The 3D printed titanium mesh with high porosity has better repair effects than that with low porosity

doi:10.21203/rs.3.rs-2076765/v1

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Research Article

The 3D printed titanium mesh with high porosity has better repair effects than that with low porosity

https://doi.org/10.21203/rs.3.rs-2076765/v1

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published 06 Jan, 2023

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Background

Most patients with insufficient bone mass suffer from severe horizontal or vertical bone defects in oral implant surgery. The purpose of this study was to compare the bone regeneration effects of titanium mesh with different porosity in the treatment of bone defects.

Methods

Nine beagle dogs were equally divided into three groups. Three months after the extraction of the first to fourth premolars of the mandible, three bone defects were randomly selected in the mandible. Bone particles and three kinds of 3D printed titanium nets with different porosity (low porosity group, 55%; medium porosity group, 62%; and high porosity group, 68%) were replanted in situ. Beagle dogs were killed 4, 8, and 12 weeks after surgery. Formalin fixed specimens were embedded in acrylic resin. The specimens were stained with micro CT and hard tissue grinding.

Results

microCT analysis showed that the trabecular thickness, trabecular number, and bone volume fraction of the high porosity group were higher than those of the other two groups. Moreover, the trabecular separation of the high porosity group decreased slightly at any time and was lower than that of the medium porosity and low porosity groups. Histological staining analysis showed that the trabecular number in the high porosity group was higher than in the other two groups at 8 and 12 weeks, and the bone volume fraction was higher than that in the other two groups at 12 weeks. Moreover, the TB. Thmp was higher than that of the LP group at 12 weeks and the trabecular separation was lower in the high porosity group at 4 and 8 weeks. The differences were statistically significant (P < 0.05).

Conclusions

3D printed titanium mesh with high porosity in a certain range may have more advantages than titanium mesh with low porosity in repairing large bone defects.

3D printed

titanium mesh

bone defects

porosity

oral surgery

In oral implant surgery, most patients with insufficient bone mass suffer from severe horizontal or vertical bone defects. The majority of those patients have severe alveolar bone atrophy or defect caused by congenital tooth loss or trauma [1, 2]. One of the key factors for the success of the implant surgery is to restore the appropriate width and height of the bone and treat the large-area bone defect [3], In the late 1960s, titanium mesh, which is different from the traditional barrier membrane (such as the absorbable collagen membrane and the nonabsorbable expanded polytetrafluorethylene membrane), was first used in the treatment of alveolar ridge defects and achieved good clinical efficacy. Moreover, the titanium mesh structure can provide good mechanical support and a sufficient space for bone regeneration for the growth and development of a new bone. It also has good clinical efficacy for bone reconstruction in patients with large-area or multi tooth jaw defects [4–6]. After placing the titanium mesh at the position of bone defect of the patient, it is important to assess the strength of the titanium mesh and the blood supply. The pressure generated by the labiobuccinator muscle movement or chewing of the patient will act on the titanium mesh. Accordingly, the titanium mesh must have a certain compressive capacity that prevents its collapse or shift to provide sufficient space and mechanical support for the growth of a new bone. A good blood supply is conducive to the metabolism of bone marrow mesenchymal stem cells, growth factors, and other substances beneficial to osteogenesis [7]. The type of material, thickness, pore size, and porosity of titanium mesh are all important factors in the design process of the titanium mesh. Those parameters mainly affect the strength of the titanium mesh, the maintenance of blood supply to the bone, bone regeneration, and soft tissue healing. Previous studies have reported a large number of animal experiments and clinical observations on the material, thickness, and pore size of titanium mesh, but there are a few studies that examined the porosity of titanium mesh. In particular, there is a scarcity in studies reporting large-scale animal experiments that accurately observe the effect of porosity of titanium mesh [8, 9]. With the recent wide application of 3D printing technology in the oral field, personalized titanium mesh that fits the anatomical shape of the alveolar ridge can be manufactured by the digital technology of the 3D printing process. It is more suitable for complex jaw loss related cases compared with the traditional titanium mesh. The size and volume of the jaw defect can be accurately calculated and analyzed through accurate computer-aided design / computer-aided manufacturing (CAD / CAM) measurements and other technologies. Moreover, a mesh structure that accurately fits the anatomy of the jaw can be designed. The personalized printed titanium mesh has a good shape, a simple operation procedure, and reduces stress on the jaw bones [10–12]. Therefore, it is important to explore and clarify the appropriate range of mesh porosity during the design and manufacture processes of the titanium mesh. This study aimed to explore the effect of porosity of 3D printed personalized titanium mesh on the repair of alveolar bone defects in large animals based on the animal model of beagle dog to provide a reference for the future design of titanium mesh.

This study was carried out with the approval of the Capital Medical University Animal Experi- ments and Experimental Animals Management Committee (Beijing, China. Approval No. AEEI-2017-104) and complied with the ARRIVE (Animal Research: Reporting of In Vivo Experiments) guidelines for preclinical animal studies. All methods were performed in accordance with the relevant guidelines and regulations.

2.1 Experimental animals

Nine beagle dogs (1–2 years old, 15 kg) were obtained from the Institute of Animal Science, Chinese Agriculture University, China. They were housed in individual cages in a controlled environment (20–25°C and RH, 40–60%). The animals were fed soft dog-food diet (Science Diet, Hill’s Pet Co., Topeka, KS, USA) and had free access to water.

2.2 Surgical procedure

Veterinary assistance was used throughout all the procedures and all efforts were exerted to minimize pain. In the first stage of surgery, all animals were preanesthetized with atropine sulfate (0.05 mg/kg intramuscular (IM) injection; Guangdong South China Pharmaceutical Co., Ltd., Guang Dong, China) and tiletamine/zolazepam (5 mg/kg IV; Zoletil 50; Virbac, Carros, France). Local anesthesia was achieved by infiltrating 1 mL of articaine (Produits Dentaires Pierre Rolland, France) containing epinephrine (1:100,000) into the mucosa at the surgical sites. Anesthesia was sustained with sevoflurane (Sevorane; Capital Medical University, Beijing, China). The buccal, lingual, and lateral walls of the alveolar sockets were preserved. The teeth were carefully extracted without damaging the extraction sockets. Multimodal analgesia was used during the perioperative period. After the tooth extraction, metacam 0.1 mg/kg (PO; Boehringer Ingemheim Co., Ridgefield, CT, USA), ketorolac 1 mg/ kg (Toradol 30 mg; Shanghai Roche Pharmaceuticals Co., Ltd., Shang Hai, China), tramadol 1.7 mg/kg [Ado- lonta injectable, Grünenthal, Huayou medical group, Beijing, China], and buprenorphine 0.01 mg/kg (Buprex; Reckitt Benckiser Pharmaceuticals Limited, Berkshire, UK) were used to reduce pain. To prevent postoperative infection, amoxicillin (20 mg/kg PO; The United Laboratories Co., Ltd., Hong Kong, China) was administered for 6 days. Each dog was fed a liquid diet for 2 weeks, followed by a soft diet in a single cage. The extraction sites were allowed to heal for 3 months.

Three months after the tooth extraction socket of the beagle dogs healed, the maxillofacial region of the beagle dogs was scanned with CBCT. The CBCT image data were obtained and saved in DICOM format. The digital files were sent to the Ti-mesh manufacturer (Digital Mesh Technology Co., Ltd, Beijing China) to create a 3D copy of the edentulous site and the adjacent teeth (Fig. 1A). The thickness of the titanium mesh design was 0.4 mm, the diameter of the circular aperture was 1.4 mm, and the porosity was set to 55%, 62%, and 68% for the low porosity (LP), medium porosity (MP), and high porosity (HP) dog groups, respectively. This model was used for the individual CAD of the digital Ti-mesh. After approval by the surgeon, class IV titanium mesh was produced by means of selective laser sintering (Yxoss CBR®) (CAM). After the selective laser sintering process, the component underwent a blasting surface treatment process(Fig. 1B,C). Finally, ultrasonic washing, sterilization, and disinfection were carried out. After completion, sterile packaging was used to seal it.

In the second stage, the mandible model of each beagle dog was printed according to the CBCT of the respective beagle dog. Then, the mandible model was measured and marked according to the distance between the bone defect design site and the canine and molar teeth, and the distance between the two bone defect sites. A simple pressed film guide plate was made to unify the position, size, and shape of the bone defect during the operation. Anesthesia and perioperative management procedures were the same as those carried out in the first stage. A horizontal incision was made along the alveolar crest ranging from the mesial region of the mandibular molar to the distal region of the canine. The buccal and lingual mucoperiosteal membranes were peeled off and the flap was turned over to expose the bone surface. Two bone defects were created on the buccal side in each quadrant with an ultrasonic osteotome according to the osteotomy guide plate. The depth, mesial distal direction, and buccolingual direction were 6 mm apart with 10 mm intervals. The autologous bone blocks taken out were ground into granules and implanted into the bone defect area. Three bone defect sites were made for each beagle dog and were randomly allocated according to the porosity (55%, 62%, and 68% for the LP group, MP group, and HP group, respectively). Then, the sites were implanted with personalized titanium mesh and bio Gide barrier membrane (Geistlich, Switzerland). The tension was reduced and the absorbable thread (vycril 5/0) was pulled up for creating tight sutures. At weeks 4, 8, and 12, three dogs were euthanized by administering concentrated sodium pentobarbital IV (Euthasol, Delmarva Laboratories, Inc., Midlothian, VA, USA). Block sections were immediately collected from the alveolar bone (Fig. 2A–K).

2.3 Micro-computed tomography (Micro-CT) evaluation

The specimens were scanned on a micro-CT system (Inveon, Siemens, Germany; 80 kV, 500 µA, 1500 ms exposure time) before mechanical and histological assessment. The trabecular thickness (Tb. Th), trabecular number (Tb. N), trabecular separation (Tb. Sp), bone surface/bone volume ratio (BS/BV), and bone volume/total volume ratio (BV/TV) were determined.

2.4 Histochemical examination

The specimens were fixed with 4% formalin, decalcified with 10% ethylenedi-aminetetraacetic acid (pH 7.0), and dehydrated through a graded series of ethanol solutions and 100% acetone. Then, the specimens were embedded in methyl methacrylate. The tissue slides (25 µm) were prepared in the buc-colingual direction parallel to the axis of the implants by an EXAKT 400CS grinding machine (Leica, Wetzlar, Germany). The slides were then stained with toluidine blue– basic fuchsin stain. Images were captured and analyzed by a light microscope (Olympus BH2 with S Plan FL2 lens, Tokyo, Japan) and a computer-digitized image analysis system (Leica Imaging System, Cambridge, England). The Tb.Th, Tb.N, Tb.Sp, BS/BV, and BV/TV were determined.

2.5 Statistical analysis

All statistical calculations were performed with SPSS 16 statistical software (SPSS, Inc., Cary, NC, USA). Statistical significance was determined by independent-samples Student’s t-test or analysis of variance (ANOVA). The p-values less than 0.05 were considered statistically significant; p < 0.05 (*), p < 0.001 (**), p < 0.0001 (****).

The healing process progressed uneventfully in all the animals and no postoperative complications were noted during the 12-week observation period. After a postoperative resting period of 3–6 days, the animals could move and leap without any notable pain or limitation.

Micro CT evaluation showed that the titanium mesh with high porosity formed more new bones. The sagittal and coronal schematic diagrams of the region of interest and the volume of new bones after 3D reconstruction could be seen. In the longitudinal comparison of the time axis, the bone defects of the titanium mesh in the 4-, 8-, and 12-week groups had different degrees of new bone formation. In the transverse comparison, the effect of new bone formation at each time node was higher with increasing the porosity (HP group > MP group > LP group; Fig. 3A, B, and C). In the longitudinal direction of the time axis of the parameter analysis, TB. Th, TB. N, and BV / TV in the bone defect area increased with the increase in the bone healing time. While TB. SP decreased with the increase in the bone healing time, indicating that the new bone density was increasing. In the horizontal comparison, the TB. Th, TB. N, and BV/TV of the titanium mesh in the HP group were higher than those in the other two groups. The TB. SP decreased slightly at any time and was lower than in the other two groups. The BV/TV, TB. Th, and TB. N in the MP group were statistically higher than those in the LP group, while the TB. SP was statistically lower than that in the LP group (all p-values < 0.05) (Fig. 3D).

Histological observation revealed that the titanium mesh with high porosity showed a good repairing effect on the bone defects in vivo. The basic fuchsin staining shows the new bone in dark pink and the mother bone in light pink, while the toluidine blue staining shows the new bone in dark blue and the mother bone in light blue. After 4 weeks, a new bone has been formed around the mother bone in the HP and MP groups, and to a lower extent in the LP group (Fig. 4A). After 8 weeks, the HP group had a large area of new bone and the MP group showed a new bone area around the mother bone, while the LP group showed a lower extent of new bone formation (Fig. 4B). After 12 weeks, a large area of new bone has been formed around the mother bone and the bone defect area has been filled in the HP and MP groups. This observation was more evident in the HP group. In the LP group, a new bone area has also been formed but with a large amount of fibrous tissue (Fig. 4C). The TB. N in the HP group was higher than that in the other two groups at 8 and 12 weeks, the BV / TV was higher in the HP group than that in the other two groups at 12 weeks, the TB. Thmp was higher in the HP group than that in the LP group at 12 weeks, and the TB. SP was lower in the HP group at 4 and 8 weeks. The differences were all statistically significant (Fig. 4D).

In oral implant surgery, titanium mesh plays an important role in the bone reconstruction in patients with large area or multiple tooth position jaw defects. Titanium mesh acts as a mechanical barrier membrane and it essentially acts as a "tent" to provide a sufficient low pressure space for the formation of new bone in alveolar ridge incremental surgery, which is conducive to the regeneration and repair of large-area bone defects [13, 14]. Recent studies have shown that titanium mesh effectively ensures that patients with bone defects obtain sufficient bone increment. The clinical effect of its combined application with absorbable biofilm is better as the biofilm prevents the rapid growth of soft tissue. Titanium mesh can act as a good mechanical support and provide a good environment for the growth of bone tissue. The bone increment effect of this treatment is better than the clinical effect of using biofilm alone [15–17]. In addition, in this study, we designed a 3D printed personalized titanium mesh. With the development of biomechanics and CBCT 3D imaging technology, we virtual reconstructed a 3D model of the bone defect through forward and reverse software, and designed a personalized titanium mesh model. The 3D printed titanium mesh has many advantages. First, it can reconstruct and design the alveolar ridge shape of the defect. It also ensures the reconstruction of aesthetics and function after implantation. Second, the titanium mesh suitable for bone defect and jaw shape can be printed out before the operation, which eliminates the need for the operator to adjust the shape of the titanium mesh twice in the hand and shortens the operation time. Third, the personalized titanium mesh can reduce the probability of postoperative titanium mesh exposure. The osteogenic effect of unexposed titanium mesh is better than that of the exposed mesh[12]. The could be attributed mainly to the lack of keratinized mucosa in the oral cavity of animals and the frenum and muscles in the mouth are often attached to the alveolar bone, thus the personalized titanium mesh substitutes the oral mucosa. Compared with the bone defect in the simple horizontal direction, horizontal and vertical bone defects are more likely to lead to postoperative exposure of the titanium mesh. Accordingly, the amount of bone formation will be significantly reduced after exposure of the titanium mesh [18–21].

Several criteria were considered at the design stage of the titanium mesh, such as the good mechanical properties, high compressive strength that can provide stable spatial support during the osteogenesis process, appropriate elastic modulus and plasticity that can reduce the pressure on the mucosa, and the good corrosion resistance of the titanium mesh. These characteristics are the key to achieve stable osteogenesis [22, 23]. The factors that were considered mainly included the material, thickness, pore size, shape, and porosity of the titanium mesh. Those factors were critical to the strength of the titanium mesh and the blood supply to the bone defect reconstruction site [24].

Previous studies have shown that pure titanium is an ideal material for titanium mesh because of its low density, high strength, corrosion resistance, good biocompatibility, and close elastic modulus to the cortical bone [25]. Clinically, titanium mesh with appropriate thickness should be selected according to the range and location of jaw defects and its mechanical properties should meet the clinical needs. Theoretically, the thicker the titanium mesh, the better the mechanical properties. However, while considering the mechanical properties of the titanium mesh, the stimulation of the thickness of the titanium mesh to the mucosa should also be considered to reduce the possibility of exposure of the titanium mesh. The titanium mesh used in this study was in accordance to the thickness design of the titanium mesh in the previosuly published studies[12]. A titanium mesh with a thickness of 0.4 mm can not only ensure sufficient strength of the titanium mesh, but also reduce its thickness [26]. In this experiment, the titanium mesh was designed as a single cell structure composed of round and spindle holes. The diameter of the round holes was fixed but the size of the spindle holes was controlled by the porosity. The purpose of our design was to facilitate the placement of different types of titanium nails. Some scholars cultured human osteoblasts on the surface of three kinds of porous titanium alloy scaffolds with different pore shapes (cubic, conical and diagonal). The results showed that the the metabolic activity of osteoblasts on the conical microporous scaffolds was significantly higher than that on the other two scaffolds. However, no significant difference was found between the metabolic activity of osteoblasts on the surfaces of cubic and diagonal structures [27]. Thus, the different pore shapes can affect the osteogenic ability of porous implants, but there is no conclusion about the optimal pore shape and its influence mechanism for regulating the bone induction performance of implants, which may be related to the difficulty in controlling the single variable of the pore shape in the experiments. The pore size design has always been the focus of titanium mesh design. The ideal pore size should not only facilitate the transportation and exchange of substances between cells, provide a convenient environment for the proliferation, and migration of osteoblasts and the growth of nerve vessels, but also ensure sufficient strength to withstand the bone stress. In general, a very small pore size will restrict the growth of cells, hinder the transportation of blood and nutrients, and lead to poor growth of osteoblasts. On the other hand, a very large pore diameter reduces the compressive property and strength of the implant material. Therefore, to determine the most suitable pore size for osteogenesis, it is necessary to find the best balance between the mechanical properties and biocompatibility of materials [28–30].

The shape of pores in the 3D printed titanium mesh is often irregular, thus the porosity is used to evaluate the volume proportion of pores in the titanium mesh [31]. Porosity is the percentage between the pore volume of a material and the total volume of the material in the natural state. It plays the same role as the pore size. The porosity of an implant can affect the free movement ability and exchange ability of substances between different pores and affect the bone growth level of the material [32, 33]. In this study, the titanium mesh with higher porosity shows better osteogenic effect in imaging and histology than that with lower porosity under the same conditions of material type, pore size, and thickness. Micro CT is an important imaging method to evaluate the osseointegration effect of implants. CT can display the bone mineral density and the microstructure of 3D bone trabeculae in the bone defect area. Compared with the traditional histological analysis method, it causes less trauma and can directly calculate the late trabecular bone structural parameters through micro CT analysis software, mainly through the TB. N, TB. SP, and TB. Th parameters. The TB. N, the maturity of bone tissue, and bone density are positively correlated with BS/BV and BV/TV [34, 35]. Methylene blue staining and toluidine blue staining are commonly used to observe the formation of new bone. In this study, we can clearly find the boundary between the mother bone and the new bone in the bone defect area of each group. After 4 weeks, a small area of new bone appeared in the HP group, while a large number of fibrous tissue still surrounded the mother bone in the LP group. After 8 weeks, the new bone in the HP group connected the bone debris. In the 12 week HP group, the bone defect area was basically filled with new bone and mother bone. In addition, the bone parameter analysis data were basically consistent with the results of the micro CT. In this study, the HP group titanium mesh showed a faster rate of new bone formation and excellent bone regeneration effect. Some scholars have reached similar conclusions through cell biology experiments. In principle, the closer the porosity of porous implants is to the porosity of human cancellous bone (70–90%), the more favorable it is for bone growth. If the porosity is too high, the compressive property and strength of the implant will be reduced, and it would be difficult to bear the stress of the bone resulting in a shortened service life. If the porosity is too low, it will hinder the material exchange of cells and affect the osteogenic ability [36, 37]. The porosity of the titanium mesh is not certain, but is closely related to the design of the pore size and shape of the titanium mesh. In this study, we designed the porosity of the titanium mesh to be 55%, 62%, and 68% in the LP, MP, and HP groups, respectively, set by researchers after 3D finite element analysis in the early stage to ensure that the titanium mesh has sufficient strength.The 3D printed titanium mesh with high porosity in a certain range may have more advantages than titanium mesh with low porosity in repairing large-area bone defects. In addition, Tamaddon et al. developed a porous titanium scaffold with a porosity of 72% by using 3D printing technology and inoculated sheep BMSCs on its surface for in vitro culture. The cells had good adhesion ability on the surface of the scaffold [38]. Reserachers prepared three kinds of porous titanium alloy scaffolds with porosities of 15.0% ± 2.9, 37.9% ± 4.0, and 70.0% ± 3.5, and planted MG-63 cells on their surfaces through 3D printing technology. The cells on the surface of the three scaffolds had a high survival rate, but the cells in the 70.0% ± 3.5 high porosity group had the highest survival rate [39]. Xu et al. prepared porous titanium alloy scaffolds with porosities of 40% and 70%, inoculated rabbit BMSCs for culture, and took dense titanium alloy as a control. The cells in the 40% and 70% porosity groups proliferated faster on the surface of the material, and the cells in the 70% porosity group grew from the edge to the pores in a shorter time with more tight connections [40].

This study shows that titanium mesh is an important auxiliary tool to solve large-area bone defects in oral implant surgery. Under the same conditions of material, pore size, shape, and thickness, 3D printed titanium mesh with higher porosity in a certain range may have more advantages than titanium mesh with low porosity in repairing large-area bone defects. The conclusions provide a reference for the porosity design of titanium mesh used in oral implant surgery.

BS/BV bone surface/bone volume ratio

BV/TV bone volume/total volume ratio

CAD computer-aided design

CAM computer-aided manufacturing

CT computed tomography

HP high porosity

LP low porosity

MP medium porosity

TB. N trabecular number

TB. SP trabecular separation

TB. Th trabecular thickness

Ethics approval and consent to participate

The present study complied with the principles of laboratory animal care and national laws on animal use, and the study was authorized by the Animal Experiments and Experimental Animal Welfare Committee of Capital Medical University, Beijing, China (protocol number AEEI-2017-104).

Consent for publication

Not applicable

Availability of data and materials

The data sets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Competing interests

None of the authors had any competing interests.

Funding

The design of the study and collection, analysis and, interpretation of data and in writing the manuscript were supported by Young Scientist Program of Beijing Stomatological Hospital, Capital Medical University, NO. YSP202208.

Authors' contributions

All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by LXW, RM, QL, and LBZ. The first draft of the manuscript was written by LXW and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Acknowledgments

Not applicable.

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No competing interests reported.

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published 06 Jan, 2023

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The 3D printed titanium mesh with high porosity has better repair effects than that with low porosity

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Abstract

Background

Methods

Results

Conclusions

Figures

1. Introduction

2. Materials And Methods

2.1 Experimental animals

2.2 Surgical procedure

2.3 Micro-computed tomography (Micro-CT) evaluation

2.4 Histochemical examination

2.5 Statistical analysis

3. Results

4. Discussion

5. Conclusions

Abbreviations

Declarations

References

Additional Declarations

Status:

Journal Publication

Version 1