TNM staging principle for the anal and rectal carcinoma according to the current classification of International Agency for Research on Cancer/World Health Organization [23].
\\n\\n
More than half of the publishers listed alongside IntechOpen (18 out of 30) are Social Science and Humanities publishers. IntechOpen is an exception to this as a leader in not only Open Access content but Open Access content across all scientific disciplines, including Physical Sciences, Engineering and Technology, Health Sciences, Life Science, and Social Sciences and Humanities.
\\n\\nOur breakdown of titles published demonstrates this with 47% PET, 31% HS, 18% LS, and 4% SSH books published.
\\n\\n“Even though ItechOpen has shown the potential of sci-tech books using an OA approach,” other publishers “have shown little interest in OA books.”
\\n\\nAdditionally, each book published by IntechOpen contains original content and research findings.
\\n\\nWe are honored to be among such prestigious publishers and we hope to continue to spearhead that growth in our quest to promote Open Access as a true pioneer in OA book publishing.
\\n\\n\\n\\n
\\n"}]',published:!0,mainMedia:null},components:[{type:"htmlEditorComponent",content:'
Simba Information has released its Open Access Book Publishing 2020 - 2024 report and has again identified IntechOpen as the world’s largest Open Access book publisher by title count.
\n\nSimba Information is a leading provider for market intelligence and forecasts in the media and publishing industry. The report, published every year, provides an overview and financial outlook for the global professional e-book publishing market.
\n\nIntechOpen, De Gruyter, and Frontiers are the largest OA book publishers by title count, with IntechOpen coming in at first place with 5,101 OA books published, a good 1,782 titles ahead of the nearest competitor.
\n\nSince the first Open Access Book Publishing report published in 2016, IntechOpen has held the top stop each year.
\n\n\n\nMore than half of the publishers listed alongside IntechOpen (18 out of 30) are Social Science and Humanities publishers. IntechOpen is an exception to this as a leader in not only Open Access content but Open Access content across all scientific disciplines, including Physical Sciences, Engineering and Technology, Health Sciences, Life Science, and Social Sciences and Humanities.
\n\nOur breakdown of titles published demonstrates this with 47% PET, 31% HS, 18% LS, and 4% SSH books published.
\n\n“Even though ItechOpen has shown the potential of sci-tech books using an OA approach,” other publishers “have shown little interest in OA books.”
\n\nAdditionally, each book published by IntechOpen contains original content and research findings.
\n\nWe are honored to be among such prestigious publishers and we hope to continue to spearhead that growth in our quest to promote Open Access as a true pioneer in OA book publishing.
\n\n\n\n
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\r\n\tPlants and plant products are considered natural sources of anthocyanin antioxidants, which have a broad spectrum of biomedical functions. Some of these functions involve advancing age‐induced oxidative stress, inflammatory responses, diverse degenerative diseases, and cardiovascular disorders. Recent studies have shown that free radicals and related species continue to attracted attention. These free radicals are majorly derived from reactive oxygen species (ROS) and reactive nitrogen species (RNS). They are further generated into our body by various endogenous systems. Free radicals can negatively affect and alter lipids, proteins and DNA and they have been implicated in a number of human diseases. This book will compile the recent breakthrough findings in the area of anthocyanin in relation to human health and disease prevention that will be useful to undergraduate, postgraduate and research scholars. It will collect chapters of scientific interest from the academicians and researchers who have vast experience in the area of anthocyanins in relation to human health.
",isbn:null,printIsbn:null,pdfIsbn:null,doi:null,price:0,priceEur:0,priceUsd:0,slug:null,numberOfPages:0,isOpenForSubmission:!1,hash:"efdcbf86261bc73187aa29a50931b330",bookSignature:"Dr. Anthony Ananga",publishedDate:null,coverURL:"https://cdn.intechopen.com/books/images_new/8309.jpg",keywords:"Biosynthesis, regulation, antioxidant, natural colorant, Anthocyanin Chemistry, Dietary Sources, Cosmeceuticals, skin health, Anticancer Activities , Exercised-Induced Natural Immunity",numberOfDownloads:null,numberOfWosCitations:0,numberOfCrossrefCitations:0,numberOfDimensionsCitations:0,numberOfTotalCitations:0,isAvailableForWebshopOrdering:!0,dateEndFirstStepPublish:"November 5th 2018",dateEndSecondStepPublish:"November 26th 2018",dateEndThirdStepPublish:"January 25th 2019",dateEndFourthStepPublish:"April 15th 2019",dateEndFifthStepPublish:"June 14th 2019",remainingDaysToSecondStep:"2 years",secondStepPassed:!0,currentStepOfPublishingProcess:5,editedByType:null,kuFlag:!1,biosketch:null,coeditorOneBiosketch:null,coeditorTwoBiosketch:null,coeditorThreeBiosketch:null,coeditorFourBiosketch:null,coeditorFiveBiosketch:null,editors:[{id:"126149",title:"Dr.",name:"Anthony",middleName:null,surname:"Ananga",slug:"anthony-ananga",fullName:"Anthony Ananga",profilePictureURL:"https://mts.intechopen.com/storage/users/126149/images/system/126149.jpeg",biography:"Dr. Anthony Ananga is an Assistant Professor in Food Science at Florida A&M University in Tallahassee Florida, USA. He has 10 years of teaching and 15 years of research experience. Dr. Ananga’s research program focuses on grape vinification and bioprocessing, with concentration in the analysis of antioxidant capacity of phytochemicals in muscadine grapes. His lab investigates the bioavailability and efficacy of these phytochemicals in preventing chronic diseases and understanding their effect in fighting obesity. He also uses the functional genomics platform to improve nutraceutical compounds in muscadine grape cells for human health benefits. In addition to that, Dr. Ananga’s lab is focused in food safety with emphasis in fruit and peanut allergens. He strives to understand, characterize, purify, and investigate major food allergens in grapes and peanut.",institutionString:"Florida A&M University",position:null,outsideEditionCount:0,totalCites:0,totalAuthoredChapters:"3",totalChapterViews:"0",totalEditedBooks:"0",institution:{name:"Florida A&M University - Florida State University College of Engineering",institutionURL:null,country:{name:"United States of America"}}}],coeditorOne:null,coeditorTwo:null,coeditorThree:null,coeditorFour:null,coeditorFive:null,topics:[{id:"6",title:"Biochemistry, Genetics and Molecular Biology",slug:"biochemistry-genetics-and-molecular-biology"}],chapters:null,productType:{id:"1",title:"Edited Volume",chapterContentType:"chapter",authoredCaption:"Edited by"},personalPublishingAssistant:{id:"280415",firstName:"Josip",lastName:"Knapic",middleName:null,title:"Mr.",imageUrl:"https://mts.intechopen.com/storage/users/280415/images/8050_n.jpg",email:"josip@intechopen.com",biography:"As an Author Service Manager my responsibilities include monitoring and facilitating all publishing activities for authors and editors. From chapter submission and review, to approval and revision, copy-editing and design, until final publication, I work closely with authors and editors to ensure a simple and easy publishing process. I maintain constant and effective communication with authors, editors and reviewers, which allows for a level of personal support that enables contributors to fully commit and concentrate on the chapters they are writing, editing, or reviewing. I assist authors in the preparation of their full chapter submissions and track important deadlines and ensure they are met. I help to coordinate internal processes such as linguistic review, and monitor the technical aspects of the process. As an ASM I am also involved in the acquisition of editors. Whether that be identifying an exceptional author and proposing an editorship collaboration, or contacting researchers who would like the opportunity to work with IntechOpen, I establish and help manage author and editor acquisition and contact."}},relatedBooks:[{type:"book",id:"6694",title:"New Trends in Ion Exchange Studies",subtitle:null,isOpenForSubmission:!1,hash:"3de8c8b090fd8faa7c11ec5b387c486a",slug:"new-trends-in-ion-exchange-studies",bookSignature:"Selcan Karakuş",coverURL:"https://cdn.intechopen.com/books/images_new/6694.jpg",editedByType:"Edited by",editors:[{id:"206110",title:"Dr.",name:"Selcan",surname:"Karakuş",slug:"selcan-karakus",fullName:"Selcan Karakuş"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"1591",title:"Infrared Spectroscopy",subtitle:"Materials Science, Engineering and Technology",isOpenForSubmission:!1,hash:"99b4b7b71a8caeb693ed762b40b017f4",slug:"infrared-spectroscopy-materials-science-engineering-and-technology",bookSignature:"Theophile Theophanides",coverURL:"https://cdn.intechopen.com/books/images_new/1591.jpg",editedByType:"Edited by",editors:[{id:"37194",title:"Dr.",name:"Theophanides",surname:"Theophile",slug:"theophanides-theophile",fullName:"Theophanides Theophile"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"3092",title:"Anopheles mosquitoes",subtitle:"New insights into malaria vectors",isOpenForSubmission:!1,hash:"c9e622485316d5e296288bf24d2b0d64",slug:"anopheles-mosquitoes-new-insights-into-malaria-vectors",bookSignature:"Sylvie Manguin",coverURL:"https://cdn.intechopen.com/books/images_new/3092.jpg",editedByType:"Edited by",editors:[{id:"50017",title:"Prof.",name:"Sylvie",surname:"Manguin",slug:"sylvie-manguin",fullName:"Sylvie Manguin"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"3161",title:"Frontiers in Guided Wave Optics and Optoelectronics",subtitle:null,isOpenForSubmission:!1,hash:"deb44e9c99f82bbce1083abea743146c",slug:"frontiers-in-guided-wave-optics-and-optoelectronics",bookSignature:"Bishnu Pal",coverURL:"https://cdn.intechopen.com/books/images_new/3161.jpg",editedByType:"Edited by",editors:[{id:"4782",title:"Prof.",name:"Bishnu",surname:"Pal",slug:"bishnu-pal",fullName:"Bishnu Pal"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"72",title:"Ionic Liquids",subtitle:"Theory, Properties, New Approaches",isOpenForSubmission:!1,hash:"d94ffa3cfa10505e3b1d676d46fcd3f5",slug:"ionic-liquids-theory-properties-new-approaches",bookSignature:"Alexander Kokorin",coverURL:"https://cdn.intechopen.com/books/images_new/72.jpg",editedByType:"Edited by",editors:[{id:"19816",title:"Prof.",name:"Alexander",surname:"Kokorin",slug:"alexander-kokorin",fullName:"Alexander Kokorin"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"1373",title:"Ionic Liquids",subtitle:"Applications and Perspectives",isOpenForSubmission:!1,hash:"5e9ae5ae9167cde4b344e499a792c41c",slug:"ionic-liquids-applications-and-perspectives",bookSignature:"Alexander Kokorin",coverURL:"https://cdn.intechopen.com/books/images_new/1373.jpg",editedByType:"Edited by",editors:[{id:"19816",title:"Prof.",name:"Alexander",surname:"Kokorin",slug:"alexander-kokorin",fullName:"Alexander Kokorin"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"57",title:"Physics and Applications of Graphene",subtitle:"Experiments",isOpenForSubmission:!1,hash:"0e6622a71cf4f02f45bfdd5691e1189a",slug:"physics-and-applications-of-graphene-experiments",bookSignature:"Sergey Mikhailov",coverURL:"https://cdn.intechopen.com/books/images_new/57.jpg",editedByType:"Edited by",editors:[{id:"16042",title:"Dr.",name:"Sergey",surname:"Mikhailov",slug:"sergey-mikhailov",fullName:"Sergey Mikhailov"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"371",title:"Abiotic Stress in Plants",subtitle:"Mechanisms and Adaptations",isOpenForSubmission:!1,hash:"588466f487e307619849d72389178a74",slug:"abiotic-stress-in-plants-mechanisms-and-adaptations",bookSignature:"Arun Shanker and B. Venkateswarlu",coverURL:"https://cdn.intechopen.com/books/images_new/371.jpg",editedByType:"Edited by",editors:[{id:"58592",title:"Dr.",name:"Arun",surname:"Shanker",slug:"arun-shanker",fullName:"Arun Shanker"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"878",title:"Phytochemicals",subtitle:"A Global Perspective of Their Role in Nutrition and Health",isOpenForSubmission:!1,hash:"ec77671f63975ef2d16192897deb6835",slug:"phytochemicals-a-global-perspective-of-their-role-in-nutrition-and-health",bookSignature:"Venketeshwer Rao",coverURL:"https://cdn.intechopen.com/books/images_new/878.jpg",editedByType:"Edited by",editors:[{id:"82663",title:"Dr.",name:"Venketeshwer",surname:"Rao",slug:"venketeshwer-rao",fullName:"Venketeshwer Rao"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"4816",title:"Face Recognition",subtitle:null,isOpenForSubmission:!1,hash:"146063b5359146b7718ea86bad47c8eb",slug:"face_recognition",bookSignature:"Kresimir Delac and Mislav Grgic",coverURL:"https://cdn.intechopen.com/books/images_new/4816.jpg",editedByType:"Edited by",editors:[{id:"528",title:"Dr.",name:"Kresimir",surname:"Delac",slug:"kresimir-delac",fullName:"Kresimir Delac"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}}]},chapter:{item:{type:"chapter",id:"52965",title:"Endoluminal Ultrasonography of the Rectum and the Anal Canal",doi:"10.5772/66081",slug:"endoluminal-ultrasonography-of-the-rectum-and-the-anal-canal",body:'\nThe anorectal pathology is very frequent in clinical practice, the patients being addressed for anal fistula, fecal incontinence, hemorrhoidal disease, anal pain, anal fissure, rectocele, rectal prolapse, and rectal tumor. After the clinical and digital rectal exam, the ultrasonography represents the next step in the diagnostic procedure. To obtain reliable details, the transducers have to be as close to the organ of interest as possible. The conventional ultrasound of this region has several limitations considering the position of these organs in the pelvic cavity. The first ultrasound images of the bowel wall using an ultrasound transducer inside a body cavity were obtained in 1950 by Wild [1]. Nowadays the technical improvements of endorectal sonography provide very precise details of rectal wall layers and adjuvant structures, including the pelvic organs. There are two main approaches with corresponding equipment:\n
Anorectal ultrasonography performed by clinicians and radiologists
Endoscopic ultrasound using flexible endoscope‐mounted systems performed by gastroenterologists
Understanding the anatomy of the anorectal region and the main clinical indications remain the cornerstone for this examination, independent of the approach and equipment.
\nThe rectum is the final part of the large intestine, which is about 12–14 cm long and has a diameter of 2–6 cm, related to the content [2]. It begins at the rectosigmoid junction, at the level of the third sacral vertebra and runs inferiorly along the curve of the sacrum to pass through the pelvic diaphragm, where it is continued with the anal canal [3]. The rectum is surrounded by fatty tissue that contains blood vessels, nerves, lymphatics, and small lymph nodes [3]. It is delineated posterior by sacro‐coccygeal bone structure, inferior by the insertion of the levator ani muscles and superior by the peritoneum [2]. The superior one‐third is covered anteriorly and laterally by the pelvic peritoneum. The middle one‐third is covered with peritoneum only anteriorly, which curves onto the bladder in the male and onto the uterus in the female. The lower one‐third lacks of peritoneum and is related anteriorly to the bladder base, ureters, seminal vesicles, and prostate in the male and to the lower uterus, cervix, and vagina in the female [3].
\nThe internal sphincter, the longitudinal muscle layer, and the external sphincter surround the anal canal. It is delineated posterior by the levator ani muscles, laterally by the ischioanal fossa, and anterior by the apex of the prostate and the membranous urethra in male and posterior wall of the vagina in female [2, 3].
\nThe sphincter anal complex is formed by the muscles that represent the continuation of circular layer of the muscularis propria of the rectum, the striated external anal sphincter, and puborectal muscles, which belong to the levator ani muscles [4]. The lowest point of the external anal sphincter represents the upper anal margin; it is called the anal verge and is the principal landmark for rectal measurements [4]. The pectinate (dentate) line is located 1.5–2 cm upwards from the anus and separates the canal anal into the anatomical part located below the line and the surgical part located above the line [4]. The surgical anal canal extends from the pectinate line to the level of the puborectalis sling, which corresponds to the anorectal junction. The pectinate line is not detectable on radiological studies, representing the endoscopic view of the demarcation between the squamous epithelium (anoderm) and the columnar epithelium [4]. The anoderm is directly attached to the internal anal sphincter [4].
\nThe mesorectum is represented by the connective tissue, located between the middle part of the rectum and the upper surface of the levator ani. The mesorectum contains lymph nodes and neurovascular bundles, fat and fibrous tissue. It is limited posterolaterally by the pelvic visceral fascia and ventrally by an upper continuation of the rectogenital membrane (Denonvilliers’ fascia). In females, this dense band forms the rectovaginal septum and in males, the rectoprostatic fascia. Laterally a tiny structure is detected, known as mesorectal or perirectal fascia [4].
\nThe rectal vascularization is provided by the rectal arteries (superior rectal artery from the inferior mesenteric artery, middle rectal artery from the internal iliac artery, and inferior rectal artery from the internal pudendal artery). The rectal venous drainage is realized by the superior rectal vein (that drains into the inferior mesenteric vein) and by the middle and inferior rectal veins (that drains into the iliac veins) [2].
\nThe lymphatic drainage is realized into three circuits:\n
superior station—drains the lymph vessels corresponding to the inferior mesenteric vessels and superior rectal vessels. This circuit has intermediate lymph nodes localized posteriorly and laterally to the rectum.
middle station—drains the lymph vessels into the iliac lymph nodes.
inferior station—drains the lymph vessels into the superficial inguinal lymph nodes [2].
Ultrasonography of the anal canal, the rectum, and the surrounding tissues using intraluminal transducers with transanal/rectal imaging provides high‐resolution imaging with clearly distinguishable tissue‐dependent echo signals. Endorectal sonography is able to depict the rectal wall layers and the adjuvant structures, including the pelvic organs with a high degree of precision. Anal endosonography is carried out to examine the sphincter muscles and the pelvic floor.
\nThe endoluminal ultrasonography is highly effective in most cases of anorectal pathology, as it provides accurate evaluation of rectal, perirectal, anal, and perianal pathology. It might be performed without preparation, but an enema significantly improves the image quality, especially in the oncological patients with stool residues [5]. The examination is carried out in the left recumbent position. In patients with sphincter insufficiency, the knee‐elbow position might be preferred [4].
\nThe endoluminal ultrasound examination is mandatorily done after digital rectal exam and preferred after a proctoscopy examination. In case of an anal stricture, an inserted finger can appreciate the possible passage of the probe.
\nA mechanical or a biplanar transducer with a frequency of 10 MHz or higher is most frequently used [2, 4, 5]. Higher frequencies provide better resolution of the rectal wall and sphincter complex, while lower ones depict better, the components of the mesorectum [4].
\nA condom containing gel is placed over the probe and a thin layer of water‐soluble lubricant is placed on the exterior of the condom [3]. The transducer is inserted in a blind gentle manner and the patient is informed about the potential discomfort or pain during the examination [2].
\nSome authors advice using a 3D 16 MHz probe for the spatial analysis of both the rectum and the surrounding tissues [6].
\nBy convention, the transducer is placed to provide the following image: the anterior aspect of the anal canal will be at 12 o’clock on the screen, right lateral will be at 9 o’clock, left lateral will be at 3 o’clock and posterior will be at 6 o’clock [3]. The depiction of all layers is possible for the whole circumference of the anal canal. At the origin of the anal canal, the “U” shape of the puborectalis sling is the main landmark and must be always identified [3].
\nFive hypoechoic and hyperechoic layers are depicted corresponding to the anal canal wall [7, 8]. These five identified layers, from inner to outer are:\n
the first hyperechoic layer corresponds to the interface between the transducer and the anal mucosal surface,
the second hypoechoic layer is represented by the subepithelial tissues, being moderately reflective. The mucosa and the dental line are not identified by endoluminal ultrasound,
the third hypoechoic layer corresponds to the internal sphincter, which is not completely symmetric, either in thickness or termination. It is continued superiorly with the circular muscle of the rectum. In elderly, this layer is inhomogeneous and more echoic [8],
the fourth hyperechoic layer represents the longitudinal muscle, without constant thickness along the entire anal canal. The increased fibrous stroma is responsible for the echoic aspect of this smooth muscle. In the inter‐sphincterian space, the longitudinal muscle and the striated muscles fibers from the levator ani forms “conjoined longitudinal layer” [9],
the fifth mixed echoic layer corresponds to the external anal sphincter; it has three parts [10]: (1) – the deep part contains the puborectalis muscle, (2) the superficial part has a broad attachment to the underside of the coccyx via the anococcygeal ligament. (3) the subcutaneous part lies below the internal sphincter.
In the axial plane, the upper part of the anal canal corresponds to the puborectalis muscle sling, the deep part of the external anal sphincter, and the complete ring of the internal anal sphincter. The middle part of the anal canal is formed by the superficial part of the external anal sphincter, the conjoined longitudinal layer, the complete ring of the internal anal sphincter, and the transverse perinea muscles. The lower part of the anal canal contains the subcutaneous components of the external anal sphincter [7].
\nFor the rectal examination, especially in oncological patients, special water‐filled balloons might be used (Figure 1). These balloons filled with about 90 ml of water compress the lesions and remove air from the rectum [5].
\nEndocavitary rectal examination – special water filled balloon.
The rectal wall consists of five layers surrounded by perirectal fat or serosa, measuring 2–3 mm. The five layers represent (Figure 2) [3]:\n
the first hyperechoic layer depicts the interface between the balloon/transducer and the mucosal surface
the second hypoechoic layer corresponds to the mucosa and the muscularis mucosa,
the third hyperechoic layer represents the submucosa the fourth hypoechoic layer identifies the muscularis propria
the fifth hyperechoic layer corresponds to the serosa or to the interface with the mesorectum. The mesorectum has an inhomogeneous pattern due to mixed anatomical structures: blood vessels, nerves, and lymphatic vessels.
The rectal wall consists of five layers surrounded by perirectal fat or serosa.
Depending on the position of the probe, the surrounding muscles are identified. The external anal sphincter is detected in the lower third of the rectum. Slightly above, it is replaced by the fibers corresponding to the levator ani muscles, that form puborectalis muscle sling. Between the puborectalis muscle sling and caudally located external sphincter, there is an intersphincterian plane filled with the lowest, tapered part of the mesorectum [11]. This plane is important for surgery and for the staging of the anal cancer [11].
\nEndorectal ultrasound provides an accurate visualization of all pelvic organs adjacent to the rectum: the bladder, the intestinal loops, the seminal vesicles, and prostate in males, and the uterus, cervix, vagina, and urethra in females [3].
\nThe endoscopic approach is nowadays frequently used by the gastroenterologist to assess the anorectal region by ultrasound. Initially, the standard radial endoscopic ultrasound scan was used. The rigid endoscopic ultrasound scan has been used since the early 1980s. Technical improvements provided different types of linear as well as radial scanning devices with frequency varying from 5 MHz to 15 MHz [12]. The echoendoscope is inserted and advanced beyond the lesion, under direct visualization to the rectosigmoid junction. The balloon is slowly inflated and the lumen is filled with water. From this position in the middle of the lumen, the scope is to achieve perpendicular imaging of the rectal wall layers. Once the bladder is identified, the image is mechanically rotated so the bladder is located at 12 o’clock position. Then the instrument is withdrawn slowly, with the transducer kept at the middle of the rectum. No torching of the instrument is recommended, as this causes tangential imaging and possible inaccurate assessment of the depth of tumor penetration. In males, upon withdrawing the probe at 12 o’clock position, the seminal vesicles and the prostate are displayed. In females, this manoeuvre brings in view the uterus and then the vagina, with a hyperechoic band in the center that represents air [13].
\nDifferent ultrasound techniques improve daily practice in benign and malignant pathology. Local contrast agents facilitate the depiction of fistulas through direct administration (Figure 3). Intravenous contrast agents define vascular pattern for tumor pathology related to anorectal region or prostate (Figure 4).
\n(a) Anal fistula—physical exam. (b) Local contrast agent (Sonovue in this particular case) was administered through the external end of the fistula for better delineation of the size and fistula tract.
(a) Anorectal tumor—surgically removed. (b) Intravenous contrast agents (Sonovue) was administered. In the venous phase, the contrast agent was washed-out from the tumor (becoming hypoechoic), permitting a better deliniation of the tumor from the adjacent organs.
Hydrogen peroxide was investigated as an image‐enhancing contrast agent for improving the depiction and the characterization of the fistulas during endoanal ultrasonography [14]. After a conventional endoanal ultrasound is performed, external perianal openings are cannulated and approximately 1 ml of peroxide is administered. After reinsertion of the endoprobe, the entire course of the echogenic fistula, including its relation to the internal and external sphincters and the levator ani muscle are depicted in real time, which facilitates surgical planning [14].
\nThe use of contrast agents within the bloodstream gained more and more applications in the last few years, as it enables the detection of very slow blood flow in vessels measuring as little as 40 μm. Contrast enhanced ultrasound (CEUS) provides valuable information regarding the characterization of a circulatory bed and the evaluation of the neoangiogenesis process [15]. Quantitative parameters are determined during the passage of the contrast agents through a region of interest, mainly by analysis of the time‐intensity curve parameters [15]. For rectal cancer, CEUS provides noninvasive biomarkers of tumor angiogenesis and might predict patient prognosis [16]. Contrast enhanced endorectal sonography increases the detection of prostate cancer and facilitates the target biopsies [17, 18].
\nThe Doppler ultrasonography provides information regarding the flow within large vessels. Doppler‐guided hemorrhoidal ligation was introduced into clinical practice 20 years ago (Figure 5) [19]. Doppler‐guided hemorrhoidal dearterialization is a safe and effective method to treat grades II–IV hemorrhoidal diseases, especially in those with previous anal surgeries or previous alterations of fecal continence, when an additional procedure might represent a risk of definitive incontinence [19].
\nDoppler ultrasonography provides information regarding the flow within large vessels in the anorectal region.
The transanal real‐time elastage in rectal cancer ranges is between 80stography was demonstrated to yield valuable information regarding elastic properties of the anal sphincter, especially in patients with fecal incontinence. A pathological elastogram is considered, when predominantly hard elements are detected. This technique was investigated in different pathologies, anorectal surgery in irradiated and non‐irradiated individuals and Crohn\'s disease. Based on studies conducted by Allgayer et al. [20, 21] the transanal real‐time elastography with quantitation of sphincter elastic properties yields no further diagnostic and prognostic information compared to conventional endosonography.
\nThe three‐dimensional ultrasound is provided from the synthesis of a high number of parallel transaxial two‐dimensional images [3]. The image can be rotated, tilted, and sliced to allow the physician to analyze different section parameters, different angles and to assess accurately distances, areas, angles, and volumes [3]. Three‐dimensional endorectal ultrasonography is useful for assessing the depth of submucosal invasion in early rectal cancer and for selecting therapeutic options [22].
\nThe management of patients with anorectal neoplasm requires specific information regarding:\n
tumor spread (T features),
detailed evaluation of mesorectal fascia,
extramural venous invasion,
lymph nodes involvement (N features),
presence of distance metastasis (M features) [4].
The tumor‐node‐metastasis (TNM) system represents the standard of care for rectal and anal staging (Table 1) [23].
\n\nThe ultrasound feature of rectal cancer is a hypoechoic lesion that disrupts the normal five‐layer sonographic structures of the rectal wall. The distal border of the tumor must be precisely depicted in relation to the anterior peritoneal reflection (in males, the relation of the distal border of the tumor to the seminal vesicles and in females, to the cervix are determined) [24].
\nThe ultrasound images relevant to T staging are:\n
Tis corresponds to the first hypoechoic layer expended, but without the second hyperechoic layer involvement.
T1 invades the submucosa, but without muscularis propria involvement, it is detected in ultrasound when the second hyperechoic layer is stippled or broken in appearance, but generally intact.
T2 ultrasound appearance is depicted when the second hyperechoic layer is completely disrupted and the mass may extend into the second hypoechoic layer.
T3 corresponds to the perirectal fat or serosa invasion, the outer hyperechoic layer is disrupted.
T4 is easy diagnosed as the tumor is extended into neighboring organs [25].
\n | Anal carcinoma | \nRectal carcinoma | \n
---|---|---|
Tx | \nPrimary tumor cannot be assessed | \nPrimary tumor cannot be assessed | \n
T0 | \nNo evidence of primary tumor | \nNo evidence of primary tumor | \n
Tis | \nCarcinoma in situ, Bowen disease, high grade squamous intraepithelial lesion (HSIL), anal intraepithelial neoplasia II‐III (AIN II‐III) | \nCarcinoma in situ: intraepithelial or invasion of lamina propria | \n
T1 | \nTumor 2 cm or less in the greatest dimension | \nTumor invades submucosa | \n
T2 | \nTumor more than 2 cm, but not more than 5 cm in the greatest dimension | \nTumor invades muscularis propria | \n
T3 | \nTumor more than 5 cm in the greatest dimension | \nTumor invades subserosa or into non‐peritonealized perirectal tissues | \n
T4 | \nTumor of any size invades adjacent organ(s) (e.g., vagina, urethra, bladder) | \nTumor perforates visceral peritoneum (T4a) and/or directly invades other organs or structures (T4b) | \n
Nx | \nRegional lymph node cannot be assessed | \nRegional lymph node cannot be assessed | \n
N0 | \nNo regional lymph node metastasis | \nNo regional lymph node metastasis | \n
N1 | \nMetastasis in the perirectal lymph nodes | \nMetastasis in 1 to 3 regional lymph nodes N1a – Metastasis in 1 regional lymph node N1b – Metastasis in 2–3 regional lymph nodes N1c – Tumor deposit(s), i.e., satellites in the subserosa or in nonperitonalized pericolic or perirectal soft tissue without regional lymph node metastasis | \n
N2 | \nMetastasis in unilateral internal iliac and/or inguinal lymph nodes | \nMetastasis in 4 or more regional lymph nodes N2a – metastasis in 4–6 regional lymph nodes N2b – metastasis in more regional lymph nodes | \n
N3 | \nMetastasis in perirectal and inguinal lymph nodes and/or bilateral internal iliac and/or bilateral inguinal lymph nodes | \n\n |
M0 | \nNo distal metastasis | \nNo distal metastasis | \n
M1 | \nDistal metastasis | \nM1a – metastasis confined to one organ M1b – metastasis in more than one organ or the peritoneum | \n
TNM staging principle for the anal and rectal carcinoma according to the current classification of International Agency for Research on Cancer/World Health Organization [23].
The accuracy of T stage in rectal cancer ranges is between 80 and 95% [26, 27]. The T2 tumors are frequently over-staged as T3 tumors, because peritumoral inflammation cannot be accurate differentiated from desmoplastic reaction [28]. From the clinical point of view, this overstaging has no significant impact as T2 tumors have the same prognosis as T3 tumors with less than 1 mm spread [4] (Figure 6). The assessment of T3 tumors is very important, especially the measurement of the depth of extramural spread in the mesorectal fat, since T3 tumors with less than 5mm mesorectal invasion have a 5‐year survival rate of 85% and T3 tumors with more than 5 mm mesorectal invasion have a 5‐year survival rate of 54% [4, 29, 30]. Minimally invasive T3 tumors present an invasion into the mesorectal fat less than 2 mm beyond the muscularis propria and advanced T3 tumor is characterized by an invasion of more than 3 mm [24]. These measurements are difficult to be performed in lower anal canal tumors, on its anterior wall or in patients with a small amount of perirectal fat [4]. The endoscopic ultrasound sensitivity for T stage is highest for advanced disease (96.4% for T3 and 95.4% for T4) compared to early disease (87.8% for T1 and 80.5% for T2) [31].
\nRectal tumor staging. T3 corresponds to the perirectal fat or serosa invasion, the outer hyperechoic layer is disrupted.
Rectal tumor staging T3. A round hypoechoic lymph node, measuring 5 mm is detected.
The extramural venous invasion is detected by magnetic resonance imaging using a score proposed by Smith et al. [32] and represents an important prognostic factor since the detected venous invasion had a 3.7 times increased relative risk of metachronous metastatic disease [33].
\nThe assessment of lymph node in patients with rectal cancer represents a debated issue. The ultrasound defines the size, border, shape, and echogenicity and enables tissue biopsy sampling. The features suggestive for malignancies are: enlarged nodes (≥1 cm in short axis), hypoechoic appearance, round shape, and smooth border (Figures 7 and 8) [24]. As the accuracy of the endocavitary ultrasound for N stage is moderate [31], fine needle aspiration should be used when critical decision regarding neo‐adjuvant chemotherapy is proposed [24].
\n\nRectal tumor. 2D ultrasound image and elastography. The rectal tumor is depicted stiffer than the tumor‐free rectal wall and the perirectal fat tissue (colored in blue).
Different new ultrasound techniques has improved the diagnosis of the rectal and anal canal tumors.
\n3D‐endocavitary ultrasound allows an accurate measurement of rectal tumors and identification of anatomical relationships, which assists the surgical planning procedure (Figure 9).
\n3D endocavitary ultrasound offers a spatial assessment of the rectal tumor.
Contrast enhanced ultrasound depicts the vascular pattern for rectal lesions [15]. Quantitative parameters might be measured during the passage of the contrast agents through a region of interest, mainly by analysis of the time‐intensity curve parameters [15]. For rectal cancer, CEUS provides noninvasive biomarkers of the neoangiogenesis and might predict patient prognosis (Figure 10) [16].
\nContrast enhanced ultrasound (Sonovue administered intravenously) depicts the vascular pattern for rectal lesions.
The elastography become an “extension” of the clinical sense, strengthening and confirming the final diagnosis by its ability to measure the tissue elasticity. Different techniques are used: strain elastography imaging (SEI), shear wave imaging (acoustic radiation force impulse imaging (ARFI) and shear wave elasticity imaging (SWEI). ARFI and SWEI are quantitative methods. No data have been published so far concerning their use in the assessment of the rectal tumors. The rectal tumors are stiffer than the tumor‐free rectal wall and the perirectal fat tissue. An optimal differentiation between benign and malignant lesions was obtained at a cut‐off value of the mean strain ratio cut‐off value of 1.25 [34] (Figures 11 and 12).
\nRectal tumor. 2D ultrasound image and elastography. The rectal tumor is depicted stiffer than the tumor‐free rectal wall and the perirectal fat tissue (colored in blue).
Lymph nodes involvement in a rectal tumor. 2D ultrasound image and elastography. The elastography identifies more malignant lymph nodes than detected by 2D ultrasound (stiffer than the tumor‐free rectal wall and the perirectal fat tissue – colored in blue).
Preoperative neoadjuvant chemo‐radiotherapy (N3–4 or lymph nodes involvement) is used to downstage rectal cancer in order to improve survival and to allow sphincter‐preserving low anterior resection [12]. Considering the necrosis, inflammation, and fibrotic changes following neoadjuvant therapy, the assessment of tumor nodes through ultrasound might not be adequate. The T re‐stage accuracy is 50% (Figure 13) [35–38]. The accuracy can be improved by depicting the intense and chaotic vasculature of residual tumor tissue through Doppler technique [39] or contrast‐enhance ultrasound [40, 41].
\nRectal tumor. (a) In diagnosis the tumor was assessed as T3, invading the perirectal fat. (b) After neoadjuvant radiochemotherapy the tumor decreased in size (8 mm), but still invaded the perirectal fat.
Endoscopic ultrasonography of rectum can also be used for rectal cancer recurrence post‐operatively with high accuracy [41, 42]. In some cases the ultrasound feature of tumor recurrence cannot be differentiate by post‐surgery fibrosis or inflammation [24]. Obtaining biopsy samples through fine needle aspiration improves the detection of rectal recurrences. Also depiction of the vascularization through Doppler techniques or CEUS can considerably increase the specificity of transrectal ultrasound in differentiating tumor relapse from fibrosis [39, 40, 43]. The endoscopic ultrasound is recommended for follow up after surgery at six months interval for two years [24]. The anastomotic sites might be revealed as cystic lesions with heterogeneous wall thickening and fine needle aspiration might detect mucin containing inflammatory cells in the absence of malignant cells [44].
\nPatients with fecal incontinence frequently associate anal sphincter injury as a consequence of obstetrical trauma, anorectal surgery or accidental injury [45]. Endoanal ultrasonography can accurate depict the anal sphincter complex and surrounding perirectal tissues [45]. Anal sphincter tears are depicted as a discontinuity of the hypoechoic structure corresponding to the internal anal sphincter or of the more heterogeneous external anal sphincter [46]. Obstetric injury is located anterior and frequently involves both sphincters [46]. The accuracy of endoanal ultrasound for sphincters disruption is very high: 95% [47, 48].
\nThe main causes for anal fistulae and abscesses are: Crohn\'s disease, post‐operative infection, radiotherapy. The Parks classification of perianal fistulae depicts four types: inter, trans, extra and suprasphincterian [49], according to their extension to the external anal sphincter and to the puborectalis muscles. The ultrasound appearance of the fistula is a hypoechoic linear structure with possible hyperechoic reflections (air) between anal canal or rectum or vagina. The use of hydrogen peroxide‐enhanced anal endosonography provides better depiction of fistula and its relation to the internal and external sphincters and the levator ani muscles [50]. Alternative to hydrogen peroxide are represented by the new ultrasound contrast agents: Levovist or SonoVue [51]. The sonographic appearance of the abscess is a mass either anechoic or hypoechoic (with internal echoes corresponding to tissue debris) [52]. This technique is recommended for fistula diagnosis and monitoring in patients with Crohn\'s disease. The use of contrast agents and 3D techniques provides accurate assessment of complex fistula mapping before planning medical or surgery treatment. Also, it is useful for puncturing the abscesses in the operating room using an echoendoscopic approach or a surgery technique [52].
\nEndoluminal ultrasonography of the rectum and the anal canal is a valuable method for the assessment and staging of rectal and anal canal tumors. It is also frequently used for perianal fistulae mapping, anal sphincter tears depiction in patients with fecal incontinence and for abscesses identification and puncturing. Different ultrasound techniques provide morphological, functional and vascular pattern accurate assessment of rectal tumors before surgery, after radiotherapy/chemotherapy, and after surgery (for the detection of relapses).
\nThe population is increasingly exposed to accidents, both in daily routine and at work. In Portugal, among 209,390 non-death accidents that occurred in 2017, almost 4% were bone fractures that are limitative for the active population and require a long time of recovery [1]. Many research groups have been working on bone regeneration for over 10 years, but this has not led to effective therapy in a clinical setting. If it was successful, it would enhance the quality of life for millions of people and significantly reduce the absence to work due to fractures which are considered the second higher cause of working day lost.
The bone is a natural composite containing organic components (mainly collagen type I and fibrillin) and inorganic crystalline minerals (such as hydroxyapatite (Hap)), defined as hard tissue [2, 3, 4]. The characteristic of the collagen fibers in their structure gives it high tensile strength and its mineral substances impart high compressive strength and thus excellent mechanical resistance.
Bone, namely in the diaphysis, is made up of cortical or compact bone that contains its own blood vessels and cells, which aid in its growth and regeneration. It has many types of cells, such as osteoblasts, osteocytes, osteoclasts, and a matrix of non-mineralized collagen (osteoid). Bone tissue comprises several functions, such as: (i) provide structural integrity, and all the necessary support to the soft tissue of the body, constituting the global support of the majority of the muscles, (ii) protect vital organs, and (iii) help to balance the minerals, since the bone tissue stores calcium and phosphate making them more resistant and able to maintain a balance of blood concentration [5, 6, 7]. Bone is known to self-regenerate: pos-natal bone maintains an intrinsic capacity for well-ordered growth, remodeling to meet mechanical needs, and renewal after damage [8].
Major bone defects are the result of injury, trauma, nonunion after a fracture, infection, or abnormality, resulting in long-term deformities, such as limb shortening, leaving patients with reduced bone structure and function [9, 10, 11]. It should be noted that the most transplanted tissue after blood is bone [12, 13].
The gold standard treatments for bone defects are still bone grafts. These can be used alone or combined with other materials in order to promote bone healing through osteoinduction, osteoconduction, and osteogenesis [14]. These bone grafts may be from autograft (taken from the patient), allograft (taken from another patient) and xenograft (obtained from an animal) origins or even manipulated with synthetic biomaterials. Additionally, prostheses can also be used, but they usually need a second surgery later on due to some complications that may appear, such as the formation of bone callus or hernias. Autografts are still considered the gold standard treatment due to their osteogenic, osteoinductive, and osteoconductive capacity. However, there is a limitation in tissue extraction from the amount that is required. Allografts taken from other donors or corpses present a high risk of immune rejection, reduced bioactivity and a high risk of pathogen transmission [7, 15, 16, 17, 18].
When there are fractures with a bone defect exceeding a critical size, the bone is not able to self-regenerate and, therefore, requires the use of a temporary implant (natural and/or synthetic) to serve as support and cells to help bone regeneration [19]. In this way, tissue engineering (TE) has emerged [20].
The concept of TE was implemented in 1993 by Langer and Vacanti. They specified that “TE is an interdisciplinary field that relates the principles of biology and engineering to the production of tissue functional substitutes” [21]. So, they presented specific characteristics and applications in biodegradable three-dimensional (3D) scaffolds. Ideally, they should be highly porous, having highly interconnected pore networks with a pore size suitable for cells to migrate and differentiate whenever necessary [22]. However, the biggest challenge of scaffolds is related to mass transport of nutrients and secretion of waste in tissue [6]. It is important cells used in 3D cultures of scaffolds be able to mimic the morphology, functionality, and biology of the tissue. These cell cultures are necessary to analyze mechanisms of chronic diseases and the impact of drug treatments or to produce different tissues for major defects in vivo, in this study, the bone. Bioreactors appeared to improve the field of cell culture on 3D support [23, 24].
This chapter intends to perform a critical analysis of the state of the art regarding full bone TE towards the selection of the most appropriate solution of temporary implants. Thus, the optimum conditions (static vs. dynamic), material, cells, and/or the inclusion of growth factors for the repair of large bone defects are discussed. Hence, there are two scientific questions to which this chapter intends to address: (i) which is the most suitable combination of scaffold design and fabrication using a certain biomaterial and biological components to facilitate or accelerate bone regeneration and (ii) what are the in vitro conditions more suitable to achieve an optimized in vivo response.
Bone tissue is known for its ability to self-regenerate on its own. However, if the fracture becomes a critical bone defect, the bone loses this ability. From 1934 to the present day, some authors argue that a bone defect becomes critical when it is over two times the diameter of the bone defect [10, 11, 25, 26, 27].
These critical-sized defects may result from infection, malformation, and traumatic injuries, which may lead to bone loss in the patient [28, 29, 30, 31, 32, 33]. In this case, as bone cannot self-regenerate, it is necessary to use a temporary implant (natural and/or synthetic) to support bone regeneration with cellular incorporation. To achieve this, successfully, it is first necessary to consider the mechanical properties of the native bone tissue.
It is known that the mechanical properties of the bone vary according to age, anatomical location, and bone quality. Within the biomechanical properties of the bone (resistance, stiffness, and fatigue), the elastic modulus is the most attracting variable in research due to its importance to characterize bone pathologies and also in the design orientation of artificial implants. Bone strength and elasticity are anisotropic. The compact bone is stronger under compression and stiffer when loaded longitudinally along the diaphyseal axis than in the transverse radial directions. In trabecular bone, its mechanical properties depend on both the porosity and the architectural desirability of the individual trabeculae [3]. The mechanical properties of human bone are summarized in Table 1.
Human bone | Trabecular | Cortical |
---|---|---|
Porosity (%) | 50.00–90.00 | 1.00–20.00 |
Young’s modulus E (GPa) | 0.05–0.10 | 17.00–20.00 |
Compressive strength (MPa) | 5.00–10.00 | 131.00–224.00 |
Tensile strength (MPa) | 1.50–38.00 | 35.00–283.00 |
Elongation at break (%) | 0.50–3.00 | 1.07–2.10 |
References | [2, 3, 34, 35] |
Human long bone properties.
Implants need to be accepted by the human body, where there are guarantees for cell survival in a safe and supportive environment. Moreover, mechanical damage or failure caused by stress shielding must be prevented. The scaffolds need to have an appropriate modulus of elasticity to match bone properties. Scaffolds with a highly porous structure are favorable for cellular activities, including fixation and proliferation, which will contribute to bone neoformation and regeneration and adjust the mechanical properties in terms of Young’s strength and modulus [36].
So, an important key factor is concerned with the type of materials to be used in the implant. Biopolymers are biocompatible and biologically active materials as they promote cell adhesion and growth.
To help in the engineering of long bone fracture regeneration, artificial fractures are typically manufactured in models in vivo [23, 37]. Various animal models are studied in vivo before its application in humans.
The bone, in vivo, is exposed to mechanical stimulation by muscle contraction and body movements, and the mechanical load induces an increase in bone mass formation [38]. During body movement, the forces applied results in changes in hydrostatic pressure, fluid flow-induced shear stress, direct cell strain, and electric fields [38, 39, 40].
In order to identify the mechanical properties necessary for humans, it is important to study what kind of in vivo studies and which animal models have been considered in the literature (see Table 1). The choice of the most appropriate animal model is an important step in clinical translation, because it will help to better understand and propose innovative strategies for bone regeneration. Each animal model has pros and cons [41], and in each study, a specific set of parameters is used. That is why it is difficult to compare the different studies available [42, 43]. There are various models that were studied in vivo for full bone regeneration. Rabbit, rat, ovine (sheep or bovine), canine, and goat are the most used.
There are six studies on the literature where a rabbit model was considered. Nather and their co-workers [44] evaluated the effect of bone marrow mesenchymal stem cells (BMMSCs) on the biological healing of a 1.5 cm cortical bone allograft in the tibia of adult rabbits. In their study it was shown that BMMSCs can improve cortical allograft binding rate, reabsorption activity, bone formation, and osteocyte cell count. In 2013, Khojasteh et al. [45] developed a scaffold using particulate mineralized bone/fibrin glue/mesenchymal stem cells (MSCs). Through the alizarin staining method, they verified that there was a deposition of mineralized matrix. This was also demonstrated by RT-PCR analysis of osteocyte markers. At the end of 3 weeks, osteocalcin, osteopontin, and collagen I messenger RNA were produced. They concluded that this implant would be a promising combination for vertical bone augmentation around implants inserted simultaneously into the tibia of rabbits. Lee et al. [46] studied the effect of autologous BMMSCs seeded into gel foam on structural bone allograft healing in 1.5 cm femoral defect of white rabbits. They concluded that the use of MSCs influenced the bone formation, resorption, and angiogenesis. Jang et al. [47] extruded porous HAp scaffolds, which were set in a drill-cut femur rabbit bone. After 4 and 8 weeks of implantation, micro-CT scanning images showed material degradation and integration of the sample into the native bone. In this period, the morphological behavior was similar in bone tissue-scaffold junction. Chowdhary et al. [48] had evaluated the early response of bone tissue to micro threads with an oxidized titanium implant (4 mm in diameter and 8 mm in length) between the macro threads. The study was tested in rabbit legs, tibia, and femur. The bone regeneration happened near the micro threads, and the bone growth in femur indicated that the cancellous bone seems to be more sensitive to micro thread stimulation. Recently, in 2018, Tovar and co-workers [49] used 3D printing, specifically robocasting/direct writing, to develop a scaffold with 100% beta-tricalcium phosphate (β-TCP) (350 μm pore diameter) in order to regenerate critical-sized rabbit radius defects in vivo. A 3 cm incision was made in a critical defect of 11 mm, approximately, in the radio, and the periosteum was resected to at least 1.5 cm proximal and distal to the defect. This scaffold proved to be good for bone tissue engineering (BTE) since at 8 weeks it showed bone formation with signs of resorption of the scaffold. The amount of bone formed was increased from week to week, regenerating the medullary space, and at 24 weeks the scaffold was significantly resorbed.
Rats are also another in vivo model referred in the literature. Saravanan et al. [50] introduced in an albino-Wistar rat with a critical-sized bone defect in the tibia a scaffold containing chitosan, gelatin, and graphene oxide by freeze drying. They concluded that this scaffold promoted increase in osteoblasts and increased the collagen content, accelerating the bridging of the rat tibial bone defect.
A model of an ovine with 35 mm tibial defect was then used by Smith et al. [51] to study full bone regeneration. They produced a scaffold using blending process of poly (L-lactic acid)-poly(ε-caprolactone) (PLLA: PCL 20:80) with and without marrow-derived skeletal stem cells. They divided the tests into three different groups: empty defect, scaffold alone, and scaffold with cells. Radiographic has shown poor bone formation upon 12 weeks. However, there was a greater tendency for bone formation in the scaffold with cells.
Regarding the canine model, two studies were published in the literature. In 1996, Bragdon and co-workers [52] showed that, in canine femurs, an oscillating motion of 20 μm does not affect osseointegration. However, 40 and 150 μm oscillating motion of implants does not support bone growth. Recently, Barba et al. [19] implanted in vivo, in a canine model calcium-deficient scaffold (0.3 mm height and 5 mm diameter) with Hap considering different pore architectures and compared with two ceramics, a biphasic calcium phosphate (BCP) and a β-TCP with rat mesenchymal stem cells (rMSCs). Pores ranged from 10 to 300 μm. With this, calcium-deficient scaffold and Hap triggered osteogenic differentiation of rMSCs. They concluded that calcium-deficient HAp foam scaffolds with a spherical concave macroporosity allow osteoinduction.
Animal studies are needed to understand bone regeneration. Variables such as the amount of bone formation and its kinetics, mechanical properties and safety obtained by the scaffold, including the presence of toxic degradation in different organs and in terms of inflammatory response need to be understood in detail [42]. However, bone fractures performed in animals do not represent the complexity of healing human fractures [23, 37]. The potential of each different type of cells both in vitro and in vivo plays here a key role.
Ko and co-workers studied the potential of human-induced pluripotent stem cells (hiPSCs) against the human bone marrow mesenchymal stem cells (hBMMSCs). Both cells were placed in rat bone defects, with a size of 2 cm, which is similar to the human value mentioned above. They concluded that both hIPSCs and hBMMSCs have osteogenic potential in vivo [53]. However, some authors showed the existence of risks of teratoma formation after transplantation in hIPSCs [28, 54, 55, 56]. In literature, the use of MSCs seems to significantly help bone regeneration in in vivo studies [31, 45, 57, 58, 59]. Some authors defend that the addition of growth factors to cell-scaffold constructs promotes bone regeneration [60]. Nevertheless, Kleinhans et al. [61] showed that a good culture capable of mimicking tissue morphology, functionality, and biology, for example, using bioreactors, is sufficient to obtain a homogeneous cell distribution of soluble factors.
There is a great deal of discussion today about the incorporation of growth factors. In this chapter, authors defend the nonnecessity of its incorporation, since upon the right environmental conditions, cells are actually able to secrete the optimal extracellular matrix (ECM) components. Therefore, a good mechanically stimulated culture combined with transcription factors influences cells to bone formation.
In vitro models are required to accurately record the physiology of healing at a site of bone fracture since bone takes weeks to differentiate in vitro [62] and wound healing can take weeks to months [23, 63]. In vitro studies are advantageous because they offer a controlled environment to experimental test molecular and cellular hypotheses. However, cells cultured in vitro are not replicates of their in vivo counterparts [28, 64].
When the bone is subjected to a mechanical force, electrical potentials are generated, which play an important role in bone remodeling. To mimic this natural process, bioreactors were created and are nowadays widely used. These 3D systems allow the control of various parameters, such as temperature, pH, oxygen concentration, growth factors, and mechanical stimuli, among others, and modulate cell growth more easily. These bioreactors can simulate the human bone environment and allow the study of the role of various factors in scaffolds or preculture scaffolds in vivo. In addition, to provide adequate nutrition and removing residues from all cells in the scaffold, fluid flow can be manipulated to physically stimulate bone growth [39]. Bone is constantly exposed to mechanical stimulation due to muscle contractions and body movements that result in changes in hydrostatic pressure, direct cell strain, fluid flow-induced shear stress, and electric fields. In addition, bone cells are more sensitive to mechanical stimulation. Therefore, providing physical stimulation in bioreactors becomes a key component of BTE strategies [65].
The following studies demonstrate the importance of performing in vitro testing in order to find the best strategy.
Jang et al. [66] developed a HAp scaffold to mimic native bone through a multipass extraction process with the addition of osteoblast-like cells, with pores of 150 ± 20 μm in diameter and with a pore structure of 50 ± 10 μm which is thin enough for rapid bone resorption. With in vivo tests and in vitro tests, they confirmed that the scaffold used is appropriate for graft without inflammatory reactions and bone formation after 8 weeks of implantation. The scaffold’s porosity is a critical parameter enabling medium exchange and nutrient diffusion, which is a key role in cell proliferation. So, the optimization of the scaffold’s porosity is important to help cell growth, formation of vascularization, and the diffusion of nutrients [67].
Roohani-Esfahani and their co-workers developed a glass–ceramic scaffold, with dimension size 6x6x6mm, by direct ink writing mimicking cortical bone with 600 μm custom-made nozzle. In the work, they concluded that a scaffold with hexagonal pore shapes (450 μm, 550 μm, 900 μm, and 1200 μm) present the highest compressive strength, compared to the other designs [68].
Abbot and co-workers, in 2016, developed a silk scaffold with osteoblasts to evaluate in vitro culture that stimulated bone differentiation and regeneration. In the end, they concluded that it was evident the mineralization in the scaffold with silk seeded with this type of cells [23].
Tovar and co-workers [49] had developed a cylindrical scaffold with 10.5 mm length, 4.5 mm outside diameter and 2.25 mm inside diameter, 330 μm struts, and around 400 μm pore spacing. They used a 330-μm-diameter extrusion nozzle with a velocity of 8 mm/s. The existence of macrometric and micrometric porosity in the scaffold helped in its degradation, which allowed the biomechanical load to the healing bone. This may explain the rapid development of bone properties in the regenerated tissue that is highly indicative of complete healing when it is complemented with the remodeling of the original bone morphology.
Recently, Barba et al. [19, 69] concluded that the geometric parameters of the scaffold, like curvature, influence bone tissue regeneration. They demonstrated that spongy scaffolds with concave pores attracted a large amount of ectopic bone compared with scaffolds with prismatic geometries.
Through the existing studies, both in vivo and in vitro, one can get an idea of both material and biological components essentials to a proper bone regeneration. In the first phase, it is necessary to understand which scaffold design is the most appropriate and which biomaterials are to combine it with the AM technique.
For bone regeneration, it is necessary to consider that the scaffold must restore the normal biomechanical role of the tissue. Table 2 shows different types of existing materials and their characteristics and some guidelines about how to obtain an ideal scaffold. However, there are other important features that need to be taken into account related to the different biological and physical signals involved in order to simulate the mechanism of remodeling in a natural environment, but more importantly, the scaffold must have the exact mechanical properties to withstand the loads the original bone held [6, 70]. The biomaterials used in the scaffolds must have a suitable rate of degradation in order to support bone regeneration. This rate of degradation depends on the corrosion resistance of the material used, which is affected by the chemical and physical characteristics of the scaffold [36].
Having into consideration the referred above and combining this information with the natural organization of bone (trabecular and cortical), the best strategy for BTE should pass by the use of collagen type I in the trabecular bone region and Hap in the cortical zone [80, 81]. Despite their advantages and the fact that they are already present in the bone native structure, their proper manipulation is only possible through their combination with synthetic polymers. The most suitable are poly(ε-caprolactone) (PCL) or polylactic acid (PLA) because they are both approved by the Food and Drug Administration. PCL is a stable, biocompatible, biodegradable polymer (from 12 to 48 months) and easy to handle to achieve the desired mechanical properties. Due to its low melting point (60°C) [82, 83], it can be easily combined with the collagen. PLA is a biocompatible polymer, more hydrophilic than PCL, and its handling is similar to the use of PCL. Hydrophilicity accelerates polymer degradation as it accelerates polymer and scaffold moisture [84]. However, it has a high melting point, which could be combined with Hap. With these materials, scaffolds can be produced with two methods: conventional and additive manufacturing (AM).
Some studies have used conventional methods for producing scaffolds. However, these methods have no adequate control over pore size and design or interconnectivity [8, 85]. In order to address these problems, since the mid-1980s [86], a new manufacturing type of technology called AM has emerged. Its potential is enormous and overcomes the capabilities of the conventional technologies to produce scaffolds with a complex architecture and with the intention to achieve an appropriate mechanical response to the desired application [36].
Nowadays there are several approaches to AM for various applications. The main approaches are fused filament fabrication (FFF), three-dimensional printing (3DP), stereolithography (SLA), and selective laser sintering (SLS). Each process goes through several steps: (i) development of the 3D model through computer-aided design (CAD); (ii) the files are stored in standard triangular language (STL) format, which is a CAD file format that supports 3D printing and computer-aided manufacturing (CAM); and (iii) these files are inserted into the input devices to create 3D models in a layer-by-layer process [36]. In addition, there are still two processes where it uses the same principles of layer manufacturing: selective laser melting (SLM) [87, 88, 89, 90] and electron beam melting (EBM) [91, 92, 93]. Both are used to produce metal scaffolds, although SLM can also process polymers and ceramics [3, 94, 95].
FFF, Figure 1, or melt-extrusion is an extrusion-based process and is the simplest 3D printing method (see Table 3) [36, 96]. Fine thermoplastic polymers in the form of filaments or granules are cast and extruded through a nozzle that allows flow in a horizontal and vertical plane (XY plane) [36]. To extrude it is necessary to have heating of the material, which causes degradation. However, the disadvantages of this technique can be overcome. The most suitable and desired mechanical properties can be achieved for the desired purpose with the combination of biomaterials. With this technique, it is already possible to extrude some bioceramics, such as HAp [97, 98, 99].
Fused Filament Fabrication (FFF) process.
Scaffolds | References | |
---|---|---|
Natural polymers | Biomaterials are widely used because of their biocompatibility, degradation, bioactivity, mechanical kinetics, tissue nonspecificity, and their intrinsic structural similarity to the extracellular matrix of native tissues. They also promote biological recognition, which can positively support cell adhesion and function | [71, 72] |
Synthetic polymers | Easy to manipulate the properties of the material to achieve the appropriate mechanical behavior. At a microscale it presents the architecture, 3D composition, and active molecular reactive groups. In a macroscale, they have porosity, stiffness, and elasticity | [6] |
Metals | Are used in long bones to better attach to the bones where there is minimal movement between the implant and the host tissue and provide physiological loading functionality to the implant site | [15, 73] |
Ceramics | Have been used because of their ability to sustain compressive loads | [6, 74, 75] |
Ideal scaffolds | ||
Should exhibit the adequate mechanical properties, pore size, and biological activity, serve as cell support, and guarantee new bone formation and thus the use of more than one material (a natural with a synthetic one) | [76, 77, 78, 79] |
Characteristics of the different materials used to produce a scaffold.
Fused filament fabrication | |
---|---|
Advantages | Disadvantages |
Speed Low cost Simplicity Flexibility | Poor surface quality Need for heating in the molding process ➔ degradation of polymer materials |
Advantages and disadvantages of the fused filament fabrication process.
It is critical that the first layer is maintained at a temperature slightly below its set point to ensure successful adhesion between the layers. The 3D structure is determined by several factors, such as nozzle diameter, deposition rate, path spacing of the same layer, layer thickness, and deposition angle [96].
In the FFF technique, it is possible to control layer thickness and print orientation. The structural geometry of scaffolds is determined by the position and orientation of the filaments, which provide various pore shapes such as triangular, parallelogram, hexagonal, and also nonuniform shapes [100]. In this technique, there are two factors that affect the filament size, and consequently the pore size, which are the deposition velocity and the rotational velocity.
Scaffold requirements in terms of response (left) and what should be taken into account (right) (adapted from [106]).
It is necessary that the scaffolds in bone regeneration be biocompatible, biodegradable, osteoinductive (raising and cell maturation), and osteoconductive (provide a platform for cell growth) [39]. Scaffolds for bone regeneration should meet several specific criteria, such as filling any bone defect, ensuring pore interconnectivity, and having a pore architecture in order to promote bone formation and facilitate the exchange of oxygen bone growth [101, 102, 103]. The design of the scaffold can influence both the mechanical properties and cellular behavior [100, 104, 105] as highlighted in Figure 2.
A satisfactory bone growth leads to certain requirements. Porosity should be above 50% and pore size between 50 and 400 μm. It is difficult to achieve a “perfect” scaffold for bone regeneration due to pore design and size and a porosity distribution that mimics the native tissue [107, 108]. In the literature, there are no quantitative criteria that specify porosity or pore size or topology for bone regeneration. Porous scaffolds ranging in size from 50 to 500 μm are known to promote cell migration and vascularization, while micropores and nanopores control interaction with proteins and ion exchange with extracellular fluids [19, 109].
The dogma of molecular biology is the basis for producing most bone cell and ECM components.
Bone remodeling is divided into five stages: activation, resorption, reversal, formation, and, finally, mineralization (see Figure 3). It is a process in which the old bone is reabsorbed and there is new bone formation. The cells that are involved in bone remodeling are osteoblasts, osteoclasts, and osteocytes, which actively participate in osseointegration and repair. Osteoclasts activate bone resorption, while osteocytes regulate bone homeostasis and osteoblasts form bone [15, 110].
In addition to bone cells, there are other cell lines that can be used in bone regeneration, which are human embryonic stem cells (hESCs), induced pluripotent stem cells (iPSCs), stem cells, and fibroblasts. According to Kuhn [111] and other workers [112, 113], hESCS present a rapidly proliferating rate. However, their transplantation induces uncontrollable spontaneous differentiation and can the teratoma formation may occur. Another type of stem cell is iPSCs. They can differentiate into several cells. However, there are studies that show that these cells can also give rise to teratomas and, in studies that distinguish high-quality lines from the iPSCs, allowed the detection of large duplications of genes that could potentially affect the differentiation and pluripotency of these cells [28, 99]. For these reasons, these cells are not considered the best ones for bone regeneration. Compared to fibroblasts, stem cells have a greater ability to migrate, so these type of cells are the most suitable cells for bone regeneration. Kargozar [58] recently studied the osteogenic potential of different MSCs, such as those derived from human bone marrow, umbilical cord (UC-MSCs) and adipose (AD-MSCs). It concluded that BMMSCs, according to collected histological data, is the most appropriate.
Bone Remodeling Cycle.
The combination of scaffold, AM, and bioreactor culture shows great potential for creating automated production ecosystems that will enable the formation of commercially available products for BTE application. Efficient nutrient and oxygen transport are important for this type of applications. To this end, bioreactor systems have tried to overcome this difficulty. Rotating-wall vessels are limited to small scaffolds as they do not provide optimal mass transport to the center of the scaffold and are not efficient in osteogenic differentiation, due to shear stress values transmitted to cells. On the other hand, agitated tanks have a major disadvantage regarding the circulating flow pattern that strikes cells against the bioreactor wall, which damages them and can lead to cellular apoptosis [114]. Finally, perfusion bioreactors are the best suited for BTE as they promote oxygenation throughout the whole scaffold, through improved mass transfer and shear stress, can expose cells to mechanical stimulation, and, therefore, obtain a much better cell distribution [6, 39, 61, 115, 116].
Scaffold architectures were designed in SolidWorks 2018 software. The design was bioinspired. This inspiration came from the natural organization of long bones, as represented in Figure 4. The diaphysis is composed of cortical bone (external region) which covers the trabecular bone (internal region). The trabecular bone has a larger surface area than the cortical bone and has a bone volume fraction ranging from 5% to a maximum of 60% [117]. It is known that the cortical zone corresponds to ~20% of the total diameter [118]. Bearing this in mind, it is expected that mimicking this type of organization, the mechanical behavior of the final scaffolds would be better and closer to the natural tissue.
Natural organization of long bones.
The design considered has a height of 10 mm and diameter of 30 mm (see Figure 5). Thus, the cortical zone, the outer part of the scaffold, has a thickness of 6 mm and the trabecular zone, the inner part, has 18 mm. In the middle, there is a canal that corresponds to the medullar cavity. As happens in the native tissue, the region corresponding to the trabecular bone presents a higher porosity than the cortical one. So, the proposed scaffold has pores with different sizes between the different parts, bigger in the trabecular and smaller in the cortical (400 and 300 μm of pore diameters, respectively). According to Zhang et al. [119], these pores are within the required values, since exceeding the pore size of 400 μm, cells do not sense the 3D, resulting in poor ECM production. Moreover, they are organized in a radial way, with a significant difference between the cortical zone and the trabecular zone.
Cylindrical scaffold.
The projected scaffold presents a total porosity of 42%, whereas the cortical part has approximately 5% porosity. This porosity mimics the normal porosity in the native bone (see Table 1) as shown by Fernandez-Yague et al. [120] and Wang et al. [3]. The trabecular zone has a porosity of approximately 57%. This porosity is also in agreement with the authors previously mentioned. However, this value is closer to the lower limit. This porosity can be improved by the addition of horizontal channels, but its inclusion would decrease the mechanical behavior of the proposed scaffold.
Since pore interconnectivity is considered by some authors a key point to cell migration and proliferation, another design is proposed, and (see Figure 6) it is inspired by a DNA strand. As the scaffold gains height, the base rotates, with a rotation angle of 36°. This was considered to guarantee that the end of the filaments was supported on all layers. Also, in this case, pores diverge gradually, so that the differences between cortical bone and trabecular bone can be noticed.
DNA chain-inspired cylindrical scaffold.
In this scaffold, pores range from 50 to 1500 μm in each layer, which is in agreement with the Zadpoor [121] and Szpalski [39]. However, the minimum required pore size is 100 μm, to make it easier to transport oxygen and nutrients and discard waste products [39, 121, 122]. For proper cell propagation, according to Bael [123], pore size should not pass the 1000 μm. Compared to the previous design presented, this one presents a slightly lower porosity in total, of around 38%, in which the cortical and trabecular parts have 22% and 49% porosity, respectively.
According to the authors Andrzejewska [34], Keaveny et al. [2], and Xiao et al. [124], the porosity of the trabecular zone is near the defined porosity values. However, the porosity of the zone corresponding to the cortical part is far above the maximum value of the defined values found in Table 1. In order to decrease this porosity, it is necessary to shrink the pore size used. Despite this limitation, this scaffold already has the advantage of fully interconnected pores, which will facilitate cell growth and the transport of oxygen and nutrients.
The combination of all supports of TE, which were described above, could lead successfully to bone formation. As biomechanics and TE advanced, it is easy to foresee the development of a new model for bone formation in which the use of an original scaffold leads to long bone fracture healing.
Bone defects are a constantly growing problem, affecting thousands of people around the world, which causes a loss in life quality, and most of the time, for an active population, it may take long periods of recovery. Until now, there are no synthetic substitutes that meet the mechanical and biological requirements for the long-term cure of critical-size bone defects. To overcome this health problem, the use of temporary biocompatible and biodegradable scaffolds becomes the best choice. Structures produced by AM have superior advantages compared to the conventional techniques, mainly due to better control over the desired architecture. Moreover, the choice of the AM technique to produce these scaffolds is essential to ensure control, namely, in terms of biological, physicochemical, and mechanical properties.
Considering all types of materials available, associated with the desired bone regeneration and the use of synthetic polymers, as PCL or PLA, combined with collagen type I for the trabecular region and Hap for cortical region, seems to be the best strategy to follow. To obtain the designed structures with these biomaterials, the most suitable AM technique is the FFF. For the selection of the final scaffold within the two proposals, further studies need to be performed. However, a third option could be also considered, which would include the cortical region of the first proposed scaffold (ensuring the required mechanical resistance) and the trabecular zone of the second one (assuring a proper porosity and pore interconnectivity to allow cell migration, nutrient, and oxygen exchange).
Among the most commonly used bioreactors for bone regeneration, perfusion bioreactors appear as the most suitable, because it improves osteogenic proliferation and differentiation due to improved mass transfer and adequate shear stress. When making a design proposal for bone regeneration, it is necessary to study the mechanical effects, such as stress and tension, and link them
This work is supported by the Fundação para a Ciência e Tecnologia (FCT) and Centro2020 through the Project references UID/Multi/04044/2019, PAMI—ROTEIRO/0328/2013 (NO. 022158), and MATIS (CENTRO-01-0145-FEDER-000014-3362). It is also funded by the projects insitu.Biomas (POCI-01-0247-FEDER-017771), Bone2Move (PTDC/CVT-CVT/31146/2017), and Stimuli2BioScaffolds (PTDC/EME-SIS/32554/2017).
The authors declare no conflict of interest.
additive manufacturing beta-tricalcium phosphate bone marrow mesenchymal stem cells bone tissue engineering. computer-aided design electron beam melting extracellular matrix Food and Drug Administration fused filament fabrication growth factors hydroxyapatite human bone marrow-derived mesenchymal stem cells human mesenchymal stem cells human embryonic stem cells mesenchymal stem cells poly(ε-caprolactone) polylactic acid rat bone marrow stromal cell stereolithography selective laser melting selective laser sintering tricalcium phosphate tissue engineering
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