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Histological and biomechanical study of dura mater applied to the technique of dura splitting decompression in Chiari type I malformation

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Abstract

Many techniques are described to treat Chiari type I malformation. One of them is a splitting of the dura, removing its outer layer only to reduce the risks of cerebrospinal fluid (CSF) leak. We try to show the effectiveness of this technique from histological and biomechanical observations of dura mater. Study was performed on 25 posterior fossa dura mater specimens from fresh human cadavers. Dural composition and architecture was assessed on 47 transversal and sagittal sections. Uniaxial mechanical tests were performed on 22 dural samples (15 entire, 7 split) to focus on the dural macroscopic mechanical behavior comparing entire and split samples and also to understand deformation mechanisms. We finally created a model of volume expansion after splitting. Dura mater was composed of predominant collagen fibers with a few elastin fibers, cranio-caudally orientated. The classical description of two distinct layers remained inconstant. Biomechanical tests showed a significant difference between entire dura, which presents an elastic fragile behavior, with a small domain where deformation is reversible with stress, and split dura, which presents an elasto-plastic behavior with a large domain of permanent strain and a lower stress level. From these experimental results, the model showed a volume increase of approximately 50% below the split area. We demonstrated the capability of the split dura mater to enlarge for suitable stress conditions and we quantified it by biomechanical tests and experimental model. Thus, dural splitting decompression seems to have a real biomechanical substrate to envision the efficacy of this Chiari type I malformation surgical technique.

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Acknowledgments

The authors thank all the team of Pr Frileux at the Ecole de Chirurgie Assistance Publique–Hopitaux de Paris, especially René Gicquelet and Djamel Taleb for their assistance.

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There is no financial disclosure. There is no conflict of interest.

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Correspondence to Dorian Chauvet.

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Ricardo Botelho, São Paulo, Brazil

Chauvet et al. developed an experimental model to test the elasticity of the inner layer of dura mater from the posterior cranial fossa under separation from its external layer. The final objective of this work is to provide experimental substrate to the use of this technique in the treatment of Chiari malformation.

One secondary but interesting fact disclosed by the authors was that a true anatomical separation between inner and outer dural layers is inconstant. Despite this finding, the authors really provided a model to study the elasticity and capacity of divided dura under hydrostatic conditions to enlarge volumetric capacity of posterior fossa cavity.

The experimental findings must be translated into practical applications. This kind of research has been termed as translational research. The same group of authors has provided (in other publication) some evidence demonstrating the effect of the posterior fossa decompression under splitting the dura mater in series of patients. Other studies will be necessary to reveal which kind of patients will benefit from this technique but the experimental model has been already developed by Chauvet et al.

Ralf Alfons Kockro, Zurich, Switzerland

This is an interesting article about the biomechanical properties of intact versus split posterior fossa dura mater in view of applying the technique of dura splitting for Chiari malformation I decompression surgery. This work nicely shows how an interdisciplinary collaboration, like in this case with materiel sciences, can shine light on a controversial surgical method. The authors have applied mechanical stress tests as well as mathematical models to analyze the dura’s mechanical deformation behavior and predict its volume expansion properties. They have demonstrated a sufficient elastic capability of split dura mater in order to provide an adequate decompressive effect during CM-I decompression surgery. These results match the group’s clinical and radiological findings. I encourage the group to present their long-term clinical findings with this decompressive surgical technique.

Jörg Klekamp, Quakenbrück, Germany

The authors describe the biomechanical properties of the posterior fossa dura mater of ten human cadavers before and after applying the dura splitting technique. The background behind this study is to provide data supporting this technique for treatment of the Chiari type I malformation avoiding opening of the entire dura and arachnoid. This is supposed to limit postoperative complications and problems with CSF fistulas in particular. Even though most of the patients with Chiari type I malformations are considerably younger than the elderly population studied here, this paper provides data supporting the rationale to decompress the foramen magnum by a craniectomy and splitting of the outer dural layer only.

However, the pathophysiology of Chiari type I malformation with or without syringomyelia involves more than just compression of spinal cord and medulla oblongata at the foramen magnum. Successful treatment of these patients requires a restoration of CSF flow at his level. This can be achieved in many patients with this technique but certainly not in all of them. Arachnoid pathologies contribute to CSF flow obstructions in a significant number of patients and are not addressed with this technique. Whether such pathologies can be excluded with sufficient accuracy by intraoperative ultrasound is a controversial issue. Consequently, the rate of postoperative decreases of syrinx sizes tends to be lower with the dura splitting technique compared to those that open the dura. The authors prove to some degree that splitting the dura can enlarge the cisterna magna. However, to recommend this technique, clinical studies must prove that it is at least as good as the standard, i.e., bony decompression and duraplasty.

Lotfi Hacein-Bey, Sacramento, USA

Chauvet et al. present the results of a rigorously and elegantly conducted study of the biomechanical and histological properties of split dura mater. Currently, the best surgical standard practice for the treatment of Chiari I malformation with or without syringomyelia is dural grafting. Although the “split dura” or “dural relaxing technique” (described in 1993 by Isu et al.) is sometimes used in association with a dural graft, and although the biomechanical and physical properties of the human dura mater (most exclusively that of the lumbar area) have been previously studied, a scientific assessment of the anatomical and physical properties of the posterior fossa dura mater had been lacking so far.

The major finding of this study is displayed in Figure 6 which demonstrates that two samples (obtained in the same patient) have significantly different stress/strain responses, the “split” sample exhibiting considerably greater elastic properties.

One important histological finding of this study is the evidence of variability in the multilayer structure of the dura mater of the posterior fossa. The authors used scanning electron microscopy and SHG microscopy techniques to study the orientation of dural layers. Perhaps further histological analysis might result in refinements in the technique of dural splitting to eliminate the risk of damage to macroscopic leaflets.

Since all dural samples in the study were obtained from cadavers 70 years and older (a limitation of the study which is acknowledged by the authors), several questions arise. Is there variability in the histological arrangement of the dura among individuals and with increasing ages? More importantly, is there significant variability between posterior fossa dural organization in Chiari I patients versus normals? Also, are there different histological arrangement and biomechanical behavior in the dura of patients with fibromyalgia and other conditions for which posterior fossa decompression has been advocated, raising a high level of controversy?

Although our understanding of the viscoelastic and biomechanical properties of the human posterior fossa dura mater needs further deepening, the authors must be congratulated on conducting a landmark study of quality. Some minor degree of validation is provided by the clinical responses reported in the 11 patients treated by the authors. The authors’ plan to conduct further biomechanical studies, including creep tests, and long-term follow-up of their patients should be awaited with interest.

Richard G. Fessler, Chicago, USA

Drs. Chauvet et al. present an interesting evaluation of the biomechanics of a newly proposed technique of treating Chiari I malformation, splitting the layers of the dura while leaving it intact overall. While the technique itself remains unproven, being supported only by a handful of patients with short-term follow-up, the idea does carry some interest.

Many practical questions are raised by the data, however. For example, since less than one fourth of the dural specimens examined had any evidence of separate identifiable layers, of what practical significance is a dura “splitting” procedure? Second, the problem with treating Chiari I malformation is usually in the long-term follow-up, during which it is common for symptoms to return. Often, this is due to “re-scarring” of the duraplasty. Is there any reason to believe that this will not happen with a dura splitting procedure?

Another question raised concerns the effect of the dura splitting. Although splitting the dura to roughly one half its original thickness would obviously lead to a weaker dura, this does not necessarily translate into greater “stretchability.” Especially since the authors own data suggest that the out layer (i.e., the one removed) has the higher concentration of elastin, and the inner layer is predominantly collagen.

Finally, as presented in the “Results” and “Discussion” sections, numerous “assumptions” were made about the dura to enable the mathematical analysis performed by the authors. Since most of these assumptions have no true validation, it is hard to attribute significance to the acquired results.

All that being said, this is a fascinating potential option, and I will look forward to further verification of its effectiveness.

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Chauvet, D., Carpentier, A., Allain, JM. et al. Histological and biomechanical study of dura mater applied to the technique of dura splitting decompression in Chiari type I malformation. Neurosurg Rev 33, 287–295 (2010). https://doi.org/10.1007/s10143-010-0261-x

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