Surgical Neurology
Volume 65, Issue 1 , Pages 42-47, January 2006

Comparative dural closure techniques: a safety study in rats

  • Pinar Akdemir Ozisik, MD

      Affiliations

    • Department of Neurosurgery, Hacettepe University Faculty of Medicine, 06100 Ankara, Turkey
    • Corresponding Author InformationCorresponding author. Tel.: +90 312 3051715; fax: +90 312 3111131. 311 West Franklin St., Apt 902, Richmond, VA 23220, USA. Tel.: +1 804 8284337; fax: +1 804 8271536.
    • ,
  • Servet Inci, MD, PhD

      Affiliations

    • Department of Neurosurgery, Hacettepe University Faculty of Medicine, 06100 Ankara, Turkey
    • ,
  • Figen Soylemezoglu, MD

      Affiliations

    • Department of Pathology, Hacettepe University Faculty of Medicine, 06100 Ankara, Turkey
    • ,
  • Hilmi Orhan, MD

      Affiliations

    • Department of Toxicology, Hacettepe University Faculty of Pharmacy, 06100 Ankara, Turkey
    • ,
  • Tuncalp Ozgen, MD, PhD

      Affiliations

    • Department of Neurosurgery, Hacettepe University Faculty of Medicine, 06100 Ankara, Turkey

Received 11 March 2005; accepted 25 April 2005.

Article Outline

Abstract 

Background

Some neurosurgical procedures have high morbidity and mortality rates due to cerebrospinal fluid (CSF) fistula development, particularly when dural defects are in relatively inaccessible areas or surrounded by friable dura. We used a rat model to test 4 different dural closure techniques to determine which one was significantly superior for achieving a watertight dural closure with minimal harm to brain tissue.

Methods

The rats were randomly divided into 2 groups. The first group (group A, n = 40) was used to test the strength of the adhesivity for CSF leakage. Histopathologic studies were used to evaluate the granulation tissue between the dura and dural graft. Effects on the brain tissue were studied in the second group (group B, n = 40) where lipid peroxidation was determined. These 2 groups consisted of 5 subgroups: control, methyl metacrylate, n-butyl cyanoacrylate, fibrin glue, and CO2 laser.

Results

Methyl metacrylate and CO2 laser techniques were inadequate for stopping dural leakage and had harmful effects on brain tissue. Cerebrospinal fluid leak was observed only in 1 rat in the n-butyl cyanoacrylate subgroup and this result was statistically significant (P = .0005), but lipid peroxidation levels for this material showed that it was not safe for dural closure in case it leaked through the dural defect. The lipid peroxidation levels of the fibrin glue subgroup were not statistically significantly different from the control group (P = .440).

Conclusions

Fibrin glue was the safest material with a CSF leakage risk that was higher than n-butyl cyanoacrylate (25% vs 12.5%) but acceptable. This study showed no relationship between the CSF leak and histopathologic findings for sealant properties of the tissue adhesives.

Abbreviation: CSF, Cerebrospinal fluid

Keywords: Cyanoacrylates, Fibrin glue, CO2 laser, Cerebrospinal fluid leak, Dural defect repair

 

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1. Introduction 

Appropriate closure of the dura is very important in preventing CSF leakage in neurosurgery, as it constitutes a barrier on the brain surface. Dural suture remains the most frequently used method of repair. Suture techniques are difficult to carry out, particularly when defects are in relatively inaccessible areas or surrounded by friable dura. This problem has led some surgeons to advocate the use of various other techniques [2], [3], [5], [26], [29]. Cyanoacrylates [1], [23], fibrin glue [18], [30], and CO2 laser [12] have all been used to achieve dural closure and/or reinforcement.

In this study we compared 4 different dural closure techniques to determine which one was significantly superior for achieving a watertight dural closure with minimal harm to brain tissue: methyl metacrylate, n-butyl cyanoacrylate, fibrin glue, and CO2 laser patch-weld.

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2. Materials and methods 

This study was designed in full compliance with the policies and procedures set by the Animal Rights and Ethics Committee of Hacettepe University. A total of 80 rats (Hacettepe University Experimental Animals Laboratory) of both sexes were used. Animals weighing 250 to 400 g were kept under conventional laboratory conditions with a standard feeding protocol. The rats were randomly divided into 2 groups. The first group (group A, n = 40) was used to test the strength of adhesivity, whereas the effects on brain tissue were studied in the second group (group B, n = 40). These 2 groups each consisted of 5 subgroups: control, methyl metacrylate, n-butyl cyanoacrylate, fibrin glue, and CO2 laser patch-weld.

2.1. Surgical procedure 

All animals were anesthetized with ketamine hydrochloride 5 mg/kg (Ketalar, 5% solution, Eczacibasi with Parke-Davis, Levent, Istanbul, Turkey) and xylazine 10 mg/kg IM (Rompun, 2% solution, Bayer, Istanbul, Turkey). They were then fixed on the table and their scalps were shaved and cleaned with 10% polyvinylpyrrolidone/iodine. Craniectomy (5 mm in diameter) was performed with a high-speed drill on the right parietal bone of all rats. The dura mater was kept intact during this procedure. The dura was then opened transversely for 3 mm and CSF leak was observed with the operating microscope. The autogenous dural grafts (4 mm in diameter) were harvested from the animals' own galea.

2.1.1. Group A 

Histopathologic changes were studied and animals were treated with methylene blue in all subgroups to evaluate dural leakage.

2.1.1.1. Control group (n = 8): sham-operated group 

The dural grafts were applied over the open dura without any attachment technique or material.

2.1.1.2. Methyl metacrylate group (n = 8) 

Methyl metacrylate (Codman Cranioplastic Type 1-Slow Set, Johnson & Johnson Medical Ltd, UK) was applied with a dropper on the edges of the dural graft over the open dura.

2.1.1.3. n-Butyl cyanoacrylate group (n = 8) 

n-Butyl cyanoacrylate (Histoacryl, B. Braun Surgical GmbH, Meisungen, Germany) was applied with a dropper on the edges of the dural graft over the opened dura.

2.1.1.4. CO2 laser group (n = 8) 

The dural graft was positioned over the defect and was welded to the dura mater at the edges using 200 to 250 mW energy produced by CO2 laser equipment (Coherent Medical Group, Palo Alto, Calif).

2.1.1.5. Fibrin glue group (n = 8) 

Fibrin glue (Tisseel Kit, Eczacıbası-Baxter, Immuno AG Österreichisches Institut Für Haemoderivative GMBH, Vienna, Austria) was applied with a dropper on the edges of the dural graft over the open dura.

The surgical area was closed with 3-0 silk. The head of the rat in the prone position was put into flexion and the suboccipital and paravertebral muscles were dissected. The atlanto-occipital membrane was observed. Methylthionine chloride (methylene blue, Hacettepe University Research Pharmacy, Ankara, Turkey) was infused into the cisterna magna at a dose of 0.05 mg/kg in 0.1 mL of 0.9% normal saline with a PPD needle and infusion pump after removing 0.1 to 0.15 mL of CSF from the cisterna magna. The rats were then moved to the 30° Trendelenburg position and the surgical area was closed with 3-0 silk.

The incisions over the craniectomy area were opened and the blue color of methylthionine chloride on the bone and subcutaneous tissue surrounding the craniectomy defect were observed and recorded 24 hours after every operation to check for CSF leakage. The incision was closed again and the rats were kept under conventional laboratory conditions.

All animals were killed 14 days after the first operation by the intravenous injection of an overdose of phenobarbital. The brain tissues of the animals were then perfused transcardially with 0.9% NaCl solution. The craniectomy area was widened and 0.5 cm3 of brain tissue residing under the duraplasty area was excised together with the dura and dural graft. The samples were stored in 4% formaldehyde for histopathologic examinations.

2.1.2. Group B 

The effect of tissue adhesives on the brain was studied. The aforementioned steps of the surgical procedure were repeated except for methylthionine chloride infusion. As methylthionine chloride (methylene blue) is a very strong reductant agent, it might have had an effect on the lipid peroxidation levels.

The control (n = 8), methyl metacrylate (n = 8), n-butyl cyanoacrylate (n = 8), CO2 laser (n = 8), and fibrin glue (n = 8) groups had also the same surgical procedures, carried out using the same techniques as described for group A (except methylthionine chloride infusion), which is followed by decapitation of the rats and obtaining of the dura and brain samples 14 days after the operation.

The samples were stored at −70°C for determination of lipid peroxidation.

2.2. Determination of lipid peroxidation 

Lipid peroxidation in brain tissues was assessed using the thiobarbituric acid (TBA) method by the Toxicology Department of Hacettepe University Faculty of Pharmacology. Tissue homogenates were prepared by homogenizing tissues in 50 mmol/L potassium phosphate buffer (pH 7.0). The samples were placed into tubes at 20 mg tissue/mL buffer and sonication was applied in an ice cup for 6 minutes followed by vortexing for 2 minutes. They were then centrifuged at 11000g at +4°C for 10 minutes. The superior phase samples were used to determine thiobarbituric acid reactive substance (TBARS) levels.

Thiobarbituric acid reactive substance levels were measured using the method of Orhan et al [27] Richard et al [28]. Tissue homogenates (100 μL) were mixed with 750 μL TBA and 8 g of 7% perchloric acid. The mixture was heated for 1 hour at 95°C. The colored section was extracted into 2 mL of n-butanol; the absorption of the TBA-MDA (malondialdehyde) complex was measured by spectrofluorometer (excitation, 532 nm; emission, 553 nm; slit, 10 nm).

Three MDA standard homogenates were also prepared; 1 mmol/L of stock MDA was prepared by hydrolysis of 1,1,3,3-tetraethoxy propane [8]. The absorption of the stock MDA homogenates was measured at 245 nm to determine the concentration of the homogenate. Three standard homogenates with 2, 6, and 10 nmol/mL concentrations were prepared using this method. The TBARS levels of brain homogenates were determined as nanomole per milligram of protein using the absorption levels of the standard homogenates with different concentrations. Protein concentration of the samples was determined using the method of Lowry et al [22] and Miller [24].

2.3. Histopathologic evaluation 

After fixation in 4% formalin solution, the specimens of rats from group A containing the operation site were embedded in paraffin, and 5 histologic sections were cut and stained with hematoxylin and eosin (HE). All sections were evaluated by the same neuropathologist.

The grading system used for semiquantitative evaluation was modified from the histologic evaluation criteria of Lasa et al [20] (Table 1).

Table 1. Grading system for quantifying histopathologic findings
Criteria/score+1+2+3+4+5
Cell typesNo cell/few inflammatory cellsInflammatory cells and few fibroblastsModerate fibroblast and inflammatory cellsFibroblast dominancyFew fibroblasts
GranulationNoneThin layerModerate thicknessThickThick
Collagen depositNoneFew fibersModerate fibersIntensive fibersDense-organized fibers
VascularizationNoneFew new capillariesModerate capillariesDense capillariesDense capillary network

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3. Results 

3.1. Evaluating CSF leak ratios 

Cerebrospinal fluid leak ratios in group A are shown in Table 2. A cross-comparison of the results obtained from each of the 4 treatment subgroups was performed. The competency of the dural closure and the presence of methylene blue dye leak through the duraplasty on postoperative day 1 were statistically analyzed using a standard χ2 test and P < .005 was accepted as statistically significant. In the n-butyl cyanoacrylate subgroup (n = 8), CSF leak was observed only in 1 rat and this result was statistically significant (P = .0005). The n-butyl cyanoacrylate technique was superior to the other techniques and provided a solid seal during the operation. Methyl metacrylate and fibrin glue had also good dural seal properties (P = .001).

Table 2. CSF leak ratios
GroupsnCSF leakRatio (%)P
Control88100
Methyl metacrylate8225.001
n-Butyl cyanoacrylate8112.5.0005
Fibrin glue8225.001
CO2 laser8675.05

3.2. Histopathologic findings 

The histopathologic changes of leptomeninges and dura in group A were semiquantitatively scored according to cell type and severity of inflammatory cell infiltration, granulation, deposition of collagen, and neovascularization. These features were semiquantitatively scored from +1 to +5. The results of the semiquantitative analyses of the histopathologic findings are summarized in Table 3 where the scores were obtained by summing up separately the (+) counts of each histopathologic criterion that was evaluated and scored for each brain sample. Increasing number of (+) meant increased granulation tissue and deposition and the maturation of collagen. As the account of positivity increased, the polymorphonuclear leukocyte infiltration decreased and fibroblast accumulation increased. A score of +5 signified cell infiltration that was about to disappear with well-formed collagen deposits. The subgroups that had a high (+) count might therefore have better attachment between dura and galea graft. Cerebrospinal fluid leakage was expected to be less in the subgroups with high (+) counts compared with the subgroups with decreased positivity at the 14th postoperative day.

Table 3. Histopathologic findings
Groups/histopathologic criteriaCell typeGranulationCollagen depositVascularization
Control26(+)28(+)25(+)26(+)
Methyl metacrylate35(+)40(+)26(+)40(+)
n-Butyl cyanoacrylate19(+)22(+)20(+)19(+)
Fibrin glue18(+)29(+)22(+)26(+)
CO2 laser27(+)28(+)31(+)27(+)

Total scores of each histopathologic criterion were obtained by summing up the (+) counts of each brain sample that was evaluated and scored for these 4 criteria separately.

Histopathologic evaluation of the brain, leptomeninges, and dura at the 14th postoperative day showed moderate fibrous tissue development in the control subgroup. Polymorphonuclear leukocytes were the dominant inflammatory cells (Fig. 1A). This seems to be a reaction secondary to the craniectomy, dural opening, placement of galeal graft, and wound closure. Methyl metacrylate had the thickest granulation tissue development, dominant fibroblastic activity with collagen fibers forming bundles (Fig. 1B), and a well-developed capillary network. In the fibrin glue and n-butyl cyanoacrylate subgroups, there was less evidence of inflammatory cell invasion than the other subgroups, and some fibroblasts were noted between the galea patch and the dura mater. Moderate granulation tissue, collagen deposition with immature collagen fibers and well-formed capillaries, and surrounding fibroblastic activity (Fig. 1C) were also observed in the fibrin glue subgroup. In the n-butyl cyanoacrylate subgroup, collagen fibers and new capillaries were less significant than the fibrin glue subgroup and there was mild to moderate granulation tissue development. The CO2 laser subgroup had the second strongest positivity for features scored after methyl metacrylate subgroup with well-formed collagen deposits and decreased cellularity (Fig. 1D).

  • View full-size image.
  • Fig. 1. 

    A: Photomicrograph showing mixed inflammatory cell infiltration (arrowhead) in the leptomeninges in the control subgroup signifying cell type +2 (hematoxylin and eosin staining, ×200). B: Spindle-shaped cells forming fascicles (arrowhead) 14 days after application of tissue adhesive (methyl-metacrylate) signifying cell type +4 (hematoxylin and eosin staining, ×200). C: Well-formed capillaries (arrowhead) and surrounding fibroblastic activity (arrows) 14 days after application of tissue adhesive (fibrin glue) signifying +4 vascularization (hematoxylin and eosin staining, ×200). D: Extracellular matrix deposition (arrows) with decreased cellularity 14 days after application of tissue adhesive (CO2 laser) signifying +5 collagen deposit (hematoxylin and eosin staining, ×200).

The methyl metacrylate and fibrin glue subgroups had the same CSF leakage ratios at postoperative day 1 (25%) despite their different histopathologic findings. However, methyl metacrylate and CO2 laser subgroups had similar histologic properties, but also they have quite different CSF leak ratios: 25% in methyl metacrylate subgroup and 75% in CO2 laser subgroup. The n-butyl cyanoacrylate and fibrin glue subgroups had moderate (+) counts and the CSF leakage ratios were 12.5% and 25%, respectively.

In conclusion, the dural sealing properties of the tissue adhesives are not completely related with the histopathologic changes of the surrounding tissue.

3.3. Lipid peroxidation levels 

Fig. 2 shows the levels of lipid peroxidation measured in rat brains in group B. These results prove that there was no statistically significant difference of lipid peroxidation levels between the control (0.88 ± 0.23 nmol/protein) and fibrin glue (1.04 ± 0.56 nmol/protein, P = .440) subgroups (P values were calculated by using the unpaired t test and compared with the control group). The other subgroups had lipid peroxidation levels statistically significantly higher than the fibrin glue and control subgroups. The methyl metacrylate subgroup had a TBARS level of 2.47 ± 0.56 nmol/protein (P = .0025), the n-butyl cyanoacrylate subgroup had a TBARS level of 1.90 ± 0.56 nmol/protein (P = .0025), and the CO2 laser subgroup had a TBARS level 1.87 ± 0.55 nmol/protein (P = .0023).

Our study demonstrated that fibrin glue does not cause extra damage to brain tissue.

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4. Discussion 

The criteria for the ideal tissue adhesive include prevention of CSF leakage, no increase in infection rate, minimal adhesions, minimal foreign body or allergic reaction, and economy and ease of application and availability. With the increasing number of skull base surgeries and variety of neurosurgical operations, tissue adhesives and different materials for dural closure have become more important.

Cyanoacrylates and fibrin glue have already been widely used in neurosurgery for years in Europe, mostly for hemostasis and dural sealing. Cyanoacrylates were demonstrated to be good sealants and hemostatic agents even on wet surfaces with bacteriostatic and bactericidal effects in the previous studies [13], [14], [19], [21], [32]. But there is still a confusion about the histopathologic findings, if it can reflect the dural sealing properties of the tissue adhesives as good as it reflects their effect on the neural tissue. And there is another issue that is not clear: if the sealing properties of the tissue adhesives depend on the surrounding tissue reaction and the granulation tissue formation. That is why this study was planned to explore and compare the effect of different tissue adhesives and CO2 laser technique on the neural tissue; not only by histopathologic evaluation but also by lipid peroxidation as a quantitative method, and the relationship between the dural sealing properties of tissue adhesives and the surrounding tissue reaction.

The n-butyl cyanoacrylate subgroup had the best dural sealing in our study, but the lipid peroxidation level of this group (TBARS = 1.90 ± 0.56 nmol/protein) was the second highest among all subgroups. It was therefore considered to be not safe enough to repair dural defects if there is a risk of contact with the nervous tissue directly. The methyl metacrylate subgroup had the highest lipid peroxidation level (TBARS = 2.47 ± 0.56 nmol/protein). This subgroup also had a higher CSF leakage ratio than the n-butyl cyanoacrylate subgroup (25%). The cyanoacrylates used in this study can therefore not be considered to be ideal tissue adhesives.

Although it has lost most of its popularity recently, CO2 laser was used in some neurosurgical procedures for meningioma, acoustic neuroma, cordoma, parasellar and suprasellar tumors, and also in experimental studies for dural sealing [16]. CO2 laser was preferred in our study because of its restricted penetration capacity compared with Nd:YAG and argon lasers [6]. Lower penetration capacity provided that the melting effect of CO2 laser on underlying cerebral tissue might be less than the other laser types. This group had the highest dural leakage ratio (75%) in our study and its lipid peroxidation levels (TBARS = 1.87 ± 0.55 nmol/protein) were statistically significantly higher than the control group (P = .0023). The CO2 laser patch-weld technique was therefore not found to be a suitable technique for dural closure.

Fibrin glue was documented by De Vries et al [9] as a protective agent for intracranial nerves during cranial base surgery without any adverse effects, and another histologic study in a rat model has showed that the application of fibrin glue does not induce extra brain or intracranial nerve damage [10]. Lipid peroxidation results in the second stage of our study also demonstrated that fibrin glue was the safest material to use for dural closure in case of leakage through the dural defect (P = .440) with an acceptable CSF leak ratio (25%), although it may still pose some serious infection problems as a human blood product.

We did not observe a relationship between CSF leak and the histopathologic findings, but there are also some conflicting reports on the histopathologic findings of tissue adhesives. CO2 laser itself had a dense inflammatory and fibrous reaction in our study; Colak et al [6] have reported its use to reduce spinal epidural fibrosis. Although some previous studies described enhanced local accumulation of mononuclear cells and promoted angiogenesis close to the wound by fibrin glue [4], [25], other studies have shown that fibrin glue reduces the severity of postsurgical intra-abdominal adhesion in rats [17], [31]. It might be due to the formation of granulation tissue, and deposition of extracellular matrix is such a process that is affected by numerous tissue-dependent and environmental factors.

The histopathologic evaluation showed that the CO2 laser subgroup followed the methyl metacrylate subgroup for the intensive formation of collagen fibers. It might be argued that an increased inflammatory response with dominant polymorphonuclear leukocyte infiltration still persisted on the 14th postoperative day. Secondary healing with fragile granulation tissue that occurred at the surgical site might be responsible for the weak dural seal in the CO2 laser subgroup, as it had the highest CSF leakage ratio among the tissue adhesive subgroups (75%). However, the methyl metacrylate subgroup that had almost similar histopathologic evaluation with the CO2 laser subgroup had quite different CSF leakage ratio (25%).

As an interesting finding, the best dural seal was achieved with n-butyl cyanoacrylate that had the least (+) counts for the severity of the inflammation, granulation, and also for deposition and the maturation of the collagen, even less than the control subgroup in our study.

Therefore, we think that the histopathologic findings might be inadequate to explain the relation between persistence-strength of the dural seal and the histologic properties of the tissue adhesives.

Animals rarely develop meningitis despite evidence of gross CSF leakage and histologic confirmation of local inflammation and granulation. Early CSF leak in human patients is difficult to avoid, more difficult to treat, and the major contributor to perioperative morbidity and mortality after some special neurosurgical approaches such as the transoral surgical approach to the brainstem, lower clivus, or superior cervical spine with a high incidence of CSF fistula, meningitis, abscess formation, and even death [7], [11], [15], [33]. That is why an immediate and persistent, strong dural seal makes a clinically important difference in the prognosis.

Our study demonstrated that fibrin glue can be safely used for patch repairing of complex dural defects, but the use of fibrin glue in sealing the dura is of limited value. The histopathologic findings also showed no correlation between sealant properties and formation and stage of granulation tissue of the compounds studied. Studies should therefore continue to search for an ideal material with more reliable sealant properties.

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PII: S0090-3019(05)00387-3

doi:10.1016/j.surneu.2005.04.047

Surgical Neurology
Volume 65, Issue 1 , Pages 42-47, January 2006

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