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‘Technology developed on the basis of real needs, in a participatory way together with people who exf cost‐legged robots, as illustrated pressed these needs, contributes significantly to their human development by enhancing their knowledge and creativity’
—E.E. Cepolina (Snail‐Aid, Italy)
1. Introduction
The mobile robotics systems are beginning in applications related to - security and the environmental surveillance: prevention of disasters and intervention during disasters with all possible kinds of missions ensuring the security.
The general objective of the International Advanced Robotics Program (IARP) [1] is, as foreseen by its status, ‘to encourage development of advanced robotic systems that can dispense with human work for difficult activities in harsh, demanding or dangerous environments, and to contribute to the revitalization and growth of the world’.
Through a first book devoted to the ‘Emerging Robotics and Sensors Technologies for Humanitarian Demining and Risky Interventions’ [2], the IARP working group HUDEM (Robotics Assistance to Mine‐clearing) summarized some important results of R&D activities focusing on the robotics and associates technologies applied to the solution of the Humanitarian demining.
The challenges posed by the use of robotics systems have been examined and partially solved in the FP7‐TIRAMISU project. The following chapters focus on the contribution of the Royal Military Academy (RMA) to these challenges.
2. Robotics systems developed at RMA
2.1. 1997–2002
Under the HUDEM’97, project funded by the Belgian Ministry of Defence, with the close cooperation of our partners of the European Network CLAWAR [4], we focused on the design and development of small low‐cost‐legged robots [10], as illustrated in Figure 3.
Wheels have the advantages of engineering simplicity, low friction on a smooth surface and they enable the robot to move at a high speed. Laying down a track for wheels to run on is a way of extending the use of wheels to soft and rough ground. But wheels and tracks have a main weakness. They have poor performance in an unstructured environment when faced with a vertical step or a discontinuous surface. More than half of Earth\'s land area precludes wheeled and tracked vehicles. In many of these natural terrains, legs are well suited.
Some reasons explain the choice of walking robots [6, 7, 8, 9]:
The last six‐legged robot we designed [5] could be equipped with a chemical sensor and followed up with a series of electro‐pneumatic platforms, among which a sliding robot could be equipped with several tools.
Several partners of the IARP and CLAWAR Working Groups HUDEM developed similar concepts, but no one could satisfy the basic requirements of cost‐effectiveness. The control of such machines is not obvious (Figure 1).
Figure 1.
Multi‐legged robot, as first prototype (AMRU 5).
2.2. 2002–2006
From the previous experience and the cost‐effectiveness requirements, it quickly appeared that a basic constraint on the design of a robot was the modularity and the conviviality of the human‐machine interface (HMI) in order to ease the interpretation of the operator.
Our next design focused on a three‐wheeled lightweight teleoperated platform (TRIDEM) that was refined under the project FP7‐TIRAMISU [11, 14,] (Figure 2).
Figure 2.
The three‐wheeled TRIDEM robot.
The last prototype of TRIDEM is controlled by a wireless joystick. An overall view of the robot control hardware is shown in Figure 3. A microcontroller placed on the robot is responsible for the robot control. The joystick is connected to a computer, via a USB port. The commands of the human operator are sent to the robot through this joystick and wireless connection between computer and microcontroller. Information concerning robot movements, the presence of an obstacle, the presence of a mine, and so on, are sent from the microcontroller to the computer. All these parameters may be visualized by a human operator, thanks to a graphical user interface (see Figure 4). A wireless video camera, mounted on the robot arm, sends images to the same graphical interface, so that a human operator is informed about the work environment of the robot.
Figure 3.
Robot control hardware.
Figure 4.
Graphical user interface (HMI).
In most robotic applications, in Humanitarian demining in particular, the robot has to be operated by an inexperienced user. Therefore, a simple and intuitive interface is required especially when the robot has many motors and degrees of freedom. We developed such an interface for TRIDEM (Figures 3 and 4).
2.3. 2006–2010
Although multi‐legged or similar multi‐wheeled robots offer promising solutions and despite the current maturity of such platforms, the preference was given to the conversion of existing commercial platforms. Exchange of information was then pursued through the organization of annual IARP workshops, some of them located in countries confronted with mined areas: Kosovo, Egypt, Tunisia, Croatia or in countries pursuing national funded R&D related to the Humanitarian demining: Austria, Japan and Belgium (Figure 5).
Figure 5.
The ROBUDEM.
At the RMA, we then focused on the adaptation of two commercial platforms: the ROBOSOFT, renamed ROBUDEM, laterally equipped with a three‐dimensional (3D) scanning carrier of a VALLON metal detector (Figure 5) and progressively adapted for an autonomous behaviour‐based navigation control [12], finally tested in the context of the FP6 project VIEW‐FINDER focusing on the Robotics assistance of security services.
A detailed study of the state‐of‐the‐art has been entrusted to Daniela Doroftei [13].
An optimal combination of sensors (location of the robot, detection of explosives and vision sensory package) was analysed and tested under the project FP7‐TIRAMISU. A partial combination has been developed at the RMA, focused on the use of a limited number of sensors: a behaviour‐based architecture for mine detection (project RSTD MB07 [13]) and a behaviour‐based navigation for search and inspection interventions (project VIEW‐Finder [15]). Figure 6 summarizes the control architecture.
Figure 6.
General control architecture of the ROBUDEM.
2.4. 2011–2015
Under the FP7‐TIRAMISU project [20], another commercial mobile robotic platform (the tEODor) was used for the integration with a metal detector array developed by VALLON (the MCMD) (Figure 7).
Figure 7.
The teoDOR equipped with the MCMD and a TCP box positioning system.
An important drawback of the standard EOD tEODor platform is that it did not feature any autonomous capabilities. To overcome such a constraint, the platform was upgraded by RMA with necessary electronics, sensors, computing power, motor control units and power sources in order to be able to execute remote‐controlled and semi‐autonomous tasks [18].
A geo‐positioning and communication device, the TCP box developed by DIALOGIS/PROTIME, partners of TIRAMISU, was integrated with the system for geo‐referencing the data.
The validation tests of the system were conducted on a dummy minefield at the SEDEE‐DOVO (Demining Service of the Belgian Defence) and led to the desired Technical Readiness Level 7.
Furthermore, a similar platform was adapted under the FP7‐ICARUS project (2012–2016—Robotics Assistance for Search and Rescue Operations), including vision capabilities enabling an assessment of terrain traversability and thereby allowing a semi‐autonomous navigation facing the traversability issues [16, 17, 19, 21].
3. Remotely piloted aircraft system (RPAS) deployment for mine action
The deployment of the remotely piloted aircraft system (RPAS) was extensively used within the TIRAMISU project [20] for the support of different scenarios (Figure 8).
Figure 8.
Overview of the complete RPAS.
Over the 3 years (2012–2015), the RPAS was deployed in test areas as well as in real missions. The next sections shortly introduce some of the missions done with the RPAS.
4. RPAS survey of honeybees
Survey of honeybees with an RPAS was a cooperation we did in 2014 together with the Croatian partners CTRO and the University of Zagreb within the TIRAMISU project. We used the RPAS in order to make the survey of honeybees by monitoring their activities and to analyse their ability to detect buried mines. The initial first proposal was prepared by Milan Bajic (CTRO) and Haris Balta (RMA) and field mission was done in the period of end of July beginning of August 2014 at the CTRO test centre in Cerovac, Croatia.
The scenario was that the conditioned (trained) honeybees fly over the area where landmines (real, with explosives, not the dummy landmines) were placed, or over area where remains of the explosive exist after the use of mechanical machines. The images shot from a RPAS (hovering or flying very slow) provided a time sequence of images of one area. Processing and analysis of time sequence enables assessment of bee\'s density in space and time.
Therefore, we used the RPAS in hover‐mode‐flying altitude around 25 m with the high‐resolution digital camera and collecting sequences of 60–85 images per each section of the minefield. Collected images were processed and analysed offline by CTRO and the University of Zagre.
5. RPAS use for hazardous suspected area
In 2015, we prepared a campaign for operational validation of RPAS [3, 22–24]. This work was conducted together with CTRO and ULB, Belgium, and partially with the support of the University of Zagreb. We used the RPAS in order to perform oblique flights and near infrared (NIR)‐mapping flights of the suspected hazardous area (SHA) and the minefields. The initial first proposal was prepared by Milan Bajic (CTRO) and Haris Balta (RMA) and A field mission was done in April 2015 in the Region Murgici, Croatia (44°38\'53.28” N 15°28\'10.55” E.). Figure 9 shows the SHA (cross‐hatched in pink colour).
Figure 9.
HSA operational area Murgici, Croatia.
6. Oblique survey of the indicators of mine presence
Some of the existing tools for the detection of mine presence indicators are limited by nadir images shooting. On the plane terrain, it is acceptable, but on hilly terrain or in mountains this is very limiting. When the RPAS is used on terrains where objects of interest (indicators of mine presence) exist, the oblique images can provide very valuable data of the mine‐suspected area. We used the RPAS on our second mission and collected data for these activities (Figure 10).
Figure 10.
Sequence of NiR images over the SHA.
General overview flight above the SHA. Flying altitude is around 120 m. Detection of a possible anomaly is shown in Figure 11.
Figure 11.
Flight above the SHA with a recognition of an anomaly.
Vertical inspection flight above the anomaly is to confirm it as shown in Figure 12.
Figure 12.
Vertical flight above the anomaly with zoom.
7. RPAS deployment in post‐flood mine action with TIRAMISU end‐user Bosnia and Herzegovina Mine Action Centre (BHMAC), 2014
RPAS was deployed in post‐flood mine action activities in Bosnia and Herzegovina in the period of May to June 2014 [3]. We used the RPAS to assist the team from the Bosnia and Herzegovina Mine Action Centre (BHMAC) in detecting the locations of Explosive Remnants of War (ERWs) and performing damage assessment, mapping and aerial inspection. The ERWs were displaced as a result of landslides caused by the floods.
Detected mine, re‐located due to the landslides, is shown in Figure 13.
Figure 13.
Detected mine in the region: Sarajevo‐Vogosca, Bosnia and Herzegovina, 4 June 2014.
First post-processed results of the regions Zavidovici‐ Dolac and Olovo, in central Bosnia and Herzegovina, with geo‐referenced aerial images, were produced (as shown in Figure 14). The RPAS was used for providing 3D‐maps, orthophotos and digital terrain models of the environment to analyse the effects of the landslides on mines and ERW. This result has been used by Bosnia and Herzegovina Mine Action Centre (BHMAC) for the localization of displaced ERW, damage assessment and documentation purposes.
Figure 14.
Sequence of oblique images around the SHA.
8. Conclusions
The development of a Robotics System for demining operations has to take several constraints into account: a high level of protection against the environmental conditions (dust, humidity, temperature, etc.), protection and resistance against vibration, mechanical shocks and instability factors, a sufficient autonomy and reliable communications between the mobile platform and the operator.
In this chapter, some of the most relevant aspects of both technical and environmental aspects have been underlined. Other robotics systems have been co‐developed with the partners of the FP7‐TIRAMISU project. We invite the reader to consult [20].
Acknowledgments
These activities were partially funded by the Belgian Ministry of Defence (HUDEM\'97, 1997–2002) (BEMAT and MB07, 2003–2008), by the European Commission (CLAWAR 1998–2002) (FP6 VIEW‐FINDER Project Contract 045541 2007–2010), (FP7 TIRAMISU Contract 284747 2012‐2015), and (FP7 ICARUS Contract 285417 2012‐2016).
\n',keywords:"robotics, demining, navigation, sensors, image processing",chapterPDFUrl:"https://cdn.intechopen.com/pdfs/53260.pdf",chapterXML:"https://mts.intechopen.com/source/xml/53260.xml",downloadPdfUrl:"/chapter/pdf-download/53260",previewPdfUrl:"/chapter/pdf-preview/53260",totalDownloads:742,totalViews:180,totalCrossrefCites:0,totalDimensionsCites:0,hasAltmetrics:0,dateSubmitted:"May 14th 2015",dateReviewed:"September 15th 2016",datePrePublished:null,datePublished:"August 30th 2017",dateFinished:null,readingETA:"0",abstract:"During the Humanitarian‐demining actions, teleoperation of sensors or multi‐sensor heads can enhance-detection process by allowing more precise scanning, which is useful for the optimization of the signal processing algorithms. This chapter summarizes the technologies and experiences developed during 16 years through national and/or European‐funded projects, illustrated by some contributions of our own laboratory, located at the Royal Military Academy of Brussels, focusing on the detection of unexploded devices and the implementation of mobile robotics systems on minefields.",reviewType:"peer-reviewed",bibtexUrl:"/chapter/bibtex/53260",risUrl:"/chapter/ris/53260",book:{slug:"mine-action-the-research-experience-of-the-royal-military-academy-of-belgium"},signatures:"Yvan Baudoin, Daniela Doroftei, Geert de Cubber, Jean‐Claude\nHabumuremyi, Haris Balta and Ioan Doroftei",authors:[{id:"176831",title:"Dr.",name:"Yvan",middleName:null,surname:"Baudoin",fullName:"Yvan Baudoin",slug:"yvan-baudoin",email:"yvan.baudoin@skynet.be",position:null,institution:null}],sections:[{id:"sec_1",title:"",level:"1"},{id:"sec_2",title:"1. Introduction",level:"1"},{id:"sec_3",title:"2. 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Landmine detection, demining and other applications. Woodhead Publishing in Mechanical Engineering, 2011. ISBN 978‐1‐84569‐786‐0'},{id:"B3",body:'Haris B., Geert De C., Yvan B., Daniela D. UAS deployment and data processing during the Balkans flooding with the support to Mine Action“8th International Advanced Robotics Programme (IARP) Workshop on Robotics for Risky Environment (RISE), 28-29 January 2015, Lisbon, Portugal.'},{id:"B4",body:'CLAWAR. www.clawar.org(accessed on 2016‐06‐22). Clawar Task 9 report, 1999.'},{id:"B5",body:'Habumureyi, J.C. Adaptive neuro‐fuzzy control for a walking robot with 6 pantograph‐based legs. PhD Thesis, Free University of Brussels, 2004.'},{id:"B6",body:'Gonzalez de Santos P., Garcia E., Estremera J., Armada M.A. SILO‐6: design and configuration of a legged robot for humanitarian demining. International Symposium Clawar, Brussels, 1998.'},{id:"B7",body:'Berns K., Kepplin V. Lauron‐II a general purpose walking machine for rough terrain\', International Symposium Hudem\'97, Royal Military Academy, Brussels, June 1999.'},{id:"B8",body:'Nonami K. Development of autonomous mine detection six‐legged walking robot for Humanitarian demining, 5th IARP Workshop, Tokyo, Japan, June 2005.'},{id:"B9",body:'Randall M.J., Pipe A.G. An intelligent control architecture and its application to walking robots. Proceedings of International Workshop on Advanced Robotics and Intelligent Machines, Salford, UK, 1997, ISSN 1363‐2698.'},{id:"B10",body:'Baudoin Y., Dorofteï I. Hierarchical control of a Hexapod walking robot. International Journal of Robotica & Management 14‐1, 2009, ISSN 1453‐2069.'},{id:"B11",body:'Doroftei I., Baudoin Y. Using mobile robots for a clean and safe environment‐a difficult challenge, in Proceedings of 2012 International Conference and Exposition on Electrical and Power Engineering (EPE), Iasi, Romania, 2012, pp. 41-46.'},{id:"B12",body:'De Cubber G., Berrabah, S.A., Doroftei D., Baudoin Y., Sahli H. Combining dense structure from motion and visual SLAM in a behavior‐based robot control architecture. International Journal of Advanced Robotics Systems, vol. 7, issue 1, 2010.'},{id:"B13",body:'Doroftei D. Behavior based navigation techniques. Internal report MoD Study MB07, October 2006 (http://mecatron.rma.ac.be/Research/Behavior‐based_Robot_Control.html).'},{id:"B14",body:'Doroftei D., Baudoin Y. Development of a semi‐autonomous demining vehicle. Proceedings of the 7th IARP WS HUDEM\'2008, The American University in Cairo (AUC), Cairo, Egypt, 28-30 March 2008.'},{id:"B15",body:'De Cubber G., Dorofeti D., Marton G. Development of a visually guided mobile robot for environmental observation as an aid for outdoor crisis management operations, Proceedings of the IARP Workshop on Environmental Maintenance & Protection, July 22-23, 2008, Baden‐Baden, Germany.'},{id:"B16",body:'De Cubber G., Doroftei D. Human victim detection and stereo‐based terrain traversability analysis for behavior‐based robot navigation, handbook using robots in hazardous environments. Landmine detection, demining and other applications. Woodhead Publishing in Mechanical Engineering, 2011, pp. 476-496. ISBN 978‐1‐84569‐786‐0.'},{id:"B17",body:'De Cubber G. Variational methods for dense depth reconstruction from monocular and binocular video sequences, PhD Thesis. VUB-RMA, 2010 (http://mecatron.rma.ac.be/Publications.html).'},{id:"B18",body:'Balta H., Wolfmayr H., Braunstein J., Baudoin Y. Integrated Mobile Robot System for Landmine Detection. Proceeding of 12th IARP WS HUDEM 2014, Zadar, 25 April 2014 (http://mecatron.rma.ac.be/pub/2014/IARP‐6‐BALTA.pdf).'},{id:"B19",body:'De Cubber G., Balta H. Terrain traversability analysis using full‐scale 3D processing. in Proceeding of 8th IARP Workshop on Robotics for Risky Environments, Lisbon, January 28, 2015.'},{id:"B20",body:'www.fp7‐tiramisu.eu (accessed on 2016‐06‐17).'},{id:"B21",body:'www.fp7‐icarus.eu (2016).'},{id:"B22",body:'De Cubber G., Balta H., Doroftei D., Baudoin Y., 2014. UAS deployment and data processing during the Balkans flooding. 12th IEEE International Symposium on Safety, Security, and Rescue Robotics 27-30 Oktobar 2014, Hokkaido, Japan.'},{id:"B23",body:'Mechanical Demining Equipment Catalogue 2010, GICHD, Geneva, January 2010. ISBN 2‐940369‐33‐X, http://www.gichd.org/fileadmin/GICHD‐resources/rec‐documents/MDE‐Catalogue‐2010.pdf, accessed on 2016‐06‐16'},{id:"B24",body:'A Study of Mechanical Application in Demining, GICHD, Geneva, May 2004. ISBN 2‐88487‐023‐7, http://www.gichd.org/fileadmin/GICHD‐resources/rec‐documents/Mechanical_study_complete.pdf, accessed on 2016‐06‐16.'}],footnotes:[],contributors:[{corresp:"yes",contributorFullName:"Yvan Baudoin",address:"yvan.baudoin@skynet.be",affiliation:'
Royal Military Academy, Department of Mechanical Engineering, Unmanned Vehicle Centre, Brussels, Belgium
Department of Mechanical Engineering, Technical University GS Asachi, IASI, Romania
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Marais",authors:[{id:"112229",title:"Prof.",name:"Chris",middleName:null,surname:"Aldrich",fullName:"Chris Aldrich",slug:"chris-aldrich"},{id:"112232",title:"Prof.",name:"Hansie",middleName:null,surname:"Knoetze",fullName:"Hansie Knoetze",slug:"hansie-knoetze"},{id:"135327",title:"Ms.",name:"Corne",middleName:null,surname:"Marais",fullName:"Corne Marais",slug:"corne-marais"}]},{id:"36189",title:"Optical Technologies for Determination of Pesticide Residue",slug:"optical-technology-for-determination-of-pesticide-residue",signatures:"Yankun Peng, Yongyu Li and Jingjing Chen",authors:[{id:"113343",title:"Prof.",name:"Yankun",middleName:null,surname:"Peng",fullName:"Yankun Peng",slug:"yankun-peng"},{id:"116636",title:"Dr.",name:"Yongyu",middleName:null,surname:"Li",fullName:"Yongyu Li",slug:"yongyu-li"},{id:"116637",title:"Dr.",name:"Jingjing",middleName:null,surname:"Chen",fullName:"Jingjing Chen",slug:"jingjing-chen"}]},{id:"36190",title:"High Resolution Far Infrared Spectra of the Semiconductor Alloys Obtained Using the Synchrotron Radiation as Source",slug:"high-resolution-spectra-of-semiconductor-s-alloys-obtained-using-the-far-infrared-synchrotron-radi",signatures:"E.M. Sheregii",authors:[{id:"102655",title:"Prof.",name:"Eugen",middleName:null,surname:"Sheregii",fullName:"Eugen Sheregii",slug:"eugen-sheregii"}]},{id:"36191",title:"Effective Reaction Monitoring of Intermediates by ATR-IR Spectroscopy Utilizing Fibre Optic Probes",slug:"effective-reaction-monitoring-of-intermediates-by-atr-ir-spectroscopy-utilizing-fibre-optic-probes",signatures:"Daniel Lumpi and Christian Braunshier",authors:[{id:"109019",title:"Dr.",name:"Christian",middleName:null,surname:"Braunshier",fullName:"Christian Braunshier",slug:"christian-braunshier"},{id:"111798",title:"MSc.",name:"Daniel",middleName:null,surname:"Lumpi",fullName:"Daniel Lumpi",slug:"daniel-lumpi"}]}]}]},onlineFirst:{chapter:{type:"chapter",id:"68254",title:"Cell Attachment and Osteoinductive Properties of Tissue Engineered, Demineralized Bone Fibers for Bone Void Filling Applications",doi:"10.5772/intechopen.88290",slug:"cell-attachment-and-osteoinductive-properties-of-tissue-engineered-demineralized-bone-fibers-for-bon",body:'\n
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1. Introduction
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Bone voids may occur due to trauma, surgery, tumor resections, or other factors. For decades, surgeons have used bone grafting to treat a wide variety of bone defects. Bone grafts may contain up to three of the vital properties necessary for bone formation: osteoconductivity, osteoinductivity, and osteogenicity [1]. The property of osteoconductivity describes the way the graft acts as a scaffold on which host cells can attach and proliferate, leading to osseointegration. Osteoinductivity, on the other hand, describes the cellular signaling potential of a graft. Whether endogenous or recombinant, specific growth factors, such as bone morphogenetic protein 2 (BMP-2), attract host cells to a graft and encourage mesenchymal stem cells to differentiate into lineage-committed bone cells. Finally, osteogenicity describes the ability of a bone graft to form bone matrix directly, which can only happen when live cells capable of producing bone matrix are contained within the graft. Bone graft options may contain varying amounts of these properties and are chosen based on the characteristics that the patient needs in order to achieve bone fusion. There are several graft options available, including autograft, synthetic bone substitutes, and allografts.
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Autologous bone is harvested from the site of surgery in the patient or a second site, such as the iliac crest. It is still considered the gold standard by many surgeons because it can theoretically provide all three vital properties for bone formation, does not provoke an immune response, and has a long history of use. However, the use of autograft bone is associated with several disadvantages such as donor site morbidity, insufficient supply, and variable quality [2, 3]. Up to 30% of patients experience significant donor site morbidity as well as infection risk, increased operative time, blood loss, and the potential for arterial and nerve injury [4]. Additionally, autograft is limited, and the quality may be poor depending on the patient’s health. For example, diabetes, low bone mass, and smoking can all increase the risk of fusion failure as well as intraoperative complications [5].
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Synthetic bone substitutes are designed with the goal of mimicking the natural properties of human bone. They can be comprised of a variety of materials including but not limited to, ceramics, cements, and bioactive glass. These grafts are generally biocompatible, osteoconductive, and may be mechanically similar to bone [6, 7]. This category of graft has typically been manufactured to contain porosity similar to bone, but may lack other desirable surface properties, such as hydrophilicity or a rough surface on which cells can attach. Synthetic bone substitutes have gained popularity due to reduced cost and ready availability; however, they may have mismatched resorption rates compared to bone and generally lack osteogenic and osteoinductive properties [8]. Some synthetics, such as recombinant human BMP-2, depend almost solely upon osteoinductivity and often result in rapid bone formation. However, several studies indicate substantial side effects, including osteolysis, heterotopic bone formation, and swelling/edema [9, 10, 11]. While synthetics have improved over the last few decades, mimicking natural bone has proven difficult, and allografts, being natural bone, have continued to be a reliable source of grafting material.
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Allograft bone is obtained from deceased human donors and has a long history of use. It is readily available in a variety of forms, shapes, and sizes providing surgeons with several graft options suitable for various procedures [12, 13, 14]. Allografts can provide up to all three properties necessary for bone formation. For example, mineralized bone allografts have similar osteoconductive properties to autograft while avoiding complications such as donor site morbidity [15]. Some mineralized grafts have been processed to increase desirable characteristics such as increased surface area on which cells can attach as well as increased coefficient of friction to prevent the graft from shifting once implanted. Other allografts, such as demineralized bone matrix (DBM) are both osteoconductive and osteoinductive. To produce DBMs, acid demineralization is used to remove a portion of the mineral component of bone, thus exposing the active signaling proteins necessary to induce new bone formation. The ability of DBMs to facilitate bone healing was demonstrated in clinical applications as early as 1889 when Dr. Nicholas Senn reported using demineralized bone as a vehicle for antiseptics to treat patients with osteomyelitis [16]. However, it was not until 1965, when Dr. Marshall Urist characterized specific proteins trapped within the bone matrix, that it was understood that bone morphogenetic proteins (BMPs) contributed to the osteoinductive property of DBMs [17]. Since the discovery of BMPs, other proteins, such as those associated with angiogenesis, have also been found to contribute to the process of bone healing and regeneration [18]. In addition to containing active signaling proteins, optimal surface characteristics of DBMs are essential for supporting cellular attachment and proliferation. For example, it is crucial to provide enough space for blood vessel formation and for the patient’s own cells to migrate into and proliferate on the scaffold [19, 20]. Therefore, some allograft processors work to maintain ideal porosity for cell migration and angiogenesis. Other processes are designed to create a hospitable topography for cell attachment and proliferation as well as to enhance handling characteristics to facilitate implantation and mitigate migration.
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DBMs are available in varying forms, including powders, putty, strips, and moldable paste. These grafts often contain carriers such as glycerol, starch, or hyaluronic acid to improve handling. Without a carrier, bone grafts may be difficult to implant in the desired area, or may drift away from the area during surgical irrigation or exposure to blood. However, despite improved handling characteristics, it has been reported that some carriers may inhibit osteoinductive potential [21]. In addition, a carrier dilutes the bone concentration and may easily elute from the surgical site, effectively reducing the implant volume. With these limitations in mind, a novel DBM with unique fiber technology was recently developed as described in Section 2. These fibers (Figure 1) are composed solely of demineralized cortical bone and are designed to provide surface features conducive for cellular attachment and easily moldable handling characteristics, all without the addition of a carrier. The purpose of this chapter is to present original research, detailing the composition, osteoinductive nature, cell attachment properties and endogenous bone growth factor content of these bone fibers through in vivo and in vitro test methods.
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Figure 1.
Rehydrated moldable demineralized fibers.
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2. Methodology
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2.1 Fiber generation
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The fibers described here are referred to as L-MDF (LifeNet Health-Moldable Demineralized Fibers, LifeNet Health, Virginia Beach, VA and clinically available as part of PliaFX® and OraGRAFT® Prime brands). The particular fibers studied below were prepared from human cortical long bones that were aseptically recovered from donors, debrided, and disassociated from marrow and trabecular bone. The resulting tissue was processed by a proprietary computer numerical controlled-milling method (CNC-milled) into long fibers and disinfected using a proprietary process. The fibers were then demineralized using proprietary procedures. Following demineralization, fiber samples were taken to quantify residual calcium levels (average 1.7%) using a calcium reagent kit (Eagle Diagnostics, Cedar Hill, TX). The demineralized fibers were then freeze-dried, placed in final packaging, and treated via low-dose, low-temperature gamma irradiation, at a level necessary to achieve a sterility assurance level (SAL) of 10−6.
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2.2 Cytotoxicity testing of L-MDF using L929 mouse fibroblasts
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The cytotoxic potential of L-MDF were quantitatively evaluated by the MTT (3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide) assay using L929 mouse fibroblasts. Three samples of 2.5 cc from each of the six donors (n = 18) were rehydrated with 5 mL sterile saline (0.99% w/v sodium chloride in water). Sample extracts were prepared by incubating 0.2 g of each sample with 1 mL of extraction medium (Minimum Essential Medium supplemented with 10% v/v fetal bovine serum, 100 U mL−1 penicillin, 100 μg mL−1 streptomycin, and 2 mM l-glutamine) for 24 ± 2 h at 37 ± 1°C. Negative and positive controls were prepared similarly. Extraction medium alone was used as an untreated control “extract” for quantitative comparison of results. L929 mouse fibroblasts were cultured in 96-well microplates to half-confluency and subsequently exposed to 100 μL of sample or control extracts for 24–26 h at 37 ± 1°C. Following extract exposure, cell viability of each well was measured using a MTT assay. The average results for each group were normalized to the untreated control to determine a percent viability. Per ISO 10993-5:2009, percent viability less than 70% indicates a cytotoxic effect.
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2.3 In vitro metabolic activity of seeded bone marrow-mesenchymal stem cells
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Human bone marrow-derived mesenchymal stem cells (BM-MSCs) seeded on L-MDF were measured for metabolic activity using an alamarBlue® assay (Bio-Rad, Raleigh, NC) over the course of 7 days. L-MDF from six donors were placed in triplicate in low-attachment 24-well cell culture plates at a density of 13.1 mg of fiber per cm2 and seeded with BM-MSCs at 62,500 cells per well on day 0. BM-MSCs without fibers served as the control. After 2–4 h in culture, 1 mL of complete media was added to each well, followed by incubation at 37°C. Samples remained in the incubator until specific time points designated for analysis, at which point media was replaced. The metabolic activity of cells adhered to the fibers was measured after 1, 4 and 7 days in culture. At each time point media was aspirated and replaced with 1 mL of 10% alamarBlue reagent and incubated for an average of 2 h at 37°C. The solution was collected from each sample, centrifuged to pellet any debris, and measured in a 96-well plate at 544 nm excitation/592 nm emission. Fluorescence was recorded using relative fluorescence units (RFUs), and values were normalized to its time-matched control. A one-way ANOVA in conjunction with a Tukey post-hoc was used to determine differences in metabolic activity over time.
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2.4 In vitro cellular attachment of seeded bone marrow-mesenchymal cells
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Scanning electron microscopy (SEM) was used to qualitatively evaluate the attachment and morphology of cells seeded on four L-MDF samples (25 ± 1 mg) at 0.5–1 h, 1 and 7 days in culture. The fibers were placed in separate glass scintillation vials with 1 mL of complete media and incubated at 37°C. Following incubation, excess media was aspirated and BM-MSCs were seeded at 100,000 per cells per vial. At each time point, corresponding vials were removed from the incubator, excess media was removed, and 3 mL of 2.5% glutaraldehyde in cacodylate buffer was added to fix the samples. Cell-seeded samples were rinsed in 0.1 M cacodylate buffer, incubated in 1% osmium tetroxide for 60 min, and then dehydrated in a series of ethanol solutions increasing in concentration up to 100%. Samples were then dried via evaporation of a chemical drying agent, hexamethyldisilazane (HMDS). Prior to imaging, all samples were sputter coated in gold palladium for 200 s at 60 mA, then secured to a holder that was placed inside a vacuum-sealed imaging chamber. Samples were then imaged at a magnification 3000× using a Zeiss Gemini HD Scanning Electron Microscope.
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2.5 In vitro growth factor analysis
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L-MDF were analyzed for the presence of BMP-2 and BMP-7 using an enzyme-linked immunosorbent assay (ELISA) (R&D Systems, Minneapolis MN). L-MDF from six donors were weighed (30 ± 10 mg per donor) and placed in microcentrifuge tubes. Samples were then rehydrated with 5 μL of Dulbecco’s Modified Eagle Medium (DMEM) per milligram of fiber, followed by the addition of purified collagenase (14.47 Units/mg of fiber). The samples were digested at 37°C with constant mixing for 16–18 h. Digestion solutions were centrifuged to remove remaining undigested components and the supernatants were collected for testing. The resulting solutions were analyzed for BMP content in triplicate using an ELISA assay. The measured BMP content was averaged across all six donors and results were reported in ng protein/g of demineralized fibers.
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2.6 In vivo osteoinductive potential (OI)
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The osteoinductive potential of L-MDF was evaluated using an in vivo athymic mouse model at NAMSA (Northwood, Ohio) following American Society for Testing and Materials (ASTM) F-2529 guidelines. Four 20–25 mg replicates of L-MDF were rehydrated with 100–150 μL of sterile 0.9% w/v sodium chloride and loaded into 0.3 cc sterile syringes. Samples were then compressed to remove excess solution, and implanted bi-laterally between the biceps femoris and superficial gluteal muscle of athymic mice. All mice were euthanized 5 weeks post-implantation by carbon dioxide inhalation. Explants were fixed with 10% formalin and bisected along the long axis. Bisects of each explant were paraffin embedded, and three slides were generated each with 4–6 μm-thick tissue sections. Once stained with hematoxylin and eosin (H&E), slides were evaluated by a blinded pathologist. The presence of cartilage, chondroblasts, chondrocytes, osteoblasts, osteocytes, osteoid, newly formed lamellar bone, and bone marrow were evaluated as new bone elements as they are indicators of endochondral bone formation process.
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3. Results
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3.1 Cytotoxicity
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Cytotoxicity assay results showed that negative and positive controls behaved as expected (i.e., percent viability ≥70% for the negative control groups and <70% for the positive control groups). The average percent viability for negative and positive controls were 94 and 4%, respectively. The average percent viability of L-MDF (91%) was above the 70% threshold, and thus, based on the criteria of the protocol and ISO 10993-5 guidelines, L-MDF are considered to be non-cytotoxic.
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3.2 L-MDF supports attachment and sustained metabolic activity of bone marrow-mesenchymal stem cells
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Overall, the cellular activity of the BM-MSCs was shown to significantly increase over the course of the 7 day investigation. The results indicated that cells seeded on L-MDF showed a significant increase in proliferation between days 4 (51.3 ± 1.2 RFU) and 7 (59.5 ± 1.5 RFU) compared to day 1 (21.3 ± 0.8 RFU) (Figure 2).
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Figure 2.
Proliferation of BM-MSCs attached to L-MDF over 7 days. The average relative fluorescence unit (RFU) values for each set of triplicate test samples were normalized to the average RFU of the corresponding control group (fibers of the respective donor cultured without cells) for all six donors. Asterisks represent statistically significant differences from day 1 proliferation activity.
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SEM images confirmed BM-MSC attachment to L-MDF within 30 min of seeding. Cells appeared rounded with numerous folds and ridges and minimal surface contact (Figure 3A). After 1 h in culture, BM-MSCs became elongated and began spreading and increasing surface contact with the fibers (Figure 3B). After 1 day, imaging showed flattened cells with multiple adhesion points and cellular extensions as well as extracellular matrix (ECM) secretion (Figure 3C). By day 7 in culture, BM-MSCs infiltrated between fibers and demonstrated cell-to-cell interactions (Figure 3D).
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Figure 3.
Representative SEM images illustrating the morphology of cells attached to L-MDF. Following culture for 30 min (A), 1 h (B), 1 day (C) or 7 days (D), respectively, the samples were fixed in 2.5% glutaraldehyde and processed for scanning electron microscopy. Images are representative of all samples evaluated and were taken at 3000× magnification. Scale bar represents 10 μm. Images were pseudo-colored in Adobe Photoshop to distinguish the cells (in yellow) from the fibers.
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3.3 L-MDF contains important growth factors and demonstrates new bone formation in vivo\n
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The ELISA results indicated the presence of growth factors in L-MDF. The average BMP-2 and 7 concentrations in the samples fibers were 11.24 ± 1.49 and 85.78 ± 6.84 ng/g, respectively (Figure 4).
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Figure 4.
BMP-2 and BMP-7 content in L-MDF. L-MDF produced from six different donors were digested in collagenase for 16–18 h. Using ELISAs, the resulting digestion solutions were tested for BMP-2 and BMP-7 content in triplicate (mean ∓ SE).
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Additionally, in the athymic mouse muscle pouch model, histological analysis revealed new bone elements around and within the implanted scaffold at time of sacrifice (5 weeks; Figure 5). Panel A shows a set of merged images that illustrate new bone elements present in the explant (4× objective). Panels B and C highlight the presence of new bone elements such as cartilage, chondroblasts/cytes, bone marrow, new blood vessels, and new bone.
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Figure 5.
H&E staining of explants from an athymic nude mouse implanted with L-MDF (*). Merged set of H&E images showing new bone elements present in the entire explant at 35 days post-implantation (4× objective). Expanded areas show the presence of new bone elements such as cartilage (^), chondroblasts/cytes (#), bone marrow ($), new blood vessels (&), and new bone (+) around L-MDF implant (*) at 35 days.
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4. Discussion
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Demineralized bone matrices (DBMs) are widely used in spinal, orthopedic, craniomaxillofacial, and dental procedures to treat bone voids. An ideal DBM provides both osteoinductive and osteoconductive properties to promote new bone formation and provide a scaffold upon which cells can attach and proliferate. Furthermore, DBMs should be malleable and resist graft migration once impacted into a bone defect. To achieve these characteristics important for bone healing, manufacturers use a variety of techniques to process and sterilize DBMs. Despite demineralization being a well-known technique, the proportion of the osteoinductive element—the demineralized bone—of clinically available DBM-based graft materials varies widely by manufacturer. Differences in carrier material and sterilization may also contribute to variability among these grafts. The moldable demineralized fibers described here represent a recently developed allograft configuration that can function as an independent bone void filler without the need of a synthetic carrier. This study was conducted to ensure L-MDF possess the necessary qualities to function in this capacity.
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An osteoinductive bone graft has the ability to induce bone growth. Factors such as residual calcium level and growth factor content play important roles in a DBM’s ability to grow bone. In particular, residual calcium level can serve as an indicator for the availability of growth factors necessary for bone formation. The literature suggests that DBMs with different degrees of residual calcium show significant differences in osteoinductivity. Zhang et al. evaluated the effects of varying degrees of demineralization, particle size, donor age, and gender on the osteoinductivity of DBM in vivo (athymic mouse model) and in vitro (alkaline phosphatase assay) [22]. The authors suggested that demineralized bone with a residual calcium level of approximately 2% is “optimally osteoinductive”. Similarly, Turonis et al. found that a 2% residual calcium level in human demineralized freeze-dried bone allograft appears to enhance osseous wound healing [23]. The L-MDF samples discussed in this chapter were demineralized using a proprietary and patented process targeted at achieving an optimized level of residual calcium of 1–4%. Furthermore, the presence of specific proteins in DBM is frequently associated with its osteoinductive potential as growth factors can provide signals that direct cellular behavior [18, 22, 24]. In particular, BMP-2 and 7 are important for bone growth as they are known for their “ability to stimulate differentiation of MSCs to osteochondroblastic lineage” [18]. Previous studies have reported a wide span of BMP-2 and BMP-7 levels in demineralized bone, with ranges from 6.5 to 110 and 44 to 125 ng/g demineralized bone, respectively. In this study, ELISA results indicated the presence of BMP-2 and 7 in L-MDF (11.24 ± 1.49 and 85.78 ± 6.84 ng/g) consistent with values reported in the literature. This milieu of growth factors illustrate that L-MDF contain the appropriate trophic factor profile necessary for bone formation and are consistent with expected physiological levels.
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The osteoinductive and osteoconductive potential of DBMs are commonly evaluated using an in vivo athymic mouse intramuscular pouch model to histologically assess new bone formation [25].
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In the study described here, histological analysis revealed the presence of new bone elements demonstrating the osteoinductive potential of L-MDF. In addition, newly formed blood vessels were observed, which can also be indicative of the osteoconductive nature of the bone graft in providing a conducive environment for new bone formation. The surface characteristics of DBMs play an important role in their ability to provide a scaffold for new bone formation [19, 20]. Bone cells need a hospitable environment in which to attach and thrive. In particular, increased surface area, a rough topography, and interconnected networks are known to promote cellular attachment and cell spreading [26]. As demonstrated by the SEM imaging presented here, the long, interconnected L-MDF create a hospitable environment for BM-MSCs to infiltrate and make cell-to-cell connections. The ability of cells not only to quickly attach to the matrix but also maintain a healthy morphology throughout the duration of culture provides evidence of the osteoconductive qualities of L-MDF.
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The need for versatile handling has led to the addition of various inert carriers in commercial DBMs. However, studies have shown that carriers may negatively affect the inherent properties of a DBM. In particular, Lee et al. concluded that Poloxamer 407-based hydrogel may inhibit MSC osteoblastic differentiation by filling up spaces between DBM powders, negatively affecting the release of growth factors [21]. In a rat calvarial defect model, investigators found that the two types of DBM had significant differences in bone regeneration, which was attributed to the type of carrier [27]. Furthermore, varying the ratio of carrier to DBM can alter handling characteristics such as malleability and resistance to graft migration. Through in vivo and in vitro analyses, studies have found that increased bone content in DBMs produces larger amounts of new bone formation [25, 28, 29]. With this is mind, L-MDF were produced by proprietary CNC-milling cortical bone to create specially designed rough surfaces allowing fibers to interlock, allowing this bone void filler to be carrier-free. The roughness also provides numerous attachment points for the cells and their lamellipodia, encouraging a flattened morphology. These interlocking fibers thereby encourage malleability, graft placement in the implant site, and resistance to irrigation, all of which represent ideal handling characteristics.
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Finally, terminal sterilization is a processing measure used to ensure the safety of DBMs by reducing the risk of disease transmission. This is in contrast to aseptic processing alone, which introduces no additional bioburden from the environment but alone does not guarantee sterile tissue [30, 31]. Unlike aseptic-only processed tissue, terminal sterilization can result in a graft with a defined sterility assurance level (SAL). For example, an SAL of 10−6 indicates a 1 out of 1,000,000 chance that a viable organism exists within any single graft [31]. Although gamma irradiation is currently the most common method for terminally sterilizing allografts, some reports suggests that gamma irradiation can negatively impact the inherent properties of DBMs. There are several factors to consider when evaluating the effects of gamma irradiation on DBMs such as dose and temperature. Irradiation performed in a high dose range or at uncontrolled temperatures can result in denaturing of the osteoinductive signaling proteins, rendering them inactive, and/or structural damage to the collagen matrix due to generation of reactive oxygen species. Weintroub and Reddi evaluated DBM samples which were irradiated on ice at varying doses [32]. Histologic analysis showed DBM irradiated at 0.5–2.5 Mrad were similar to the non-irradiated control, indicating no effect on the induction properties of the implant. In another study, investigators found that DBM irradiated on dry ice (−72°C) demonstrated new bone formation comparable to non-irradiated samples [33]. These results demonstrate DBMs irradiated at low dose and low temperatures are expected to retain properties important to clinical performance. Thus, L-MDF are terminally sterilized to an SAL of 10−6 using low-dose, ultra-low temperature gamma irradiation to avoid negative impacts to the osteoinductive and osteoconductive potential, as verified by the results presented here.
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5. Conclusion
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L-MDF were engineered with the ideal characteristics of a DBM in mind. The cortical bone fibers are demineralized to target optimal levels of residual calcium to yield tissue with osteoinductive potential, and also terminally sterilized to minimize the risk of disease transmission. The results presented here demonstrate that L-MDF exhibit the osteoinductive potential and osteoconductive properties desirable to promote bone formation while also being easy to handle for surgical procedures. These characteristics suggest that L-MDF are a suitable option to treat bone defects in a number of orthopedic, spinal, trauma, craniomaxillofacial, and dental applications.
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Acknowledgments
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We would like to acknowledge Breanne Gjurich PhD, Evans Wralstad, Alana Sampson MS, Yao Akpamagbo MS, and Davorka Softic MS for their contributions to study design, analysis and interpretation of data presented in the chapter.
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Conflicts of interest
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JBM, NC, PS, and MM are employees of LifeNet Health, a nonprofit organization.
\n
\n',keywords:"demineralized bone matrix, osteoinductive, osteoconductive, allograft, growth factors, bone formation",chapterPDFUrl:"https://cdn.intechopen.com/pdfs/68254.pdf",chapterXML:"https://mts.intechopen.com/source/xml/68254.xml",downloadPdfUrl:"/chapter/pdf-download/68254",previewPdfUrl:"/chapter/pdf-preview/68254",totalDownloads:184,totalViews:0,totalCrossrefCites:0,dateSubmitted:"April 1st 2019",dateReviewed:"June 28th 2019",datePrePublished:"July 23rd 2019",datePublished:"February 10th 2021",dateFinished:"July 23rd 2019",readingETA:"0",abstract:"Demineralized bone matrices (DBMs) have been used in a wide variety of clinical applications involving bone repair. Ideally, DBMs should provide osteoinductive and osteoconductive properties, while offering versatile handling capabilities. With this, a novel fiber technology, LifeNet Health-Moldable Demineralized Fibers (L-MDF), was recently developed. Human cortical bone was milled and demineralized to produce L-MDF. Subsequently, the fibers were lyophilized and terminally sterilized using low-dose and low-temperature gamma irradiation. Using L929 mouse fibroblasts, L-MDF underwent cytotoxicity testing to confirm lack of a cytotoxic response. An alamarBlue assay and scanning electron microscopy demonstrated L-MDF supported the cellular function and attachment of bone-marrow mesenchymal stem cells (BM-MSCs). Using an enzyme-linked immunosorbent assay, L-MDF demonstrated BMP-2 and 7 levels similar to those reported in the literature. In vivo data from an athymic mouse model implanted with L-MDF demonstrated the formation of new bone elements and blood vessels. This study showed that L-MDF have the necessary characteristics of a bone void filler to treat osseous defects.",reviewType:"peer-reviewed",bibtexUrl:"/chapter/bibtex/68254",risUrl:"/chapter/ris/68254",signatures:"Julie B. McLean, Nigeste Carter, Payal Sohoni and Mark A. Moore",book:{id:"9406",title:"Clinical Implementation of Bone Regeneration and Maintenance",subtitle:null,fullTitle:"Clinical Implementation of Bone Regeneration and Maintenance",slug:"clinical-implementation-of-bone-regeneration-and-maintenance",publishedDate:"February 10th 2021",bookSignature:"Mike Barbeck, Nahum Rosenberg, Patrick Rider, Željka Perić Kačarević and Ole Jung",coverURL:"https://cdn.intechopen.com/books/images_new/9406.jpg",licenceType:"CC BY 3.0",editedByType:"Edited by",editors:[{id:"204918",title:"Dr.",name:"Mike",middleName:null,surname:"Barbeck",slug:"mike-barbeck",fullName:"Mike Barbeck"}],productType:{id:"1",title:"Edited Volume",chapterContentType:"chapter",authoredCaption:"Edited by"}},authors:[{id:"300414",title:"Dr.",name:"Mark A.",middleName:null,surname:"Moore",fullName:"Mark A. Moore",slug:"mark-a.-moore",email:"mark_moore@lifenethealth.org",position:null,institution:null},{id:"307867",title:"Ms.",name:"Nigeste",middleName:null,surname:"Carter",fullName:"Nigeste Carter",slug:"nigeste-carter",email:"nigeste_carter@lifenethealth.org",position:null,institution:null},{id:"308626",title:"Dr.",name:"Julie",middleName:null,surname:"McLean",fullName:"Julie McLean",slug:"julie-mclean",email:"julie_mclean@lifenethealth.org",position:null,institution:null},{id:"308627",title:"Ms.",name:"Payal",middleName:null,surname:"Sohoni",fullName:"Payal Sohoni",slug:"payal-sohoni",email:"payal_sohoni@lifenethealth.org",position:null,institution:null}],sections:[{id:"sec_1",title:"1. Introduction",level:"1"},{id:"sec_2",title:"2. Methodology",level:"1"},{id:"sec_2_2",title:"2.1 Fiber generation",level:"2"},{id:"sec_3_2",title:"2.2 Cytotoxicity testing of L-MDF using L929 mouse fibroblasts",level:"2"},{id:"sec_4_2",title:"2.3 In vitro metabolic activity of seeded bone marrow-mesenchymal stem cells",level:"2"},{id:"sec_5_2",title:"2.4 In vitro cellular attachment of seeded bone marrow-mesenchymal cells",level:"2"},{id:"sec_6_2",title:"2.5 In vitro growth factor analysis",level:"2"},{id:"sec_7_2",title:"2.6 In vivo osteoinductive potential (OI)",level:"2"},{id:"sec_9",title:"3. Results",level:"1"},{id:"sec_9_2",title:"3.1 Cytotoxicity",level:"2"},{id:"sec_10_2",title:"3.2 L-MDF supports attachment and sustained metabolic activity of bone marrow-mesenchymal stem cells",level:"2"},{id:"sec_11_2",title:"3.3 L-MDF contains important growth factors and demonstrates new bone formation in vivo\n",level:"2"},{id:"sec_13",title:"4. Discussion",level:"1"},{id:"sec_14",title:"5. Conclusion",level:"1"},{id:"sec_15",title:"Acknowledgments",level:"1"},{id:"sec_15",title:"Conflicts of interest",level:"1"}],chapterReferences:[{id:"B1",body:'\nKhan WS, Rayan F, Dhinsa BS, Marsh D. An osteoconductive, osteoinductive, and osteogenic tissue-engineered product for trauma and orthopaedic surgery: How far are we? Stem Cells International. 2012;2012:236231\n'},{id:"B2",body:'\nWang W, Yeung KWK. Bone grafts and biomaterials substitutes for bone defect repair: A review. Bioactive Materials. 2017;2(4):224-247\n'},{id:"B3",body:'\nOommen AT, Krishnamoorthy VP, Poonnoose PM, Korula RJ. Fate of bone grafting for acetabular defects in total hip replacement. Indian Journal of Orthopaedics. 2015;49(2):181-186\n'},{id:"B4",body:'\nYounger EM, Chapman MW. Morbidity at bone graft donor sites. Journal of Orthopaedic Trauma. 1989;3(3):192-195\n'},{id:"B5",body:'\nPark SB, Chung CK. Strategies of spinal fusion on osteoporotic spine. Journal of Korean Neurosurgical Association. 2011;49(6):317-322\n'},{id:"B6",body:'\nLobb DC, DeGeorge BR Jr, Chhabra AB. Bone graft substitutes: Current concepts and future expectations. The Journal of Hand Surgery. 2019;44(6):497-505.e2\n'},{id:"B7",body:'\nKlifto CS, Gandi SD, Sapienza A. Bone graft options in upper-extremity surgery. The Journal of Hand Surgery. 2018;43(8):755-761.e2\n'},{id:"B8",body:'\nFernandez de Grado G, Keller L, Idoux-Gillet Y, Wagner Q , Musset A-M, Benkirane-Jessel N, et al. Bone substitutes: A review of their characteristics, clinical use, and perspectives for large bone defects management. Journal of Tissue Engineering. 2018;9:1-18\n'},{id:"B9",body:'\nBurkus JK, Sandhu HS, Gornet MF. Influence of rhBMP-2 on the healing patterns associated with allograft interbody constructs in comparison with autograft. Spine (Phila Pa 1976). 2006;31(7):775-781\n'},{id:"B10",body:'\nMcClellan JW, Mulconrey DS, Forbes RJ, Fullmer N. Vertebral bone resorption after transforaminal lumbar interbody fusion with bone morphogenetic protein (rhBMP-2). Journal of Spinal Disorders and Techniques. 2006;19(7):483-486\n'},{id:"B11",body:'\nLewandrowski KU, Nanson C, Calderon R. Vertebral osteolysis after posterior interbody lumbar fusion with recombinant human bone morphogenetic protein 2: A report of five cases. The Spine Journal. 2007;7(5):609-614\n'},{id:"B12",body:'\nJames CDT. Sir William Macewen. Proceedings of the Royal Society of Medicine. 1974;67(4):237-242\n'},{id:"B13",body:'\nde Boer HH. The history of bone grafts. Clinical Orthopaedics and Related Research. 1988;226:292-298\n'},{id:"B14",body:'\nZimmermann G, Moghaddam A. Allograft bone matrix versus synthetic bone graft substitutes. Injury. 2011;42:S16-S21\n'},{id:"B15",body:'\nMiller LE, Block JE. Safety and effectiveness of bone allografts in anterior cervical discectomy and fusion surgery. Spine (Phila Pa 1976). 2011;36(24):2045-2050\n'},{id:"B16",body:'\nSenn N. On the healing of aseptic bone cavities by implantation of anti-septic decalcified bone. The American Journal of the Medical Sciences. 1889;98:219-243\n'},{id:"B17",body:'\nUrist MR, Strates BS. The classic: Bone morphogenetic protein. Clinical Orthopaedics and Related Research. 2009;467(12):3051-3062\n'},{id:"B18",body:'\nLieberman JR, Daluiski A, Einhorn TA. The role of growth factors in the repair of bone. Biology and clinical applications. The Journal of Bone and Joint Surgery. American Volume. 2002;84(6):1032-1044\n'},{id:"B19",body:'\nKarageorgiou V, Kaplan D. Porosity of 3D biomaterial scaffolds and osteogenesis. Biomaterials. 2005;26(27):5474-5491\n'},{id:"B20",body:'\nRodriguez RU, Kemper N, Breathwaite E, Dutta SM, Hsu EL, Hsu WK, et al. Demineralized bone matrix fibers formable as general and custom 3D printed mold-based implants for promoting bone regeneration. Biofabrication. 2016;8(3):035007\n'},{id:"B21",body:'\nLee JH, Baek HR, Lee KM, Lee HK, Im SB, Kim YS, et al. The effect of poloxamer 407-based hydrogel on the osteoinductivity of demineralized bone matrix. Clinics in Orthopedic Surgery. 2014;6(4):455-461\n'},{id:"B22",body:'\nZhang M, Powers RM Jr, Wolfinbarger L Jr. Effect(s) of the demineralization process on the osteoinductivity of demineralized bone matrix. Journal of Periodontology. 1997;68(11):1085-1092\n'},{id:"B23",body:'\nTuronis JW, McPherson JC 3rd, Cuenin MF, Hokett SD, Peacock ME, Sharawy M. The effect of residual calcium in decalcified freeze-dried bone allograft in a critical-sized defect in the Rattus norvegicus calvarium. The Journal of Oral Implantology. 2006;32(2):55-62\n'},{id:"B24",body:'\nWolfinbarger L, Eisenlohr LM, Ruth K. Demineralized bone matrix: Maximizing new bone formation for successful bone implantation. In: Pietrzak WS, editor. Musculoskeletal Tissue Regeneration: Biological Materials and Methods. Totowa, NJ: Humana Press; 2008. pp. 93-117\n'},{id:"B25",body:'\nBoyan BD, Ranly DM, McMillan J, Sunwoo M, Roche K, Schwartz Z. Osteoinductive ability of human allograft formulations. Journal of Periodontology. 2006;77(9):1555-1563\n'},{id:"B26",body:'\nMurphy MB, Suzuki RK, Sand TT, Chaput CD, Gregory CA. Short term culture of human mesenchymal stem cells with commercial osteoconductive carriers provides unique insights into biocompatibility. Journal of Clinical Medicine. 2013;2(3):49-66\n'},{id:"B27",body:'\nTavakol S, Khoshzaban A, Azami M, Kashani IR, Tavakol H, Yazdanifar M, et al. The effect of carrier type on bone regeneration of demineralized bone matrix in vivo. The Journal of Craniofacial Surgery. 2013;24(6):2135-2140\n'},{id:"B28",body:'\nHan B, Tang B, Nimni ME. Quantitative and sensitive in vitro assay for osteoinductive activity of demineralized bone matrix. Journal of Orthopaedic Research. 2003;21(4):648-654\n'},{id:"B29",body:'\nAtti E, Abjornson C, Diegmann M, Zhang K, Cammisa FP, Myers ER. High resolution X-ray computed tomography as a technique to study osteoinductivity of demineralized bone matrix. The Spine Journal. 2003;3(5):120\n'},{id:"B30",body:'\nVangsness CT Jr, Wagner PP, Moore TM, Roberts MR. Overview of safety issues concerning the preparation and processing of soft-tissue allografts. Arthroscopy: The Journal of Arthroscopic and Related Surgery: Official Publication of the Arthroscopy Association of North America and the International Arthroscopy Association. 2006;22(12):1351-1358\n'},{id:"B31",body:'\nVangsness CT Jr, Garcia IA, Mills CR, Kainer MA, Roberts MR, Moore TM. Allograft transplantation in the knee: Tissue regulation, procurement, processing, and sterilization. The American Journal of Sports Medicine. 2003;31(3):474-481\n'},{id:"B32",body:'\nWientroub S, Reddi AH. Influence of irradiation on the osteoinductive potential of demineralized bone matrix. Calcified Tissue International. 1988;42(4):255-260\n'},{id:"B33",body:'\nDziedzic-Goclawska A, Ostrowski K, Stachowicz W, Michalik J, Grzesik W. Effect of radiation sterilization on the osteoinductive properties and the rate of remodeling of bone implants preserved by lyophilization and deep-freezing. Clinical Orthopaedics and Related Research. 1991;272:30-37\n'}],footnotes:[],contributors:[{corresp:null,contributorFullName:"Julie B. McLean",address:null,affiliation:'
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IntechOpen collaborates with Enago, through its sister brand, Ulatus, one of the world’s leading providers of book translation services. Their services are designed to convey the essence of your work to readers from across the globe in the language they understand.
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