CC BY
289. Cengiz, I.F.; Oliveira, J.M.; Reis, R. L. Micro-computed tomography characterization of tissue engineering scaffolds: Effects of pixel size and rotation step. J. Mater. Sci. Mater. Med. 2017, 28.
10. Boerckel, J.D.; Mason, D.E.; McDermott, A.M.; Alsberg, E. Microcom-puted tomography: Approaches and applications in bioengineering. Stem Cell Res. Ther. 2014, 5, 1-12
11. Liao, C.-W.; Fuh, L.-J.; Shen, Y.-W.; Huang, H.-L.; Kuo, C.-W.; Tsai, M.-T.; Hsu, J.-T. Self-assembled micro-computed tomography for dental education. PLoS ONE2018, 13, e0209698.
12. Deyhle, H.; Schmidli, F.; Krastl, G.; Müller, B. Evaluating tooth restorations: Micro-computed tomography in practical training for students in dentistry. Int. Soc. Optical Eng. 2010, 7804, 780417.
13. Sandholzer, M.A.; Walmsley, A.D.; Lumley, P.J.; Landini, G. Radiologic evaluation of heat-induced shrinkage and shape preservation of human teeth using microCT. J. Forensic Radiol. Imaging2013, 1, 107-111.
14. Rutty, G.N.; Brough, A.; Biggs, M.J.P.; Robinson, C.; Lawes, S.D.A.; Hainsworth, S. V. The role of micro-computed tomography in forensic investigations. Forensic Sci. Int. 2013, 225, 60-66.
15. Leeson, D. The digital factory in both the modern dental lab and clinic. Dent. Mater. 2019, 1, 43-52.
16. Bouxsein M. L., Boyd S. K., Christiansen B. A., Guldberg R. E., Jepsen K. J., Muller R. Guidelines for assessment of bone microstructure in rodents using micro-computed tomography // Journal of Bone and Mineral Research. 2010. Vol. 25, N 7. P. 1468-1486. D0l:10.1002/jbmr.141.
Received 15.07.2022 Revised 18.07.2022 Accepted 23.07.2022
INFORMATION ABOUT AUTHORS
Dolgalev Alexander Alexandrovich, PhD, MD, Head of the Center for Innovation and Technology Transfer, Professor of the Department of General Practice Dentistry and Pediatric Dentistry of Stavropol State Medical University of the Ministry of Health of the Russian Federation, Professor of the Department of Clinical Dentistry with a course of OS and MFS of Pyatigorsk Medical and Pharmaceutical Institute-branch of the Volgograd State Medical University, Stavropol, Russian Federation. ORCID: https://orcid.org/0000-0002-6352-6750. Tel. +79624404861, e-mail: [email protected]
Rzhepakovsky Igor Vladimirovich, Candidate of Biological Sciences, Associate Professor at the Department of Applied Biotechnology, leading researcher of the interdepartmental research and education laboratory of experimental immunomorphology, immunopathology and immunobiotechnology, North-Caucasus Federal University, Stavropol, Russian Federation. Tel. +79054164981, e-mail: [email protected]
Danaev Aslan Baradinovich, Head of the Saverclinica Centre for Training in the Basics of Lean Manufacturing in Health Care at the institute of additional professional education, Stavropol State Medical University of the Ministry of Health of the Russian Federation, Stavropol, Russian Federation. ORCID: https://orcid.org/0000-0003-4754-3l0l. Tel. +79289111148, e-mail: [email protected]
Avanisyan Vazgen Mikhailovich, the 5-th grade student of the Faculty of Dentistry of the Stavropol State Medical University of the Ministry of Health of the Russian Federation, Stavropol, Russian Federation. ORCID: https://orcid.org/0000-0002-0316-5957. Tel. +79286338995, e-mail: [email protected]
Shulga Galina Sergeevna, the 4-th grade student of the Faculty of Dentistry of the Stavropol State Medical University of the Ministry of Health of the Russian Federation, Stavropol, Russian Federation. ORCID: https://orcid.org/0000-0003-2328-6948. Tel. +79288266451 e-mail: [email protected]
Korobkeev Artemy Aleksandrovich, the 3-th grade student of the Faculty of Dentistry of the Stavropol State Medical University of the Ministry of Health of the Russian Federation, Stavropol, Russian Federation. ORCID: https://orcid.org/0000-0001-6188-2578. Tel. +79624429874, e-mail: [email protected]
DOI:10.33667/2782-4101 -2022-2-21 -26
TISSUE-ENGINEERED BONE IMPLANTS FOR THE REPLACEMENT OF JAWBONE DEFECTS. LITERATURE REVIEW
Konstantin Kobets, Artak Kazaryan, Saddam Bopkhoev
Peoples' Friendship University of Russia (RUDN University), 6 Miklukho-Maklaya St., Moscow, 117198, Russian Federation
SUMMARY
The purpose of the study: to trace the development of methods of bone implants for the replacement of jawbone defects: from ceramic and polymeric scaffolds to complex tissue-engineered structures with stem cells, growth factors and vascular anastomoses based on literature data.
Materials and methods: searching, systematization and analysis of scientific data on various types of 3D-printed bone implants and their effectiveness in replacing bone defects.
Conclusions: Modern technologies of 3D-printing, cell and tissue engineering, microvascular surgical techniques closely approach scientists and clinicians to creation of an artificial bone implant which in the body must become a living structure capable of integrating with the patient's bone. Only complex approach which includes reconstruction of the implant of individual shape and sufficient mechanical strength, giving of osteoinductive and osteogenic properties, providing of internal axial and external angiogenesis is the basis for such tissue-engineered construction.
KEYWORDS: artificial tissue implants, bone vascularisation, bone implants, bone engineering, bone the defects reconstruction, arteriovenous loop.
CONFLICT of INTEREST. The authors declare no conflict of interest.
Introduction
Tissue damage caused by trauma, cancer and infectious processes can lead to extensive defects and deformities requiring reconstructive surgery. More than 500,000 people with head and neck cancers are identified each year (Cohen et al., 2018). Modern surgical treatment of malignant lesions implies one-stage removal of resection defects. For this purpose, vascularized bone or combined bone-soft tissue autografts are the «gold standard» [Huang et al. [Huang et al., 2016]. For example, for mandibular reconstruction, the peroneal autograft on microvascular anastomosis is most often used. Its advantages are a long vascular stem, vessel diameter, suitable length and thickness of the bone, the possibility of performing reconstruction over a long distance, the possibility of including a muscle or skin component with a flap, stable bone structure that allows intraosseous implantation and further orthopedic prosthesis, minimal resorption [Tereshchuk et al., 2018].
However, all autotransplant surgeries have disadvantages and limitations. First, it is an additional surgical procedure of graft taking, defect or instability of the donor site, deformation and pain in the donor site, risk of infection (Lakhiani et al., 2016; Simon et al., 2003; Hartman et al., 2002). The main factor determining the nutrition and «survival» of the graft at the microvascular anastomosis is the patency of the anastomosis itself. This can be influenced by surgical technique, anaesthetic and medication support, and postoperative regimen.
Despite the impressive success of microsurgical procedures in tissue and organ transplantation, the development of artificial tissue-engineered constructs to replace bone and other tissue defects is a promising area. Advances in cell engineering (the ability to cultivate deterministic cells), genetics and molecular biology (synthesis of cytokines and growth factors), 3D-printing of matrices and scaffolds of the right shape with biocompatible materials facilitate this.
This review focuses on current advances in tissue engineering in the development of vascularised tissue implants (VTIs), especially bone implants. The requirements for VTIs are described and systematised, the technologies for VTI creation are reviewed and the results of their use in in vivo experiments are given.
Materials and methods
The scientific literature for this review was collected from the following on-line databases and libraries: https: //elibrary. ru/, https://scholar. google. ru/, https://pubmed. ncbi. nlm.
nih. gov, https://www. sciencedirect. com/. Search was performed using the following keywords: artificial tissue implants, bone vascularization, bone implants, bone engineering, bone defect reconstruction, arteriovenous loop; no date restrictions.
Discussion
3D-prototyping of bone implant
Currently, it is possible to produce a biocompatible bone implant (scaffold) of any geometric shape, including an individual one for each particular patient using 3D-printing [Tereshchuk S. V. et al., 2019, Kim et al., 2021].
Due to the nature of the material used for 3D-printing and the architectonics of 3D-printing, bone implants usually have osteoconductive properties, i.e. they are a matrix for bone tissue formation on their basis. Adding growth factors, cytokines and cells to their composition can additionally give osteoinductive and osteogenic properties [Muraev A. A. et al., 2013].
Thus the usage of biphasic calcium phosphate as a scaffold is much more effective than using pure hydroxyapatite and beta-tricalcium phosphate (HA and b-TCP) [Kohri M et al., 1993; Nery et al., 1992]. The pores and their number and size in the scaffold play an important role in the process of surrounding tissue ingrowth into the material and the osseointegration of the material. If the pore size is below 100 ^m, fibrovascular encapsulation of the implant may occur; 100-500 ^m is considered optimal [Kühne et al. 1994].
In addition to its effect on the regeneration of the bone tissue itself, pore size affects vascular growth, which is more pronounced in large pores (Druecke D et al., 2004).
It is important to understand that in order for a complete bone implant to form, a vascular structure must be formed in its structure to nourish it.
External and internal vascularisation
Vascularisation is a key link in the growth of new and regeneration of damaged tissue. When creating osteoplastic materials for the replacement of small bone defects, vascular endothelial growth factor (VEGF) may be included in the material composition. Thanks to VEGF a well-developed microcirculatory channel is formed in the regeneration zone [Muraev A. A. et al., 2012; 2012].
This approach refers to external neovascularisation, i.e., the microvascular bed is «connected» to existing adjacent
Results of the study
https://elibrary.ru/ https://scholar. google. ru/ https://pubmed.ncbi.nlm.nih.gov https://www.sciencedire ct. com/.
Artificial tissue implants 1 45 8198 15
Bone vascularisation 35 1850 97 1347
Bone implants 1248 32200 1034 14609
Bone engineering 256 11300 373 988
Bone defect reconstruction 42 2030 179 294
Arteriovenous loop 49 2520 210 520
arterioles. This type of neovascularization is ineffective when the size of the bone defect is large and in places that have been exposed to radiation [Lokmic Z et al, 2006; Tanaka et al, 2000]. This is the reason why the formation, development and survival of new cells in the centre of large constructions is limited at the beginning of vascularisa-tion. If when a scaffold is implanted into an area where there is good vascularisation there will be development of a vascular network, then further transplantation into the recipient area will result in cessation of blood supply, as there is no subsequent connection to the vascular network in the defect site.
These problems have led to the development of new methods of neoangiogenesis for artificial tissue-engineered constructs, namely internal vascularisation. Internal vascularization is a method in which an artery or vein serves as a source of new vessels for tissue creation, which further allows the implant to be transferred to the recipient area by means of microvascular anastomoses [Tanaka Y et al., 2003; Erol et al., 1980; Khouri et al., 1991].
As mentioned above, 3D-printing allows the creation of artificial implants of defined macro- and micro-architecture. Therefore, the next step, in order to provide internal vascularisation, was to prefabricate channels for the vascular bed within the bone implant. With the prefabrication techniques it is possible to obtain the desired vascularised flap with an axial type from a flap with incidental vascularisation. With the arteriovenous loop it has become possible to implant grafts in highly vascularised areas and after a certain period to graft with connection to the local vascular network with microvascular anastomoses for tissue and cell feeding.
3D-printing of the channels for the new vessels should be guided by the structure of the vascular bed of the jawbone tissue and the surrounding vessels. The diameter of the lingual artery is 2.3±0.1 mm, the facial artery is 2.2±0.2 mm, the diameter of the maxillary artery is 3.3±0.3 cm [Lukyan-ov V. G. 1971] According to Jiang G. H. et al. the diameter of the left facial artery is 1.4-4.7 mm (mean 2.83±0.77 mm), the right one is 1.6-4.3 mm (mean 2.81±0.79 mm) [Jiang et al., 2008].
Volikov V. V described the structure of the microvascular system of the maxilla alveolar process in norm and in case of tooth loss. Thus, in the presence of all teeth, the vascular system is represented by tubular structures with a rounded cross-section, located mostly perpendicular to the bone surface, with numerous anastomoses. The vascularisation of the bone tissue is satisfactory. The arterial vessels have
a thin wall.
The diameter of the veins exceeds the diameter of the arteries by 2-4 times. Morphometric analysis of the periodontal vessels revealed that in intact dentition the number of vessels in 1 sq.mm. in the projection of the 11th tooth was 18,25 ± 3,58, in the projection of the 21st tooth - 19,05 ± 3,26, in the projection of the 16th tooth - 19,10 ± 4,01, in the projection of the 26th tooth - 19,30 ± 3,27 (at p<0,05). In the projection of all studied teeth the number of vessels in 1 sq.mm. was more in women in comparison with men. In comparison with the group of patients with intact den-
tition in partial and total adentia the number of vessels in 1 sq.mm. decreased by 20 % and 60 % respectively, vessel diameter was 40 %> and 70 %>, the thickness of the vascular wall increased by 2 and 4 times respectively. [Volikov V. V. et al., 2015].
Revascularised bone implants
The next step in the evolution of artificial bone implants (ABI) was to combine the tissue-engineered structure with living vessels by introducing a main feeding vessel into them. As such a vessel an arteriovenous loop or a vascular stalk is used, which is placed directly in the bone implant (BI) or under it. It was shown that the feeding vessel allows good vascularization of the BI, due to the formation of a microcirculatory channel around it [Khouri et al. 1991; Tan et al., 2004; Hirase et al., 1987; Morrison et al., 1990]. Such work is actively carried out in vivo on animal models. For this purpose the highly vascularized regions are chosen, where the prefabricated BI is placed and after some time it is transferred into the bone defect with the connection to the local vascular network with the help of the microvascular anastomoses. The vascular axis becomes a supporting vessel after transplantation and microsurgical anastomoses with the local vessels to allow the new vessels to live and integrate.
As an axial vessel, the arteriovenous loop has proven most effective (Tanaka et al., 2003; Cassell et al., 2002; Kneser et al., 2006).
Because of mechanical stimulation, the level of VEGF (vascular endothelial growth factor) increases when a vascular graft is introduced into the arterial circulation (Nath et al., 2003; Dvorak et al., 1995). The local inflammatory reaction that occurs during surgical intervention on a vessel causes an angiogenic reaction. VEGF levels in platelets increase under the influence of proinflammatory chemokines [Nath et al., 2003]. In microvascular anastomoses there is an increase in endothelial cells in microvascular anastomoses due to the combination of blood shear stress and turbulent current changes [Davies et al., 1986].
Once the main vessel in the BI is integrated and the vascularisation process is complete, the BI is transferred to the recipient area to repair the bone defect and connected to the recipient vessel. By 8 weeks, there is significant vascularisation of the matrix with an arteriovenous loop (Kneser et al., 2006).
Arteriovenous loop
An arteriovenous loop (AVP) is a pathological direct connection between an artery and a vein (congenital or acquired), creating blood flow bypassing the capillary network. Pathological to normal tissues, in the experiment AVP promoted flow-induced axial vascularisation. Thus, placed in the central part of the bone implant, AVP is a source of «axial vascularization», which in combination with peripheral angiogenesis («external vascularization») provides adequate blood supply and thus opens significant prospects in solving the problem of increasing the survival of cells comprising the BI [Leibig et al., 2016].
In 1980, Erol and Spira developed the arteriovenous loop method (AVP) in experimental animals [Erol et al., 1980;]. The authors used rats weighing 250-350 grams. An artery and vein were exposed on one side of the femoral vessels, and a venous graft was obtained on the other side. Next, the vessels were prepared by ligating the proximal part of the vein and the distal end of the artery. The venous graft was washed with heparin and then two end-to-end anastomoses were applied: the proximal end of the artery and the distal end of the vein. The criterion of the vessel patency was the pulsation of the venous loop. The loop was inserted into the implantation chamber and then closed from above with the second part of the implant. The chamber was closed and tied with 6/0 non-absorbable sutures. The skin was sutured 4/0-5/0. Postoperatively, heparin was injected intravenously. IVG (interpositional vein grafts) is necessary to avoid tension in the loop between the artery and vein, and is a good inducer for early angiogenesis (Polykandriotis et al., 2007; Schmidt et al., 2013). The loop is completely isolated, allowing vascularisation at the expense of the AV loop. This results in hypoxia in the chamber, which is a stimulus for neoangiogenesis. Hypoxia and cell proliferation reach their peak on day 7 [Lokmic Z et al, 2006].
Experiments using the arteriovenous loop method are also possible in other animals such as rabbits, dogs, sheep [Wu X et al., 2015; Eweida et al., 2017; Dong et al., 2012]. Experiments on larger animals have provided the rationale for the clinical use of the method.
AVP has been used in various experimental models. To create the BIs, the AVP method was combined with different scaffolds, including growth factors and cells: mesenchymal stem cells (MSCs) [Arkudas et al., 2017; Kim HY et al., 2018; Boos et al., 2012; Buehrer et al., 2014] or osteoblasts [Arkudas et al., 2007]. For cell differentiation, a number of authors have added specific growth factors to CIs. The combination of MSCs (mesenchymal stem cells) and BMP-2 (Bone morphogenetic protein-2) leads to accelerated bone development in the AB loop [Buehrer et al., 2014].
There are studies that focus on the possibility of growth of muscle tissue, heart tissue, soft tissue, lymphatic vessels and internal organs [Tee et al., 2012; Messina et al., 2005; Witt et al., 2017; Fiegel et al., 2008; Brown et al., 2006; Robering et al., 2018].
Work on lymphatic vessels is at a very early stage and clinically very much in demand, with Jan Robering working on lymphatic tissue development using an AV loop [Robering et al., 2018].
Bone implants can be different in sizes, depending on the zone of the defect, the size of the AVP is chosen according to its size (Cassell et al., 2001; Hofer et al., 2003). It has been shown that creation of additional external perforations in the BI results in faster vascular growth from the surrounding implant tissues [Dolderer et al., 2010]. Thus, in perforated implants there is an increase in angiogenesis in the arteriovenous loop due to the connection to the additional external vascular network, which significantly reduces the time of pre-vascularization and tissue formation [Arkudas et al., 2012].
Preclinical in vivo studies on large animals using a long AVP and large BIs of clinically relevant size can be considered. Justus Beier et al. in a study on sheep formed an AVP using a saphenous artery and femoral vein in a large model, with an implant size of 2.8 cm long, 1.8 cm wide and 1.8 cm high and with a volume of 16 cm [Beier et al., 2009]. Wu X in a study on dogs formed an AVP from the saphenous artery and femoral vein, which allowed the IVG not to be used [Wu X et al., 2015]. The success of this technique has also been shown in rabbits using the saphenous artery and femoral vein [Eweida et al., 2017].
Studies have shown that the less flexion of the AVP, the less likely to develop thrombosis, also the non-use of IVG (interpositional vein grafts) simultaneously with saphenous artery and femoral vein anastomosis is possible, as the anastomosis length between the artery and vein is sufficient and there is no tension [Dong et al, 2012; Weigand et al., 2015; Eweida et al., 2013]. However, several studies show that IVG (interpositional vein grafts) is an important factor in angiogenesis [Polykandriotis et al., 2007; Schmidt et al., 2013].
There may be a reduced risk of thrombosis with the AV-beam, less surgical experience is possible with this technique, but studies show that the loop is more effective for angiogenesis within the scaffold. The vascular bundle has a lower degree of vascularisation but better balance between the bone formation and the scaffold [Rudolph et al., 2020].
Conclusion
Modern 3D-printing, cell and tissue engineering and microvascular surgical techniques have brought scientists and clinicians closer to the creation of an artificial bone implant, which in the body must become a living structure capable of integrating with the patient's bone. Only a comprehensive approach that includes recreating an implant with an individual shape and sufficient mechanical strength, imparting osteoinductive and osteogenic properties, ensuring internal axial and external angiogenesis, is basic for such a tissue-engineered structure.
References
1. Cohen N, Fedewa S, Chen AY. Epidemiology and Demographics of the Head and Neck Cancer Population. Oral Maxillofac Surg Clin North Am. 2018 Nov;30(4):381-395. Doi: 10.1016lj.coms.2018.06.001. Epub 2018 Aug 3. PMID: 30078696.
2. Huang RL, Kobayashi E, Liu K, Li Q. Bone Graft Prefabrication Following the In Vivo BioreactorPrinciple. Ebiomedicine. 2016 Oct;12:43-54. Doi:10.1016lj.ebiom.2016.09.016. Epub 2016 Sep 20. PMID: 27693103; PMCID: PMC5078640.
3. Tereshchuk S, Sukharev V. Refined Approach to Preservation of the Inferior Alveolar Nerve during Resection and Primary Reconstruction of the Mandible. Craniomaxillofac Trauma Reconstr. 2019 Mar,12(1):34-38. Doi: 10.1055ls-00381639348. Epub 2018 Mar28. PMID: 30815213; PMCID: PMC6391257.
4. Lakhiani C, defazio MV, Han K, Falola R, Evans K. Donor-Site Morbidity Following Free Tissue Harvest from the Thigh: a Systematic Review and Pooled Analysis of Complications. J ReconstrMicrosurg. 2016 Jun;32(5):342-57. Doi: 10.1055ls-0036-1583301. Epub 2016 May 4. PMID: 27144952.
5. Rogers SN, Lakshmiah SR, Narayan B, Lowe D, Brownson P, Brown JS, Vaughan ED. A comparison of the long-term morbidity following deep circumflex iliac and fibula free flaps for reconstruction following head and neck cancer. Plast Reconstr Surg. 2003 Nov;112(6):1517-25; discussion 1526-7. Doi: 10.1097/01.PRS.0000082817.26407.86. PMID: 14578779.
6. Hartman EH, Spauwen PH, Jansen JA. Donor-site complications in vascularized bone flap surgery. J Invest Surg. 2002 Jul-Aug;l5(4):l85-97. Doi: 10.1080/08941930290085967. PMID: 12217183.
7. Tereshchuk S. V., Ivanov S. Y., Sukharev V. A., Role of adaptive technologies in modern reconstructive chirogy, Military Medical Journal. 2019. T. 340. № 10. C. 28-32.
8. Kim EV, Petronyuk YS, Guseynov NA, Tereshchuk SV, Popov AA, Volkov AV, Gorshenev VN, Olkhov AA, Levin VM, Dymnikov AB, Rodionov VE, Tumanyan GA, Ivashkevich SG, Bonartsev AP, Borozdkin LL. Biocom-patibility and Bioresorption of 3D-Printed Polylactide and Polyglycolide Tissue Membranes. Bull Exp Biol Med. 2021 Jan;170(3):356-359. Doi: 10.1007/s10517-021-05066-x. Epub 2021 Jan 16. PMID: 33452990.
9. Muraev A. A. et al., Ivanov S. Yu., Kibardin A., Dymnikov A. B., Larin S. S. Possibilities of creating bioceramic bone substituting materials by 3D-prototyping», Proceedings of III International Scientific and Practical Conference «New Technologies of Bio-ceramics Creation and Application in Regenerative Medicine»; Tomsk Polytechnic University.- Tomsk: Tomsk Polytechnic University Press, 2013, pp. 120-124
10. Kohri M, Miki K, Waite DE, Nakajima H, Okabe T. In vitro stability of bi-phasic calcium phosphate ceramics. Biomaterials. 1993;14(4):299-304. Doi: 10.1016/0142-9612(93)90122-i. PMID: 8386558.
11. Nery EB, legeros RZ, Lynch KL, Lee K. Tissue response to biphasic calcium phosphate ceramic with different ratios of HA/beta TCP in periodontal osseous defects. J Periodontol. 1992 Sep;63(9):729-35. Doi: 10.1902/jop.1992.63.9.729. PMID: 1335498.
12. Kühne JH, Bartl R, Frisch B, Hammer C, Jansson V, Zimmer M. Bone formation in coralline hydroxyapatite. Effects of pore size studied in rabbits. Acta Orthop Scand. 1994 Jun;65(3):246-52. Doi: 10.3109/17453679408995448. PMID: 8042473.
13. Druecke D, Langer S, Lamme E, Pieper J, Ugarkovic M, Steinau HU, Homann HH. Neovascularization of poly(ether ester) block-copolymer scaffolds in vivo: long-term studies using intravital fluorescent microscopy. J Biomed Mater Res A. 2004 Jan 1;68(1):10-8. Doi: 10.1002/ jbm.a.20016. PMID: 14661244.
14. Muraev A.A., Ivanov S. Y., Artifexova A.A., Ryabova V. M., Volodi-na E. V., Polyakova I. N. Study of biological properties of new osteoplas-tic material based on non-mineralized collagen containing vascular endothelial growth factor in bone defects replacement // Modern technologies in medicine, ' 1, 2012, pp. 21-26.;
15. Muraev A.A., Ivanov S. Y., Ryabova V.M., Artifexova F. F., Volodi-na E. V., Polyakova I. N. Toxicity and biological activity of a new osteosubstituting material based on non-mineralized collagen containing vascular endothelial growth factor. // Modern technologies in medicine, № 3, 2012, p. 19-26
16. Lokmic Z, Stillaert F, Morrison WA, Thompson EW, Mitchell GM. An arteriovenous loop in a protected space generates a permanent, highly vascular, tissueengineered construct. FASEB J. 2007Feb;21(2):511-22. Doi: 10.1096/fj.06-6614com. Epub 2006 Dec 16. PMID: 17172640.
17. Tanaka Y, Tsutsumi A, Crowe DM, Tajima S, Morrison WA. Generation of an autologous tissue (matrix) flap by combining an arteriovenous shunt loop with artificial skin in rats: preliminary report. Br J Plast Surg. 2000 Jan;53(1):51-7. Doi: 10.1054/bjps.1999.3186. PMID: 10657450.
18. Tanaka Y, Sung KC, Tsutsumi A, Ohba S, Ueda K, Morrison WA. Tissue engineering skin flaps: which vascular carrier, arteriovenous shunt loop or arteriovenous bundle, has more potential for angiogenesis and tissue generation. Plast. Reconstr. Surg. 2003 Nov; 112(6):1636-44. Doi: 10.1097/01.PRS.0000086140.49022.AB. PMID: 14578795.
19. Erol OO, Sira M. New capillary bed formation with a surgically constructed arteriovenous fistula. Plast Reconstr Surg. 1980 Jul;66(l):l09-l5. Doi: 10.1097/00006534-198007000-00021. PMID: 6156468.
20. Khouri RK, Upton J, Shaw WW. Prefabrication of composite free flaps through staged microvascular transfer: an experimental and clinical study. Plast Reconstr Surg. 1991 Jan;87(1):108-15. Doi: 10.1097/00006534-199101000-00017. PMID: 1984254.
21. Lukyanov V. G. Intraorgan relationships of vessels and nerves of periosteum of upper and lower jaws / V. G. Lukyanov // Dentistry.- 1971.-№ 2.-C. 82-85.
22. Jiang GH, Yan JH, Lin CL, Huang Y, Wen H, Li WM. [Anatomic study of the facial artery using multislice spiral CT angiography]. Nan Fang Yi Ke Da Xue Xue Bao. 2008 Mar;28(3):457-9. Chinese. PMID: 18359713.
23. Volikov V. V., Andreeva I. V. Morphological peculiarities of arteries and vasculature of maxillary mandibular paradontium in intact dentition, partial and complete adentia // Materials of annual scientific conference of Academician I. P. Pavlov Ryazan State Medical University, dedicated to the 65th anniversary of the university in the Ryazan region. Ryazan: 2015 P. 272-274
24. Tan BK, Chen HC, He TM, Song IC. Flap prefabrication - the bridge between conventional flaps and tissue-engineered flaps. Ann Acad Med Singap. 2004 Sep;33(5):662-6. PMID: 15536673.
25. Hirase Y, Valauri FA, Buncke HJ, Newlin LY. Customized prefabricated neovascularized free flaps. Microsurgery. l987;8(4):2l8-24. Doi: 10.1002/micr.1920080410. PMID: 3323773.
26. Morrison WA, Dvir E, Doi K, Hurley JV, Hickey MJ, O'Brien BM. Prefabrication of thin transferable axial-pattern skin flaps: an experimental study in rabbits. Br J Plast Surg. 1990 Nov;43(6):645-54. Doi: 10.1016/0007-1226(90)90184-2. PMID: 1701673.
27. Cassell OC, Hofer SO, Morrison WA, Knight KR. Vascularisation of tissue-engineered grafts: the regulation of angiogenesis in reconstructive surgery and in disease states. Br J Plast Surg. 2002 Dec;55(8):603-10. Doi: 10.1054/bjps.2002.3950. PMID: 12550111.
28. Kneser U, Polykandriotis E, Ohnolz J, Heidner K, Grabinger L, Euler S, Amann KU, Hess A, Brune K, Greil P, Stürzl M, Horch RE. Engineering of vascularized transplantable bone tissues: induction of axial vascularization in an osteoconductive matrix using an arteriovenous loop. Tissue Eng. 2006 Jul;12(7):172131. Doi: 10.1089/ten.2006.12.1721. PMID: 16889503.
29. Nath KA, Kanakiriya SK Grande JP, Croatt AJ, Katusic ZS. Increased venous proinflammatory gene expression and intimal hyperplasia in an aor-to-caval fistula model in the rat. Am J Pathol. 2003 Jun;l62(6):2079-90. Doi: 10.1016/S00029440(10)64339-8. PMID: 12759262; PMCID: PMC 1868137.
30. Dvorak HF, Detmar M, Claffey KP, Nagy JA, van de Water L, Senger DR. Vascular permeability factor/vascular endothelial growth factor: an important mediator of angiogenesis in malignancy and inflammation. Int Arch Allergy Immunol. 1995 May-Jun;107(1-3):233-5. Doi: 10.1159/000236988. PMID: 7542074.
31. Davies PF, Remuzzi A, Gordon EJ, Dewey CF Jr, Gimbrone MA Jr. Turbulent fluid shear stress induces vascular endothelial cell turnover in vitro. Proc Natl Acad Sci U S A. 1986 Apr;83(7):2114-7. Doi: 10.1073/ pnas.83.7.2114. PMID: 3457378; PMCID: PMC323241.
32. Leibig N, Wietbrock JO, Bigdeli AK, Horch RE, Kremer T, Kneser U, Schmidt VJ. Flow-Induced Axial Vascularization: The Arteriovenous Loop in Angiogenesis and Tissue Engineering. Plast Reconstr Surg. 2016 Oct;138(4):825-835. Doi: 10.1097/PRS.0000000000002554. PMID: 27673517.
33. Polykandriotis E, Tjiawi J, Euler S, Arkudas A, Hess A, Brune K, Greil P, Lametschwandtner A, Horch RE, Kneser U. The venous graft as an effector of early angiogenesis in a fibrin matrix. Microvasc Res. 2008 Jan;75(l):25-33. Doi: 10.1016/j.mvr.2007.04.003. Epub2007 Apr 18. PMID: 17544455.
34. Schmidt VJ, Hilgert JG, Covi JM, Weis C, Wietbrock JO, de Wit C, Horch RE, Kneser U. High flow conditions increase connexin43 expression in a rat arteriovenous and angioinductive loop model. Plos One. 2013 Nov 13;8(11): e78782. Doi: 10.1371/journal.pone.0078782. PMID: 24236049; PMCID: PMC 3827249.
35. Wu X, Wang Q, Kang N, Wu J, Gu C, Bi J, Lv T, Xie F, Hu J, Liu X, Cao Y, Xiao R. The effects of different vascular carrier patterns on the angiogenesis and osteogenesis of BMSC-TCP-based tissue-engineered bone in beagle dogs. J Tissue Eng Regen Med. 2017Feb;11(2):542-552. Doi: 10.1002/term.2076. Epub 2015 Aug 7. PMID: 26251084.
36. Eweida A, Fathi I, Eltawila AM, Elsherif AM, Elkerm Y, Harhaus L, Kneser U, Sakr MF. Pattern of Bone Generation after Irradiation in Vascularized Tissue Engineered Constructs. J Reconstr Microsurg. 2018 Feb;34(2):130-137. Doi: 10.1055/s-0037-1607322. Epub 2017 Oct 30. PMID: 29084413.
37. Dong QS, Shang HT, Wu W, Chen FL, Zhang JR, Guo JP, Mao TQ. Prefabrication of axial vascularized tissue engineering coral bone by an arteriovenous loop: a better model. Mater Sci Eng C Mater Biol Appl. 2012 Aug 1;32(6):1536-41. Doi: 10.1016/j.msec.2012.04.039. Epub2012 Apr28. PMID: 24364957.
38. Arkudas A, Lipp A, Buehrer G, Arnold I, Dafinova D, Brandl A, Beier JP,, Körner C, LyerS, Alexiou C, Kneser U, Horch RE. Pedicled Transplantation of Axially Vascularized Bone Constructs in a Critical Size Femoral Defect. Tissue Eng Part A. 2018 Mar;24(5-6):479-492. Doi: 10.1089/ten. TEA.2017.0110. Elpub 2017 Oct 25. PMID: 28851253.
39. Kim HY, Lee JH, Lee HAR, Park JS, Woo DK, Lee HC, Rho GJ, Byun JH, Oh SH. Sustained Release of BMP-2 from Porous Particles with Leaf-Stacked Structure for Bone Regeneration. ACS Appl Mater Interfaces. 2018 Jun 27;10(25):21091-21102. Doi: 10.1021/acsami.8b02141. Epub 2018 Jun 12. PMID: 29863327.
40. Boos AM, Loew JS, Weigand A, Deschler G, Klumpp D, Arkudas A, Bleiziffer O, Gulle H, Kneser U, Horch RE, Beier JP. Engineering axially vascularized bone in the sheep arteriovenous-loop model. J Tissue Eng Regen Med. 2013 Aug;7(8):654-64. Doi: 10.1002/term.1457. Epub 2012 Mar22. PMID: 22438065.
41. Buehrer G, Balzer A, Arnold I, Beier JP, Koerner C, Bleiziffer O, Brandl A, Weis C, Horch RE, Kneser U, Arkudas A. Combination of BMP2 and mscs significantly increases bone formation in the rat arteriovenous loop model. Tissue Eng. Part A. 2015 Jan;21(1-2):96-105. Doi: 10.1089/ten.TEA.2014.0028. Epub 2014 Nov 7. PMID: 25135080; PMCID: PMC 4293096.
42. Arkudas A, Beier JP, Heidner K, Tjiawi J, Polykandriotis E, Srour S, Sturzl M, Horch RE, Kneser U. Axial prevascularization of porous matrices using an arteriovenous loop promotes survival and differentiation of transplanted autologous osteoblasts. Tissue Eng. 2007 Jul;13(7):1549-60. Doi: 10.1089/ten.2006.0387. PMID: 17518756.
43. Tee R, Morrison WA, Dusting GJ, Liu GS, Choi YS, Hsiao ST, Dilley RJ. Transplantation of engineered cardiac muscle flaps in syngeneic rats. Tissue Eng Part A. 2012 Oct;18(19-20):1992-9. Doi: 10.1089/ten. TEA.2012.0151. Epub 2012 Sep4. PMID: 22793168; PMCID: PMC3463279.
44. Messina A, Bortolotto SK, Cassell OC, Kelly J, Abberton KM, Morrison WA. Generation of a vascularized organoid using skeletal muscle as the inductive source. FASEB J. 2005 Sep;19(11):1570-2. Doi: 10.1096/ fj.04-3241fje. Epub 2005 Jul 12. PMID: 16014398.
45. Witt R, Weigand A, Boos AM, Cai A, Dippold D, Boccaccini AR, Schubert DW, Hardt M, Lange C, Arkudas A, Horch RE, Beier JP. Mesenchymal stem cells and myoblast differentiation under HGF and IGF-1 stimulation for 3D-skeletal muscle tissue engineering. BMC Cell Biol. 2017 Feb 28;18(1):15. Doi: 10.1186/s12860-0170131-2. PMID: 28245809; PMCID: PMC5331627.
46. Fiegel HC, Pryymachuk G, Rath S, Bleiziffer O, Beier JP, Bruns H, Kluth D, MetzgerR, Horch RE, TillH, KneserU. Foetalhepatocyte transplantation in a vascularized AV-Loop transplantation model in the rat. J Cell Mol Med. 2010 Jan;14(1-2):267-74. Doi: 10.1111/j.1582-4934.2008.00369.x. Epub 2008 May 24. PMID: 18505475; PMCID: PMC3837593.
47. Brown DL, Meagher PJ, Knight KR, Keramidaris E, Romeo-Meeuw R, Penington AJ, Morrison WA. Survival and function of transplanted islet cells on an in vivo, vascularized tissue engineering platform in the rat: A pilot study. Cell Transplant. 2006;15(4):319-24. Retraction in: Morrison WA. Cell Transplant. 2008;16(10):1071. PMID: 16898225.
48. Robering JW, Weigand A, Pfuhlmann R, Horch RE, Beier JP, Boos AM. Mesenchymal stem cells promote lymphangiogenic properties of lymphatic endothelial cells. J Cell Mol Med. 2018 Aug;22(8):3740-3750. Doi: 10.1111/jcmm. 13590. Epub 2018 May 11. PMID: 29752774; PMCID: PMC 6050462.
49. Cassell OC, Morrison WA, Messina A, Penington AJ, Thompson EW, Stevens GW, Perera JM, Kleinman HK, Hurley JV, Romeo R, Knight KR. The influence of extracellular matrix on the generation of vascularized, engineered, transplantable tissue. Ann N Y Acad Sci. 2001 Nov;944:429-42. Doi: 10.1111/j.17496632.2001.tb03853.x. PMID: 11797691.
50. Hof er SO, Knight KM, Cooper-White JJ, O'Connor AJ, Perera JM, romeomeeuw R, Penington AJ, Knight KR, Morrison WA, Messina A. Increasing the volume of vascularized tissue formation in engineered constructs: an experimental study in rats. Plast Reconstr Surg. 2003 Mar;111(3):1186-92; discussion 1193-4. Doi: 10.1097/01. PRS.0000046034.02158.EB. PMID: 12621190.
51. Dolderer JH, Kehrer A, Schiller SM, Schröder UH, Kohler K, Schaller HE, Siegel-Axel D. De-novo Generierung von vaskularisiertem Gewebe mittels unterschiedlicher Gefässstielkonfigurationen in perforierten und geschlossenen Wachstumskammern [De-novo generation of vascularized tissue using different configurations of vascular pedicles in perforated and closed chambers]. Wien Med Wochenschr. 2010 Mar, 160(5-6):139-46. German. Doi: 10.1007/s10354-009-0734-0. PMID: 20364417.
52. Arkudas A, Pryymachuk G, Beier JP, Weigel L, Körner C, Singer RF, Bleiziffer O, Polykandriotis E, Horch RE, Kneser U. Combination of extrinsic and intrinsic pathways significantly accelerates axial vascularisation of bioartificial tissues. Plast Reconstr Surg. 2012 Jan;129(1):55e-65e. Doi: 10.1097/PRS.0b013e3182361f97. PMID: 22186585.
53. Beier JP, Horch RE, Arkudas A, Polykandriotis E, Bleiziffer O, Adamek E, Hess A, Kneser U. De novo generation of axially vascularized tissue in a large animal model. Microsurgery. 2009;29(1):42-51. Doi: 10.1002/ micr.20564. PMID: 18853419.
54. Weigand A, Beier JP, Hess A, Gerber T, Arkudas A, Horch RE, Boos AM. Acceleration of vascularized bone tissue-engineered constructs in a large animal model combining intrinsic and extrinsic vasculariza-tion. Tissue Eng Part A. 2015 May;21(9-10):1680-94. Doi: 10.1089/ten. TEA.2014.0568. Epub 2015 Apr 15. PMID: 25760576.
55. Eweida AM, Nabawi AS, Abouarab M, Kayed M, Elhammady H, Eta-by A, Khalil MR, Shawky MS, Kneser U, Horch RE, Nagy N, Marei MK. Enhancing mandibular bone regeneration and perfusion via axial vascularization of scaffolds. Clin Oral Investig. 2014 Jul;18(6):1671-8. Doi: 10.1007/s00784-013-1143-8. Epub 2013 Nov 19. PMID: 24248640.
Received 06.08.2022 Revised 10.08.2022 Accepted 20.08.2022
INFORMATION ABOUT AUTHORS
Kobets Konstantin Konstantinovich, Assistant of the department of Oral and Maxillofacial Surgery and Surgical Dentistry of the Medical Institute of Peoples Friendship University of Russia (RUDN University). ORCID: https://orcid.org/0000-0002-8141-0460, SPIN-code: 8706-7429. Tel. +79150999889; e-mail: [email protected]
Kazaryan Artak Artyomovich, the 4-th grade student of the Dental Faculty of the Medical Institute of Peoples' Friendship University of Russia. ORCID: https://orcid.org/0000-0003-0669-9353. Tel. +79629392500, e-mail: [email protected]
Bopkhoev Saddam Visingireevich, Postgraduate student of the department of Oral and Maxillofacial Surgery and Surgical Dentistry of the Medical Institute of the Peoples' Friendship University of Russia (RUDN University). ORCID: https://orcid.org/0000-0003-0431-0033, SPIN-code: 9308-5544. Tel. +79252200108, e-mail: [email protected]
