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Keywords:

  • Epilepsy;
  • Mesial temporal lobe epilepsy;
  • Epilepsy surgery;
  • Foramen ovale electrodes;
  • EEG

Abstract

  1. Top of page
  2. Abstract
  3. METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgments
  7. REFERENCES

Summary: Purpose: We analyze a series of patients with mesial temporal lobe epilepsy (MTLE) associated with hippocampal sclerosis (HS) submitted to presurgical investigation with scalp sphenoidal, followed by foramen ovale electrodes (FO), and, when necessary, with depth temporal electrodes. We sought to evaluate the clinical utility of FO in patients with MTLE-HS.

Methods: We included patients who had phase I investigation with bitemporal independent seizures, nonlateralized ictal onsets, or ictal onset initiating in the side contralateral to the side of hippocampal sclerosis. Patients whose implanted FO failed to demonstrate an unambiguous unilateral ictal onset were later evaluated with depth hippocampal electrodes.

Results: Between May 1994 and December 2004, 64 patients met our inclusion criteria: 33 female (51.5%) and 31 male subjects (48.5%). The mean age at enrollment was 37.66 ± 10.6 years (range, 12–56 years). The groups with nonlateralized surface ictal EEG onsets and contralateral EEG onsets had a greater chance of lateralization with FO when compared with the group with bilateral independent seizures on surface EEG (p < 0.01). Foramen ovale electrodes lateralized the seizures in 60% of patients. Seventy percent of patients became seizure free after temporal lobectomy. Five patients were implanted with depth temporal electrodes after FO video-EEG monitoring. The depth-electrode EEG onsets confirmed the results of FO video-EEG monitoring in all patients, and the surgery was refused.

Conclusions: In MTLE-HS, FO is a reliable method for lateralization of seizures that are not clearly recorded by surface EEGs.

Mesial temporal lobe epilepsy associated with hippocampal sclerosis (MTLE-HS) is the commonest type of pharmacologically intractable epilepsy. However, after a careful preoperative evaluation, 60–70% of MTLE-HS patients can be rendered seizure free after temporal lobectomy (1).

In many candidates for temporal lobe resection, the seizure focus can be accurately lateralized and patients selected for surgery by using noninvasive investigations, such as high-resolution magnetic resonance imaging (MRI), noninvasive video-EEG monitoring, and positron emission tomography (PET) and single-photon emission computed tomography (SPECT) studies (2). Surface interictal and ictal EEG recordings remain an essential element of the presurgical evaluation in patients with MTLE-HS to demonstrate the presence of unilateral epileptogenesis. Notably, the definition of the seizure-onset zone by surface ictal EEG generally provides an accurate estimation of the epileptogenic zone, defined as the area of cortex necessary and sufficient for the generation of clinical seizures (3).

However, in ∼30% of MTLE-HS patients, scalp-sphenoidal EEG recordings fail to demonstrate an unambiguous unilateral ictal onset, showing contralateral, bitemporal independent, and nonlateralized ictal onsets, or the surface EEG recordings are not interpretable because of movement artifacts (4,5). Conversely, a bilateral scalp onset is still compatible with a unilateral mesial temporal onset and should not deter further surgical assessment (6).

When noninvasive studies remain nonconcordant or uncertain regarding the localization of seizure onset, invasive studies such as those with depth electrodes may be needed (7). Nevertheless, the proportion of patients evaluated with depth electrodes has decreased over the last decade, because of our increasing ability to localize epileptogenic lesions such as HS with high-resolution MRI, and because invasive electrodes carry considerable costs and risks of complications (3).

To record from the mesiobasal aspect of the temporal lobe, Wieser et al. (8–10) developed a subdural electrode inserted through the foramen ovale (FO). This procedure is safe and can be an alternative to invasive implantation of depth electrodes in MTLE patients who are candidates for temporal lobectomy.

Here we describe a series of patients with MTLE-HS submitted to a progressive presurgical investigation with scalp sphenoidal, followed by FO and depth temporal electrodes when necessary. Our findings agreed with previous descriptions showing that, in patients whose surface EEG fails to demonstrate an unequivocal unilateral ictal onset, FO might provide relevant and sufficient information to give an indication for resective surgery.

METHODS

  1. Top of page
  2. Abstract
  3. METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgments
  7. REFERENCES

Subjects

Patients with suspected MTLE-HS evaluated at the Ribeirão Preto Epilepsy Surgery Center at University of São Paulo School of Medicine, between January 1996 and June 2004, were included in the study. The presurgical protocol was approved by our University Hospital Ethics Committee, and an informed consent was obtained from all subjects.

Phase I investigation for epilepsy surgery consisted of an assessment made by a neurologist with expertise in epileptology, structural and functional neuroimaging, neuropsychological examination, and scalp-sphenoidal video-EEG monitoring.

The decision to implant FO was based on the results of the phase I investigation. Patients with a clear hypothesis regarding the location of the epileptogenic zone in mesial temporal lobes, but whose surface EEGs failed to demonstrate unilateral ictal onsets, were submitted to investigation with FO. When implanted FO also failed to demonstrate an unambiguous unilateral ictal onset, patients were further evaluated with depth temporal electrodes.

The inclusion criteria were (a) medical history and seizure semiology consistent with intractable MTLE, usually with epigastric, autonomic, or psychic auras, followed by behavioral arrest, progressive clouding of consciousness, oroalimentary and manual automatisms, and autonomic phenomena; (b) no other lesion than the presence of atrophy or hippocampal signal changes at high-resolution MRI; and (c) ictal EEG with bitemporal independent ictal EEG onsets, nonlateralized ictal onsets, or ictal onsets initiating contralateral to the temporal lobe with focal abnormalities detected on high-resolution MRI.

Vídeo-EEG monitoring

Video-EEG analysis

EEG signals were obtained by using a digital video-EEG system (Vangard Systems, Cleveland Clinic Foundation, Cleveland, OH, U.S.A.). Surface electrodes were placed over the scalp according to the international 10–20 system, added by temporal electrodes positioned according to the “10–10 system” plus bilaterally placed sphenoidal electrodes. At least two events similar to the patient's habitual seizures were recorded.

Interictal spikes

The frequency, lateralization ratio, and localization of interictal spikes (ISs) were visually assessed by board-certified electroencephalographers. For the analysis of ISs, 5-min EEG samples were collected every hour, 24 h/day. Spikes and sharp waves were defined according to the International Federation of Clinical Neurophysiology guidelines.

Ictal-onset zone

The ictal-onset zone (IOZ) was independently assessed on ictal video-EEG by two investigators, and when the results were discordant, they were reviewed together to achieve agreement about the localization and lateralization of seizure onset.

Foramen ovale electrodes insertion

Commercially available FOs (AdTech) with four contacts at 5-mm intervals were implanted percutaneously with the aid of a fluoroscope under light general anesthesia. Electrodes were positioned in such way that the tip (contact 1) was located at the end of the ambient cistern, with contact 4 placed just above the level of the foramen ovale. Immediately after the procedure, a skull radiograph was taken to confirm whether the FO implantation positions were adequate and bilaterally symmetrical.

MRI-guided stereotactic depth electrode implantation

A surgical plan based on an entry and target points on axial and sagittal images was defined for the insertion of depth electrodes. Navigational views, using three-planar images, were performed to determine which structures the electrodes would pass through to be correctly placed in the amygdala and hippocampus. The correct site of depth electrode implantation was confirmed by MRI.

Neuroimaging

Neuroimaging studies included high-resolution MRI (1.5-T Siemens Magneton Vision, Erlangen, Germany) with special protocols for epilepsy and interictal and ictal SPECT. Based on visual analysis of MRI, the neuroradiologists classified hippocampal sclerosis as (a) unilateral, when hippocampal atrophy (on T1-weighted 1-mm isotropic-voxel SPGR sequence) or increased signal (on T2-weighted sequences: turbo-spin echo and fluid-attenuated inversion recovery sequences) were observed in one side; or (b) bilateral, when the hippocampal changes were observed on both sides.

If the abnormality was increased signal intensity without hippocampal atrophy, the radiologists did not classify it as HS. However, increased hippocampal signal intensities were considered abnormal for the lateralization of neuroimaging features and for the correlation with ictal studies.

Surgical outcome was defined according to the classification proposed by Engel (11).

Statistical analysis

The χ2 test or Fisher's exact test was used to establish correlation between categoric variables. A t test or Mann–Whitney test was used to analyze numeric variables, such as age at seizure onset, age, or epilepsy duration.

RESULTS

  1. Top of page
  2. Abstract
  3. METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgments
  7. REFERENCES

Clinical and demographic data

The clinical, demographic, MRI, and neurophysiologic data are summarized in Table 1. Between 1996 and 2004, 65 patients were submitted to evaluation with FO and were included in the analysis: 35 female (53.8%) and 30 male patients (46.2%). The mean age at enrollment was 37.8 ± 10.1 years (range, 12–59 years). The mean age at epilepsy onset was 12.2 ± 6.9 years (range, 1–36 years). The epilepsy duration was 25.5 years ± 9.8 years (range, 4–45 years). The mean seizure frequency before surgery was 6.8 ± 7.5 seizures per month. Thirty-five (53.8%) patients had initial precipitant insults (IPIs), and prolonged febrile seizure was the most common type of IPI (60%). The mean age at IPI was 3.2 ± 4.7 years (range, 1–28 years).

Table 1. Demographic, clinical, MR imaging, and neurophysiologic data of TLE patients submitted to FO evaluation
Patient nAge /SexAge at onsetEpilepsy durationIPIType of IPIMRI resultsSeizure lateralization during surface EEGFO (ictal onsets)Procedure after FO evaluationDepth electrodes resultsPostsurgery outcome (Engel)
  1. HS, hippocampal sclerosis; prol, probable.

 133/F 231No-Left HSIndependent bilateralBilateralWaiting depth electrodes--
 243/F 736No-Right HSLeft (contralateral)RightWaiting depth electrodes--
 335/M26 9YesProl febrile seizureBilateral > leftIndependent bilateralLeftLeft temporal lobectomy-I
 440/F 832YesProl febrile seizureRight HSIndependent bilateralRightRight temporal lobectomy-I
 523/M 716YesProl febrile seizureBilateral > rightLeft (contralateral)RightRight temporal lobectomy-I
 625/M1114No-Left HSRight (contralateral)LeftLeft temporal lobectomy-I
 728/M 820No-Right HSNonlateralizedRightRight temporal lobectomy--
 853/F1439No-Right HSIndependent bilateralBilateralWaiting depth electrodes--
 938/F1820No-Right HSIndependent bilateralBilateralDepth electrodesBilateralDenied surgery
1053/F1241No-Bilateral symmetricIndependent bilateralBilateralWaiting depth electrodes--
1119/M 910YesProl febrile seizureBilateral > rightLeft (contralateral)RightRight temporal lobectomy-III
1222/M 715YesProl febrile seizureBilateral > rightLeft (contralateral)LeftWaiting depth electrodes--
1319/F 217YesProl febrile seizureRight HSLeft (contralateral)RightRight temporal lobectomy-I
1448/F 939No-Right HSNonlateralizedRightRight temporal lobectomy-I
1532/F1121YesMeningitisBilateral > leftRight (contralateral)LeftLeft temporal lobectomy-I
1639/F1128No-Right HSLeft (contralateral)RightRight temporal lobectomy-I
1741/M1625No-Bilateral > leftNonlateralizedLeftLeft temporal lobectomy--
1834/F 727No-Left HSNonlateralizedLeftLeft temporal lobectomy-IV
1936/M 432No-Bilateral > leftIndependent bilateralBilateralDepth electrodesBilateralDenied surgery
2039/M2019No-Bilateral > rightLeft (contralateral)BilateralWaiting depth electrodes--
2148/F 840No-Mild left hypersignalRight (contralateral)LeftRefused surgery--
2235/F 926No-Left HSIndependent bilateralBilateralWaiting depth electrodes--
2346/F2026No-Bilateral > leftIndependent bilateralLeftLeft temporal lobectomy-I
2443/F1231No-Bilateral > rightNonlateralizedRightRefused surgery--
2535/F1223YesProl febrile seizureRight HSIndependent bilateralLeftDepth electrodesBilateralDenied surgery
2612/F 210YesProl febrile seizureLeft HSIndependent bilateralBilateralWaiting depth electrodes--
2737/M1423YesProl febrile seizureLeft HSIndependent bilateralLeftLeft temporal lobectomy-I
2845/M 738YesProl febrile seizureBilateral symmetricIndependent bilateralRightRefused surgery--
2938/F1127YesMeningitisBilateral > leftNonlateralizedLeftLeft temporal lobectomy-III
3059/M1544YesMeningitisBilateral > rightLeft (contralateral)LeftWaiting WADA test--
3132/F 626YesStatus epilepticusLeft HSRight (contralateral)LeftLeft temporal lobectomy-III
3235/F287YesStatus epilepticusBilateral > leftIndependent bilateralLeftRefused surgery--
3348/F2028No-Bilateral > rightNonlateralizedRightRight temporal lobectomy-I
3454/M 945No-Bilateral > leftIndependent bilateralBilateralLeft temporal lobectomy-III
3551/M2229No-Right HSLeft (contralateral)BilateralRefused surgery--
3645/M1233YesStatus epilepticusLeft HSIndependent bilateralBilateralDepth electrodesBilateralDenied surgery
3737/M1423No-Bilateral > leftRight (contralateral)BilateralWaiting depth electrodes--
3829/M21 8YesProl febrile seizureBilateral > rightNonlateralizedRightRight temporal lobectomy-I
3925/F1411YesMeningitisBilateral > leftIndependent bilateralBilateralLeft temporal lobectomy-III
4028/M1216YesProl febrile seizureRight HSLeft (contralateral)RightRight temporal lobectomy-I
4138/M 731YesProl febrile seizureRight HSLeft (contralateral)RightRight temporal lobectomy-I
4245/F1035YesProl febrile seizureRight HSLeft (contralateral)RightRight temporal lobectomy-I
4357/F3621YesProl febrile seizureBilateral > rightLeft (contralateral)LeftWaiting depth electrodes--
4445/F1233YesProl febrile seizureLeft HSRight (contralateral)BilateralWaiting depth electrodes--
4537/F1819No-Right HSIndependent bilateralLeftWaiting depth electrodes--
4615/M11 4YesProl febrile seizureLeft HSNonlateralizedBilateralLeft temporal lobectomy-I
4744/F1232No-Bilateral symmetricNonlateralizedRightRight temporal lobectomy-I
4836/M1521YesProl febrile seizureBilateral > leftIndependent bilateralLeftRisk of memory deficit--
4950/F1238No-Right HSIndependent bilateralBilateralRisk of memory deficit--
5047/F1334YesStatus epilepticusMild bilateral hypersignalNonlateralizedRightRight temporal lobectomy-III
5143/F1132YesProl febrile seizureBilateral symmetricIndependent bilateralBilateralWaiting depth electrodes--
5239/F1524YesProl febrile seizureRight HSNonlateralizedRightRight temporal lobectomy-I
5325/M 718YesProl febrile seizureRight HSNonlateralizedRightRight temporal lobectomy-I
5436/M1917No-Left HSRight (contralateral)RightWaiting depth electrodes--
5538/M 137YesStatus epilepticusBilateral > leftIndependent bilateralLeftLeft temporal lobectomy-I
5642/M1230No-Left HSNonlateralizedLeftLeft temporal lobectomy-I
5748/M2226No-Bilateral > rightLeft (contralateral)LeftWaiting depth electrodes--
5844/M3014No-Mild bilateral hypersignalIndependent bilateralBilateralWaiting depth electrodes--
5946/M 541YesProl febrile seizureLeft HSRight (contralateral)RightRisk of memory deficit-Denied surgery
6041/F1922YesStatus epilepticusLeft HSIndependent bilateralLeftLeft temporal lobectomy-II
6130/F 327YesMeningitisLeft HSIndependent bilateralLeftRefused surgery--
6235/M1421YesBrain traumaBilateral > leftRight (contralateral)BilateralDepth electrodesBilateralDenied surgery
6324/F 717YesCerebral abscessBilateral > rightNonlateralizedBilateralWaiting surgery--
6446/F 640No-Bilateral > rightIndependent bilateralBilateralRight temporal lobectomy-IV
6524/M 420No-Right HSNonlateralizedRightRight temporal lobectomy-I

MRI findings

Thirty-one (47.6%) had bilateral abnormalities, 25 with bilateral asymmetrical and six with bilateral symmetrical abnormalities. Thirty-four patients had unilateral MRI findings: 18 (27.7%) patients had right HS, 15 (26.2%) patients had left HS, and mild left increased hippocampus signal intensity without hippocampal atrophy was found in one (1.5%) patient.

EEG data

The mean duration of video-EEG monitoring (VEEG) with scalp-sphenoidal electrodes was 6.0 ± 2 days (range, 2–13 days). The median of recorded seizures was five seizures (range, 2–17 seizures). The most frequent reason for FO implantation was independent bilateral seizures revealed by surface EEG in 26 (40.0%) patients, followed by surface EEG onsets contralateral to the side of hippocampal atrophy in 23 (35.4%) patients, and nonlateralized ictal discharge onsets in 16 (24.6%) patients. In the nonlateralized group, eight (50%) patients had bilateral HS.

FO evaluation revealed unilateral EEG onsets ipsilateral to the side of HS in 19 patients with unilateral HS and ipsilateral to the side of the more intense HS in 14 patients with bilateral asymmetrical HS.

In the nonlateralized group by surface EEG, 14 (87.5%) of 16 patients had lateralized EEGs during FO evaluation. In the group with contralateral surface EEG onsets, the proportion of patients with lateralized EEGs was 52.2% (12 of 23 patients). These groups had a greater chance of lateralization with FO when compared with the group with bilateral independent seizures on surface EEG (34.6%, nine of 26; p < 0.01). In eight patients, the FO EEG onsets were unilateral but contralateral to the side of HS, and depth electrodes were indicated.

In relation to the lateralization of HS, 10 (32.2%) of 31 patients with bilateral HS revealed bilateral EEG onsets during FO recording, and 10 (29.41%) of 34 patients with unilateral HS had bilateral EEG onsets (p = 0.66, Fisher's Exact test).

Five patients were submitted to implantation of depth temporal electrodes after FO video-EEG monitoring. The indications for depth electrodes were bilateral EEG onsets (four patients) and seizures contralateral to the side of HS (one patient) revealed during FO evaluation. The depth-electrode evaluation results yielded findings very similar to the results of FO VEEG monitoring in all patients, and the surgery was refused. Fifteen (23%) patients who had bilateral or contralateral EEG onsets on FO recordings are currently waiting for depth-electrode evaluation.

In one patient, the FO electrode had bilateral independent EEG onsets and depth electrodes were added, allowing simultaneous FO and depth-electrode recordings. MR imaging of implanted electrodes revealed that the FO electrodes were in close relation to the parahippocampal gyrus (Fig. 1B and C). The EEG recordings in this patient revealed that the time of EEG onsets in FO electrodes were within 0.3 to 1.7 s apart from the EEG onsets in depth hippocampal electrodes (Fig. 2A).

imageimageimage

Figure 1. A: Radiography from skull of patient 29 showing symmetrical bilateral positioning of foramen ovale (FO) electrodes. Coronal (B) T1 and sagittal (C) magnetic resonance imaging images showing the position of depth (arrowheads) and FO electrodes (arrows).

imageimageimage

Figure 2. A: Simultaneous foramen ovale (FO) (FO1 to FO8) and depth-electrode recordings from anterior hippocampus (AH1 to AH10) of patient 29, showing a right temporal lobe seizure EEG onset in AH2 and AH4 (black arrow), apart only 0.3 s away from FO2 and FO4 EEG onset (white arrow). B, C: Progression of seizure 10 and 30 s after the seizure onset.

Complications

The complications related to FO implantation were transitory, as follows: (a) temporary facial pain (12 patients); (b) hypoesthesia in trigeminal territory (three patients); (c) temporomandibular joint dysfunction (two patients); (d) recurrence of labial herpes (two patients); (e) retromandibular hematoma (one patient); and (f) transient complete atrioventricular block induced by FO insertion, despite premedication with atropine (one patient). In three patients, the insertion of FO was difficult, and the recordings revealed asymmetry of the background EEG.

Postsurgical data

In 31 (47.7%) patients, the results of FO revealed unilateral EEG onsets, and temporal lobectomy was performed. Two additional patients with >90% of seizures originating from the side of unilateral HS underwent temporal lobectomy. Twenty-three (70%) of 33 patients had good postsurgical outcome after temporal lobectomy (Engel classes I and II). The proportion of patients with Engel I seizure outcome was 80% in patients with unilateral HS in comparison with 53.8% in patients with bilateral HS (p = 0.05). In all patients who underwent temporal lobectomy, pathologic examination of the resected temporal tissue revealed severe neuronal loss and gliosis in the CA1 and CA4 regions, prosubiculum, and hilus, and discrete or moderate neuronal loss of CA2 region and fascia dentata granule cells.

Six patients refused the procedure, and three other patients with bilateral HS had the surgery contraindicated because of risk of considerable memory deficits revealed by intracarotid amobarbital memory testing.

DISCUSSION

  1. Top of page
  2. Abstract
  3. METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgments
  7. REFERENCES

Available data from autopsy and surgical studies suggest that patients with temporal lobe epilepsy frequently have bilateral hippocampal damage (12,13). However, HS is usually asymmetrical and, when preoperative evaluation data are concordant with the side of hippocampal atrophy, temporal lobectomy can be indicated, and postsurgery outcome is usually good (1). Clinical decision making is more complicated when neurophysiologic and neuroimaging data indicate bilateral involvement of mesial structures (1,3). Although data from the present series indicate frequent bilateral involvement of mesial structures, we found evidence that FO evaluation provide accurate neurophysiologic data about lateralization of seizures that were not clearly lateralized by surface EEGs.

In other words, despite the hypothetically poor postsurgery outcome suggested by bilateral surface EEG onsets and the high rate of patients with bilateral HS, FO evaluation substantially affected the presurgical evaluation, indicating the side of temporal lobectomy in two thirds of these MTLE patients. It is important to emphasize that this proportion was similar in patients with bilateral and unilateral HS revealed by MRI.

The signal-to-noise ratio of FO is better than that in the scalp-sphenoidal electrode recordings (7–10). Therefore many electrophysiologic events with lateralizing value are detected by FO but remain undetected by scalp-sphenoidal contacts (14,15). In our series, this permitted the indication of temporal lobectomy in 60% of cases that were not lateralized by scalp-sphenoidal electrodes, with the great advantages of being nontraumatic to the brain and of carrying much less risk for the patient than the more-invasive depth electrodes. Moreover, even in a sample of patients with bilateral HS on MRI and apparent bilateral surface ictal EEG onsets, 70% of the patients had good postsurgical outcome after temporal lobectomy, provided that unilateral EEG onsets were defined by FO. This proportion is very similar to previous descriptions of patients with MTLE (1,10,11).

It should be stressed, however, that the FO recording technique addresses only specific questions: if the seizures originate in the mesiobasal temporal lobe structures and if they are consistently lateralized. In other words, a clear hypothesis should exist regarding the location of the epileptogenic zone, derived from noninvasive studies. In previous descriptions of FO, it has been stated that, in comparison to the presurgical examination using intracerebral depth recordings, the information gained by FO electrode recording is limited, and that the FO technique cannot substitute for a proper depth-electrode evaluation (9). However, this conclusion was drawn before the recent advances of neuroimaging. The advent of high-resolution MRI has allowed the proper selection of patients that might benefit from FO recordings, namely MTLE patients, excluding those patients with epileptogenic lesions outside the mesiobasal structures.

In all the five patients in whom the result of FO electrodes showed bilateral independent or nonlateralized ictal onsets, further recordings with depth electrodes confirmed the findings. This can be explained by the evidence of the intimate relation of the properly placed FO electrode with the parahippocampal gyrus, uncus, and lingual gyrus (Fig. 1C), and by the good correlation between the ictal onsets in FO and depth electrodes (Fig. 2A).

In conclusion, our results indicate that, in properly selected patients, FO is a reliable method for lateralization of seizures that are not clearly recorded by surface EEGs, usually providing sufficient information to indicate epilepsy surgery. In addition, FO implantation is relatively simple, well tolerated, and can substantially facilitate the presurgical evaluation of patients who are candidates for temporal lobectomy surgery by decreasing the risks of invasive neurophysiologic evaluation without excessive loss of information.

Acknowledgments

  1. Top of page
  2. Abstract
  3. METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgments
  7. REFERENCES

Acknowledgment:  This work was supported by FAPESP/CINAPCE Project 0556447-7. Roger Walz was supported by CNPq (472840/2004-5 and 301379/2005-0). Marino M. Bianchin was supported by FAPESD Project (02103743-0).

REFERENCES

  1. Top of page
  2. Abstract
  3. METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgments
  7. REFERENCES
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