Home Life Sciences Effect of autologous platelet-rich plasma on new bone formation and viability of a Marburg bone graft
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Effect of autologous platelet-rich plasma on new bone formation and viability of a Marburg bone graft

  • Dina Saginova , Elyarbek Tashmetov EMAIL logo , Berik Tuleubaev and Yevgeniy Kamyshanskiy
Published/Copyright: November 21, 2023
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Open Life Sciences
From the journal Open Life Sciences Volume 18 Issue 1

Abstract

This study aimed to compare the new bone formation, the process of remodeling, and the viability of bone grafts, using a combination of platelet-rich plasma (PRP) and Marburg bone graft versus bone grafts without any additional elements. For this study, 48 rabbits (with 24 rabbits in each group) were used. Bone defects were made in the femur, and the bone graft used was the human femoral head prepared according to the Marburg Bone Bank. Rabbits were divided into the following groups: heat-treated bone graft (HTBG group) and HTBG with PRP (HTBG + PRP group). After 14, 30, and 60 days post-surgery, the assessment of the results involved X-ray, histopathological, and histomorphometric analyses. The greater new bone formation was detected in the HTBG + PRP group on the 14 and 30 day (p < 0.001). Furthermore, the group using bone grafts with PRP demonstrated notably enhanced remodeling, characterized by stronger bone integration, more significant graft remineralization, and a circular pattern of newly formed bone. The PRP–bone graft complex improves bone tissue repair in the bone defect in the initial stages of bone regeneration. PRP has been identified to enhance the remodeling process and amplify the osteoconductive and osteoinductive capabilities of HTBGs.

Keywords: bone graft; bone defect; PRP; Marburg bone bank system

1 Introduction

Bone defects commonly manifest as a result of bone resection, metabolic pathologies, traumatic events, and neoplasms. Annually, these osseous deficiencies necessitate more than one million reconstructive surgical interventions [1,2]. The main principle of treatment of defects of any etiology is their filling with bone substitutes. Autologous bone is the “gold standard” [3,4]. First, this is due to the fact that the autologous bone does not cause any immunological reactions. Second, it has simultaneously both osteoinductive and osteoconductive properties – the former is represented by bone cells and growth factors. The limited availability of autologous bone and the accompanying trauma induced by the harvesting procedure restrict its use in clinical practice [3,4,5]. Synthetic bone grafts serve as an alternative to autologous graft options due to their extensive accessibility, gradual biodegradation, and lack of risks such as donor-site morbidity and viral transmission [6–9]. Yet, their biological role is constrained, particularly in fracture healing, because of their purely osteoconductive nature, mechanical properties, and absence of angiogenic attributes [1,6,10,11]. On the other hand, allogenous bone grafts, sourced from humans or human cadavers, are subject to sterile processing before transplantation to a recipient. The osteoconductive and occasionally osteoinductive potential of these grafts can vary based on the preparation process [1,3,7].

The Marburg Bone Bank-prepared bone graft is a type of bone allograft widely used in orthopedic surgery. These grafts are extensively processed to remove cellular material, leaving behind only the mineralized bone matrix. The processed bone matrix provides a scaffold for new bone growth, which can lead to faster and more complete healing [12–15]. Nevertheless, the osteoinductive capability of processed (chemically or physically) allogeneic bone is not clearly established, given that osteogenic cells are eradicated during the tissue manipulation process. This leads to the partial retention of osteoinductive substances, which may contribute to suboptimal clinical effects. Currently, there has been a surge in interest regarding the use of growth factors and morphogens as potential agents for conferring osteoinductivity to bone substitutes [16–18].

Platelet-rich plasma (PRP) obtained from autologous blood represents a significant resource for delivering high levels of growth factors, including platelet-derived growth factor (PDGF), transforming growth factor beta, epidermal growth factor, vascular endothelial growth factor, and insulin-like growth factor I. These factors are vital in tissue growth and progression, and their introduction to the site of bone defects is crucial [19,20]. PRP has shown potential for use in combination with bone grafts, as in vitro studies have demonstrated a notable increase in osteoblast proliferation upon the addition of PRP [19]. Furthermore, incorporating PRP with graft materials has been shown to reduce the duration required for graft consolidation, maturation, and improvement of trabecular bone density [20–23]. These findings suggest that PRP may compensate for the limited osteogenic potential of thermally disinfected bone grafts to promote osteogenesis in bone defects. However, there is limited information regarding the synergistic effects of PRP and Marburg-prepared bone graft on bone healing. Therefore, the purpose of this study is to perform a comparative assessment of the new bone formation, the process of remodeling, and the viability of bone grafts, using a combination of PRP with bone grafts prepared by the Marburg Bone Bank System versus bone allografts without any additional elements.

2 Methods

2.1 Preparation of Marburg bone grafts

In this study, femoral heads prepared by the Marburg Bank were used as bone graft (Figure 1). These femoral heads were obtained from a living donor who had undergone hip joint arthroplasty surgery in compliance with national regulations [24,25]. During hip joint endoprosthetics, the head of the femur is removed from the operating room and subjected to a series of mechanical cleaning procedures in sterile conditions to eliminate any soft tissue, cartilage, and ligaments. The femoral heads were placed in a disposable sterile container and filled with 0.9% NaCl solution in a volume of 300 ml, and then they were sealed and subjected to a heat treatment process in a Lobator SD-2 (Telos Company, Germany) device for a total of 94 min, maintaining a temperature of 82.5°C in the femoral head for at least 15 min, according to the established protocol. The sterility of the container was verified at the end of the cycle through a specific opening, and then, the liquid was completely drained. The bone allografts were then stored in a freezer at −80°C as per the recommended protocol [13,26]. Two hours before the experiment, the femoral head was unfrozen at room temperature and cut into chips. To ensure a consistent ratio of ingredients, a specific weight was used to standardize the mixture of bone graft with PRP 0.5 g bone allograft/0.5 ml PRP.

Figure 1 Heat-treated femoral head (a) and scanning electron microscopic view of bone graft (b).
Figure 1

Heat-treated femoral head (a) and scanning electron microscopic view of bone graft (b).

  1. Informed consent: Informed consent has been obtained from all individuals included in this study.

  2. Ethical approval: The research related to human use has been complied with all the relevant national regulations, institutional policies and in accordance with the tenets of the Helsinki Declaration, and has been approved by the authors' institutional review board or equivalent committee.

2.2 Preparation of PRP

Prior to each surgical intervention (approximately 30 min before transplantation), 5 ml of blood was collected from the heart into siliconized tubes containing 3.8% sodium citrate at a blood/citrate ratio of 9:1 [27]. PRP was procured via two-step centrifugation [28]. Initial centrifugation involved the separation of blood cell elements using a laboratory centrifuge, with tubes centrifuged at 900 G for 8 min at ambient temperature, yielding two primary components: the blood cell component (BCC) in the lower fraction and in the upper fraction. Subsequent centrifugation entailed marking a point 6 mm beneath the line demarcating the BCC. To augment the total platelet count for the second centrifugation, all contents above the mark were transferred to another 5 ml vacuum tube devoid of anticoagulant. The sample was then centrifuged once more at 1,500 G for 5 min to obtain two components: platelet-poor plasma (PPP) and PRP. Approximately 0.5 ml of PRP was separated from the PPP. The PRP (0.5 ml) was combined with 0.5 g of bone graft and used to fill the created defect.

2.3 Animals and surgical procedures

In this investigation, 48 outbred rabbits were acquired, comprising adult males (6–7 months old) with an average weight of 3,025 ± 87 g. The animals were housed in cages and allowed to acclimate for a duration of 2 weeks. All procedures involving the animals adhered to the protection guidelines of DIRECTIVE 2010/63/EU for animals used in scientific research [29] and were approved by the University Animal Care Committee (UACC) under protocol № 27 dated 27.09.2020. Throughout the study, the rabbits were maintained at room temperature (22 ± 2°C), with 40–50% humidity, and subjected to a 12 h light–dark cycle. The animals were provided with standard rabbit pellets and tap water for sustenance.

Following Russell and Burch’s bioethical principles of replacement, reduction, and refinement, the sample size for animal experimentation in this study was established as the minimum number of animals necessary to yield statistically significant outcomes [30].

The rabbits were randomly allocated into two groups (n = 24 per group) and underwent the same surgical procedure. Three hours before, the rabbits received an intramuscular (i.m.) injection of gentamycin 0.1 ml/kg (Mapichem, Switzerland). Animals were anesthetized with an i.m. injection of Zoletil 0,1 mg/kg (Virbac, USA) and Rometar 5 mg/kg (Bioveta, Czech Republic). Following hip skin disinfection, an incision was made in the distal femur. The periosteum was then lifted, and a 5 mm diameter unicortical bone defect was created in the distal femoral metaphysis using a drill (Figure 2) [31]. Then, based on the experimental group assignment, the bone defects in the first group were treated with a heat-treated bone graft (HTBG group), whereas in the second group, the defects were treated with the HTBG with autologous PRP (HTBG + PRP group). The surgical wound was sutured with absorbable sutures (5-0 Vicryl, Ethicon, Johnson & Johnson, USA). After surgery, each animal received i.m. injections of gentamycin 0.1 ml/kg (Mapichem, Switzerland) and ketonal 0.04 ml/kg (Sandoz, Slovenia) for 3 days. Daily postoperative observations were made to monitor the healing progress according to a predetermined schedule for consecutive days. There were no complications or deaths in the postoperative period. At 14, 30, and 60 days, 8 animals from each group (16 rabbits for each time period) were sacrificed according to ethical standards by intravenous administration of lethal doses of Zoletil 50 mg/ml and the distal femur was harvested.

Figure 2 Bone defect in rabbit femur (a) and bone defect after filling with HTBG (b).
Figure 2

Bone defect in rabbit femur (a) and bone defect after filling with HTBG (b).

  1. Ethical approval: The research related to animal use has been complied with all the relevant national regulations and institutional policies for the care and use of animals and has been approved by the UACC.

2.4 Histopathological examination

Prior to histological analysis, the specimens were fixed in 10% neutral buffered formalin for a duration of 24 h, followed by decalcification in Biodec R solution (Bio-Optica Milano SPA) for an additional 24 h. Subsequently, the samples were rinsed in phosphate buffer (pH = 7.4). Upon achieving optimal bone tissue softening (decalcification), a bone incision was executed. The tissue was then fixed in 10% formalin at 4°C for 24 h, washed with tap water, and dehydrated using a series of ascending alcohol concentrations (70, 90, 95, and 100%). The samples were then immersed in xylene and embedded in paraffin blocks. Tissue sections with a thickness of 5 μm were prepared using a Leica SM 2000R sliding microtome. Once prepared, the tissue sections were treated with hematoxylin and eosin for overall tissue morphological analysis, identification of inflammatory infiltrate and necrosis, and Masson’s trichrome to evaluate bone graft remodeling and new bone formation [32].

2.4.1 Hematoxylin and eosin staining process

The tissue slices were submerged in Mayer’s hematoxylin for a quarter of an hour, followed by a 5 min rinse with water. Thereafter, the sections were subjected to a minute-long eosin staining.

2.4.2 Masson’s trichrome staining procedure

A commercial kit (Trichrome Stain (Masson) Biovitrim TU 9398-001-89079081-2012) was used for Masson trichrome staining. After dewaxing and rehydration, the slide specimens were placed in Bouin’s solution at 56°C for a duration of 15 min. This was succeeded by a 5 min tap water rinse. The application of Weigert’s hematoxylin lasted 5 min, followed by another 5 min wash with tap water, and a quick rinse in distilled water. The slides were subsequently stained with Biebrich’s scarlet acid fuchsin for 5 min, rinsed in distilled water, and bathed in phosphoric–tungstic–phosphomolybdenum acid for an additional 5 min. A 5 min application of aniline blue was the next step, and finally, the slides were secured in 1% acetic acid for a period of 2 min.

Microscopic examination of the preparations was carried out on a Zeiss AxioLab 4.0 microscope with a magnification of ×400. AxioVision 7.2 software for Windows was used to analyze and photograph the images.

Two independent investigators with expertise in animal models conducted the morphometric study, uninformed of the group each animal belonged to. The terminology used in the histomorphometric analysis adhered to the guidelines provided by the Histomorphometry Nomenclature Committee of the American Society for Bone and Mineral Research [33].

The following parameters were determined:

  1. The percentage of newly formed bone tissue

  2. Histopathological pattern of bone graft remodeling.

The morphometric evaluation of bone tissue was carried out within an area defined radially by the defect’s edges and laterally by the native femur along with the outer boundary of the bone graft and/or the newly generated bone tissue. This estimate was represented as a percentage of the total defect zone area. For each bone defect, three histological sections were analyzed and their average value was computed. Tissues indicative of a non-specific reparative process, such as vessels or bone canal width, were not included in the quantification and constituted the smallest percentage in the bone callus area [34,35].

The process of distinguishing between bone graft remodeling, new bone formation, and differentiation from residual and lysed bone grafts was accomplished through different staining characteristics of bones at various stages of maturity and differences in staining between newly formed bone fragments and the graft. The chromatic distinction between the bone graft, which stained more toward red, and the newly formed bone, which stained blue, was examined using Masson’s trichrome.

A morphometric assessment of graft remodeling was conducted by identifying the dominant histomorphometric pattern of the bone graft within the newly formed bone defect.

Histomorphometric patterns of bone graft remodeling included:

  1. Positive bone graft remodeling: this involved remodeling with bone integration, graft remineralization, and the circular formation of new bone tissue.

  2. Negative bone graft remodeling: this represented remodeling with resorption and fibrotic replacement of the bone graft.

These patterns of bone graft remodeling are illustrated in Figure 3.

Figure 3 Histopathologic patterns of bone graft remodeling: (a) positive remodeling with integration, remineralization, and circular formation of newly formed bone tissue (Masson’s trichrome × 40. Scale bar, 500 µm) and (b) negative remodeling with resorption and fibrotic replacement of the bone graft (Masson’s trichrome × 40. scale bar, 500 µm).
Figure 3

Histopathologic patterns of bone graft remodeling: (a) positive remodeling with integration, remineralization, and circular formation of newly formed bone tissue (Masson’s trichrome × 40. Scale bar, 500 µm) and (b) negative remodeling with resorption and fibrotic replacement of the bone graft (Masson’s trichrome × 40. scale bar, 500 µm).

Bone graft remodeling was assessed according to a scale: minimal – less than 10%, moderate – 11–50%, and pronounced – more than 50%.

2.5 X-ray imaging

Radiological examinations were conducted 2 h prior to the termination of the animals from the study at the intervals of 14, 30, and 60 days, using frontal and lateral projections on a radiological machine (Platinum, Apelem, France).

The radiological data were analyzed according to the adapted Lane and Sandhu radiograph evaluation method (Table 1) [36]. Average scores were determined for each metric, followed by the aggregation of scores across various metrics (such as periosteal reaction, defect size, presence of new growth in the defect, bone remodeling, and bone allograft remodeling). This cumulative score was used to quantify the degree of healing in each group. The bone formation in each defect was independently scored by three radiologists. The group that achieved the highest overall radiological score was deemed to have experienced the most successful healing.

Table 1

Radiological assessment of bone defect healing

No. Characteristics Points
1 Periosteal reaction
Yes 1
No 0
2 Remodeling and resorption of the bone graft
No change 0
Partial 1
Full 2
3 Defect size
No change or increase 0
Decrease of less than 25% 1
By 25–50% decrease 2
By 50–75% decrease 3
More than 75% 4
No defect 5
4 Filling bone defect with regenerate
Yes 1
No 0
5 Bone remodeling
Complete 2
Bone marrow canal 1
No 0
Maximum radiological score 11

2.6 Statistical analysis

All experimental values are displayed as mean and standard deviations. Comparisons between two groups were made using the chi-squared test with Yates continuity correction and Mann–Whitney test, while multiple comparisons were made using Pearson’s chi-squared test. Statistical analysis of the research results was performed using IBM SPSS Statistics 20.0 and STATISTICA 10. A p-value of <0.05 was deemed to indicate statistical significance.

3 Results

3.1 Histological and morphometric analyses of newly formed bone tissue

On day 14 for the HTBG group, the newly formed bone tissue constituted 41.5% of the total (Figure 5a). The area of the bone defect was characterized by the development of individual heterogeneous bundles of new bone tissue. These bundles contained lacunae with osteocytes and an abundance of vascular channels. The emerging bone beams were uneven, primarily thin, with focal bridging regions and sporadic contacts, mostly at the ends of bone passages (Figure 4a). In the HTBG + PRP group, the new bone formation made up 58% of the total (Figure 5a). There was a progressive increase in the formed bone tissue, featuring haphazardly arranged Haversian canals and widespread, broad bone trabeculae with numerous extensive bridge-like contacts (Figure 4d).

Figure 4 Microphotographs of stage-specific closure of the cortical plate defect in the study groups 14, 30, and 60 days after implantation (Masson’s trichrome × 40. Scale bar, 500 µm) (a–c) – HTBG group: (a) negative remodeling of the bone graft with lysis and resorption; single heterogeneous bundles of newly formed bone tissue are not integrated with the bone graft; (b) lysed bone graft is replaced by fibrous tissue, and the remaining fragments are integrated with newly formed bone beams; and (c) defect area is closed by newly formed bone tissue with foci of disorderly distribution of mature and immature bone matrix; (d–f) – HTBG with PRP (HTBG + PRP group): (d) positive remodeling of the bone graft with bone integration, remineralization, and circular formation of newly formed bone tissue, partial closure of the defect with newly formed bone beams; (e) the osteotomy site is closed with mature bone tissue with multiple wide bridge-like contacts between newly formed bone beams; and (f) the defect area is closed with mature bone tissue.
Figure 4

Microphotographs of stage-specific closure of the cortical plate defect in the study groups 14, 30, and 60 days after implantation (Masson’s trichrome × 40. Scale bar, 500 µm) (a–c) – HTBG group: (a) negative remodeling of the bone graft with lysis and resorption; single heterogeneous bundles of newly formed bone tissue are not integrated with the bone graft; (b) lysed bone graft is replaced by fibrous tissue, and the remaining fragments are integrated with newly formed bone beams; and (c) defect area is closed by newly formed bone tissue with foci of disorderly distribution of mature and immature bone matrix; (d–f) – HTBG with PRP (HTBG + PRP group): (d) positive remodeling of the bone graft with bone integration, remineralization, and circular formation of newly formed bone tissue, partial closure of the defect with newly formed bone beams; (e) the osteotomy site is closed with mature bone tissue with multiple wide bridge-like contacts between newly formed bone beams; and (f) the defect area is closed with mature bone tissue.

Figure 5 Histological image of newly formed bone tissue and positive bone graft remodeling in the defect area after 14, 30, and 60 days: (a) comparison of the amount of newly formed bone tissue between groups (*p < 0.01, **p < 0.001) and (b) comparison of positive bone graft remodeling between groups (*p < 0.01, **p < 0.001).
Figure 5

Histological image of newly formed bone tissue and positive bone graft remodeling in the defect area after 14, 30, and 60 days: (a) comparison of the amount of newly formed bone tissue between groups (*p < 0.01, **p < 0.001) and (b) comparison of positive bone graft remodeling between groups (*p < 0.01, **p < 0.001).

On the 30th day, the newly formed bone tissue in the HTBG group accounted for 80.5% of the total (Figure 5a). The bone tissue consisted of haphazardly arranged bone trabeculae and tendons that were merging into lamellar structures. The bone tract exhibited significant mineralization and robust longitudinal growth (Figure 4b). Meanwhile, in the HTBG + PRP group on day 30, the bone tissue constituted 84.5% of the total (Figure 5a), with the defect area made up of dense mineralized bone tissue containing Haversian canals of varying sizes.

By day 60 in both HTBG and HTBG + PRP groups, the defect site revealed formed bone tissue with normal development of bone trabeculae, predominantly composed of spindle-shaped osteocytes (Figures 4c,f and 5a).

Neither the HTBG group nor the HTBG + PRP group displayed evidence of chondroid or bone callus hyperplasia on the histological sections. Instead, thin layers of fibrous tissue and blood vessels were visible, along with varying extents of bone graft resorption and the presence of fibrovascular structures. These observations were similar across both groups, and no additional histological alterations were attributable to the use of PRP.

3.2 Comparative analysis of bone graft remodeling

On day 14 in the HTBG group, less than 20% exhibited positive remodeling of the bone graft, while in the HTBG + PRP group, a statistically significant positive remodeling of the bone graft was observed (Figure 5a and b).

On the 30th day in the HTBG group, most of the lysed fragments of the bone graft had been replaced by fibrous tissue, while positive bone graft remodeling was seen in all the remaining fragments. For the HTBG + PRP group, the tissue composition consisted of remaining bone graft fragments closely interacting with the newly formed bone and osteoid tissue. There was noticeable active integration of the bone allograft with the new bone and pronounced positive bone graft remodeling (Figure 5b). No statistically significant difference was observed between the groups at this point.

By day 60 in both HTBG and HTBG + PRP groups, newly formed bone tissue without bone graft fragments was seen at the defect site. However, the histological material in the HTBG group also revealed areas with osteoid tissue (forming bone tissue) and regions with a random distribution of mature and immature bone matrix, while the HTBG + PRP group exhibited a consistent and uniform distribution of mature bone tissue (Figure 5b).

3.3 Comparative characterization of inflammatory and necrotic pattern

At 14 days in both HTBG and HTBG + PRP groups, a single reactive cell infiltrate without necrotic changes was observed at the defect site. At 30 and 60 days, all regions of surgically created defects showed no signs of inflammatory cell infiltration, infection indicators (polymorphonuclear cells, lymphocytes, macrophages, and multinucleated cells), or tissue necrosis.

3.4 Radiographic evaluation

The lateromedial X-ray images illustrated distinct areas of radiolucent bone defect in the femur of all animals after a 2 week period (Figure 6a). The boundaries of the scaffolds began to blur, and a high-density signal appeared on the periphery of the bone defect, suggesting new bone formation in the affected areas for both groups. Notably, the HTBG + PRP group demonstrated a statistically significant (p < 0.01) enhancement in the radiographic score in comparison with the HTBG group after 14 days (Figure 6b).

Figure 6 Radiographic assessment of femoral bone defect healing: (a) radiographic images after 14, 30, and 60 days and (b) comparison radiographic score between groups (*p < 0.05).
Figure 6

Radiographic assessment of femoral bone defect healing: (a) radiographic images after 14, 30, and 60 days and (b) comparison radiographic score between groups (*p < 0.05).

By the end of 30 days, the materials implanted in the bone had been substituted by newly grown bone, partially filling in the bone defects (Figure 6a). The defect areas in the bone were largely unobservable in both groups. There was an increased radiopacity in the femur where HTBG + PRP was implanted, demonstrating a higher radiographic score than the adjacent bone and notably greater than that in the HTBG group (Figure 6b).

At the 60 day mark, the areas of bone defect were no longer discernible in either group. All groups exhibited enhanced radiopacity in the femur, with a non-significant uptick in radiographic score (Figure 6b).

4 Discussion

This study provides an examination of bone graft remodeling and the healing pattern of newly formed bone following the application of the Marburg bone graft with and without PRP, based on an animal model experiment. The evaluation incorporates radiological, histopathological, and histomorphometric assessments.

Our findings demonstrate that the use of PRP with thermally disinfected bone graft significantly enhances bone formation when compared to the group using bone graft alone, without additional biocomponents. Particularly, the PRP group displayed a notably larger volume of newly formed bone tissue and higher radiologic scores on the 14th and 30th day, compared to the group without PRP (p < 0.001). Furthermore, the defect area in the PRP group revealed a more pronounced proliferation of mature bone tissue that was integrated with the allograft, and it showed the presence of chaotically arranged Haversian canals and horizontally expanding bone trabeculae. The results we obtained supplement the existing evidence demonstrating that the combination of PRP and thermally treated bone is just as effective as the combination of PRP with other graft materials. Several researchers [22,33] have suggested that combining PRP does not necessarily result in a significant boost in osteogenesis. This could potentially be due to high-temperature treatment of the biomaterial causing irreversible changes, which may diminish the impact of growth factors present in PRP [37]. Drawing on our findings, we postulate that using PRP with heat-treated bone enhances the initial stage of osteogenesis. Consequently, the early phase of fracture healing with a Marburg bone graft could be expedited through appropriate growth factor stimulation, via the synergistic effect of PRP. This process might lower the occurrence of non-unions and infections.

Previously, it was shown that PRP improves the regenerative properties of connective and epithelial tissue by increasing the activity of fibroblast-like cells and stimulating cell proliferation [38–42]. We believe that bone graft in combination with PRP improves osteoconductive potential and induces an osteoinductive effect, which is reflected in the enhancement and acceleration of growth and maturation of bone tissue in the defect area.

On the 14th and 30th day, the group using PRP showed a dominant pattern of positive bone graft remodeling in the histopathological analysis, revealing improved viability of the bone graft and a greater proportion of mature bone matrix compared to the group using only bone graft. Despite being a commonly used and convenient method, bone repair with bone grafts has some drawbacks, such as poor bone graft viability and negative remodeling of the bone graft. These issues can lead to relative delays in bone repair or disjointed, uneven healing of the bone defect. This gradual replacement process might result in persistent zones of bone necrosis [43]. Our findings suggest that PRP can effectively diminish the resorption of a thermally treated bone graft, bolster the integration of newly formed bone with the graft surface, and expedite the bone graft remodeling process. This has promising implications not only for bone grafting, but also for other orthopedic scenarios requiring bone remodeling with minimized necrosis risks.

In earlier studies, PRP has been shown to improve angiogenesis in the area of bone defects [44–46]. The process of angiogenesis is significant and necessary for tropism, growth, and maturation of bone tissue [45,47]. Previously [44], we found that in groups, the formation of more dense zones of maturing and mature bone tissue was observed in zones with a relatively large number of microvessels. We believe that the PRP-induced effect of bone growth and maturation activity is more likely associated with a direct effect on angiogenesis and indirectly on an osteoinductive effect.

Our investigation revealed that, as per the histological and radiological findings, there was no significant difference in bone healing between the HTBG and HTBG + PRP groups at the end of 60 days. We propose that this lack of difference may be attributed to the completion of the active phase of osteogenesis, resulting in complete closure of the bone defect. However, it is important to acknowledge that bone tissue reconstruction and remodeling are complex processes that continue beyond the active phase of osteogenesis [1,6]. These processes involve the reorganization and reshaping of the newly formed bone tissue, ensuring its strength and functionality. Although complete closure of the bone defect may have been achieved, the ongoing reconstruction and remodeling could still be taking place [17,42]. This ongoing process might contribute to the lack of significant difference observed at day 60. This suggests the need for additional research to fully understand these processes.

As previously demonstrated, approximately 90% of the bone lamina is composed of mature lamellar bone tissue, with the remaining 10% comprising lacunae, Haversian canals filled with vessels and nerve fibers, as well as fibrous and cartilaginous tissues [48]. The lamellar structure of the bone lamina, integrated with a system of channels, offers not just nutritional support but also mechanical resilience, as bone’s resistance to deformation relies not merely on its mineral content but also on its intricate internal microstructure, a crucial outcome of successful defect repair. Bone tissue repair conventionally transpires in a stage-specific manner, encompassing a phase of dynamic growth and a maturation phase distinguished by the emergence of channels for nutrition and trophicity. This maturation phase is signaled by a relatively minor decline in bone tissue quantity due to focal resorption. According to our study, the bone plate in the defect zone for the HTBG + PRP group at 60 days displayed a minor reduction in bone tissue quantity. This aligns with the process of bone reconstruction and the formation of Haversian canals and may be perceived as a stage of bone tissue maturation [49]. Conversely, in the group without PRP, at 60 days, there was a tendency toward an increase in bone tissue, accompanied by regions displaying haphazard distribution of immature bone matrix. This suggests an extended potential for bone growth and a relative delay in maturation. We posit that the use of PRP with a HTBG not only enhances the osteoconductive and osteoinductive potential of the graft, but also expedites the maturation process of the newly formed bone tissue.

Furthermore, we showed that in the PRP group, there were no abnormalities in bone repair associated with insufficient or excessive bone formation. Newly formed bone tissue in both groups was characterized by normal histopattern: (1) the bone plate did not extend beyond the thickness of the bone defect and did not pass to the bone plate outside the defect, (2) had a laminar layered structure with a focal chaotic pattern in the area of predominantly Haversian canals, and (3) the relative amount of bone tissue and Haversian canals did not differ both between groups and from the structure of the bone outside the bone defect.

A key advantage of this study lies in the comparative evaluation of using a Marburg bone graft in conjunction with PRP, during both early and late phases of bone defect healing. This approach facilitated the discovery of osteoregeneration stimulation in the early stages through the use of PRP. The use of a standardized rabbit femoral defect model, alongside histological and morphometric analysis, further strengthens the validity of the study.

Limitations: The precise mechanism of PRP’s impact on bone tissue is still subject to debate. Is its role direct, influencing osteosynthesis and bone maturation, or does it indirectly promote a favorable macroenvironment with a high index of angiogenesis? These queries could be addressed in subsequent research. Additionally, the evaluation of bone regeneration relied solely on histological and radiographic analyses, which, although informative, did not fully exhaust all the potential analytical methods. Techniques like micro-computed tomography and immunohistochemistry were not used. These could have contributed to a more well-rounded comprehension of bone regeneration by scrutinizing the structural aspects, cellular elements, and gene expression profiles of the regenerated bone. These limitations should be considered when interpreting the results and should influence the design of future studies to fill these potential knowledge gaps.

5 Conclusions

Thus, our experiment with rabbits demonstrated that the combined application of Marburg bone grafts and PRP enhances the viability of the bone graft within the defect zone. We found that PRP improves the integration of the graft with the bone and accelerates the remodeling process of the bone graft. We believe that the primary effect of enhancing the osteoconductive and osteoinductive potentials, as well as the improvement of bone graft remodeling, is tied to the formation of a locally favorable microenvironment with active perfusion–diffusion potential within the stromal framework. This in turn encourages more active growth and maturation of the bone tissue.

  1. Funding information: This research has been funded by the Science Committee of the Ministry of Education and Science of the Republic of Kazakhstan (Grant No. AP09260954).

  2. Author contributions: Conceptualization, D.S. and E.T.; methodology, Ye.K. and B.T.; software, Ye.K. and E.T.; validation, D.S. and Ye.K.; formal analysis, D.S. and B.T.; investigation, E.T. and Ye.K.; resources, B.T.; data curation, D.S.; writing – original draft preparation, E.T. and Ye.K.; writing – review and editing, D.S. and B.T.; visualization, E.T.; supervision, D.S.; project administration, D.S.; funding acquisition, Ye.K. All authors have read and agreed to the published version of the manuscript.

  3. Conflict of interest: Authors state no conflict of interest.

  4. Data availability statement: The datasets generated during and/or analyzed during the current study are available from the corresponding author on a reasonable request.

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Received: 2023-05-04
Revised: 2023-07-13
Accepted: 2023-10-02
Published Online: 2023-11-21

© 2023 the author(s), published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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  171. Advances in diagnosis and treatment of perimenopausal syndrome
  172. A study of forensic genetics: ITO index distribution and kinship judgment between two individuals
  173. Acute lupus pneumonitis resembling miliary tuberculosis: A case-based review
  174. Plasma levels of CD36 and glutathione as biomarkers for ruptured intracranial aneurysm
  175. Fractalkine modulates pulmonary angiogenesis and tube formation by modulating CX3CR1 and growth factors in PVECs
  176. Novel risk prediction models for deep vein thrombosis after thoracotomy and thoracoscopic lung cancer resections, involving coagulation and immune function
  177. Exploring the diagnostic markers of essential tremor: A study based on machine learning algorithms
  178. Evaluation of effects of small-incision approach treatment on proximal tibia fracture by deep learning algorithm-based magnetic resonance imaging
  179. An online diagnosis method for cancer lesions based on intelligent imaging analysis
  180. Medical imaging in rheumatoid arthritis: A review on deep learning approach
  181. Predictive analytics in smart healthcare for child mortality prediction using a machine learning approach
  182. Utility of neutrophil–lymphocyte ratio and platelet–lymphocyte ratio in predicting acute-on-chronic liver failure survival
  183. A biomedical decision support system for meta-analysis of bilateral upper-limb training in stroke patients with hemiplegia
  184. TNF-α and IL-8 levels are positively correlated with hypobaric hypoxic pulmonary hypertension and pulmonary vascular remodeling in rats
  185. Stochastic gradient descent optimisation for convolutional neural network for medical image segmentation
  186. Comparison of the prognostic value of four different critical illness scores in patients with sepsis-induced coagulopathy
  187. Application and teaching of computer molecular simulation embedded technology and artificial intelligence in drug research and development
  188. Hepatobiliary surgery based on intelligent image segmentation technology
  189. Value of brain injury-related indicators based on neural network in the diagnosis of neonatal hypoxic-ischemic encephalopathy
  190. Analysis of early diagnosis methods for asymmetric dementia in brain MR images based on genetic medical technology
  191. Early diagnosis for the onset of peri-implantitis based on artificial neural network
  192. Clinical significance of the detection of serum IgG4 and IgG4/IgG ratio in patients with thyroid-associated ophthalmopathy
  193. Forecast of pain degree of lumbar disc herniation based on back propagation neural network
  194. SPA-UNet: A liver tumor segmentation network based on fused multi-scale features
  195. Systematic evaluation of clinical efficacy of CYP1B1 gene polymorphism in EGFR mutant non-small cell lung cancer observed by medical image
  196. Rehabilitation effect of intelligent rehabilitation training system on hemiplegic limb spasms after stroke
  197. A novel approach for minimising anti-aliasing effects in EEG data acquisition
  198. ErbB4 promotes M2 activation of macrophages in idiopathic pulmonary fibrosis
  199. Clinical role of CYP1B1 gene polymorphism in prediction of postoperative chemotherapy efficacy in NSCLC based on individualized health model
  200. Lung nodule segmentation via semi-residual multi-resolution neural networks
  201. Evaluation of brain nerve function in ICU patients with Delirium by deep learning algorithm-based resting state MRI
  202. A data mining technique for detecting malignant mesothelioma cancer using multiple regression analysis
  203. Markov model combined with MR diffusion tensor imaging for predicting the onset of Alzheimer’s disease
  204. Effectiveness of the treatment of depression associated with cancer and neuroimaging changes in depression-related brain regions in patients treated with the mediator-deuterium acupuncture method
  205. Molecular mechanism of colorectal cancer and screening of molecular markers based on bioinformatics analysis
  206. Monitoring and evaluation of anesthesia depth status data based on neuroscience
  207. Exploring the conformational dynamics and thermodynamics of EGFR S768I and G719X + S768I mutations in non-small cell lung cancer: An in silico approaches
  208. Optimised feature selection-driven convolutional neural network using gray level co-occurrence matrix for detection of cervical cancer
  209. Incidence of different pressure patterns of spinal cerebellar ataxia and analysis of imaging and genetic diagnosis
  210. Pathogenic bacteria and treatment resistance in older cardiovascular disease patients with lung infection and risk prediction model
  211. Adoption value of support vector machine algorithm-based computed tomography imaging in the diagnosis of secondary pulmonary fungal infections in patients with malignant hematological disorders
  212. From slides to insights: Harnessing deep learning for prognostic survival prediction in human colorectal cancer histology
  213. Ecology and Environmental Science
  214. Monitoring of hourly carbon dioxide concentration under different land use types in arid ecosystem
  215. Comparing the differences of prokaryotic microbial community between pit walls and bottom from Chinese liquor revealed by 16S rRNA gene sequencing
  216. Effects of cadmium stress on fruits germination and growth of two herbage species
  217. Bamboo charcoal affects soil properties and bacterial community in tea plantations
  218. Optimization of biogas potential using kinetic models, response surface methodology, and instrumental evidence for biodegradation of tannery fleshings during anaerobic digestion
  219. Understory vegetation diversity patterns of Platycladus orientalis and Pinus elliottii communities in Central and Southern China
  220. Studies on macrofungi diversity and discovery of new species of Abortiporus from Baotianman World Biosphere Reserve
  221. Food Science
  222. Effect of berrycactus fruit (Myrtillocactus geometrizans) on glutamate, glutamine, and GABA levels in the frontal cortex of rats fed with a high-fat diet
  223. Guesstimate of thymoquinone diversity in Nigella sativa L. genotypes and elite varieties collected from Indian states using HPTLC technique
  224. Analysis of bacterial community structure of Fuzhuan tea with different processing techniques
  225. Untargeted metabolomics reveals sour jujube kernel benefiting the nutritional value and flavor of Morchella esculenta
  226. Mycobiota in Slovak wine grapes: A case study from the small Carpathians wine region
  227. Elemental analysis of Fadogia ancylantha leaves used as a nutraceutical in Mashonaland West Province, Zimbabwe
  228. Microbiological transglutaminase: Biotechnological application in the food industry
  229. Influence of solvent-free extraction of fish oil from catfish (Clarias magur) heads using a Taguchi orthogonal array design: A qualitative and quantitative approach
  230. Chromatographic analysis of the chemical composition and anticancer activities of Curcuma longa extract cultivated in Palestine
  231. The potential for the use of leghemoglobin and plant ferritin as sources of iron
  232. Investigating the association between dietary patterns and glycemic control among children and adolescents with T1DM
  233. Bioengineering and Biotechnology
  234. Biocompatibility and osteointegration capability of β-TCP manufactured by stereolithography 3D printing: In vitro study
  235. Clinical characteristics and the prognosis of diabetic foot in Tibet: A single center, retrospective study
  236. Agriculture
  237. Biofertilizer and NPSB fertilizer application effects on nodulation and productivity of common bean (Phaseolus vulgaris L.) at Sodo Zuria, Southern Ethiopia
  238. On correlation between canopy vegetation and growth indexes of maize varieties with different nitrogen efficiencies
  239. Exopolysaccharides from Pseudomonas tolaasii inhibit the growth of Pleurotus ostreatus mycelia
  240. A transcriptomic evaluation of the mechanism of programmed cell death of the replaceable bud in Chinese chestnut
  241. Melatonin enhances salt tolerance in sorghum by modulating photosynthetic performance, osmoregulation, antioxidant defense, and ion homeostasis
  242. Effects of plant density on alfalfa (Medicago sativa L.) seed yield in western Heilongjiang areas
  243. Identification of rice leaf diseases and deficiency disorders using a novel DeepBatch technique
  244. Artificial intelligence and internet of things oriented sustainable precision farming: Towards modern agriculture
  245. Animal Sciences
  246. Effect of ketogenic diet on exercise tolerance and transcriptome of gastrocnemius in mice
  247. Combined analysis of mRNA–miRNA from testis tissue in Tibetan sheep with different FecB genotypes
  248. Isolation, identification, and drug resistance of a partially isolated bacterium from the gill of Siniperca chuatsi
  249. Tracking behavioral changes of confined sows from the first mating to the third parity
  250. The sequencing of the key genes and end products in the TLR4 signaling pathway from the kidney of Rana dybowskii exposed to Aeromonas hydrophila
  251. Development of a new candidate vaccine against piglet diarrhea caused by Escherichia coli
  252. Plant Sciences
  253. Crown and diameter structure of pure Pinus massoniana Lamb. forest in Hunan province, China
  254. Genetic evaluation and germplasm identification analysis on ITS2, trnL-F, and psbA-trnH of alfalfa varieties germplasm resources
  255. Tissue culture and rapid propagation technology for Gentiana rhodantha
  256. Effects of cadmium on the synthesis of active ingredients in Salvia miltiorrhiza
  257. Cloning and expression analysis of VrNAC13 gene in mung bean
  258. Chlorate-induced molecular floral transition revealed by transcriptomes
  259. Effects of warming and drought on growth and development of soybean in Hailun region
  260. Effects of different light conditions on transient expression and biomass in Nicotiana benthamiana leaves
  261. Comparative analysis of the rhizosphere microbiome and medicinally active ingredients of Atractylodes lancea from different geographical origins
  262. Distinguish Dianthus species or varieties based on chloroplast genomes
  263. Comparative transcriptomes reveal molecular mechanisms of apple blossoms of different tolerance genotypes to chilling injury
  264. Study on fresh processing key technology and quality influence of Cut Ophiopogonis Radix based on multi-index evaluation
  265. An advanced approach for fig leaf disease detection and classification: Leveraging image processing and enhanced support vector machine methodology
  266. Erratum
  267. Erratum to “Protein Z modulates the metastasis of lung adenocarcinoma cells”
  268. Erratum to “BRCA1 subcellular localization regulated by PI3K signaling pathway in triple-negative breast cancer MDA-MB-231 cells and hormone-sensitive T47D cells”
  269. Retraction
  270. Retraction to “Protocatechuic acid attenuates cerebral aneurysm formation and progression by inhibiting TNF-alpha/Nrf-2/NF-kB-mediated inflammatory mechanisms in experimental rats”
https://doi.org/10.1515/biol-2022-0761
Keywords for this article
bone graft; bone defect; PRP; Marburg bone bank system
Creative Commons
BY 4.0

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  217. Bamboo charcoal affects soil properties and bacterial community in tea plantations
  218. Optimization of biogas potential using kinetic models, response surface methodology, and instrumental evidence for biodegradation of tannery fleshings during anaerobic digestion
  219. Understory vegetation diversity patterns of Platycladus orientalis and Pinus elliottii communities in Central and Southern China
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  223. Guesstimate of thymoquinone diversity in Nigella sativa L. genotypes and elite varieties collected from Indian states using HPTLC technique
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  226. Mycobiota in Slovak wine grapes: A case study from the small Carpathians wine region
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  232. Investigating the association between dietary patterns and glycemic control among children and adolescents with T1DM
  233. Bioengineering and Biotechnology
  234. Biocompatibility and osteointegration capability of β-TCP manufactured by stereolithography 3D printing: In vitro study
  235. Clinical characteristics and the prognosis of diabetic foot in Tibet: A single center, retrospective study
  236. Agriculture
  237. Biofertilizer and NPSB fertilizer application effects on nodulation and productivity of common bean (Phaseolus vulgaris L.) at Sodo Zuria, Southern Ethiopia
  238. On correlation between canopy vegetation and growth indexes of maize varieties with different nitrogen efficiencies
  239. Exopolysaccharides from Pseudomonas tolaasii inhibit the growth of Pleurotus ostreatus mycelia
  240. A transcriptomic evaluation of the mechanism of programmed cell death of the replaceable bud in Chinese chestnut
  241. Melatonin enhances salt tolerance in sorghum by modulating photosynthetic performance, osmoregulation, antioxidant defense, and ion homeostasis
  242. Effects of plant density on alfalfa (Medicago sativa L.) seed yield in western Heilongjiang areas
  243. Identification of rice leaf diseases and deficiency disorders using a novel DeepBatch technique
  244. Artificial intelligence and internet of things oriented sustainable precision farming: Towards modern agriculture
  245. Animal Sciences
  246. Effect of ketogenic diet on exercise tolerance and transcriptome of gastrocnemius in mice
  247. Combined analysis of mRNA–miRNA from testis tissue in Tibetan sheep with different FecB genotypes
  248. Isolation, identification, and drug resistance of a partially isolated bacterium from the gill of Siniperca chuatsi
  249. Tracking behavioral changes of confined sows from the first mating to the third parity
  250. The sequencing of the key genes and end products in the TLR4 signaling pathway from the kidney of Rana dybowskii exposed to Aeromonas hydrophila
  251. Development of a new candidate vaccine against piglet diarrhea caused by Escherichia coli
  252. Plant Sciences
  253. Crown and diameter structure of pure Pinus massoniana Lamb. forest in Hunan province, China
  254. Genetic evaluation and germplasm identification analysis on ITS2, trnL-F, and psbA-trnH of alfalfa varieties germplasm resources
  255. Tissue culture and rapid propagation technology for Gentiana rhodantha
  256. Effects of cadmium on the synthesis of active ingredients in Salvia miltiorrhiza
  257. Cloning and expression analysis of VrNAC13 gene in mung bean
  258. Chlorate-induced molecular floral transition revealed by transcriptomes
  259. Effects of warming and drought on growth and development of soybean in Hailun region
  260. Effects of different light conditions on transient expression and biomass in Nicotiana benthamiana leaves
  261. Comparative analysis of the rhizosphere microbiome and medicinally active ingredients of Atractylodes lancea from different geographical origins
  262. Distinguish Dianthus species or varieties based on chloroplast genomes
  263. Comparative transcriptomes reveal molecular mechanisms of apple blossoms of different tolerance genotypes to chilling injury
  264. Study on fresh processing key technology and quality influence of Cut Ophiopogonis Radix based on multi-index evaluation
  265. An advanced approach for fig leaf disease detection and classification: Leveraging image processing and enhanced support vector machine methodology
  266. Erratum
  267. Erratum to “Protein Z modulates the metastasis of lung adenocarcinoma cells”
  268. Erratum to “BRCA1 subcellular localization regulated by PI3K signaling pathway in triple-negative breast cancer MDA-MB-231 cells and hormone-sensitive T47D cells”
  269. Retraction
  270. Retraction to “Protocatechuic acid attenuates cerebral aneurysm formation and progression by inhibiting TNF-alpha/Nrf-2/NF-kB-mediated inflammatory mechanisms in experimental rats”
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