Diagnosis is made by examination of cutaneous warts during physical examination. Warts that look suspicious (eg, discolored) should be sampled by biopsy because of the known risk of malignant transformation of these lesions. In addition, suspicious anogenital warts should also be sampled, particularly as these lesions may be clinically indistinguishable from squamous epithelial lesions. Renal transplant candidates and recipients should have a pap smear yearly due to the increased risk of cervical cancer in this population [85]. HPV viral load by PCR is also utilized on clinical specimens.
Patients with preexisting lesions should receive treatment before transplantation. An HPV vaccine has been developed, although its role prior to transplantation remains to be determined. Currently, it is recommended for use pre-transplant in the FDA-approved patient populations [85]. After transplantation, high-risk patients (those with a history of warts, keratoses, skin cancer, or long-term immunosuppression) should be followed up by a dermatologist every 3 to 6 months. Patients must be educated to avoid excessive sun exposure, to wear protective clothing when in the sun, and to use sunscreen to protect them. For those patients (or their partners) with anogenital lesions, sexual transmission should be avoided by abstinence or condoms (although condoms do not provide complete protection).
It is recommended that warts causing physical and/or psychological signs or symptoms be treated with cytotoxic agents that destroy the infected epidermis, such as salicylic acid, lactic acid, or cryotherapy. In addition, surgical removal and physical ablation are often employed; a more rare treatment includes stimulation of the local immune response in the infected area [85].
Polyomavirus nephropathy (PVN) is a significant cause of morbidity and graft loss in renal transplant recipients, and is described in great detail in another chapter of this textbook.
Chronic hepatitis B virus (HBV) infection was traditionally considered a risk factor for poorer patient and graft survival after kidney transplantation [86]. In the more recent era, which is distinguished by the availability of oral anti-viral agents, analysis of OPTN/UNOS data has shown equivalent patient and graft survival in HBV(+) versus HBV(-) kidney transplant recipients [87]. The risk of liver failure does, however, continue to be increased in HBV(+) patients [87].
HBV(+) patients on anti-viral therapy should be monitored every three months after transplantation, specifically for viral load (HBV DNA) and ALT, both to monitor efficacy as well as assess for development of resistance [88]. In addition, those with cirrhosis should be monitored yearly for development of hepatocellular carcinoma (HCC) via hepatic ultrasound and alpha fetoprotein [88].
All patients should be vaccinated against HBV, preferably before beginning dialysis due to poorer immune response to the vaccine in dialysis and transplant patients [89]. Re-vaccination should occur when hepatitis B surface antibody titers fall below 10 mIU/mL [88]. Utilization of nucleoside or nucleotide analogues to suppress HBV viral load in HBV-infected kidney transplant recipients has led to reduction in mortality, although development of hepatocellular carcinoma still exists and requires routine monitoring [90]. All HBV surface antigen positive transplant recipients should receive prophylaxis with tenofovir, entecavir, or lamivudine, although concerns over lamivudine resistance limit its use [88]. Use of interferon therapy after transplant is not recommended due to risk of precipitating rejection [88].
Hepatitis C is the leading indication for liver transplantation in the United States, and up to 38% of kidney transplant recipients worldwide have hepatitis C infection [91]. Hepatitis C infection is associated with poorer patient and graft survival after kidney transplantation as compared to Hepatitis C(-) patients, however, outcome after transplant is better than remaining on dialysis [92]. As with hepatitis B, it is important to clear the virus or decrease viral load before transplantation due to risk of rejection with post-transplant interferon.
After transplant, the ALT of HCV(+) patients should be monitored monthly for 6 months, and then every 3 to 6 months thereafter [88].
Use of interferon therapy after kidney transplantation is not recommended due to risk of precipitating rejection, and should be used only when benefit clearly outweighs the risk of rejection [88]. This may include patients with fibrosing cholestatic hepatitis or life-threatening vasculitis. The use of newer oral agents for hepatitis C (including telaprevir and boceprevir) is contraindicated in transplant recipients due to lack of research studies [93]. Pharmacokinetic studies conducted in healthy volunteers have demonstrated significant drug interactions between telaprevir and cyclosporine or tacrolimus, which could lead to life-threatening toxicity [93, 94].
Based on the limited number of cases of WNV infection in transplant recipients, it appears that delayed seroconversion due to immunosuppression may occur, leading to delayed diagnosis. Other diagnostic methods such as PCR may be used, although that method is not useful in all patients [99]. Transplant recipients should be educated about the risks of WNV infection, particularly in endemic areas. Patients should be encouraged to use insect repellant and to avoid the outdoors during the periods of dawn and dusk, when mosquitoes are most active. Treatment of WMV in recipients of solid-organ transplants has generally been empiric and supportive. Both interferon and ribavirin have in vitro activity against WNV, but available data are not sufficient to associate use of these agents with clinical outcome. In addition, IVIG may be useful. Reduction or discontinuation of immunosuppression, based on the clinical situation, is most likely important adjunct treatment.
Because of the likelihood of poor response to vaccines after transplantation due to inability to mount an optimal effective response, it is very important to have all vaccinations up to date before transplantation, and to carefully consider timing of administration in the post-transplant period [104]. Influenza (inactivated) and pneumococcal vaccines should be given at their recommended schedules after transplantation, in order to confer as much protection to the patient as possible [105]. Household contacts of transplant patients should also receive the inactivated influenza vaccine on an annual basis. Live vaccines should be avoided in transplant recipients, however their household contacts may receive live vaccines if necessary, with the exception of smallpox and oral-poliovirus vaccines [105]. More details about vaccination can be found in other chapters within this book.
Reactivation of latent parasitic infection in previously infected patients or de novo infection by natural means or through the donated organs is of increasing concern in the transplant community. Multiple factors are contributing to increased incidence, including the presence of transplant centers in endemic areas, donor and/or recipient travel from endemic areas to Western countries for transplant, transplant tourism, immigrants with latent infection, leisure travel by recipients, and use of non-cyclosporine based immune regimens [106]. Parasitic diseases affecting transplant recipients are outlined in Table 1.
Protozoa: Non-Intestinal | Toxoplasmosis ( | Brain abscess, chorioretinitis, pneumonitis, disseminated disease | PJP prophylaxis with TMP/SMX covers Toxoplasmosis |
Chagas Disease | Panniculitis or other subcutaneous involvement; myocarditis and encephalitis less common | Donors from indiginous areas should be tested | |
(Old World and New World) | Visceral: fever, enlarged spleen, pancytopenia, malabsorption, interstitial pneumonitis | Mortality usually related to bacterial superinfection | |
Malaria ( | Fever, hemolysis, thrombocytopenia | Identification of species important for treatment due to resistance patterns | |
Babesiosis (Babesia species) | Fever, malaise, hemolytic anemia, possible adult respiratory distress syndrome | May be difficult to distinguish babesiosis from malaria; morphology and DNA testing used to distinguish | |
Keratitis, granulomatous amoebic encephalitis, pulmonary lesions, cutaneous lesions, sinusitis, disseminated disease | Biopsy diagnosis of cutaneous lesions and cerebrospinal fluid examination essential for diagnosis | ||
Protozoa: Intestinal | Gastroenteritis, eosinophilia | Difficult to eradicate; reduction in immunosuppression may be important in clearing infection. Reduce risk by drinking only municipal or bottled water | |
Amebic colitis, liver abscess; less commonly pulmonary, cardiac, brain involvement | Reduce risk by drinking only municipal or bottled water | ||
Pulmonary involvement, bacterial sepsis/meningitis (Gram negative GI organisms), acute, severe abdominal disease, eosinophilia | Difficult to eradicate; high mortality with disseminated infection | ||
Schistosomiasis ( | Abdominal pain, anorexia, diarrhea; hematuria, dysuria, urinary frequency; fibrosis of liver or bladder and ureters | Reduce risk by avoiding fresh water in endemic regions | |
Echinococcosis | Liver failure; possible extrahepatic involvement in lungs, brain | May be difficult to distinguish from hepatic malignancy |
Parasitic diseases affecting transplant recipients
There are a number of clinically significant drug interactions and toxicities that must be considered when treating infection in the transplant population (see Table 2). Drug levels of several of the primary immunosuppressants must therefore be monitored frequently and dose adjustment is needed to achieve the desired level of the immunosuppressant [107]. This is important to remember both when initiating and discontinuing therapy.
Azole Antifungals (systemic) | Increase levels of cyclosporine, tacrolimus, sirolimus and everolimus via Cytochrome P450 3A4 inhibition | Empiric dose adjustment of immunosuppressant is recommended when initiating azole therapy |
Clotrimazole (topical) [108, 109] | Increase levels of tacrolimus (and possibly others) via Cytochrome P450 3A4 inhibition in the gut | Dose adjustment often necessary |
Amphotericin B | Enhanced nephrotoxicity | When therapy needed for invasive fungal infection, liposomal formulations preferred to reduce risk of nephrotoxicity |
Aminoglycosides | Enhanced nephrotoxicity | Avoid when possible |
Macrolide antibiotics | Increase levels of cyclosporine, tacrolimus, sirolimus and everolimus via Cytochrome P450 3A4 inhibition Effect most pronounced with erythromycin and clarithromycin; more rare with azithromycin | Empiric dose adjustment of immunosuppressant is recommended when initiating macrolide therapy, particularly erythromycin or clarithromycin |
Rifamycins | Decrease levels of cyclosporine, tacrolimus, sirolimus and everolimus via Cytochrome P450 3A4 induction | Empiric dose adjustment of immunosuppressant is recommended when initiating rifamycin therapy |
Ganciclovir, Valganciclovir | Enhanced bone marrow suppression | Monitor WBC and platelet counts |
Foscarnet, Cidofovir | Enhanced nephrotoxicity | Avoid when possible |
Important Drug Interactions and Toxicities with Anti-Infective Agents and Immunosuppressants
The net state of immunosuppression also affects the development of post-transplant malignancy. This includes not only
Non-melanoma skin cancers are the most common malignancy seen in the organ transplant population, and the incidence of these cancers is 3 to 5 times that of the general population. Although both basal (BCC) and squamous cell carcinoma (SCC) occur, SCC tends to occur more frequently in transplant recipients, as compared to a predominance of BCC in the general population. Both SCC and BCC occur at a younger age when compared to the general population. In addition, SCC tends to be more aggressive in transplant recipients as compared to the course in the general population [110]. This includes an increased number of primary tumors, deep tissue spread, perineural and lymphatic invasion, recurrence, and need for radiation or chemotherapy [110]. Guidelines for the management of transplant patients with SCC were published in 2004 [111]. Recurrent, de novo and donor-transmitted melanoma are also a concern in transplant recipients [112]. Guidelines for proposed reduction in immunosuppression for transplant patients with skin cancers are available [113].
Renal cell carcinoma (RCC) of the native kidney(s) is diagnosed in 0.3% to 4.8% of kidney transplant recipients [114, 115], and in the transplant kidney in approximately 0.2% [116]. Patients with pre-transplant cystic lesions are more likely to develop RCC by three years after transplant compared to those without (2.3% vs. 0.7%, respectively) [115]. Risk factors for developing RCC after transplant have included pre-transplant cystic disease/lesions, male gender, African-American race, older recipients (> 65 years at transplant), longer time on dialysis prior to transplant, older donor age (> 55 years), and treatment of acute rejection within 1 year of transplant [114, 115]. Most cases of RCC have papillary or clear cell histology, and RCC in one kidney is associated with RCC in the contralateral native kidney. Most cases are diagnosed incidentally, are low-grade, and are managed by native nephrectomy. More aggressive tumors may require chemotherapy, minimization or change in immunosuppression, and/or radiation. Interestingly, the mTOR inhibitor everolimus is FDA-approved as second line therapy for advanced RCC, and thus may be a preferred immunosuppressant in this setting.
Historically, post-transplant lymphoproliferative disorder (PTLD) has been a major concern for solid organ transplant recipients. A recent analysis of Scientific Registry of Transplant Recipients (SRTR) data for 156,740 kidney transplant recipients found an incidence of 0.7% at 5 years and 1.4% at 10 years [117]. This analysis, similar to prior reports, showed a clear distinction between early (less than 2 years after transplant) and late-onset (more than 2 years) PTLD. Risk factors for early PTLD on multivariate analysis include age 19 or younger at transplant, non-Hispanic white ethnicity, EBV negative serostatus at transplant, and CMV negative serostatus at transplant, while risk factors for late PTLD include age 19 or younger or 50 years or older at transplant and non-Hispanic white ethnicity. The use of induction therapy, including when the analysis was limited to T cell depleting agents, did not increase the risk of PTLD. In addition to PTLD, elderly transplant recipients are at increased risk for various hematologic malignancies [118]. Treatment of PTLD may include reduction in immunosuppression, surgery, anti-viral therapy, chemotherapy (including immunochemotherapy (rituximab)), and/or radiation.
Epstein Barr Virus (EBV) | Non-Hodgkin Lymphoma, Hodgkin Lymphoma, PTLD, Nasopharyngeal |
Human Papillomavirus | Cervix, Vulva, Vagina, Penis, Anus, Oropharynx |
Hepatitis B and Hepatitis C | Liver |
Human Herpesvirus 8 (HHV8) | Kaposi sarcoma |
Helicobacter pylori | Stomach |
Oncogenic Infectious Agents
In summary, complications of over-immunosuppression after solid-organ transplantation can lead to significant morbidity and mortality if not promptly diagnosed and treated. However, the growing armamentarium of knowledge, diagnostic tools and therapeutic agents available for the prevention and treatment of these infections and malignancies will continue to improve the quality of care for these patients.
Intercellular communication is essential to homeostasis and is largely dependent on the cellular secretome [1]. An emerging awareness of the role that the extracellular environment plays is evident in the field of secreted vesicles. The vesicular contribution to the tumor microenvironment (TME) has furthered our understanding of the communication between cells and the surrounding stroma [2]. This relationship has also elucidated many potential therapeutic targets and possible transporters of chemotherapeutics [3, 4]. There are multiple extracellular vesicle types, characterized by biogenesis, size, and common protein markers [5, 6]. Of these, exosomes are the smallest, with sizes ranging from 30 to 150 nm [6]. These vesicles have the most complex synthesis, emerging from the endocytic pathway. They arise from intraluminal invaginations into a multivesicular body (MVB) and are released from the cell when the MVB fuses with the plasma membrane. Exosomes consist of intracellular material surrounded by a lipid membrane that reflects the cellular membrane of the host cell [7]. These specific vesicles have demonstrated promise in several fields of research, including rheumatoid arthritis [8, 9] and neurodegenerative disease [10], but primarily in cancer [11, 12]. Tumor-derived exosomes (TEX) contain oncoproteins and oncogenes from the cell of origin and thus are very influential in intercellular communication. Numerous studies have used these luminal proteins and genes to better understand tumor growth and metastasis, as well as for improving diagnostic, prognostic, and therapeutic methods [13, 14].
\nWhile there has been an exponential growth in research focused on exosome biology, clarification on the mechanisms of transport between the cell of origin and the recipient cell is essential to maximizing on exosome potential in treating and diagnosing disease. The methods by which exosomes influence the cells with which they interact are still under review. Some exosomes have been shown to fuse to the recipient cell [15, 16], while others are internalized by specific receptor-ligand interactions [17, 18] or by stimulating an indirect uptake by macropinocytosis [19]. Exosome binding to cells has been seen both as a mechanism of transferring luminal contents [15, 16] and as an initial step in the endocytosis process [17, 20]. The significance of the effects of cell-exosome binding in comparison to internalization is still unknown. Most types of endocytosis have been described in the process of exosome uptake [21], but which factors determine the specific mechanism used, are still unclear. Previous reviews have clearly identified a number of ligands and receptors involved in exosome trafficking [21, 22, 23], but little is known about the dependence of uptake mechanism on cell-type. This review presents the current understanding of the endocytosis process utilized by specific cells involved in exosomal internalization.
\nEndocytosis is a basic cellular function that is performed by all cell types in the process of maintaining homeostasis. Many of the molecules essential for cellular function are small enough to cross the cell membrane either passively or actively, however, other structures, such as exosomes, are too large and require a more complicated process. This general process of internalization is called endocytosis and is separated into various types based on the shape [24] and the size of particles internalized [25]. There are many well-written reviews covering the specifics of the endocytic pathways [25, 26], but here we will address them only superficially. Classification under the umbrella of endocytosis varies, but the major methods include phagocytosis, macropinocytosis, clathrin-mediated endocytosis, caveolin-mediated endocytosis, and clathrin/caveolin-independent or lipid raft-mediated endocytosis [25, 26]. Receptor-mediated endocytosis (RME) is an additional type that is often considered to be a subcategory under several of those previously mentioned (Figure 1).
\nEndocytosis pathways involved in exosome uptake: (A) Phagocytosis, (B) Macropinocytosis, (C) Clathrin-mediated endocytosis, (D) Caveolin-mediated endocytosis, (E) Lipid Raft-dependent or clathrin−/caveolin-independent endocytosis, (F) Receptor-mediated endocytosis.
Phagocytosis is the mechanism by which specialized cells (such as macrophages and monocytes) engulf large particles (>0.5 μm) by way of receptor/ligand interactions [25, 27] (Figure 1A). Promiscuous receptors allow for a broad range of ligand recognition and binding, facilitating a key role phagocytes play in clearing apoptotic cells [27]. Exosomes, derived from a diverse population of cells, present a vast array of available ligands that make phagocytes ideal recipient cells. This process of phagocytosis is designed to not only internalize extracellular material by enveloping it, but also to regulate the immune response by presenting degraded proteins as antigens on the phagocyte surface [25]. Tumor-derived exosomes influence immune involvement in the tumor [28, 29] which may be facilitated by this mechanism of endocytosis. Other non-phagocytic cells, such as epithelial cells, Sertoli, liver endothelial, astrocytes, and cancer cells have also been shown to perform phagocytosis [27], potentially expanding the impact of exosomal communication. It is therefore important to define how the process of phagocytosis influences exosome function and if that influence is cell type dependent.
\nWhile phagocytosis or “cell eating” involves ingestion of large molecules, macropinocytosis (“cell drinking”) internalizes slightly smaller particles (>1 μm) [25] (Figure 1B). This method is a way for cells to sample the external environment without specific receptors or ligands. It is a constitutive process in specialized antigen presenting cells, but is stimulated by growth factors in most others [30]. Macropinocytosis has a unique membrane ruffling process caused by projections from the cell surface encircling extracellular fluid and fusing to the membrane [25], resulting in an increased membrane surface area and volume of engulfed material. Nakase et al., showed that stimulation of the epidermal growth factor (EGF) receptor, either by soluble EGF or exosome-bound, increased exosome internalization 27-fold through the activation of macropinocytosis [19].
\nThe next three mechanisms, clathrin-dependent, caveolae-dependent, and clathrin/caveolae-independent, are facilitated by specific membrane proteins/structures: clathrin, caveolae, and lipid rafts. Clathrin is an intracellular protein that forms a coat around an invaginating vesicle facilitating formation and internalization [31] (Figure 1C). These vesicles internalize material around 120 nm [25], which is within the exosome size range. Stimulation can occur through receptor/ligand mediation or can be constitutive, depending on cell-type and receptor presence, but clathrin-mediated endocytosis (CME) occurs in all cell types [31]. Data continues to show that the extracellular cargo of these clathrin-coated vesicles can drive the specific mechanisms and protein interactions of internalization [32], giving way for exosome surface proteins to influence uptake. Two proteins used extensively to describe the details of CME are transferrin (Tf) and low density lipoprotein (LDL) and their respective receptors [25], which are all (except LDL) found on the surface of exosomes [33, 34]. Overexpression of transferrin receptors on cancer cells [35] may also contribute to increased exosomal uptake and clathrin-mediated endocytosis in tumors, as there have been shown to be 50–80 percent more receptors on the cancer cell compared to the non-cancer cell [36].
\nCaveolin is similar to clathrin, as it forms a coat around membrane invaginations called caveolae and facilitates the entry of extracellular material (Figure 1D). These are particularly prevalent on endothelial cells but have been found on a wide distribution of cell types [25]. Caveolae are about half the size of clathrin-coated vesicles, limiting their cargo to smaller structures [25] but still covering some of the exosome size range. This type of endocytosis as well as lipid raft-dependent uptake, plays a key role in lipid transport and homeostasis [25]. One of the defining factors of the exosome membrane is its slightly altered lipid profile, which has been shown to influence internalization [37]. Two proteins commonly active in caveolae-dependent endocytosis, which have also been identified on the surface of exosomes, are the insulin receptor and albumin [34, 38, 39]. The cellular insulin receptor itself has also recently been found to influence exosome uptake [18].
\nLipid dependence is not only characteristic of caveolae-dependent endocytosis, but also clathrin/caveolae-independent processes. Lipid raft-dependent (or clathrin/caveolae-independent) endocytosis is similar to caveolae-dependent, except for the absence of the protein cav-1. Lipid rafts are 40-50 nm sections of the membrane with a high percentage of glycosphingolipids and cholesterol, and are anchoring points for many membrane proteins [40]. Lipid rafts are involved in exosome biogenesis and trafficking [41, 42, 43] and exosome uptake has been reduced by blocking lipid raft endocytosis [44] (Figure 1E).
\nAs mentioned previously, RME is an endocytosis pathway that can fit under several of the other categories (Figure 1F). The term and pathway were originally considered to be interchangeable with CME, but it is now understood that not all RME is dependent on clathrin [25]. Receptor-ligand interactions play a role in phagocytosis [25, 27], macropinocytosis [19], and lipid raft-dependent endocytosis [40]. Exosome internalization has been linked to multiple receptor-ligand interactions in each of these pathways [19, 20]. Each subtype of endocytosis has been identified in the exosome internalization process (Table 1) but additional research is needed to determine the driving factors behind the specific mechanisms. One hypothesized factor is that the recipient cell type may determine the specific type of internalization.
\nEndocytosis pathway | \nRecipient cell type | \nRecipient cell line | \nExosome cell of origin | \nReferences | \n
---|---|---|---|---|
Phagocytosis | \nMacrophage | \nRAW264.7 | \nLeukemia cell (K562 or MT4) | \n[20] | \n
\n | Macrophage | \nJ774 | \nRat reticulocyte | \n[52] | \n
\n | Macrophage | \nPrimary | \nTrophoblast (Sw71) | \n[58] | \n
\n | Monocytes | \nPrimary | \nActivated T cell | \n[50] | \n
\n | Macrophage | \nPeritoneal | \nMouse melanoma cell (B16BL6) | \n[51] | \n
\n | Macrophage | \nMouse bone marrow-derived | \nMouse CRC (CT-26) | \n[54] | \n
\n | Microglia | \nMG6 | \nPheochromocytoma (PC12) | \n[117] | \n
\n | Microglia | \nBV-2 | \nNeuron (N2a) | \n[49] | \n
\n | Dendritic cell | \nMouse primary | \nMouse dendritic cell | \n[15] | \n
\n | Epithelial | \nOvarian cancer (SKOV3) | \nOvarian cancer cell (SKOV3) | \n[97] | \n
\n | Epithelial | \nAlveolar cells (A549) | \nDendritic cell | \n[66] | \n
Macropinocytosis | \nEpithelial | \nCervical cancer (HeLa) | \nEpidermoid carcinoma (A431) | \n[90] | \n
\n | Epithelial | \nEpidermoid carcinoma (A431), Pancreatic carcinoma (MIA PaCa-2) | \nCervical cancer cell (HeLa) | \n[19] | \n
\n | Epithelial | \nOvarian cancer (SKOV3) | \nOvarian cancer cell (SKOV3) | \n[97] | \n
\n | Epithelial | \nBreast cancer (MCF7) | \nNormal breast epithelial cell (MCF-10A)—exosome mimetics | \n[96] | \n
\n | Endothelial | \nCerebral vascular (hCMEC D3) | \nMacrophage (RAW264.7) | \n[89] | \n
\n | Microglia | \nPrimary mouse | \nMouse oligodendrocyte (Oli-neu) | \n[56] | \n
\n | Neuron precursor cell | \nPheochromocytoma (PC12) | \nPheochromocytoma (PC12) | \n[114] | \n
Clathrin-mediated endocytosis | \nEpithelial | \nOvarian cancer (SKOV3) | \nOvarian cancer cell (SKOV3) | \n[97] | \n
\n | Epithelial | \nAlveolar cells (A549) | \nDendritic cell | \n[66] | \n
\n | Epithelial | \nGastric cancer (AGS, MKN1) | \nGastric cancer cell (AGS, MKN1) | \n[94] | \n
\n | Epithelial | \nBreast cancer (MCF7) | \nNormal breast epithelial cell (MCF-10A)—exosome mimetics | \n[96] | \n
\n | Endothelial | \nCerebral vascular endothelial (hCMEC D3) | \nMacrophage (RAW264.7) | \n[89] | \n
\n | Endothelial | \nBrain microvascular endothelial | \nEmbryonic kidney cell (Hek293T) | \n[87] | \n
\n | Neuron | \nCortical mouse neuron | \nOligodendrocyte (Oli-neu) | \n[115] | \n
\n | Neuron precursor cell | \nPheochromocytoma (PC12) | \nPheochromocytoma (PC12) | \n[114] | \n
Caveolin-dependent endocytosis | \nEpithelial | \nCervical cancer (HeLa) | \nEpidermoid carcinoma (A431) | \n[90] | \n
\n | Epithelial | \n(CNE1, HONE1, NU-GC-3, A549) | \nEBV-infected B cells | \n[95] | \n
\n | Epithelial | \nBreast cancer (MCF7) | \nNormal breast epithelial cell (MCF-10A)—exosome mimetics | \n[96] | \n
\n | Endothelial | \nCerebral vascular endothelial (hCMEC D3) | \nMacrophage (RAW264.7) | \n[89] | \n
\n | Endothelial | \nBrain microvascular endothelial | \nEmbryonic kidney cell (Hek293T) | \n[87] | \n
Lipid raft-dependent endocytosis | \nDendritic cell | \nMouse primary | \nMouse dendritic cell | \n[15] | \n
\n | Dendritic cell (DC), T cell | \nMonocyte derived primary DC, T cell (Jurkat) | \nT cell (Jurkat) | \n[75] | \n
\n | Epithelial, endothelial | \nGlioblastoma (U87), umbilical vein endothelial (HUVEC) | \nGlioblastoma (U87) | \n[43] | \n
\n | Epithelial | \nOvarian cancer (SKOV3) | \nOvarian cancer cell (SKOV3) | \n[97] | \n
\n | Epithelial | \nBreast carcinoma (BT549) | \nBreast carcinoma (BT549) | \n[44] | \n
\n | Epithelial, macrophage, endothelial | \nMelanoma (A375), (RAW264.7), dermal microvascular endothelial (HMVEC) | \nMelanoma (A375) | \n[46] | \n
\n | Endothelial | \nBrain microvascular endothelial | \nEmbryonic kidney cell (Hek293T) | \n[87] | \n
\n | B cell | \nMantle cell lymphoma (Jeko1) | \nMantle cell lymphoma (Jeko1) | \n[61] | \n
Endocytosis pathways involved in exosome internalization in various cell types.
As introduced previously, some cells are uniquely designed to internalize extracellular material through phagocytosis. Those cells generally considered “professional” phagocytes are monocytes, macrophages, and neutrophils [25] with dendritic cells, osteoclasts, and eosinophils occasionally included [27]. Phagocytosis is dependent on receptor/ligand interactions, relying on a vast array of different receptors and ligands. Some of the established receptors include Fc receptors, integrins, pattern-recognition receptors, phosphatidylserine (PS) receptors, and scavenger receptors [45]. Macrophage uptake of exosomes has been shown to involve many of these receptors including scavenger receptors [46, 47, 48], PS/PS receptors [20, 48, 49, 50, 51], lectins [17, 52, 53] and Fc receptors [54].
\nHowever, internalization of extracellular material by phagocytes does not always fit perfectly with the hallmarks of phagocytosis. Some phagocytic receptors, such as integrins (αvβ3), scavenger receptors (CD68 and CD36), and CD14, facilitate the tethering of apoptotic cells to the phagocyte surface, but then are unable to initiate internalization without other means, such as PS and PS receptor binding [55]. The PS/PS receptor interaction also stimulates membrane ruffling and vacuole appearance—classic hallmarks of macropinocytosis [55]. Phagocytes are primarily involved in phagocytosis, but this evidence supports the idea that multiple modes of endocytosis are operational in the same cell. This is not unique to apoptotic cell uptake, but has been seen with exosome internalization by microglia (phagocytic cells in the brain) exhibiting a dependence on PS in a macropinocytic manner [49, 56]. Cooperation between multiple receptors appears to be an important characteristic of endocytosis in phagocytic cells. Plebenak et al., showed that the scavenger receptor SR-B1 on macrophages, when blocked, reduces exosome uptake, but with further testing on melanoma cells this blocking was dependent both on the receptor as well as on cholesterol flux in the lipid rafts [46], broadening the endocytosis landscape of phagocytes to include lipid raft-dependent endocytosis.
\nThe dependence of phagocytosis on extracellular- facing PS, which on healthy cells is expressed only on the cytosolic side of the membrane, is evidence that the material to be ingested influences the endocytic pathway of phagocytes. Further support of this interaction is found in the hypothesis that exosomes “target” specific recipient cells [48, 57]. Macrophage uptake (Figure 2A) of TEX is dependent on the presence of cellular scavenger receptors or exosomal PS [20, 46, 48, 51, 56], while non-tumor cell-derived exosomes require the presence of a heterogeneity of receptors. When internalized by macrophages and monocytes, hepatic stellate cell-derived exosomes require Fc receptors [54]; B cell, dendritic cell and reticulocyte-derived exosomes use lectins [52, 53]; trophoblast-derived exosomes bind to integrins [58]; and T cell-derived exosomes need scavenger receptors [50] (Table 2). Costa-Silva et al., showed that when comparing TEX to normal cell-derived exosomes, Kupffer cells, liver-specific macrophages, preferentially internalized TEX [57]. The significance of the exosome surface topography is therefore influential in directing a specific endocytosis pathway. Phagocytes are responsible for internalization of extracellular material and are so named based on the primary use of phagocytosis, but as seen above, other endocytic pathways are utilized, especially in the context of exosomal internalization.
\nCell-specific internalization of exosomes by antigen presenting cells: (A) macrophage, (B) B cell and (C) Dendritic cells each employ multiple endocytic pathways in the uptake of exosomes. Macrophages utilize multiple endocytic pathways in the uptake of exosomes. B Cells and dendritic cells (DC) both employ multiple endocytic pathways in the uptake of exsomes. Lipid rafts, integrins and adhesion molecules are used by B cells while tetraspanins and adhesion molecules are the more common receptors found in DC-exosome interactions. Intercellular adhesion molecule 1 (ICAM-1), Dendritic Cell-Specific Intercellular adhesion molecule-3-Grabbing Non-integrin (DC-SIGN).
Protein | \nCell type | \nExosome origin | \nReferences | \n
---|---|---|---|
Scavenger receptor | \nMacrophage | \nHek293 (embryonic kidney cells) | \n[47] | \n
Phosphatidylserine (PS) | \nMacrophage, microglia | \nNeuron, melanoma, oligodendrocytes | \n[49, 50, 51, 56] | \n
PS receptor | \nMacrophage | \nActivated T cells | \n[50] | \n
TIM4 | \nMacrophage | \nK562, MT4 (leukemia cell lines) | \n[20] | \n
Lectins | \nLymph node cells, splenic cells, pancreatic adenocarcinoma, lung fibroblast, macrophage, dendritic cell, hCMEC/D3(brain endothelial cells), platelet, HeLa | \nPancreatic adenocarcinoma, reticulocyte, B cell, macrophage, mesenchymal stem cell | \n[17, 48, 52, 53, 65, 89, 72, 103] | \n
Fc receptors | \nMacrophage | \nCT26 (colon carcinoma cells) | \n[54] | \n
Integrins | \nMacrophage, B cell | \nTrophoblast, pancreatic adenocarcinoma cells | \n[17, 58] | \n
Tetraspanins | \nB cell, pancreatic adenocarcinoma, endothelial cell | \nPancreatic adenocarcinoma cells | \n[17, 48, 106] | \n
EGFR | \nA431 (epidermoid carcinoma cells) | \nHeLa cells | \n[19] | \n
CD11c | \nLymph node cells/splenic cells | \nPancreatic adenocarcinoma cells | \n[17] | \n
CD11b | \nLymph node cells/splenic cells | \nPancreatic adenocarcinoma cells | \n[17] | \n
CD44 | \nLymph node cells/splenic cells | \nPancreatic adenocarcinoma cells | \n[17] | \n
CD49d/CD106 | \nLymph node cells/splenic cells | \nPancreatic adenocarcinoma cells | \n[17] | \n
Tspan8 | \nEndothelial cell | \nPancreatic adenocarcinoma cells | \n[48, 106] | \n
ICAM-1/LFA-1 | \nDendritic cell, hCMEC/D3 (brain endothelial cells), aortic endothelium, HUVEC | \nDendritic cells, pancreatic adenocarcinoma cells, T cells, macrophage | \n[16, 17, 37, 65, 69, 89] | \n
DC-SIGN | \nDendritic cell | \nBreast milk | \n[70] | \n
HSPG | \nU87 (glioblastoma cells), CAG (myeloma), HUVEC, SW780 (bladder cancer cells) | \nU-87 cells, myeloma cells, SW780 cells | \n[63, 99, 100, 101] | \n
Cad-11 | \nPC3-mm2 (prostate cancer cells) | \nOsteoblasts | \n[104] | \n
Syncytin | \nChoriocarcinoma cells | \nTrophoblasts | \n[105] | \n
SNAP 25 | \nNeuron | \nMesenchymal stromal cells | \n[116] | \n
CD62L | \nLymph node cells, splenic cells, pancreatic adenocarcinoma, lung fibroblasts | \nPancreatic adenocarcinoma | \n[17, 48] | \n
Galectin 5 | \nMacrophage | \nReticulocyte | \n[52] | \n
CD169/ α2,3-linked sialic acid | \nLymph node cells, splenic cells | \nB cell | \n[53] | \n
C-type lectin/C-type lectin receptor | \nDendritic cell, brain endothelial cell (hCMEC/D3) | \nMacrophage | \n[65, 89] | \n
P-selectin/PSGL-1 | \nPlatelet | \nMacrophage | \n[72] | \n
Proteins involved in exosomal uptake.
The antigen presenting cells (APCs) include primary phagocytes such as macrophages, but also B cells and dendritic cells [59]. The immune response is heavily dependent on the recognition of foreign structures, such as peptides, for activation. These APCs sample the extracellular environment, digest and display peptides on their surface, and then present these peptides to immune cells that can execute the response. The intercellular trafficking of immune regulating proteins, such as the major histocompatibility complexes (MHC) [28], by exosomes has the potential to either stimulate or block the immune response, dependent on the exosomal contents [17]. Uptake of exosomes plays an important role in B cell and DC cell proliferation, protein presentation, and interactions with other immune cells [17].
\nB cells perform multiple functions as an immune cell, including presenting antigens to T cells in order to stimulate additional immune responses. B cells traditionally operate though clathrin-mediated endocytosis, relying heavily on the B-cell receptor [60]. However, when it comes to exosome internalization, B cells have shown a greater dependence on lipid rafts and various receptors, such as adhesion molecules and tetraspanins [17] than on clathrin, indicating a preference for clathrin-independent and receptor-mediated endocytosis (Figure 2B). In analyzing B cell uptake of exosomes, using the mantle cell lymphoma (mutated immature B cell) cell line, Jeko-1, Hazan-Halevy et al., found dynamin, epidermal growth factor receptor (EGFR), and cholesterol to be involved in exosome internalization instead of clathrin [61]. EGFR is a well-established target in cancer therapy, particularly with lung cancer [62] and its role in exosome internalization may lend clarity and power to multiple existing and future chemotherapeutics. Additional exosomal surface proteins, with receptor functions, have been identified as participants in B cell internalization of TEX, including integrins (CD49) and cell adhesion molecules (intercellular adhesion molecule 1—ICAM-1/CD54 and CD62L) [17].
\nThese protein interactions between the cell and the exosomal membranes are essential steps in the influence the exosome has on the recipient cell. Exosomes derived from myeloma cells, cancerous plasma (mature B) cells, are dependent on the interaction between exosomal fibronectin and cellular heparan sulfate in order to form a bond between cell and exosome, resulting in modification of intracellular signaling [63]. As seen with these cells, the effects caused by the exosomes are not entirely dependent on uptake, even though the standard operation of APCs requires internalization. Some exosome-cell binding (as opposed to internalization) may be sufficient, or specifically designed, to alter intracellular processes, including signaling, as is also seen with dendritic cell-derived exosomes and T cell function [16]. While the influence of heparan sulfate on internalization in B cells is still unclear, there is evidence linking heparan sulfate proteoglycans to exosomal internalization which indicates that while it wasn’t assessed in these cells, the uptake may still be present [21, 22, 23]. Whether these differing mechanisms and protein participants of uptake in the B cell population are dependent on normal versus oncologic physiology of recipient cells, or on the origin of the exosome population (tumor-derived versus non-tumor derived) is yet to be determined.
\nThese heterogeneous protein profiles are specific to each cell type and contribute to the comparative ability of each cell to internalize exosomes. In line with the role of B cells, it was found that they readily take in exosomes, in contrast to other immune cells such as T cells and natural killer cells [61, 64]. This suggests that certain immune cells are more effective at endocytosing exosomes than others, consistent with the primary functions of these specific cell types. Additional groups have shown that while B cells internalize exosomes, the uptake is significantly less than that of macrophages and dendritic cells, but similar to T cells [17]. This was shown in non-mutated mouse cells and may also illustrate important differences between cancer cell and normal cell internalization mechanisms.
\nDendritic cells (DC) can be classified as both APCs and as phagocytes since internalization of extracellular material is a crucial part of their role in the immune system. Endocytosis pathways involved in exosome uptake in these cells have been tested with various endocytic blockers, including cytochalasin D (inhibits actin polymerization), EDTA (chelates calcium), and decreased temperature (reducing active cellular processes) [15, 37, 65, 66]. As dendritic cells mature, their mode of endocytosis changes; starting first with macropinocytosis, and then in the mature cell, receptor-mediated endocytosis and phagocytosis prevails [67] (Figure 2C). Despite the evidence of phagocytosis in mature DCs, it was demonstrated that immature DCs are more adept at exosomal uptake [37, 68]. Developmental preference for exosome uptake may shed light on why cancer cells, which often have similar profiles to developing cells and are subject to continuous proliferation, are so responsive to modification by exosomes. Also, immature DCs play a role in immunologic tolerance and so are less likely to activate T cells, while mature DCs activate T cell immunity [15]. This down-regulation of the adaptive immune response by immature DCs would be advantageous for tumors and so TEX may specifically target immature DCs, explaining the increase in uptake. While the mechanism is still unknown, dendritic cells are also more likely to take up TEX or DC-derived exosomes than B and T cells, as seen with fluorescent staining
Many of the studies of exosome internalization by DCs have revealed dependence on various adhesion molecules. The ubiquity of these proteins on exosomes, leukocytes, and endothelial cells promotes the non-specific internalization characteristic of DCs. The involvement of ICAM-1 and/or its ligand, lymphocyte function-associated antigen (LFA-1), in DC-exosome interaction has been shown both
In addition to binding to membrane receptors, dendritic cell endocytosis is dependent on lipid rafts and the lipid components of the cell membrane, particularly with viral or bacterial uptake [73, 74]. As viruses and exosomes are similar in size, endocytosis mechanisms are often common between these two structures [22]. Lipid-dependent endocytosis is evident in exosome uptake by DCs as illustrated with DC- and T-cell derived exosomes [15, 75]. While proteins have been the most common structure analyzed in connection with exosomal uptake, the membrane cholesterol concentration of recipient cells [15] as well as the lipid profile of the exosomal membrane [75] both play a role in uptake of exosomes by dendritic cells and need further clarification.
\nIn addition to the previously mentioned cells, two other circulating cells/structures have also been found to endocytose exosomes, platelets and T cells. Platelets are cell fragments involved in blood coagulation that are unique in their formation as they are devoid of a nucleus and some organelles. Despite a reduced intracellular load, they are involved in binding extracellular vesicles. They do so through the interaction of cellular P-selectin and vesicular P-selectin glycoprotein ligand-1 (PSGL-1) as well as PS [72]. Data suggests that binding facilitates fusion of the exosomes to the platelets, transferring of material and enhancing platelet coagulation activity [72]. This speaks to the impact of these exosomes on intracellular communication, both in the variability and specificity of recipient cells, since binding and fusion occurred preferentially in the activated platelets [72] (Figure 3A). The exosomes in this study came from monocytes, suggesting this interaction could be a key player in coagulation at a site of injury.
\nCell-specific internalization of exosomes: (A) Platelet-exosome interactions have been linked to fusion as well as the binding to PSGL-1 and phosphatidylserine, (B) T cell are influenced through their surface interactions with exosomes.
T cells are the effector cells of the immune system and intercellular communication is essential for activation. Endocytosis, while not a primary function of T cells, is important to T cell receptor signaling [76] as well as other functions. Dynamin-dependent endocytosis [76], phagocytosis [77], and RME [78] are some of the mechanisms involved in T cell interaction with its surrounding environment. In relation to exosomes, T cells operate through RME [17, 79, 80] and lipid raft-dependent endocytosis [75]. However, T cells do not always readily uptake exosomes as was found in a comparison with other blood cell types. In a peripheral blood mononuclear cell culture, when uptake by monocytes was blocked, internalization by T-cells increased [47], suggesting that T cell uptake may be an adaptive response to increased exosome concentration. When exosome uptake was compared to multiple splenic leukocytes [15] or peripheral blood leukocytes [64], T cells showed minimal internalization. T cell activity is often regulated by surface interactions with other cells, such as with the T cell receptor and the MHC II/antigen interaction with APCs. Exosomal influence on T cells may therefore operate similarly with surface interaction instead of exosome internalization (Figure 3B). When cultured with DC or DC-derived exosomes, T cells acquired functional surface molecules including MHC II from exosomes through direct exosome interaction with the T cell membrane, while still showing little evidence of internalization [81]. Mouse T cells do not express MHC II and after incubation with these exosomes, this protein was identified on the surface of the T cell, suggesting the binding of exosomes to cellular membranes is sufficient to transfer material, without internalization [81]. Further research into the transfer of material between exosomes and immune cells may elucidate the role exosomes play in immune regulation in the tumor microenvironment. Depending on the cell type involved, exosome-mediated communication and manipulation may not be entirely dependent on endocytosis.
\nEpithelial and endothelial cells are responsible for lining most of the organs, spaces, and blood vessels in the body. They are in a prime position to be exposed to and actively endocytose a wide variety of extracellular material. Due to this broad selection, the specific mechanisms utilized are dependent on the cell subtype as well as the character of the endocytosed material [82, 83, 84]. With such variability, it is no surprise that exosome uptake by epithelial and endothelial cells is just as diverse (Figure 4). Cellular location of these cells is crucial in cancer biology as most of the TEX will be in close proximity to epithelial and endothelial cells either in the circulatory system or during paracrine spread in solid tumors. While there have been many studies on cell-exosome interaction in these cells, there is still much work needed to clearly understand all of the factors that dictate the endocytic mechanism of epithelial and endothelial cells from different tissues.
\nCell-specific internalization of exosomes: (A) epithelial and (B) endothelial cells. Epithelial cells and endothelial cells show the most diversity in exosome uptake of all the cell types. Multiple receptor involved in the internalization process are expressed on both cell types, including tetraspanins, adhesion molecules, and heparan sulfate peptidoglycans (HSPG). Intercellular adhesion molecule 1 (ICAM-1).
A unique finding in exosome studies with epithelial and endothelial cells is the dependence of uptake on intracellular signaling. Svensson et al., discovered that exosome internalization is dependent on the proper functioning of the signaling pathway, ERK1/2-HSP27 [43]. The promotion of endocytosis through intracellular signaling has been shown previously with EGFR-cSrc-ERK1/2 pathways in epithelial cells [85] and the Ras-PI3K pathway with virus uptake by fibroblasts [86]. However, little is known about how these pathways facilitate exosome internalization. The ability of exosomes to cross the blood–brain barrier and be endocytosed by the microvascular endothelial cells in the brain is also dependent on signaling. Tumor necrosis factor (TNFα) signaling, as is seen in stroke models, enhances exosome uptake [87]. Intracellular signaling may provide a regulatory mechanism to control exosome internalization. Some studies described previously have shown that fusion of exosomes to the cell membrane, without endocytosis, can influence intracellular signaling [63], but these are the first to show how intracellular signaling specifically impacts the endocytosis mechanism of exosomes. These results illustrate the complexity of exosome-cell interactions and where additional research is needed. The interdependence of exosome-cell interactions and intracellular signaling are unexplored areas with vast therapeutic potential and are necessary to better understand how extracellular vesicles influence their environment.
\nOther characteristics are influential in directing endocytosis in epithelial cells including vesicle size, lipid profile, and protein profile (Figure 4A). In epithelial cells, particle size dictates entry mechanism with macropinocytosis as one of the pathways operative at a size range that corresponds with exosomes [88]. This pattern is supported by multiple studies where exosome internalization was decreased when key aspects of macropinocytosis were targeted. Macropinocytosis was blocked with an inhibitor of Na+/H+ exchange (which affects Rac1 activation and actin reorganization) in human cerebral microvascular endothelial cells (hCMEC/D3) [89] and HeLa cells, as well as with an inhibitor of phosphoinositide 3-kinase (PI3K) (influences membrane ruffling and macropinosome formation) [19, 90] with concomitant decreases in exosome internalization. Assessing the same pathway but from an activating instead of inhibiting direction, exosome internalization was stimulated by activation of epidermal growth factor receptor (which activates Rac family members) in HeLa cells [19]. Membrane extensions, or filopodia, that facilitate the formation of the macropinosome and are regulated by Rac1 activation have also been shown to influence exosome internalization in hepatocyte (Huh7) and kidney (Hek293) cells [91], furthering the support that exosomes utilize macropinocytosis in multiple epithelial cell lines.
\nThe lipid profile of the exosomes and membrane integrity of the cell are also important contributors to vesicle uptake in several different types of epithelial and endothelial cells. While macrophages readily recognize external-facing PS, these cells can also utilize exosomal PS in the process of internalization, as was shown when pre-incubating exosomes with Annexin V inhibited uptake by HeLa cells (cervical cancer epithelial cells), A375 and A431 cells (squamous skin cancer cells) [92] and in human umbilical vein endothelial cells (HUVEC) [93]. Disruption of cellular lipid raft integrity through cholesterol depletion or sequestration reduced exosome uptake in U87 human glioblastoma epithelial cells [43], hCME/D3 human cerebral microvascular cells [89], HeLa cells [43, 90], HUVECs [43, 46], and A375 cells [46]. Lipid rafts play a key role in many of the functions of epithelial cells, including the protein binding interactions between cell and extracellular environment. Also, some of the most central components to epithelial cell function are proteins that interact closely with the environment such as integrins and adhesion molecules, and are anchored into lipid rafts.
\nProtein interactions are essential to epithelial and endothelial function and are closely tied to several of the most common endocytosis pathways used by these cells. Clathrin-dependent endocytosis has been shown in gastric [94], nasopharyngeal [95], breast [96], ovarian cancer epithelial cells [97] and HUVECs [98]. Caveolin-dependence was seen in breast [96] and nasopharyngeal cancer [95], however, caveolin-1 showed negative regulation in glioblastoma cell lines [43] (Figure 4B). General receptor-mediated uptake has been shown with several proteins including heparan sulfate peptidoglycan (HSPG) in glioblastoma cells and HUVECs [99, 100] and in the transitional epithelial cells of the bladder [101]; intercellular adhesion molecule (ICAM1) in hCMEC/D3 cells [89], rat aortic endothelial cells [48], and HUVECs [102]; lectins in cervical cancer [103], HUVECs [102], rat aortic endothelial cells [48] and hCMEC/D3 cells [89]; cad-11 in prostate cancer [104]; syncytin proteins in choriocarcinoma [105] and tetraspanins in an
The extracellular matrix (ECM) and stroma are important contributors to cellular homeostasis and function. This is particularly evident in tumors when evaluating the role of the tumor microenvironment (TME) on the survival and progression of the tumor cells. Fibroblasts are the major component of this extracellular environment. In normal physiology, they promote stromal stability, while in cancer, they contribute to altered ECM, increased angiogenesis, and metastasis [108]. These cells are in a pivotal position to interact with circulating exosomes and their internalization can have a compounding effect on the surrounding environment. Fibroblasts have been shown to participate primarily in clathrin-mediated endocytosis [109, 110] and occasionally receptor-mediated endocytosis [111]. Interestingly, RME [48, 106] and macropinocytosis [91] are the mechanisms by which fibroblasts have been shown to internalize exosomes (Figure 5). Tetraspanins are important proteins in fibroblast function and migration [112]. This protein family is well represented on the exosomal surface and is key to the uptake in many different cell types [48]. Additionally, evidence shows that the smaller the size of the vesicle, the more likely the fibroblast is to use receptors to internalize particles [111]. These three qualities lend support to the evidence of RME as a key pathway for fibroblasts to endocytose exosomes.
\nCell-specific internalization of exosomes: fibroblasts. Fibroblasts take up exosomes with tetraspanins and utilize multiple endocytic pathways.
The nervous system is a uniquely isolated environment with limited connection to the systemic circulation. This characteristic has long impeded therapeutic delivery for brain pathologies. The potential of exosome transport, however, is particularly poignant, as exosomes have been observed selectively targeting neurons and glial cells, successfully crossing the blood brain barrier [113]. Improving our understanding of endocytosis mechanisms involved in these particular cells is essential to therapeutic progression. Clathrin-mediated endocytosis is the most commonly observed pathway with exosomal trafficking between neurons and glial cells [114, 115]. However, some neurons also utilize macropinocytosis [114] and specific receptors, such as SNAP25 (a SNARE family protein) [116], to take up exosomes (Figure 6). Microglia performs phagocytosis similar to their counterparts in the extra-neuronal environment [117]. Using exosomes from two different sources, Chivet et al., illustrated the specificity of exosome targeting seen elsewhere in the body, is also evident in the nervous system. Exosomes from a neuroblastoma cell line (N2a) were preferentially internalized by astrocytes and oligodendrocytes, whereas exosomes from cortical neurons were primarily taken up by hippocampal neurons [118]. It was also shown that pre-synaptic regions were the primary site of internalization of these exosomes [118]. Endocytosis is an important process in the pre-synaptic membrane to recycle released synaptic vesicles [119], indicating that the exosomes may capitalize on this constitutive process for entrance to the neuron. Whether exosomes primarily utilize the specific clathrin-mediated endocytosis in this region [119] or are simply taken by chance with the constant bulk endocytosis [120] still remains unclear. Exosome uptake is a developing area of neuro-research, but with significant potential for therapeutics, it is growing rapidly.
\nCell-specific internalization of exosomes: neurons. Neurons use similar pathways but receptor/ligand binding has less variability. Synaptosomal associated protein 25 (SNAP25).
Exosomes are internalized by a multitude of cell types and play an important role in cellular physiology. Our grasp of the mechanisms of this internalization is growing as we are better able to identify characteristics of the cell and the vesicles that facilitate uptake. Pathologic states, such as cancer, have played an integral role in our understanding of how the cellular-exosomal interaction proceeds. Clarity is still needed to better understand the mechanisms by which exosome internalization is so varied from cell to cell and within the same cell. As we have seen with fibroblasts, the vesicle size can dictate mechanism of uptake [111]. The presence or abundance of specific proteins such as scavenger receptors on macrophages [46, 47, 48] and lipid profiles in several types of cells, such as external-facing phosphatidylserine [20, 48, 49, 56] all contribute to the specificity of uptake. As has been discussed, cell type can dictate uptake mechanism, particularly with phagocytic cells and professional antigen presenting cells, but even within these specialized cells, differing mechanisms occur regularly and further evaluation is needed to parse the primary determinants.
\nVarious types of endocytosis have been identified as possible mechanisms of intercellular transport of exosomal contents to include macropinocytosis [19, 56, 114], phagocytosis [20], clathrin-mediated [52, 114], caveolin-dependent [95], lipid raft-dependent [43, 46], and clathrin- /caveolin-independent [61] endocytosis. Though much about these processes is unique, there are some aspects where functional overlap exists between them. Macropinocytosis is a form of endocytosis that consists of membrane ruffles forming intracellular vesicles to internalize large amounts of extracellular fluid [30]. This varies from other forms of endocytosis in its formation of separate and distinct intracellular vesicles (macropinosomes) and the internalization of material that is considered non-specific exosomal has been recorded in microglia [56], human epidermoid carcinoma-derived A431 cells stimulated by endothelial growth factor receptor (EGFR) and by the pancreatic cancer MiaPaCa-2 cell line [19]. Macropinocytosis is not selective in which molecules are internalized from the extracellular environment, and so uptake may be dictated simply by proximity to the cells and not targeted by the exosome specifically [121]. However, it has been shown that some exosomes naturally induce macropinocytosis internalization [90] and others, through manipulation of exosomal content, can selectively activate this mechanism in order to increase uptake [122]. Phagocytosis is a much more common method of taking up exosomes, especially with phagocytic cells of the immune system. Feng et al., showed that two leukemia cell lines, K562 and MT4, solely utilized phagocytosis for exosome internalization [20, 121].
\nFour other general categories of endocytosis focus on specific cellular proteins that facilitate the uptake of particles. Clathrin and caveolin are both cytosolic proteins that form specific pits with which to internalize various substances [25]. The exact reasons why and when a cell uses clathrin, caveolin, or neither, is still incompletely understood but particle size and cell type seem to play a role [43, 115, 121]. Caveolin-dependent endocytosis is important in albumin uptake, cholesterol transport, and intracellular signaling. Due to the small size of the caveolae, its endocytosed material tends to be smaller than 60 nm [25]. Clathrin-dependent mechanisms however can internalize particles up to 120 nm. The size restrictions may indicate, with further investigation into which uptake mechanism is utilized by which cells, a possible functional difference between vesicle sizes within the current exosome size range [121]. The clathrin-dependent process is involved in many different cell types and functions ranging from vesicle recycling in the neuronal synapse to organ development and ion homeostasis [25]. Many of the common, well-known endocytosis receptors utilize clathrin coated pits, such as low-density lipoprotein receptor (LDLR) and transferrin receptor (TfR). One of the most commonly used ways to determine which of these mechanisms is in operation is through inhibitory drugs or knocking down certain key players [121]. Dynamin, a GTPase, facilitates the fission of the intracellular clathrin coated vesicle [25, 123]. Dynasore, an inhibitor of dynamin, has been utilized to effectively block endocytosis of extracellular vesicles and establish clathrin-mediated endocytosis as a mechanism of uptake for these vesicles [21, 52, 56]. Following siRNA downregulation of caveolin-1 (the primary protein involved in caveolae-dependent endocytosis), exosome internalization was significantly reduced in B cells [95, 121]. Inhibitory drugs have also been useful in the determination of a third mechanism, lipid-raft mediated endocytosis. The lipid raft is a small portion of the plasma membrane, rich in sphingolipids and sterols, that facilitates various cellular processes [124]. Use of methyl-β-cyclodextrin (MβCD), which alters the cholesterol content of the membrane and disrupts lipid rafts, has been seen by several groups to impair exosomal internalization [43, 44, 97]. While lipid raft-dependent endocytosis is the primary clathrin- and caveolae-independent mechanism, other pathways and independent interactions have been described in the internalization of exosomes [61, 124]. Endocytosis is the primary method of exosomal delivery of its contents but research is still needed to understand what determines the specific mechanism whether it is cell type, exosome type, or condition specific [121].
\nExosome stability, ubiquitous presence, and influential contents make them ideal candidates for therapeutic modalities in a wide variety of pathologies. The significance of exosomal contribution to the cellular network throughout the body still carries untapped potential for conquering some of the most pressing current health challenges including cancer and neurodegeneration. Understanding how these exosomes interact with and enter the myriad of cells in the body will empower our ability to capitalize on this natural social network.
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\n'}]},successStories:{items:[]},authorsAndEditors:{filterParams:{},profiles:[{id:"396",title:"Dr.",name:"Vedran",middleName:null,surname:"Kordic",slug:"vedran-kordic",fullName:"Vedran Kordic",position:null,profilePictureURL:"https://mts.intechopen.com/storage/users/396/images/7281_n.png",biography:"After obtaining his Master's degree in Mechanical Engineering he continued his education at the Vienna University of Technology where he obtained his PhD degree in 2004. He worked as a researcher at the Automation and Control Institute, Faculty of Electrical Engineering, Vienna University of Technology until 2008. His studies in robotics lead him not only to a PhD degree but also inspired him to co-found and build the International Journal of Advanced Robotic Systems - world's first Open Access journal in the field of robotics.",institutionString:null,institution:{name:"TU Wien",country:{name:"Austria"}}},{id:"441",title:"Ph.D.",name:"Jaekyu",middleName:null,surname:"Park",slug:"jaekyu-park",fullName:"Jaekyu Park",position:null,profilePictureURL:"https://mts.intechopen.com/storage/users/441/images/1881_n.jpg",biography:null,institutionString:null,institution:{name:"LG Corporation (South Korea)",country:{name:"Korea, South"}}},{id:"465",title:"Dr.",name:"Christian",middleName:null,surname:"Martens",slug:"christian-martens",fullName:"Christian Martens",position:null,profilePictureURL:"//cdnintech.com/web/frontend/www/assets/author.svg",biography:null,institutionString:null,institution:{name:"Rheinmetall (Germany)",country:{name:"Germany"}}},{id:"479",title:"Dr.",name:"Valentina",middleName:null,surname:"Colla",slug:"valentina-colla",fullName:"Valentina Colla",position:null,profilePictureURL:"https://mts.intechopen.com/storage/users/479/images/358_n.jpg",biography:null,institutionString:null,institution:{name:"Sant'Anna School of Advanced Studies",country:{name:"Italy"}}},{id:"494",title:"PhD",name:"Loris",middleName:null,surname:"Nanni",slug:"loris-nanni",fullName:"Loris Nanni",position:null,profilePictureURL:"https://mts.intechopen.com/storage/users/494/images/system/494.jpg",biography:"Loris Nanni received his Master Degree cum laude on June-2002 from the University of Bologna, and the April 26th 2006 he received his Ph.D. in Computer Engineering at DEIS, University of Bologna. On September, 29th 2006 he has won a post PhD fellowship from the university of Bologna (from October 2006 to October 2008), at the competitive examination he was ranked first in the industrial engineering area. He extensively served as referee for several international journals. He is author/coauthor of more than 100 research papers. He has been involved in some projects supported by MURST and European Community. His research interests include pattern recognition, bioinformatics, and biometric systems (fingerprint classification and recognition, signature verification, face recognition).",institutionString:null,institution:null},{id:"496",title:"Dr.",name:"Carlos",middleName:null,surname:"Leon",slug:"carlos-leon",fullName:"Carlos Leon",position:null,profilePictureURL:"//cdnintech.com/web/frontend/www/assets/author.svg",biography:null,institutionString:null,institution:{name:"University of Seville",country:{name:"Spain"}}},{id:"512",title:"Dr.",name:"Dayang",middleName:null,surname:"Jawawi",slug:"dayang-jawawi",fullName:"Dayang Jawawi",position:null,profilePictureURL:"//cdnintech.com/web/frontend/www/assets/author.svg",biography:null,institutionString:null,institution:{name:"University of Technology Malaysia",country:{name:"Malaysia"}}},{id:"528",title:"Dr.",name:"Kresimir",middleName:null,surname:"Delac",slug:"kresimir-delac",fullName:"Kresimir Delac",position:null,profilePictureURL:"https://mts.intechopen.com/storage/users/528/images/system/528.jpg",biography:"K. Delac received his B.Sc.E.E. degree in 2003 and is currentlypursuing a Ph.D. degree at the University of Zagreb, Faculty of Electrical Engineering andComputing. His current research interests are digital image analysis, pattern recognition andbiometrics.",institutionString:null,institution:{name:"University of Zagreb",country:{name:"Croatia"}}},{id:"557",title:"Dr.",name:"Andon",middleName:"Venelinov",surname:"Topalov",slug:"andon-topalov",fullName:"Andon Topalov",position:null,profilePictureURL:"https://mts.intechopen.com/storage/users/557/images/1927_n.jpg",biography:"Dr. Andon V. Topalov received the MSc degree in Control Engineering from the Faculty of Information Systems, Technologies, and Automation at Moscow State University of Civil Engineering (MGGU) in 1979. He then received his PhD degree in Control Engineering from the Department of Automation and Remote Control at Moscow State Mining University (MGSU), Moscow, in 1984. From 1985 to 1986, he was a Research Fellow in the Research Institute for Electronic Equipment, ZZU AD, Plovdiv, Bulgaria. In 1986, he joined the Department of Control Systems, Technical University of Sofia at the Plovdiv campus, where he is presently a Full Professor. He has held long-term visiting Professor/Scholar positions at various institutions in South Korea, Turkey, Mexico, Greece, Belgium, UK, and Germany. And he has coauthored one book and authored or coauthored more than 80 research papers in conference proceedings and journals. His current research interests are in the fields of intelligent control and robotics.",institutionString:null,institution:{name:"Technical University of Sofia",country:{name:"Bulgaria"}}},{id:"585",title:"Prof.",name:"Munir",middleName:null,surname:"Merdan",slug:"munir-merdan",fullName:"Munir Merdan",position:null,profilePictureURL:"https://mts.intechopen.com/storage/users/585/images/system/585.jpg",biography:"Munir Merdan received the M.Sc. degree in mechanical engineering from the Technical University of Sarajevo, Bosnia and Herzegovina, in 2001, and the Ph.D. degree in electrical engineering from the Vienna University of Technology, Vienna, Austria, in 2009.Since 2005, he has been at the Automation and Control Institute, Vienna University of Technology, where he is currently a Senior Researcher. His research interests include the application of agent technology for achieving agile control in the manufacturing environment.",institutionString:null,institution:null},{id:"605",title:"Prof",name:"Dil",middleName:null,surname:"Hussain",slug:"dil-hussain",fullName:"Dil Hussain",position:null,profilePictureURL:"https://mts.intechopen.com/storage/users/605/images/system/605.jpg",biography:"Dr. Dil Muhammad Akbar Hussain is a professor of Electronics Engineering & Computer Science at the Department of Energy Technology, Aalborg University Denmark. Professor Akbar has a Master degree in Digital Electronics from Govt. College University, Lahore Pakistan and a P-hD degree in Control Engineering from the School of Engineering and Applied Sciences, University of Sussex United Kingdom. Aalborg University has Two Satellite Campuses, one in Copenhagen (Aalborg University Copenhagen) and the other in Esbjerg (Aalborg University Esbjerg).\n· He is a member of prestigious IEEE (Institute of Electrical and Electronics Engineers), and IAENG (International Association of Engineers) organizations. \n· He is the chief Editor of the Journal of Software Engineering.\n· He is the member of the Editorial Board of International Journal of Computer Science and Software Technology (IJCSST) and International Journal of Computer Engineering and Information Technology. \n· He is also the Editor of Communication in Computer and Information Science CCIS-20 by Springer.\n· Reviewer For Many Conferences\nHe is the lead person in making collaboration agreements between Aalborg University and many universities of Pakistan, for which the MOU’s (Memorandum of Understanding) have been signed.\nProfessor Akbar is working in Academia since 1990, he started his career as a Lab demonstrator/TA at the University of Sussex. After finishing his P. hD degree in 1992, he served in the Industry as a Scientific Officer and continued his academic career as a visiting scholar for a number of educational institutions. In 1996 he joined National University of Science & Technology Pakistan (NUST) as an Associate Professor; NUST is one of the top few universities in Pakistan. In 1999 he joined an International Company Lineo Inc, Canada as Manager Compiler Group, where he headed the group for developing Compiler Tool Chain and Porting of Operating Systems for the BLACKfin processor. The processor development was a joint venture by Intel and Analog Devices. In 2002 Lineo Inc., was taken over by another company, so he joined Aalborg University Denmark as an Assistant Professor.\nProfessor Akbar has truly a multi-disciplined career and he continued his legacy and making progress in many areas of his interests both in teaching and research. He has contributed in stochastic estimation of control area especially, in the Multiple Target Tracking and Interactive Multiple Model (IMM) research, Ball & Beam Control Problem, Robotics, Levitation Control. He has contributed in developing Algorithms for Fingerprint Matching, Computer Vision and Face Recognition. He has been supervising Pattern Recognition, Formal Languages and Distributed Processing projects for several years. He has reviewed many books on Management, Computer Science. Currently, he is an active and permanent reviewer for many international conferences and symposia and the program committee member for many international conferences.\nIn teaching he has taught the core computer science subjects like, Digital Design, Real Time Embedded System Programming, Operating Systems, Software Engineering, Data Structures, Databases, Compiler Construction. In the Engineering side, Digital Signal Processing, Computer Architecture, Electronics Devices, Digital Filtering and Engineering Management.\nApart from his Academic Interest and activities he loves sport especially, Cricket, Football, Snooker and Squash. He plays cricket for Esbjerg city in the second division team as an opener wicket keeper batsman. 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I am a Senior Lecturer in the Department of Parasitology and Entomology, Nnamdi Azikiwe University, Awka.",institutionString:null,institution:{name:"Nnamdi Azikiwe University",country:{name:"Nigeria"}}},{id:"284232",title:"Mr.",name:"Nikunj",middleName:"U",surname:"Tandel",slug:"nikunj-tandel",fullName:"Nikunj Tandel",position:null,profilePictureURL:"https://mts.intechopen.com/storage/users/284232/images/8275_n.jpg",biography:'Mr. Nikunj Tandel has completed his Master\'s degree in Biotechnology from VIT University, India in the year of 2012. He is having 8 years of research experience especially in the field of malaria epidemiology, immunology, and nanoparticle-based drug delivery system against the infectious diseases, autoimmune disorders and cancer. He has worked for the NIH funded-International Center of Excellence in Malaria Research project "Center for the study of complex malaria in India (CSCMi)" in collaboration with New York University. The preliminary objectives of the study are to understand and develop the evidence-based tools and interventions for the control and prevention of malaria in different sites of the INDIA. Alongside, with the help of next-generation genomics study, the team has studied the antimalarial drug resistance in India. Further, he has extended his research in the development of Humanized mice for the study of liver-stage malaria and identification of molecular marker(s) for the Artemisinin resistance. At present, his research focuses on understanding the role of B cells in the activation of CD8+ T cells in malaria. Received the CSIR-SRF (Senior Research Fellow) award-2018, FIMSA (Federation of Immunological Societies of Asia-Oceania) Travel Bursary award to attend the IUIS-IIS-FIMSA Immunology course-2019',institutionString:"Nirma University",institution:{name:"Nirma University",country:{name:"India"}}},{id:"334383",title:"Ph.D.",name:"Simone",middleName:"Ulrich",surname:"Ulrich Picoli",slug:"simone-ulrich-picoli",fullName:"Simone Ulrich Picoli",position:null,profilePictureURL:"https://mts.intechopen.com/storage/users/334383/images/15919_n.jpg",biography:"Graduated in Pharmacy from Universidade Luterana do Brasil (1999), Master in Agricultural and Environmental Microbiology from Federal University of Rio Grande do Sul (2002), Specialization in Clinical Microbiology from Universidade de São Paulo, USP (2007) and PhD in Sciences in Gastroenterology and Hepatology (2012). She is currently an Adjunct Professor at Feevale University in Medicine and Biomedicine courses and a permanent professor of the Academic Master\\'s Degree in Virology. She has experience in the field of Microbiology, with an emphasis on Bacteriology, working mainly on the following topics: bacteriophages, bacterial resistance, clinical microbiology and food microbiology.",institutionString:null,institution:{name:"Universidade Feevale",country:{name:"Brazil"}}},{id:"229220",title:"Dr.",name:"Amjad",middleName:"Islam",surname:"Aqib",slug:"amjad-aqib",fullName:"Amjad Aqib",position:null,profilePictureURL:"https://mts.intechopen.com/storage/users/229220/images/system/229220.png",biography:"Dr. Amjad Islam Aqib obtained a DVM and MSc (Hons) from University of Agriculture Faisalabad (UAF), Pakistan, and a PhD from the University of Veterinary and Animal Sciences Lahore, Pakistan. Dr. Aqib joined the Department of Clinical Medicine and Surgery at UAF for one year as an assistant professor where he developed a research laboratory designated for pathogenic bacteria. Since 2018, he has been Assistant Professor/Officer in-charge, Department of Medicine, Manager Research Operations and Development-ORIC, and President One Health Club at Cholistan University of Veterinary and Animal Sciences, Bahawalpur, Pakistan. He has nearly 100 publications to his credit. His research interests include epidemiological patterns and molecular analysis of antimicrobial resistance and modulation and vaccine development against animal pathogens of public health concern.",institutionString:"Cholistan University of Veterinary and Animal Sciences",institution:{name:"University of Agriculture Faisalabad",country:{name:"Pakistan"}}},{id:"333753",title:"Dr.",name:"Rais",middleName:null,surname:"Ahmed",slug:"rais-ahmed",fullName:"Rais Ahmed",position:null,profilePictureURL:"https://mts.intechopen.com/storage/users/333753/images/20168_n.jpg",biography:null,institutionString:null,institution:{name:"University of Agriculture Faisalabad",country:{name:"Pakistan"}}},{id:"62900",title:"Prof.",name:"Fethi",middleName:null,surname:"Derbel",slug:"fethi-derbel",fullName:"Fethi Derbel",position:null,profilePictureURL:"https://mts.intechopen.com/storage/users/62900/images/system/62900.jpeg",biography:"Professor Fethi Derbel was born in 1960 in Tunisia. He received his medical degree from the Sousse Faculty of Medicine at Sousse, University of Sousse, Tunisia. He completed his surgical residency in General Surgery at the University Hospital Farhat Hached of Sousse and was a member of the Unit of Liver Transplantation in the University of Rennes, France. He then worked in the Department of Surgery at the Sahloul University Hospital in Sousse. Professor Derbel is presently working at the Clinique les Oliviers, Sousse, Tunisia. His hospital activities are mostly concerned with laparoscopic, colorectal, pancreatic, hepatobiliary, and gastric surgery. He is also very interested in hernia surgery and performs ventral hernia repairs and inguinal hernia repairs. He has been a member of the GREPA and Tunisian Hernia Society (THS). During his residency, he managed patients suffering from diabetic foot, and he was very interested in this pathology. For this reason, he decided to coordinate a book project dealing with the diabetic foot. Professor Derbel has published many articles in journals and collaborates intensively with IntechOpen Access Publisher as an editor.",institutionString:"Clinique les Oliviers",institution:null},{id:"300144",title:"Dr.",name:"Meriem",middleName:null,surname:"Braiki",slug:"meriem-braiki",fullName:"Meriem Braiki",position:null,profilePictureURL:"https://mts.intechopen.com/storage/users/300144/images/system/300144.jpg",biography:"Dr. Meriem Braiki is a specialist in pediatric surgeon from Tunisia. She was born in 1985. She received her medical degree from the University of Medicine at Sousse, Tunisia. She achieved her surgical residency training periods in Pediatric Surgery departments at University Hospitals in Monastir, Tunis and France.\r\nShe is currently working at the Pediatric surgery department, Sidi Bouzid Hospital, Tunisia. Her hospital activities are mostly concerned with laparoscopic, parietal, urological and digestive surgery. She has published several articles in diffrent journals.",institutionString:"Sidi Bouzid Regional Hospital",institution:null},{id:"229481",title:"Dr.",name:"Erika M.",middleName:"Martins",surname:"de Carvalho",slug:"erika-m.-de-carvalho",fullName:"Erika M. de Carvalho",position:null,profilePictureURL:"https://mts.intechopen.com/storage/users/229481/images/6397_n.jpg",biography:null,institutionString:null,institution:{name:"Oswaldo Cruz Foundation",country:{name:"Brazil"}}},{id:"186537",title:"Prof.",name:"Tonay",middleName:null,surname:"Inceboz",slug:"tonay-inceboz",fullName:"Tonay Inceboz",position:null,profilePictureURL:"https://mts.intechopen.com/storage/users/186537/images/system/186537.jfif",biography:"I was graduated from Ege University of Medical Faculty (Turkey) in 1988 and completed his Med. PhD degree in Medical Parasitology at the same university. I became an Associate Professor in 2008 and Professor in 2014. I am currently working as a Professor at the Department of Medical Parasitology at Dokuz Eylul University, Izmir, Turkey.\n\nI have given many lectures, presentations in different academic meetings. I have more than 60 articles in peer-reviewed journals, 18 book chapters, 1 book editorship.\n\nMy research interests are Echinococcus granulosus, Echinococcus multilocularis (diagnosis, life cycle, in vitro and in vivo cultivation), and Trichomonas vaginalis (diagnosis, PCR, and in vitro cultivation).",institutionString:"Dokuz Eylül University",institution:{name:"Dokuz Eylül University",country:{name:"Turkey"}}},{id:"71812",title:"Prof.",name:"Hanem Fathy",middleName:"Fathy",surname:"Khater",slug:"hanem-fathy-khater",fullName:"Hanem Fathy Khater",position:null,profilePictureURL:"https://mts.intechopen.com/storage/users/71812/images/1167_n.jpg",biography:"Prof. Khater is a Professor of Parasitology at Benha University, Egypt. She studied for her doctoral degree, at the Department of Entomology, College of Agriculture, Food and Natural Resources, University of Missouri, Columbia, USA. She has completed her Ph.D. degrees in Parasitology in Egypt, from where she got the award for “the best scientific Ph.D. dissertation”. She worked at the School of Biological Sciences, Bristol, England, the UK in controlling insects of medical and veterinary importance as a grant from Newton Mosharafa, the British Council. Her research is focused on searching of pesticides against mosquitoes, house flies, lice, green bottle fly, camel nasal botfly, soft and hard ticks, mites, and the diamondback moth as well as control of several parasites using safe and natural materials to avoid drug resistances and environmental contamination.",institutionString:null,institution:{name:"Banha University",country:{name:"Egypt"}}},{id:"99780",title:"Prof.",name:"Omolade",middleName:"Olayinka",surname:"Okwa",slug:"omolade-okwa",fullName:"Omolade Okwa",position:null,profilePictureURL:"https://mts.intechopen.com/storage/users/99780/images/system/99780.jpg",biography:"Omolade Olayinka Okwa is presently a Professor of Parasitology at Lagos State University, Nigeria. She has a PhD in Parasitology (1997), an MSc in Cellular Parasitology (1992), and a BSc (Hons) Zoology (1990) all from the University of Ibadan, Nigeria. She teaches parasitology at the undergraduate and postgraduate levels. She was a recipient of a Commonwealth fellowship supported by British Council tenable at the Centre for Entomology and Parasitology (CAEP), Keele University, United Kingdom between 2004 and 2005. She was awarded an Honorary Visiting Research Fellow at the same university from 2005 to 2007. \nShe has been an external examiner to the Department of Veterinary Microbiology and Parasitology, University of Ibadan, MSc programme between 2010 and 2012. She is a member of the Nigerian Society of Experimental Biology (NISEB), Parasitology and Public Health Society of Nigeria (PPSN), Science Association of Nigeria (SAN), Zoological Society of Nigeria (ZSN), and is Vice Chairperson of the Organisation of Women in Science (OWSG), LASU chapter. She served as Head of Department of Zoology and Environmental Biology, Lagos State University from 2007 to 2010 and 2014 to 2016. She is a reviewer for several local and international journals such as Unilag Journal of Science, Libyan Journal of Medicine, Journal of Medicine and Medical Sciences, and Annual Research and Review in Science. \nShe has authored 45 scientific research publications in local and international journals, 8 scientific reviews, 4 books, and 3 book chapters, which includes the books “Malaria Parasites” and “Malaria” which are IntechOpen access publications.",institutionString:"Lagos State University",institution:{name:"Lagos State University",country:{name:"Nigeria"}}},{id:"273100",title:"Dr.",name:"Vijay",middleName:null,surname:"Gayam",slug:"vijay-gayam",fullName:"Vijay Gayam",position:null,profilePictureURL:"https://mts.intechopen.com/storage/users/273100/images/system/273100.jpeg",biography:"Dr. Vijay Bhaskar Reddy Gayam is currently practicing as an internist at Interfaith Medical Center in Brooklyn, New York, USA. He is also a Clinical Assistant Professor at the SUNY Downstate University Hospital and Adjunct Professor of Medicine at the American University of Antigua. He is a holder of an M.B.B.S. degree bestowed to him by Osmania Medical College and received his M.D. at Interfaith Medical Center. His career goals thus far have heavily focused on direct patient care, medical education, and clinical research. He currently serves in two leadership capacities; Assistant Program Director of Medicine at Interfaith Medical Center and as a Councilor for the American\r\nFederation for Medical Research. As a true academician and researcher, he has more than 50 papers indexed in international peer-reviewed journals. He has also presented numerous papers in multiple national and international scientific conferences. His areas of research interest include general internal medicine, gastroenterology and hepatology. He serves as an editor, editorial board member and reviewer for multiple international journals. His research on Hepatitis C has been very successful and has led to multiple research awards, including the 'Equity in Prevention and Treatment Award” from the New York Department of Health Viral Hepatitis Symposium (2018) and the 'Presidential Poster Award” awarded to him by the American College of Gastroenterology (2018). He was also awarded 'Outstanding Clinician in General Medicine” by Venus International Foundation for his extensive research expertise and services, perform over and above the standard expected in the advancement of healthcare, patient safety and quality of care.",institutionString:"Interfaith Medical Center",institution:{name:"Interfaith Medical Center",country:{name:"United States of America"}}},{id:"93517",title:"Dr.",name:"Clement",middleName:"Adebajo",surname:"Meseko",slug:"clement-meseko",fullName:"Clement Meseko",position:null,profilePictureURL:"https://mts.intechopen.com/storage/users/93517/images/system/93517.jpg",biography:"Dr. Clement Meseko obtained DVM and PhD degree in Veterinary Medicine and Virology respectively. He has worked for over 20 years in both private and public sectors including the academia, contributing to knowledge and control of infectious disease. Through the application of epidemiological skill, classical and molecular virological skills, he investigates viruses of economic and public health importance for the mitigation of the negative impact on people, animal and the environment in the context of Onehealth. \r\nDr. Meseko’s field experience on animal and zoonotic diseases and pathogen dynamics at the human-animal interface over the years shaped his carrier in research and scientific inquiries. He has been part of the investigation of Highly Pathogenic Avian Influenza incursions in sub Saharan Africa and monitors swine Influenza (Pandemic influenza Virus) agro-ecology and potential for interspecies transmission. He has authored and reviewed a number of journal articles and book chapters.",institutionString:"National Veterinary Research Institute",institution:{name:"National Veterinary Research Institute",country:{name:"Nigeria"}}},{id:"158026",title:"Prof.",name:"Shailendra K.",middleName:null,surname:"Saxena",slug:"shailendra-k.-saxena",fullName:"Shailendra K. Saxena",position:null,profilePictureURL:"https://s3.us-east-1.amazonaws.com/intech-files/0030O00002bRET3QAO/Profile_Picture_2022-05-10T10:10:26.jpeg",biography:"Professor Dr. Shailendra K. Saxena is a vice dean and professor at King George's Medical University, Lucknow, India. His research interests involve understanding the molecular mechanisms of host defense during human viral infections and developing new predictive, preventive, and therapeutic strategies for them using Japanese encephalitis virus (JEV), HIV, and emerging viruses as a model via stem cell and cell culture technologies. His research work has been published in various high-impact factor journals (Science, PNAS, Nature Medicine) with a high number of citations. He has received many awards and honors in India and abroad including various Young Scientist Awards, BBSRC India Partnering Award, and Dr. JC Bose National Award of Department of Biotechnology, Min. of Science and Technology, Govt. of India. Dr. Saxena is a fellow of various international societies/academies including the Royal College of Pathologists, United Kingdom; Royal Society of Medicine, London; Royal Society of Biology, United Kingdom; Royal Society of Chemistry, London; and Academy of Translational Medicine Professionals, Austria. He was named a Global Leader in Science by The Scientist. He is also an international opinion leader/expert in vaccination for Japanese encephalitis by IPIC (UK).",institutionString:"King George's Medical University",institution:{name:"King George's Medical University",country:{name:"India"}}},{id:"94928",title:"Dr.",name:"Takuo",middleName:null,surname:"Mizukami",slug:"takuo-mizukami",fullName:"Takuo Mizukami",position:null,profilePictureURL:"https://mts.intechopen.com/storage/users/94928/images/6402_n.jpg",biography:null,institutionString:null,institution:{name:"National Institute of Infectious Diseases",country:{name:"Japan"}}},{id:"233433",title:"Dr.",name:"Yulia",middleName:null,surname:"Desheva",slug:"yulia-desheva",fullName:"Yulia Desheva",position:null,profilePictureURL:"https://mts.intechopen.com/storage/users/233433/images/system/233433.png",biography:"Dr. Yulia Desheva is a leading researcher at the Institute of Experimental Medicine, St. Petersburg, Russia. She is a professor in the Stomatology Faculty, St. Petersburg State University. She has expertise in the development and evaluation of a wide range of live mucosal vaccines against influenza and bacterial complications. Her research interests include immunity against influenza and COVID-19 and the development of immunization schemes for high-risk individuals.",institutionString:'Federal State Budgetary Scientific Institution "Institute of Experimental Medicine"',institution:null},{id:"238958",title:"Mr.",name:"Atamjit",middleName:null,surname:"Singh",slug:"atamjit-singh",fullName:"Atamjit Singh",position:null,profilePictureURL:"https://mts.intechopen.com/storage/users/238958/images/6575_n.jpg",biography:null,institutionString:null,institution:null},{id:"252058",title:"M.Sc.",name:"Juan",middleName:null,surname:"Sulca",slug:"juan-sulca",fullName:"Juan Sulca",position:null,profilePictureURL:"https://mts.intechopen.com/storage/users/252058/images/12834_n.jpg",biography:null,institutionString:null,institution:null},{id:"191392",title:"Dr.",name:"Marimuthu",middleName:null,surname:"Govindarajan",slug:"marimuthu-govindarajan",fullName:"Marimuthu Govindarajan",position:null,profilePictureURL:"https://mts.intechopen.com/storage/users/191392/images/5828_n.jpg",biography:"Dr. M. Govindarajan completed his BSc degree in Zoology at Government Arts College (Autonomous), Kumbakonam, and MSc, MPhil, and PhD degrees at Annamalai University, Annamalai Nagar, Tamil Nadu, India. He is serving as an assistant professor at the Department of Zoology, Annamalai University. His research interests include isolation, identification, and characterization of biologically active molecules from plants and microbes. He has identified more than 20 pure compounds with high mosquitocidal activity and also conducted high-quality research on photochemistry and nanosynthesis. He has published more than 150 studies in journals with impact factor and 2 books in Lambert Academic Publishing, Germany. He serves as an editorial board member in various national and international scientific journals.",institutionString:null,institution:null},{id:"274660",title:"Dr.",name:"Damodar",middleName:null,surname:"Paudel",slug:"damodar-paudel",fullName:"Damodar Paudel",position:null,profilePictureURL:"https://mts.intechopen.com/storage/users/274660/images/8176_n.jpg",biography:"I am DrDamodar Paudel,currently working as consultant Physician in Nepal police Hospital.",institutionString:null,institution:null},{id:"241562",title:"Dr.",name:"Melvin",middleName:null,surname:"Sanicas",slug:"melvin-sanicas",fullName:"Melvin Sanicas",position:null,profilePictureURL:"https://mts.intechopen.com/storage/users/241562/images/6699_n.jpg",biography:null,institutionString:null,institution:null},{id:"117248",title:"Dr.",name:"Andrew",middleName:null,surname:"Macnab",slug:"andrew-macnab",fullName:"Andrew Macnab",position:null,profilePictureURL:"//cdnintech.com/web/frontend/www/assets/author.svg",biography:null,institutionString:null,institution:{name:"University of British Columbia",country:{name:"Canada"}}},{id:"322007",title:"Dr.",name:"Maria Elizbeth",middleName:null,surname:"Alvarez-Sánchez",slug:"maria-elizbeth-alvarez-sanchez",fullName:"Maria Elizbeth Alvarez-Sánchez",position:null,profilePictureURL:"//cdnintech.com/web/frontend/www/assets/author.svg",biography:null,institutionString:null,institution:{name:"Universidad Autónoma de la Ciudad de México",country:{name:"Mexico"}}},{id:"337443",title:"Dr.",name:"Juan",middleName:null,surname:"A. Gonzalez-Sanchez",slug:"juan-a.-gonzalez-sanchez",fullName:"Juan A. Gonzalez-Sanchez",position:null,profilePictureURL:"//cdnintech.com/web/frontend/www/assets/author.svg",biography:null,institutionString:null,institution:{name:"University of Puerto Rico System",country:{name:"United States of America"}}},{id:"337446",title:"Dr.",name:"Maria",middleName:null,surname:"Zavala-Colon",slug:"maria-zavala-colon",fullName:"Maria Zavala-Colon",position:null,profilePictureURL:"//cdnintech.com/web/frontend/www/assets/author.svg",biography:null,institutionString:null,institution:{name:"University of Puerto Rico, Medical Sciences Campus",country:{name:"United States of America"}}}]}},subseries:{item:{id:"8",type:"subseries",title:"Bioinspired Technology and Biomechanics",keywords:"Bioinspired Systems, Biomechanics, Assistive Technology, Rehabilitation",scope:'Bioinspired technologies take advantage of understanding the actual biological system to provide solutions to problems in several areas. Recently, bioinspired systems have been successfully employing biomechanics to develop and improve assistive technology and rehabilitation devices. The research topic "Bioinspired Technology and Biomechanics" welcomes studies reporting recent advances in bioinspired technologies that contribute to individuals\' health, inclusion, and rehabilitation. Possible contributions can address (but are not limited to) the following research topics: Bioinspired design and control of exoskeletons, orthoses, and prostheses; Experimental evaluation of the effect of assistive devices (e.g., influence on gait, balance, and neuromuscular system); Bioinspired technologies for rehabilitation, including clinical studies reporting evaluations; Application of neuromuscular and biomechanical models to the development of bioinspired technology.',coverUrl:"https://cdn.intechopen.com/series_topics/covers/8.jpg",hasOnlineFirst:!0,hasPublishedBooks:!0,annualVolume:11404,editor:{id:"144937",title:"Prof.",name:"Adriano",middleName:"De Oliveira",surname:"Andrade",slug:"adriano-andrade",fullName:"Adriano Andrade",profilePictureURL:"https://s3.us-east-1.amazonaws.com/intech-files/0030O00002bRC8QQAW/Profile_Picture_1625219101815",biography:"Dr. Adriano de Oliveira Andrade graduated in Electrical Engineering at the Federal University of Goiás (Brazil) in 1997. He received his MSc and PhD in Biomedical Engineering respectively from the Federal University of Uberlândia (UFU, Brazil) in 2000 and from the University of Reading (UK) in 2005. He completed a one-year Post-Doctoral Fellowship awarded by the DFAIT (Foreign Affairs and International Trade Canada) at the Institute of Biomedical Engineering of the University of New Brunswick (Canada) in 2010. Currently, he is Professor in the Faculty of Electrical Engineering (UFU). He has authored and co-authored more than 200 peer-reviewed publications in Biomedical Engineering. He has been a researcher of The National Council for Scientific and Technological Development (CNPq-Brazil) since 2009. He has served as an ad-hoc consultant for CNPq, CAPES (Coordination for the Improvement of Higher Education Personnel), FINEP (Brazilian Innovation Agency), and other funding bodies on several occasions. He was the Secretary of the Brazilian Society of Biomedical Engineering (SBEB) from 2015 to 2016, President of SBEB (2017-2018) and Vice-President of SBEB (2019-2020). He was the head of the undergraduate program in Biomedical Engineering of the Federal University of Uberlândia (2015 - June/2019) and the head of the Centre for Innovation and Technology Assessment in Health (NIATS/UFU) since 2010. He is the head of the Postgraduate Program in Biomedical Engineering (UFU, July/2019 - to date). He was the secretary of the Parkinson's Disease Association of Uberlândia (2018-2019). Dr. Andrade's primary area of research is focused towards getting information from the neuromuscular system to understand its strategies of organization, adaptation and controlling in the context of motor neuron diseases. 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Finally, the tissue engineering subcategory will support topics such as the fundamentals of stem cells and progenitor cells and their proliferation, differentiation, bioreactors for three-dimensional culture and studies of phenotypic changes, stem and progenitor cells, both short and long term, ex vivo and in vivo implantation both in preclinical models and also in clinical trials.",annualVolume:11405,isOpenForSubmission:!0,coverUrl:"https://cdn.intechopen.com/series_topics/covers/9.jpg",editor:{id:"126286",title:"Dr.",name:"Luis",middleName:"Jesús",surname:"Villarreal-Gómez",fullName:"Luis Villarreal-Gómez",profilePictureURL:"https://mts.intechopen.com/storage/users/126286/images/system/126286.jpg",institutionString:null,institution:{name:"Autonomous University of Baja California",institutionURL:null,country:{name:"Mexico"}}},editorTwo:null,editorThree:null,editorialBoard:[{id:"35539",title:"Dr.",name:"Cecilia",middleName:null,surname:"Cristea",fullName:"Cecilia Cristea",profilePictureURL:"https://s3.us-east-1.amazonaws.com/intech-files/0030O00002aYQ65QAG/Profile_Picture_1621007741527",institutionString:null,institution:{name:"Iuliu Hațieganu University of Medicine and Pharmacy",institutionURL:null,country:{name:"Romania"}}},{id:"40735",title:"Dr.",name:"Gil",middleName:"Alberto Batista",surname:"Gonçalves",fullName:"Gil Gonçalves",profilePictureURL:"https://s3.us-east-1.amazonaws.com/intech-files/0030O00002aYRLGQA4/Profile_Picture_1628492612759",institutionString:null,institution:{name:"University of Aveiro",institutionURL:null,country:{name:"Portugal"}}},{id:"211725",title:"Associate Prof.",name:"Johann F.",middleName:null,surname:"Osma",fullName:"Johann F. 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