Acta Neurochir (2011) 153:148–155 DOI 10.1007/s00701-010-0762-y
CLINICAL ARTICLE
Hemostatic matrix sealant in neurosurgery: a clinical and imaging study Roberto Gazzeri & Marcelo Galarza & Massimiliano Neroni & Alex Alfieri & Marco Giordano
Received: 10 June 2010 / Accepted: 30 July 2010 / Published online: 12 August 2010 # Springer-Verlag 2010
Abstract Object The aim of this study was to investigate prospectively the efficacy and safety of Floseal hemostatic matrix. Methods A total of 214 patients (87 males, 127 females; mean age 56.2 years) undergoing cranial (71.4%), craniospinal (0.9%), and spinal (27.5%) procedures with the use of gelatin thrombin hemostatic matrix (Floseal) were included in this prospective study. The indications for its use, surgical techniques, time to bleeding control, and associated complications were recorded. Results Effective hemostasis, defined as cessation of bleeding, was achieved no later than 3 min after topical agent application in all patients except in 11 cases, in which R. Gazzeri (*) : M. Neroni Department of Neurosurgery, San Giovanni-Addolorata Hospital, Via O. Tommasini 13, 00162 Rome, Italy e-mail: robertogazzeri@gmail.com R. Gazzeri Centre for Minimally Invasive Neurosurgery, Prince of Wales Private Hospital, Sydney, Australia M. Galarza Department of Neurosurgery, Hospital Universitario Virgen de la Arrixaca, Murcia, Spain A. Alfieri Klinik und Poliklinik fßr Neurochirurgie, Martin-Luther Universität Halle-Wittenberg, Halle, Germany M. Giordano Department of Pathology, San Giovanni-Addolorata Hospital, Rome, Italy
the hemostatic application was repeated. Rebleeding was disclosed in four patients 1 day after initial surgery. In one case, an intracerebral abscess developed after a malignant glioma removal. No other patient developed allergic reactions or local or systemic complications associated with the hemostatic sealant. Conclusion In this study, matrix hemostatic sealant helped to control operative bleeding in cranial and spinal surgery, reducing damage to the surrounding healthy nervous tissue while shortening surgical timing. Other than safe, the immediate hemostatic effect is an advantage in the settings of refractory bleeding. Keywords Intracerebral hemorrhage . Spontaneous hematoma . Hemostatic sealant . Cranial hemostasis . Spinal hemostasis . Floseal
Introduction Adequate hemostasis in cranial and spinal surgery is of paramount importance in a neurosurgeon daily practice. Generalized ooze bleeding from the surgical walls cavity, usually coming from surface vessels of the dura mater or nervous tissue, may be bothersome, and it can usually be controlled with additional bipolar cautery or additional use of topical hemostatic agents. Nevertheless, thermal and mechanical coagulation may show disadvantages in eloquent areas or even properly controlling bleeding. Although bipolar cautery may arrest bleeding from the operative field, this method bear the risk of healthy nervous tissue destruction, with deleterious neurological sequelae. In addition, a variety of hemostatic agents, such as peroxide, fibrin glue, among others, are used by neurosurgeons depending on the type, source, and
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location of bleeding. Floseal matrix hemostatic sealant (Baxter) is a mixture of a gelatin matrix and a thrombin component mixed together at the time of use: Both components promote hemostasis and interact synergistically to facilitate the formation of the clot at the bleeding site [1]. Although there are published reports about its use [11, 14, 15], only two publications refer specifically to intracranial application [2, 4], yet this hemostatic agent is on the market since years. The present study was prospectively conducted to evaluate the efficacy, safety, and handling of Floseal in a wide range of cranial and spinal procedures such as spontaneous intracerebral hemorrhages, cerebral tumors, and degenerative spinal disease.
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Results Patient characteristics Between January 2005 and January 2009, 214 consecutive patients were prospectively enrolled in this study, of whom 87 were male (40.7%) and 127 were female (59.3%); their mean age was 56.2 (range 18–75 years old, standard deviation 15.8 years). The patients underwent cranial neurosurgery in 153 cases (71.4%) using either a craniotomy (138) or craniectomy (15), craniocervical junction procedures in two cases (0.9%), and spinal approaches in 59 cases (27.5%; Table 1). Most of cranial surgical approaches included supratentorial craniotomy (n=140) whereas 13 patients underwent a posterior fossa surgery.
Materials and methods
Diagnoses and indications
This study was designed as a prospective, non-randomized clinical and imaging-based trial. A consecutive series of patients between 18 and 75 years of age, who were scheduled for elective and emergency cranial and spinal surgery, were included until a total of 214 applications were achieved. Preoperative exclusion criteria included internal CSF shunting, or a systemic or local infection. Intraoperative inclusion criteria were persistent and excessive bleeding that required more than the standard techniques for hemostasis (bipolar coagulation, use of cellulose, and collagen sponge) or when these methods were excessively time-consuming, or could lead to injury of healthy neural tissue. In each case, the decision to use the hemostatic matrix was made by the surgeon according to his/her preference and the intraoperative situation. The primary endpoint was defined as no hemorrhage in the operative cave after hemostatic matrix application. The following data were collected and analyzed for all patients: age, sex, diagnosis, diagnosis, operative site, scheduled or emergency neurosurgical procedures, and length of procedure. The preoperative clinical laboratory tests included a complete electrolyte panel, liver function tests, full blood count with differential, prothrombin time, and partial thromboplastin time. Intraoperative source and type of bleeding (arterial, venous, or generalized venous oozing), time to bleeding control, and quantity of hemostatic matrix used were evaluated. After surgery, the patients were evaluated for the following assessments: laboratory tests (alkaline phosphatase, blood urea, creatinine, and leukocyte count), neurological examination, adverse events at 7-day postoperative, and 1-month follow-up visits. All the patients underwent postoperative cranial or spinal MR or CT imaging on the immediate follow-up and on following follow-up visits.
The most common pathological diagnosis was brain tumor, accounting for 75 patients (35%), whereas traumatic conditions occurred in 53 cases (24.7%) and degenerative spinal disorders in 45 cases (21%). In 179 patients, the surgical course of action involved the use of standard techniques for hemostasis initially (i.e., bipolar cautery, use of cottonoid peroxide, oxidized cellulose, or collagen sponge): When these measures failed or were inadequate, Floseal was applied directly to the site of bleeding (Tables 2 and 3). The other 35 patients with spontaneous supratentorial intracerebral hemorrhage were treated with a minimally invasive technique previously reported, using initially for the hemostasis only the hemostatic matrix sealant [4] (Figs. 1 and 2). In all cranial and spinal cases, the time to prepare gelatin thrombin matrix ready to use did not exceed 1 min. Effective hemostasis defined as cessation of bleeding after topical hemostatic agent application was Table 1 Characteristics of cranial and spinal approaches Operation
Approaches
Cranial Supratentorial Infratentorial Craniospinal Spinal Anterior Posterior Cervical Cervicothoracic Thoracic Lumbar Total
Number of patients (%) 153 (71.4) 140 13 2 (0.9) 59 (27.5) 6 53 18 1 3 37 214 (100)
150 Table 2 Summary of diagnosis in 153 patients undergoing cranial surgery
ICH intracranial hemorrhage
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Number of patients (%)
Glioma Spontaneous ICH Traumatic ICH Meningioma Extra-axial hematoma/cranial base fracture Metastasis Schwannoma Pituitary Adenoma
achieved no later than 3 min in all patients except in 11 cases. In these latter, the bleeding was finally stopped after a new application of gelatin thrombin matrix (Table 4). In 16 cases, bleeding occurred from a tear along a venous sinus (superior sagittal sinus in ten cases and transverse sinus in six cases). In these cases that could not be repaired by suture, a piece of oxidized cellulose (Surgicel, Ethicon, Inc., Somerville, NJ, USA) or gelatin sponge (Spongostan, Ethicon, Somerville, NJ, USA) was placed over the bleeding gap of the venous sinus (Fig. 3). Thereafter, hemostasis was achieved by additional application of the hemostatic matrix over the cellulose or sponge, and the gelatin thrombin matrix was held in place by a cottonoid. The conformation of the cellulose or sponge enabled the gelatin matrix to enter in the underlying venous sinus avoiding the possibility of sinus thrombosis and embolism. In two cases, hemostasis was reinforced applying over the matrix additional oxidized cellulose or gelatin sponge and sealed with fibrin glue (Tisseel, Baxter Healthcare, Vienna, Austria). In the two cases of craniocervical junction surgery, important bleeding from the venous plexus around the vertebral artery was controlled with application of Floseal, and the excess of hemostatic matrix was not removed. In all anterior and posterior spinal approaches, where source of bleeding was not visible because originating from torn epidural venous plexus underneath neural structures or Table 3 Spinal approaches in 59 patients Spinal procedures Anterior cervical discectomy Cervical laminoplasty Cervical laminectomy Cervicothoracic laminectomy Thoracic laminectomy Lumbar laminectomy Posterior lumbar fusion Microdiscectomy Total
Number of patients (%) 6 7 5 1 3 26 9 2 59
(10.1) (11.8) (8.4) (1.6) (5) (44) (15.2) (3.3) (100)
37 35 26 25 16 11 2 1
(24.1) (22.8) (16.9) (16.3) (10.4) (7.1) (1.3) (0.6)
bone, after delivery of the hemostatic matrix and subsequent hemostasis, the granular matrix was removed to avoid neural compression in the spinal canal. Follow-up clinical and neurological examination was performed on day 1 postoperatively, at discharge and at 1 month. All identified neurological deficits were already present prior to surgical intervention or were known potential complications of the type of operation performed. No patient developed allergic reactions or systemic complications as embolism and infection associated with the use of Floseal. Postoperative MR imaging or CT were performed after surgery, at discharge, and after 1 month in 164 patients (76.6%). Normal postoperative conditions were found, without signs of inflammation, perilesional edema, or scar formation attributable to the hemostatic sealant. Successful hemostasis was achieved in 211 (98.5%) patients. There were four cases (1.8%) of delayed hemorrhage (Table 5). One patient with spontaneous intracranial hemorrhage (ICH) presented with rebleeding–hematoma enlargement combined with neurological deterioration 2 days after surgery; thus, reoperation was performed with the same minimally invasive technique. In one case of rebleeding 12 h after traumatic ICH surgery, we performed a histological examination of the granular matrix in contact with the brain: The specimen showed the presence of granules of the gelatin matrix after releasing the thrombin, exerting also a mechanical compression on the nervous tissue with minimal inflammatory reaction (Fig. 4). In one case of extra-axial hematoma, the patient developed a status epilepticus 3 days after surgery, with a normal postoperative brain CT scan. Seizures were controlled pharmacologically and the patient was discharged after 20 days. A patient who had surgery for a malignant glioma developed a brain abscess. He was reoperated 1 week after initial surgery. Neurosurgical wound infections were recorded in three patients. No complications occurred in the 59 patients undergoing spinal procedures. Clinical laboratory test results (mean values) revealed no significant difference between the preoperative data compared with the findings obtained at 1 month postsurgery.
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Fig. 1 Case 12: a axial, b coronal, and c sagittal CT scans demonstrating a parietal hematoma. d Postoperative CT scan after surgical evacuation using Floseal
Discussion We report our experience with the use of matrix hemostatic sealant in over 214 cranial and spinal procedures (representing 5.9% of the total number of patients operated in the same period of time). Other than bipolar coagulation, a variety of local hemostatic techniques and agents are used by neurosurgeons: microfibrillar collagen (Avitene), oxidized cellulose (Surgicel; Ethicon, Inc., Somerville, NJ, USA) or fibrin glue (Tisseel; Baxter AG, Vienna, Austria) Fig. 2 Case 30: a preoperative CT scan showing a frontal intracerebral hematoma. b Postoperative scan after minimally invasive surgery and use of Floseal
to achieve control of bleeding from the brain parenchyma, dural venous sinuses, and spinal venous plexus. Yet, sometimes these hemostatic agents may be difficult to apply on the walls of the operative cave through a narrow operating channel. Also bipolar coagulation at a bleeding site frequently provides complete control of bleeding but is often time-consuming, leading to a wide enlargement of the working channel. Floseal has been demonstrated to be safe and biocompatible as compared with hemostatic agents currently in use [12]. In neurosurgical literature, there are
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Table 4 Characteristics of intraoperative source of bleeding Source of bleeding Generalized venous oozing Epidural venous plexus bleeding Venous sinuses bleeding Arterial capillary bleeding
Fig. 3 Artist illustration showing a bleeding from a tear on superior sagittal sinus; b application of a patch of gelatin sponge over the tear; c Floseal is injected over the gelatin sponge, which enables the gelatin matrix to enter in the underlying venous sinus avoiding the possibility of sinus thrombosis and embolism; d a cottonoid is applied over the gelatin matrix; and e after 3 min the cottonoid is removed without irrigation, leaving the excess of Floseal hemostatic matrix on site
Number of patients (%) 128 61 16 9
(59.8) (28.5) (7.4) (4.2)
only two other reports of use of this hemostatic agent in cerebral surgery [2, 4]. Capillary ooze is a generalized problem at the end of intracerebral tumor removal or hematoma evacuation and the use of hemostatic sealant solved that problem expeditiously in all our cases. We injected this agent with a syringe tip, and the granular nature of the gelatin matrix enabled the material to conform to any irregular surgical cave geometry. The hemostatic matrix is hydrophilic and adheres well to wet tissue, in contrast to other agents as fibrin glue, which need a dry surface. The granular gelatin particles conformed to the
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Table 5 Incidence of postoperative complications Complication Rebleeding Abscess Status epilepticus
Number of patients (%) 4 (1.8) 1 (0.4) 1 (0.4)
Pathology 2 malignant gliomas, 1 spontaneous ICH, 1 traumatic ICH 1 malignant glioma 1 extra-axial hematoma
ICH intracerebral hemorrhage
bleeding site swelling approximately 20% restricting blood flow and providing a mechanically stable matrix around which the fibrin clot conformed. Blood percolating through the spaces between the granules was exposed to high concentration of thrombin and fibrinogen and was converted in fibrin polymer resulting in a clot that remains in place at the tissue surface, providing a sealing effect at the bleeding site. Excess granular material not incorporated in the hemostatic clot was carefully removed by gentle irrigation, without disrupting the hemostatic seal, thus reducing the volume of the gelatin matrix–thrombin solution mixture in the surgical cavity. In this prospective study, we observed adequate hemostasis in all patients, except 11 cases in whom the hemostatic matrix application was repeated after 4 min to stop a persistent bleeding. In this study, four cases presented rebleeding or delayed hemorrhage in the operative field; the reported rate of postoperative hematomas in neurosurgery varies between 0.7% and 8% [3, 5, 6, 13] depending on the treated pathology and the type of surgery (cranial or spinal); Palmer [13] reported 55% of patients with postoperative hemorrhagic complications died or had an unfavorable outcome, while in our cases only one patient (25%) had an unfavorable outcome. In the present study,
Fig. 4 Photomicrographs of the granular gelatin matrix 1 day after application in a traumatic intracerebral hematoma. The amorphous granules are in contact with the brain tissue. There is minimal inflammatory reaction. H&E, original magnification ×100
one patient (0.4%) experienced a deep surgical site infection: an intracerebral abscess developed 5 days after a malignant glioma removal. A meaningful comparison can be made between the present study and clinical studies of neurosurgery-related sepsis [10]. Surgical site infection rate strongly correlates with the duration of the surgical procedure [7, 10]. In the study of Korinek [7], in which the overall infection rate was 4.0%, the infection rate for patients with surgery was lasting longer than 32.5%. Narotam et al. reported similar results, with an overall infection rate of 0.8% for clean surgery, but an infection rate of 13.4% for clean surgery was lasting more than 4 h [10]. There is a theoretical danger of aggravating perilesional brain edema increasing local thrombin concentrations. Direct infusion of large doses of thrombin into brain may cause brain edema formation and inflammatory cell infiltration; such edema partly results from a direct opening of the blood–brain barrier. In our series, few minutes after injection of Floseal, the thrombin and gelatin matrix were removed by gentle irrigation and suction by the site of application, thus reducing the concentration of intraparenchymal thrombin, leaving a clear operative field. Control head CT scan performed after surgery demonstrated absence of perilesional edema formation secondary to hemostatic application in all cases. Of concern with hemostatic medications is the potential of thrombotic complications; there are isolated unpublished case reports of thromboembolic complications secondary to injection of gelatin hemostatic matrix over a bleeding venous sinus tear. In the present study using oxidized cellulose or gelatin sponge as a web to prevent migration of Floseal into the venous sinus, we did not observe any embolism nor sinus thrombosis. The presence of Surgicel over the bleeding sinus tear permitted adequate coherence of the gelatin granules with effective hemostasis. In these cases, excess of gelatin matrix was not removed from the bleeding site, while in two cases the clot was reinforced with fibrin glue. In this series, all patients with ICH had main and quick decompression of the hematoma, with a minimally invasive procedure and in no case we had seen clinical deterioration from edema or residual hematoma. We had one case with a rebleeding that was operated 2 days after first surgery. Yet, our overall clinical results compared with the reviewed
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literature of ICH surgery showed a better outcome. In our series, 58% of patients achieved good recovery with a mortality rate of 13%, while poor outcome in other series of patients treated with craniotomy ranged from 50% to 98% and mortality from 23% to 78% [8, 9]. Our spinal cases, including cervical and lumbar procedures, had no postoperative hematomas. When a mini-invasive spinal approach is used, even mild intraoperative hemorrhage can lessen visibility in the confined operative field of view. Occasionally, continuous epidural venous bleeding during posterior spinal approaches may be bothersome, difficult to control, and time-consuming, but it can usually be controlled by use of hemostatic agents, pressure, and patience. In majority of cases of anterior cervical microdiscectomy, source of bleeding is not visible because it originates from a torn venous plexus underneath the bone, usually after decompression of the uncovertebral joints. One major concern about the use of hemostatic agents in spine surgery is that there is danger of aggravating compression of the neural structures. Preclinical studies [12] demonstrated swelling following exposure to fluid is 11% for Floseal compared to 135 for cellulose, 260% for collagen, and 320% for gelatin. Compared to other hemostatic agents, median time to biodegradation was 30 days for gelatin thrombin hemostatic sealant versus 60 days for cellulose and more than 90 days for collagen agents. One potential concern when using any biological hemostatic agent is the risk of virus transmission. Although these are protein products, there has been no documented case of viral transmission through gelatin matrix hemostatic sealant to date. After evaluation in a multicenter, prospective, clinical trial, it has been approved for clinical use by the USA Food and Drug Administration [14]. Safety and biocompatibility after direct application of Floseal to neural tissue has been demonstrated in preclinical studies [12]. Inflammatory reaction to Floseal in the brain was reported to be equivalent to the reaction of other commonly used neurosurgical hemostatic agents with a minor median time to biodegradation compared to the other implanted hemostatic materials. A relative caveat of this study is the lack of a control group. Yet, we may infer that because of this product, since its introduction in our daily practice, we have shortened our mean operative times. In our series, there was no evidence of any immune-mediated coagulopathy after exposure to thrombin; there was no adverse event directly related to the application of the hemostatic agent to the brain. The additional cost to the surgical procedure secondary to one application of Floseal (5 ml) in our institutions is roughly 260 euros: Although this issue is particularly relevant in less developed countries, cost analysis was not performed in this study. Future studies incorporating cost–benefit analysis are necessary to provide us with some guidance. Floseal is a safe and efficacious tool for neurosurgeons in cases of difficult intraoperative bleeding. We prefer to
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use it as a second-line hemostatic agent in every day cranial and spinal surgery, only if hemostasis cannot be reached by traditional methods, and as a first-line agent in cases of minimally invasive treatment for ICH.
Conflicts of interest None.
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Comment This is an interesting paper summarizing the large surgical experience of the authors on the use of Floseal as a hemostatic agent in various cranial and spinal neurosurgical procedures. The conclusions are clear and convincingly discussed. This report is timely due because of the inherent importance of the topic and the relatively scant relevant literature. The cost of Floseal is an issue that the authors barely address, particularly relevant outside of the Western world in less developed countries. In this study, the decision to use the hemostatic matrix was made by the surgeon according to his/her preference and the intraoperative situation. Were the surgeons convinced that hemostasis could not be reached by traditional methods before applying the matrix? On the other hand, a percentage of about 6% of cranial and spinal procedures during which Floseal was applied seems to be reasonably adequate. I agree with the authors that Floseal represents a safe and efficacious method for controlling difficult intraoperative situations, but it must not be intended as the primary option for achieving hemostasis.
Domenico d'Avella Padova, Italy
155 This article addresses an important issue. It investigates safety and efficacy in the use of Floseal, a hemostatic agent with widespread use despite the fact that it reached the market not too long ago. The authors have found an indication for its use in roughly 5% of all cases operated in the timeframe of the study. Indications and recommendations for the use of Floseal along with pearls to minimize any possible deleterious effects of the product are discussed. Widespread capillary or bone oozing is apparently the best indication for its use. Standard hemostasis procedures must always precede the use of any of these agents. Therefore, the argument of bipolar coagulation being timeconsuming and therefore tedious is missing the point. Conformity to the cavity created especially in brain surgery is clearly an advantage. As a personal note, I have never found that regular hemostasis with bipolar, irrigation, and a little Gellfoam could not do the job for hemostasis in one or two level anterior cervical discectomies and fusion. For the younger generation and those starting their practices, the word should remain that nothing is more efficacious than regular hemostasis and that these adjuncts are of great value if not unduly used.
Manuel Cunha e Sa Almada, Portugal