Letter to the Editor: Should osseointegration be a target to achieve during cranioplasty?

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TO THE EDITOR: We read with great interest the paper by Schwarz et al.3 (Schwarz F, Dünisch P, Walter J, et al: Cranioplasty after decompressive craniectomy: is there a rationale for an initial artificial bone-substitute implant? A single-center experience after 631 procedures. J Neurosurg 124:710–715, March 2016). Based on a retrospective series of patients who underwent cranioplasty after decompressive craniotomy, the authors suggest that patients younger than 30 years of age and older patients with a fragmented bone flap may be candidates for an initial artificial bone substitute, rather than an autograft, because of the high incidence of bone flap necrosis. We believe that the authors missed the important concept of achieving osseointegration between the bone flap and the skull.

The term osseointegration was used for the first time by Albrektsson et al. in 19861 in the field of otiatrics, to define a “direct structural and functional connection between vital bone and the surface of an implant subjected to load.” The process of osseointegration is well researched in the fields of orthopedics, maxillofacial surgery, and spine surgery, but may not have been adequately considered in cranial neurosurgery. The facilitation of osseointegration means understanding bone biology and physiology, as well as the various factors that influence bone healing and related technical measures. Fractured bone is genetically programmed to heal without the interposition of connective scar tissue. This is unique to bone tissue and is probably linked to the role of support tasks and protection played by bone itself. These functions would be at risk in the case of a fractured bone that had healed with an interposed scar.

We can easily compare the healing process of a bone fracture with the healing process of a craniolacunia when an operculum bone is placed. This process occurs both during the cranioplasty and at the end of the surgical procedure after the dura mater is closed, along with the bone operculum repositioning.

The healing of the skull and the restoration of its integrity depends on both biological and mechanical requirements. The biological requirements depend on the presence of bone cells that are capable of supporting healing and an adequate vascular supply. The mechanical requirements obey the degree of rigidity and stability of the “craniolacunia–bone flap” system, which mainly depends on the surgical fixation technique. Rigidity is defined as the ability of the system to withstand forces that may deform it, whereas stability is the absence of either micro- or macromovements of the bone flap.

The system's stability can also be influenced by the intracranial pressure, as well as by external pressures that can be transferred directly onto the bone flap. Based on the mechanical stability and resistance conditions, the healing of fractured bone can occur in either a direct or indirect manner. When absolute and adequate stability exists, surgeons can implement direct healing, whether or not there is a gap between the skull and bone operculum. When the edges between the bone flap and skull are aligned to the point of compression, healing can be direct and does not lead to the formation of a callus. The osteoclasts behave like the head of a drill, creating channels in the interface between the skull and bone flap. Thereafter, these channels are colonized by osteoblasts to form osteons that are considered bone bridges between the 2 bone fragments.

However, the most common condition of healing between the craniolacunia and the bone operculum, in conditions of stability, is the presence of a gap in the interface between the craniolacunia and bone flap. The osteoblasts that deposit osteoid tissue in the gap promote the formation of lamellar bone that is transversely oriented. This process is favored by the positioning within the gap of osteoconductive material, such as bone dust, and promoted by the presence of blood. The insertion of hemostatic material in the gap is not encouraged because it supports the formation of fibrous tissue.

Indirect healing takes place when adequate rigidity and stability exists between the craniolacunia and the bone flap. For this reason, the body implements mechanisms that lead from a biomechanical point of view to the progressive reduction of movement between bone and implants (Perren's theory).2 The biological steps start from the formation of a hematoma in the soft tissues that surround the gap between the skull and bone flap, followed by replacement by granulation tissue and bone reabsorption of margins as a result of the action of osteoclasts. The granulation tissue remodels the connective tissue, whose cells have the highest capacity for proliferation within a moving environment. The connective tissue remodels fibrocartilage tissue that can partially calcify as a consequence of the osteoblasts to obtain osteofibrointegration (with a low capacity for resistance to mechanical forces). In case of abnormal osteoclast activity, bone reabsorption is established.

In conclusion, to obtain osseointegration, the bone flap and the margins of the craniolacunia must be viable without interposed fibrous tissue,4 and appropriate biological and mechanical factors are required. We encourage neurosurgeons to obtain osseointegration with autologous bone both during cranioplasty procedures and in the surgical closing phase after craniotomy. The bone flaps have to be placed to sustain and assist extensive cell colonization and anchorage to the existing bone, ultimately leading to osseointegration, which also allows biomechanical competence to be gained. Osteoconductivity ensures physical and mechanical integration with the surrounding bone, which prevents micromovements, bone flap necrosis, and bone reabsorption.

References

  • 1

    Albrektsson TZarb GWorthington PEriksson AR: The long-term efficacy of currently used dental implants: a review and proposed criteria of success. Int J Oral Maxillofac Implants 1:11251986

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  • 2

    Perren SM: Physical and biological aspects of fractures healing with special reference to internal fixation. Clin Orthop Relat Res 138:1751961979

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  • 3

    Schwarz FDünisch PWalter JSakr YKalff REwald C: Cranioplasty after decompressive craniectomy: is there a rationale for an initial artificial bone-substitute implant? A single-center experience after 631 procedures. J Neurosurg 124:7107152016

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  • 4

    Zanotti BVVerlicchi AParodi PC: Topics in Medicine: Special Issue 1–4. Cranial Demolition and Reconstruction: One-Step Surgical Procedure TrentNew Magazine Edizioni2010

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Disclosures

The authors report no conflict of interest.

Response

We thank Drs. Stefini and Zanetti for their careful analysis of our paper. The authors have stated that we have not gone into detail about osteointegration. They state that different mechanical and biological factors (e.g., a mixture of bone dust and blood) seem to be responsible for bone healing and the consolidation of the bone flap with the skull. Also they discuss their belief that the reduction of macro- and micromovement of the bone flap should result in an improvement of bone healing. They have mainly referenced Perren's 1979 study.2

Evidence in the current literature differs from Drs. Stefini and Zanetti's opinion regarding the role of micromovement. Kassis et al. and Yamaji et al. have shown that micromovement does improve bone healing.1,3 These authors used long bones as study objects. To the best of our knowledge, there are no comparable studies in which the skull is used as a study object. In relation to macromovement, in the section “Operation Procedures” we did state that every bone had been fixed with rigid titanium plates.

Regarding biological factors, the use of bone dust was not possible in our operations, because all cranioplasties done with an autograft were operations that were performed after cryoconservation of the bone flap. Cryoconservation of bone dust was not done. To compare the different surgical techniques, a prospective randomized study would be beneficial.

References

  • 1

    Kassis BGlorion CTabib WBlanchard OPouliquen JC: Callus response to micromovement after elongation in the rabbit. J Pediatr Orthop 16:4804831996

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    • Export Citation
  • 2

    Perren SM: Physical and biological aspects of fractures healing with special reference to internal fixation. Clin Orthop Relat Res 138:1751961979

    • Search Google Scholar
    • Export Citation
  • 3

    Yamaji TKenichi AWolf SAugat PClaes L: The effect of micromovement on callus formation. J Orthop Sci 6:5715752001

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Article Information

INCLUDE WHEN CITING Published online July 22, 2016; DOI: 10.3171/2016.3.JNS16709.

© AANS, except where prohibited by US copyright law.

Headings

References

  • 1

    Albrektsson TZarb GWorthington PEriksson AR: The long-term efficacy of currently used dental implants: a review and proposed criteria of success. Int J Oral Maxillofac Implants 1:11251986

    • Search Google Scholar
    • Export Citation
  • 2

    Perren SM: Physical and biological aspects of fractures healing with special reference to internal fixation. Clin Orthop Relat Res 138:1751961979

    • Search Google Scholar
    • Export Citation
  • 3

    Schwarz FDünisch PWalter JSakr YKalff REwald C: Cranioplasty after decompressive craniectomy: is there a rationale for an initial artificial bone-substitute implant? A single-center experience after 631 procedures. J Neurosurg 124:7107152016

    • Search Google Scholar
    • Export Citation
  • 4

    Zanotti BVVerlicchi AParodi PC: Topics in Medicine: Special Issue 1–4. Cranial Demolition and Reconstruction: One-Step Surgical Procedure TrentNew Magazine Edizioni2010

    • Search Google Scholar
    • Export Citation
  • 1

    Kassis BGlorion CTabib WBlanchard OPouliquen JC: Callus response to micromovement after elongation in the rabbit. J Pediatr Orthop 16:4804831996

    • Search Google Scholar
    • Export Citation
  • 2

    Perren SM: Physical and biological aspects of fractures healing with special reference to internal fixation. Clin Orthop Relat Res 138:1751961979

    • Search Google Scholar
    • Export Citation
  • 3

    Yamaji TKenichi AWolf SAugat PClaes L: The effect of micromovement on callus formation. J Orthop Sci 6:5715752001

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