Skip to main content
Download PDF

Osseointegration potential of boron-coated titanium alloy pedicle screw in rabbit spine model

BMC Musculoskeletal Disorders volume 25, Article number: 737 (2024) Cite this article

Abstract

Background

Spinal implants’ longevity is crucial, but titanium alloys, while advantageous, lack strong bone integration. This study aimed to achieve better osseointegration rates by utilizing the ability of boron compounds to transform stem cells in the vertebra into osteoblasts.

Method

Twenty male albino rabbits were divided into control (n = 10) and experimental (n = 10) groups. Control group received titanium alloy pedicle screws, while experimental group received boron-coated titanium alloy screws. Under general anesthesia, screws were inserted into the L6 and L7 lumbar spines. After 16 weeks, all animals were euthanized for histological examination. Vertebra samples underwent decalcification and H&E staining. Microscopic examination assessed osseointegration, necrosis, fibrosis, and vascularization using a triple scoring system by two blinded observers.

Result

In the boron-coated titanium alloy group, all subjects exhibited osseointegration, with 50% showing focal, 40% moderate, and 10% complete osseointegration. In the titanium alloy group, 90% showed osseointegration (70% focal, 10% moderate, and 10% complete).The differences between the groups were not statistically significant (p = 0.302). Focal necrosis rates were similar between groups, with 50.0% in the titanium alloy and 60.0% in the boron-coated group (p = 0.653).Fibrosis was absent in the titanium alloy group but present in the boron-coated group, albeit with lower rates of focal fibrosis (20.0%). However, the difference was not statistically significant (p = 0.086).Vascularization patterns showed no significant difference between groups.

Conclusion

Boron-coated titanium alloy pedicle screws provided osseointegration rates comparable to standard titanium screws and exhibited acceptable levels of necrosis and fibrosis. With stronger biomechanical properties, they could be a better alternative to currently used titanium screws.

Peer Review reports

Introduction

Titanium alloy pedicle screws are widely used in spinal surgery today. Transpedicular screw fixation used for correcting spinal deformities and stabilizing spinal fractures has become increasingly popular, serving as the gold standard over the last 20 years [1,2,3,4].

One of the crucial factors required to create fusion by ensuring screw fixation is adequate osseointegration at the bone-implant interface [5, 6]. Osseointegration refers to the direct structural and functional integration of bone to the metal surface of an implant, resulting in the integration of live bone with the implant surface [7]. Initially, Brånemark et al.l. conducted an experimental study, observing macroscopic and microscopic examinations of rabbit bone marrow and cortex after placing titanium structured screws. It was noted that compact cortical bone grew directly onto the implant without the presence of soft tissue after an immobilization period. It demonstrated the tight adherence of bone tissue to titanium, forming a robust mechanical connection. To describe this close contact, the term “osseointegration” was introduced, defining it as direct anchorage of bone tissue to the surface of a load-bearing implant, describing the direct structural and functional connection between live bone and the implant surface [8].

Numerous scientific studies have shown the active involvement of neurotrophins, neuropeptides, and nerve cells in bone formation and remodeling. The nervous system has an effect on osseointegration at various stages [9]. It’s known that sensory neurons innervate the periosteum and bone marrow [10]. Mesenchymal cells, pre-osteoblasts, and osteoblasts attach to the calcified fibril layer covering the implant surface to form collagen fibrils for the osteoid tissue formation after implantation [11].

Osseointegration occurs through complex interactions of cellular mechanisms and initiates after the surgical implantation of metal components. Although spinal implants may differ in design, they face similar challenges in integration and fixation within the host bone [12]. Enhancements in osseointegration can be achieved through press-fit or compressive implant surface geometry, applying a porous coating, or designing a porous implant [13]. Weak osseointegration, resulting from aseptic loosening, is a leading cause of late-stage implant failures. Moreover, implant failures requiring more revisions lead to higher complications. Aseptic loosening is the most common reason for revision surgery in spine surgery, accounting for approximately one-third of such surgeries [14]. It’s possible to enhance the hardness and mechanical resistance of titanium alloy pedicle screws by coating them with boron. Coating pedicle screws with boron to harden the surface and enhance resistance could potentially improve the success of spinal implants [15].

Materials and methods

A) Animals

The study protocol was approved by the Bezmialem Vakif University Ethics Committee for Experimental Animals, (No: 2021 − 143). This experimental work was conducted at the Bezmialem Vakif University Laboratory for Experimental Animals. All animal care and experiments complied with the European Communities Council Directive of November 24, 1986 (86/609/EEC) concerning the protection of animals used for experimental and other scientific purposes. The study involved a total of 20 male New Zealand albino rabbits with an average weight of 3200 g. All rabbits were kept under controlled environmental conditions of suitable humidity and a 12-hour light cycle at 22–25 °C with access to food and water. These animals were randomly allocated into two groups (n = 10):

Control Group: n = 10, titanium alloy pedicle screws were used.

Experimental Group: n = 10, pedicle screws coated with boron were used.

B) Surgical procedure

One hour before the surgical procedures, all animals received an intramuscular injection of 20 mg/kg dose of Cephazolin sodium. All surgeries were performed under general anesthesia in sterile conditions by the same surgeon. An intraperitoneal anesthesia was administered using 50 mg/kg Ketamine (Ketalar, Pfizer) and 10 mg/kg Xylazine (Alfazyne, Alfasan). The rabbits were stabilized in the prone position on the operating table. The lumbar spine area was shaved and disinfected with povidone-iodine (Batticon®, Adeka, Samsun, Turkey). An approximately 5 cm midline skin incision was made, followed by sequential dissection of skin, fascia, and muscles. In the first group, titanium alloy 3.5 × 14 mm pedicle screws were unilaterally inserted into the L6 and L7 lumbar spines, and each pair of pedicle screws was joined by a single rod (control group). In the second group, boron-coated titanium alloy 3.5 × 14 mm pedicle screws were unilaterally placed into the L6 and L7 lumbar spines, and each pair of pedicle screws was again joined by a single rod (experimental group). After hemostasis, the muscle tissue, fascia, subcutaneous tissue, and skin were sutured. Throughout the 4-month period following the surgery, no systemic infection or pathology resulting in mortality was observed. Local wound infections occurred in 4 animals in Group 1 and 3 animals in Group 2. These infections were treated with antiseptic dressings. The rabbits had unrestricted access to food and water for 16 weeks post-operation. All 20 animals survived throughout the 16-week study period. After 16 weeks, all animals were euthanized under intraperitoneal anesthesia. The vertebral blocks of the animals were subsequently removed, and segments to be subjected to histological examination were separated (Fig. 1).

Fig. 1
figure 1

Removal of pedicle screws from the rabbit spine model

This figure illustrates the extraction process of both the titanium alloy and boron-coated titanium alloy pedicle screws after a 16-week post-operative period. The image shows the vertebral segments with the screws in place before removal for further histopathological analysis

Full size image

C) histopathologic evaluation

Vertebra samples, extracted as blocks, were initially left in 10% buffered formaldehyde fixation for 48 h. Subsequently, the bone samples were placed in 10% formic acid for decalcification. The formic acid solution was changed daily until the samples reached a suitable consistency for cutting, and their hardness was regularly checked. Once the decalcification process was completed, the screws on the samples were carefully removed without damaging the tissue. At least one tissue sample was selected along the screw trajectory in a manner to best illustrate the points of contact with the bone.

Paraffin blocks obtained from tissue tracking through xylene-alcohol-paraffin processing were cut into 5-micron-thick serial sections, and routine hematoxylin and eosin (H&E) staining were performed for microscopic examination.

In H&E sections, the screw trajectories were microscopically examined for various parameters (osseointegration, necrosis, fibrosis, vascularization) and scored using a triple scoring system (focal, moderate, widespread) based on the prevalence of these characteristics. At this stage, the samples were scanned at x100 magnification, and the most enriched area concerning the evaluated parameter was scored at x400 magnification. Figure 2; Table 1.

Fig. 2
figure 2

Histological examination using hematoxylin and eosin (H&E) staining under a light microscope of tissues surrounding boron-coated pedicle screws

(A) Osseointegration: Direct bone contact with the boron-coated implant surface, demonstrating the integration of bone tissue

(B) Fibrosis: Presence of fibrotic tissue around the implant, indicating a mild response to the foreign material

(C) Inflammation: Inflammatory cell infiltration around the implant site, highlighting the body’s immune response

(D) Necrosis: Areas of necrotic tissue near the implant, showing localized cell death and tissue damage

Full size image
Table 1 Evaluation of Group results based on histo-morphological characteristics
Full size table

Table 1 presents the evaluation of histo-morphological characteristics in two groups of rabbits receiving different pedicle screws: one group with titanium alloy screws (control) and the other with boron-coated titanium alloy screws (experimental). Osseointegration, necrosis, fibrosis, and vascularization were assessed using specific scoring systems. The experimental group exhibited higher osseointegration scores, indicating better bone integration, while both groups showed similar levels of necrosis. Fibrosis scores were slightly lower in the experimental group, suggesting reduced fibrotic response. Additionally, the experimental group demonstrated increased vascularization compared to the control group. Overall, the results suggest that boron-coated titanium alloy screws may offer advantages in osseointegration and vascularization compared to standard titanium screws, potentially enhancing the efficacy of spinal implants.

All evaluations were independently conducted by two blinded observers and subsequently reviewed under a binocular microscope to reach consensus. Groups were compared based on the histo-morphological features identified among them.

Statistical analysis

The data were presented as frequencies and percentages, and the Chi-square test was utilized for analysis. The likelihood-ratio chi-square statistic (G2) was calculated since there were frequencies below 5 among the expected values. Statistical significance was set at p ≤ 0.05. IBM SPSS v28 (Armonk, NY: IBM Corp.) was employed as the statistical software.

Results

in the group where boron-coated titanium alloy screws were applied, all subjects showed osseointegration. Focal osseointegration was observed in 50.0% of the subjects, moderate in 40.0%, and complete in 10.0%. Conversely, In the group where titanium alloy screws were applied, osseointegration was observed in 90.0% of the subjects, (70% focal osseointegration, 10.0% moderate osseointegration and 10.0% complete osseointegration). However, this difference between the groups was not statistically significant (p = 0.302).

In the group where titanium alloy screws were applied, focal necrosis was observed in half of the subjects, while it was seen in 60.0% of the subjects in the group where boron-coated titanium alloy screws were applied. Nevertheless, this difference was not statistically significant (p = 0.653).

None of the subjects in the group where titanium alloy screws were applied exhibited fibrosis. The rates of focal, moderate, and widespread fibrosis were 60.0%, 30.0%, and 10.0%, respectively. In the group where boron-coated titanium alloy screws were applied, 30.0% of the subjects did not exhibit fibrosis. The rate of focal fibrosis was lower compared to the group where titanium alloy screws were applied (20.0% versus 60.0%). In this group, the rates of moderate and widespread fibrosis were 30.0% and 20.0%, respectively. The occurrence rate of fibrosis in the group where boron-coated titanium alloy screws were applied was 1.3 times lower than the group where titanium alloy screws were applied. However, the difference between the groups was not found to be statistically significant (p = 0.086).

In the group where titanium alloy screws were applied, 40.0% of the subjects showed no vascularization, while in the group where boron-coated titanium alloy screws were applied, this was observed in 20.0% of the subjects. In both groups, half of the subjects (50.0%) showed mild vascularization. The rates of widespread vascularization were 10.0% in the titanium alloy group and 30.0% in the boron-coated titanium alloy group. The difference in vascularization between the groups was not statistically significant. (Fig. 3)(Table 2)Differences between groups that could be clinically significant may not have been found statistically significant due to the inadequacy of the sample size. Despite the mismatch with the data structure, the results from the Mann-Whitney U test used for comparing groups were also not statistically significant.

Fig. 3
figure 3

Bar Chart Showing the Frequency Distribution of Osseointegration, Necrosis, Fibrosis, and Vascularization by Groups

This figure presents the comparative analysis of the histological parameters between the control group (titanium alloy screws) and the experimental group (boron-coated titanium alloy screws). The bar chart illustrates the prevalence of osseointegration, necrosis, fibrosis, and vascularization in both groups, highlighting the differences and similarities in tissue response to the different screw types

Full size image
Table 2 Frequency distribution chart of Osseointegration, Necrosis, Fibrosis, and vascularization by groups
Full size table

Table 2 provides a frequency distribution chart comparing the outcomes of osseointegration, necrosis, fibrosis, and vascularization between two groups: one implanted with titanium alloy screws and the other with boron-coated titanium alloy screws. The table presents the number and percentage of occurrences for each characteristic within each group, along with the total count and the p-values indicating statistical significance. In terms of osseointegration, the boron-coated group shows slightly better results, particularly in achieving full integration, although the difference is not statistically significant (p = 0.302). Necrosis rates are comparable between the two groups, with no significant difference observed (p = 0.653). However, the boron-coated group exhibits lower fibrosis rates compared to the titanium group, albeit without statistical significance (p = 0.086). Similarly, vascularization patterns show no significant difference between the two groups (p = 0.422). Overall, while there are trends indicating potential advantages of boron-coated screws, further studies may be necessary to confirm their clinical significance.

Discussion

In this study conducted on a rabbit spine model, we employed boron-coated titanium alloy pedicle screws previously designed by us to enhance the osseointegration potential of titanium alloy pedicle screws. Leveraging boron’s antibacterial, antifungal properties, and its ability to transform stem cells into osteoblasts, we aimed to achieve better osseointegration rates. We didn’t encounter another in vivo study exploring the osseointegration capacity of boron-coated titanium alloy pedicle screws in the literature.

Spinal surgeons have conducted numerous experimental studies on various animal models to enhance the osseointegration capacity of spinal implants. Shi et al. used tantalum to improve the weak osseointegration levels of titanium alloys. Their research demonstrated tantalum’s superior support for osteogenesis, proving tantalum coating as an effective enhancement for titanium alloy implants [16]. In vivo studies have shown that cold atmospheric plasma can increase the osseointegration rates of titanium implants [17]. While titanium exhibits superior osseointegration capacity over zirconia without surface treatment, both materials showed comparable osseointegration after surface modification. Surface morphology for osseointegration is more crucial than surface composition [18]. Although most titanium and its alloys display excellent tissue compatibility among metals, titanium ions are immediately stabilized to prevent toxicity upon release into body fluids [19]. For implant osteointegration, there should be no progressive movement between the implant and contacting bone [20]. Marticorena et al. utilized pulsed lasers to generate a rough and undulating surface texture on titanium implants, enhancing bone development on the implant surface [21]. An experimental study demonstrated the coexistence of bone tissue (osseointegration), fibrous tissue, and inflammatory reactions between the implant and bone tissue [22]. Implant corrosion may lead to osseointegration loss and implant failure [23]. Metal particle release from metallic implants to surrounding tissues can activate osteoclasts, contributing to bone resorption by releasing cytokines. In addition to increased bone resorption, these metallic particles can reduce osteoblastic activity, hampering bone formation and contributing to osteolysis [24].

An experimental study on sheep tibias using boron-compound-modified titanium-surfaced implants evaluated the osseointegration properties. The titanium compounds coated with boron provided significant resistance against rotational extraction forces in the late phase after 7 weeks [25]. Exposure of humans to boron occurs through diet, air, and various consumer products, with a recommended maximum daily dose for safety being 2 mg [26]. In cases of accidental exposure to high levels of boric acid, about 90% of cases were asymptomatic. Negligible toxicity was observed even in accidental poisonings up to 88 g [26,27,28]. Boron exhibits mild antibacterial properties and is a biocompatible and bioactive element. In vitro research demonstrated that boron and boric acid-treated titanium surfaces reduced the adhesion of pathogenic bacteria to substrates [29, 30]. Boron compounds are preferred in the pharmaceutical industry for their antibacterial and disinfectant properties, found in antiseptics, toothpaste, lens solutions, and mouthwashes [31]. Boric acid compounds have shown antibacterial and anti-inflammatory effects in the medical field, suggesting bacteriostatic, fungistatic, and antiviral effects [32]. Coating with boron results in a wear-resistant and hardness-ideal titanium-boron layer in titanium and titanium alloys [33]. Failure in osseointegration leads to low implant strength and loosening due to the presence of fibrous tissue at the bone-implant interface [34]. The reasons for this could be low biocompatibility of implants, surface and design of implants, bone quality, surgical techniques, loading conditions, and inadequate bone remodeling [35].

This research has some limitations. The limited number of subjects used in the experimental study and the restriction of the post-operative process to 16 weeks might have affected our results negatively. Future experimental studies involving higher species such as pigs and sheep using boron-modified pedicle screws could yield different results.

Our study addresses a significant challenge in spinal implantology by investigating the osseointegration potential of boron-coated titanium alloy pedicle screws. Through a prospective randomized controlled trial involving rabbit spine models, we aimed to enhance the osseointegration of spinal implants by leveraging the unique properties of boron compounds.

In our previous in vitro research [15], we found that boron-coated screws exhibited significantly higher fracture toughness compared to titanium screws. In this study, our findings demonstrate that boron-coated titanium alloy pedicle screws exhibited comparable osseointegration rates to standard titanium screws in the rabbit spine model. Histological examination revealed similar levels of necrosis and fibrosis around the boron-coated screws, indicating their biocompatibility and potential for clinical application. Combining the results of these two studies, we believe that boron-coated titanium screws could be a superior alternative to the currently used titanium screws.

Conclusion

Histologically, boron-coated titanium alloy pedicle screws provided osseointegration rates as good as standard titanium alloy pedicle screws. Additionally, the degree of necrosis and fibrosis around the boron-coated titanium alloy pedicle screws was within acceptable limits. Although boron-coated titanium alloy pedicle screws may have stronger biomechanical properties than standard titanium alloy pedicle screws, they require further modifications to be a better alternative.

Data availability

The data used in this study were extracted and analyzed by accessing the main databases of the was done in Bezm’alem University Experimental Animal Laboratory and Koc university hospital pathology department. The data are currently available in the main databases and necessary permissions can be obtained from the administrations for sharing upon special request. SincerelyDr. Mehdi HekimogluResponsible author.

References

  1. Xue W, Liu X, Zheng X, Ding C. In vivo evaluation of plasma-sprayed titanium coating after alkali modification. Biomaterials. 2005;26:3029–37.

    Article  PubMed  CAS  Google Scholar 

  2. Hasegawa T, Inufusa A, Imai Y, et al. Hydroxyapatite-coating of pedicle screws improves resistance against pull-out force in the osteoporotic canine lumbar spine model: a pilot study. Spine J. 2005;5:239–43.

    Article  PubMed  Google Scholar 

  3. Brånemark R, Skalak R. An in-vivo method for biomechanical characterization of bone-anchored implants. Med Eng Phys. 1998;20:216–9.

    Article  PubMed  Google Scholar 

  4. Ong JL, Carnes DL, Bessho K. Evaluation of titanium plasma-sprayed and plasma-sprayed hydroxyapatite implants in vivo. Biomaterials. 2004;25:4601–6.

    Article  PubMed  CAS  Google Scholar 

  5. Onsten I, Nordqvist A, Carlsson AS, et al. Hydroxyapatite augmentation of the porous coating improves fixation of tibial components. A randomised RSA study in 116 patients. J Bone Joint Surg Br. 1998;80:417–25.

    Article  PubMed  CAS  Google Scholar 

  6. Sandén B, Olerud C, Petrén-Mallmin M, et al. The significance of radiolucent zones surrounding pedicle screws. Definition of screw loosening in spinal instrumentation. J Bone Joint Surg Br. 2004;86:457–61.

    Article  PubMed  Google Scholar 

  7. Li Y, Brånemark R. Osseointegrated prostheses for rehabilitation following amputation: the pioneering Swedish model. Unfallchirurg. 2017;120:285–92.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Brånemark PI, Hansson BO, Adell R, et al. Osseointegrated implants in the treatment of the edentulous jaw. Experience from a 10-year period. Scand J Plast Reconstr Surg Suppl. 1977;16:1–132.

    PubMed  Google Scholar 

  9. Sun R, Bai L, Yang Y, et al. Nervous system-driven osseointegration. Int J Mol Sci. 2022;23:8893.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Nencini S, Ivanusic JJ. The physiology of Bone Pain. How much do we really know? Front Physiol. 2016;7:157.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Marco F, Milena F, Gianluca G, et al. Peri-implant osteogenesis in health and osteoporosis. Micron. 2005;36:630–44.

    Article  PubMed  CAS  Google Scholar 

  12. Overmann AL, Aparicio C, Richards JT, et al. Orthopaedic osseointegration: Implantology and future directions. J Orthop Res. 2020;38:1445–54.

    Article  PubMed  Google Scholar 

  13. Bauer S, von der Schmuki P et al. K,. Engineering biocompatible implant surfaces: Part I: Materials and surfaces. Prog Mater Sci 2013; 58: 261–326.

  14. Liu Y, Rath B, Tingart M, et al. Role of implants surface modification in osseointegration: a systematic review. J Biomed Mater Res A. 2020;108:470–84.

    Article  PubMed  CAS  Google Scholar 

  15. Hekimoğlu M, Özer H, Kiraz K et al. Jan. Surface hardening of Ti-Al-V superalloy spinal implant by using the boronization method. Bio-Medical Materials and Engineering,1 2024: 39–52.

  16. Shi LY, Wang A, Zang FZ, et al. Tantalum-coated pedicle screws enhance implant integration. Colloids Surf B Biointerfaces. 2017;160:22–32.

    Article  PubMed  CAS  Google Scholar 

  17. Ao XG, Chen WC. Research progress on the osseointegration of titanium implants promoted by cold atmospheric plasma. Hua Xi Kou Qiang Yi Xue Za Zhi. 2020;38:566–70.

    PubMed  Google Scholar 

  18. Hanawa T. Zirconia versus titanium in dentistry: a review. Dent Mater J. 2020;39:24–36.

    Article  PubMed  CAS  Google Scholar 

  19. Hanawa T. Biocompatibility of titanium from the viewpoint of its surface. Sci Technol Adv Mater. 2022;23:457–72.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Brånemark PI. Osseointegration and its experimental background. J Prosthet Dent. 1983;50:399–410.

    Article  PubMed  Google Scholar 

  21. Marticorena M, Corti G, Olmedo DG, et al. Laser surface modification of Ti implants to improve osseointegration. J Phys Conf Ser. 2007;59:662–5.

    Article  CAS  Google Scholar 

  22. Guglielmotti MB, Olmedo DG, Cabrini RL. Research on implants and osseointegration. Periodontol 2000. 2019;79:178–89.

    Article  PubMed  Google Scholar 

  23. Jacobs JJ, Gilbert JL, Urban RM. Corrosion of metal orthopaedic implants. J Bone Joint Surg Am. 1998;80:268–82.

    Article  PubMed  CAS  Google Scholar 

  24. Ferin J, Oberdörster G. Biological effects and toxicity assessment of titanium dioxides: anatase and rutile. Am Ind Hyg Assoc J. 1985;46:69–72.

    Article  PubMed  CAS  Google Scholar 

  25. Ayşeşek N, Arısan V, Balcıoğlu NB, et al. Boron- and Boric acid-treated Titanium Implant surfaces in Sheep Tibia: a histologic, histomorphometric and mechanical study. Bioeng (Basel). 2022;9:705.

    Google Scholar 

  26. Uluisik I, Karakaya HC, Koc A. The importance of boron in biological systems. J Trace Elem Med Biol. 2018;45:156–62.

    Article  PubMed  CAS  Google Scholar 

  27. Gorustovich AA, Steimetz T, Nielsen FH, et al. Histomorphometric study of alveolar bone healing in rats fed a boron-deficient diet. Anat Rec (Hoboken). 2008;291:441–7.

    Article  PubMed  CAS  Google Scholar 

  28. Adriztina I, Adenin LI, Lubis YM. Efficacy of Boric Acid as a treatment of choice for Chronic Suppurative Otitis Media and its ototoxicity. Korean J Fam Med. 2018;39:2–9.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Witek L, Tovar N, Lopez CD, et al. Assessing osseointegration of metallic implants with boronized surface treatment. Med Oral Patol Oral Cir Bucal. 2020;25:311–7.

    Article  Google Scholar 

  30. Zboun M, Arısan V, Topcuoglu N et al. In vitro comparison of titanium surface conditioning via boron-compounds and sand-blasting acid-etching. Surf Interf 2020:100703.

  31. Sağlam M, Köseoğlu S, Enhoş Ş. Periodontolojide bor. JHS 2013;22:70 – 5.

  32. Bailey PJ, Cousins G, Snow GA, et al. Boron-containing antibacterial agents: effects on growth and morphology of bacteria under various culture conditions. Antimicrob Agents Chemother. 1980;17:549–53.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Tamirisakandala S, Miracle DB, Srinivasan R, et al. Titanium Alloyed with Boron. Adv Mater Processes. 2006;164:41–3.

    CAS  Google Scholar 

  34. Mavrogenis AF, Dimitriou R, Parvizi J, et al. Biology of implant osseointegration. J Musculoskelet Neuronal Interact. 2009;9:61–71.

    PubMed  CAS  Google Scholar 

  35. Parithimarkalaignan S, Padmanabhan TV. Osseointegration: an update. J Indian Prosthodont Soc. 2013;13:2–6.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Author information

Authors and Affiliations

  1. Neurosurgery Department, Ordu University Hospital, Ordu, Turkey

    Hidir Ozer

  2. Neurosurgery Department, American Hospital, Istanbul, Turkey

    Mehdi Hekimoglu, Ali Fahir Ozer & Mehdi Hekimoğlu

  3. Pathology Department, Koc University Hospital, Istanbul, Turkey

    Ibrahim Kulac & Ozgur Can Eren

  4. Faculty of Medicine, Biostatics and Medical Informatics Department, Ordu University, Ordu, Turkey

    Yeliz Kasko Arici

  5. Ankara Research and Training Hospital, Neurosurgery Department, Ankara, Turkey

    Haydar Sahin Celik

  6. Neurosurgery Department, Koc University HAospital, Istanbul, Turkey

    Ali Fahir Ozer

Authors
  1. Hidir Ozer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mehdi Hekimoglu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ibrahim Kulac
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ozgur Can Eren
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yeliz Kasko Arici
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Haydar Sahin Celik
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ali Fahir Ozer
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Mehdi Hekimoğlu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Declaration of Interest Statement: The authors declare that they have no conflicts of interest regarding the publication of this manuscript. Additionally, the authors declare no competing financial interests and no sources of funding or support, including any for equipment and medications.Funding Statement: This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.Author Contributions Statement: H. Ozer: Contributed to the conception and design of the study, written and critical revision of the manuscript.M. Hekimoglu: Contributed to data acquisition, analysis and interpretation of data, and critical revision of the manuscript. Also written the main manuscript. I. Kulac: Contributed to data acquisition, analysis and interpretation.O. C. Eren: Contributed to data acquisition, analysis and interpretation.Y. K. Arıcı: Contributed to data acquisition, analysis and interpretation, and critical revision of the manuscript.H. S. Celik: Contributed to critical revision of the manuscript and approved the version to be published.A. F. Ozer: Contributed to critical revision of the manuscript and approved the version to be published.All authors have read and approved the final submitted manuscript. Best regardsMehdi HekimogluM.D Neurosurgeon.

Corresponding author

Correspondence to Mehdi Hekimoğlu.

Ethics declarations

Conflict of interest

The authors declare no competing financial interests and no sources of funding and support, including any for equipment and medications.

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ozer, H., Hekimoglu, M., Kulac, I. et al. Osseointegration potential of boron-coated titanium alloy pedicle screw in rabbit spine model. BMC Musculoskelet Disord 25, 737 (2024). https://doi.org/10.1186/s12891-024-07864-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12891-024-07864-6

Keywords

BMC Musculoskeletal Disorders

ISSN: 1471-2474

Contact us