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Risk Factors for Infective Complications with Long-Term Subdural Electrode Implantation in Patients with Medically Intractable Partial Epilepsy
Original Article
Risk Factors for Infective Complications with Long-Term Subdural Electrode Implantation in Patients with Medically Intractable Partial Epilepsy Sumiya Shibata1, Takeharu Kunieda1, Rika Inano1, Masahiro Sawada1, Yukihiro Yamao1, Takayuki Kikuchi1, Riki Matsumoto2, Akio Ikeda2, Ryosuke Takahashi3, Nobuhiro Mikuni4, Jun Takahashi5, Susumu Miyamoto1
OBJECTIVE: To evaluate infective complications with intracranial electroencephalography (EEG) recording so as to lessen them.
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METHODS: A database of intracranial monitoring cases with subdural electrodes at Kyoto University Hospital between May 1992 and March 2012 was retrospectively reviewed.
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RESULTS: This analysis included 46 EEG monitoring sessions. Infective complications related to intracranial electrodes occurred in 4 monitoring sessions (8.7%; 3 male patients). Causative agents were identified as Staphylococcus aureus in 3 monitoring sessions and Staphylococcus epidermidis in 1 session. In univariate analysis, the season of monitoring was identified as the sole significant risk factor. More infective complications occurred when monitoring occurred in autumn. More infective complications tended to occur in patients who had implantation in the right side or discontinuation of intravenously administered prophylactic antibiotics, although these factors were not statistically significant. Age, sex, duration of monitoring, number of electrodes, and pathologic diagnosis did not seem to be associated with an increased risk of infective complications. Infective complications had no significant influence on seizure outcome.
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CONCLUSIONS: Invasive EEG monitoring during autumn might be a risk factor in terms of infective complications. S aureus was a common pathogen.
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INTRODUCTION
A
lthough intracranial electroencephalography (EEG) monitoring has greater sensitivity and spatial specificity than scalp EEG, it also has some shortcomings (38). One shortcoming is that intracranial EEG monitoring is associated with neurosurgical procedures. Implantation of subdural grid electrodes inevitably accompanies a craniotomy. Insertion of depth electrodes requires not only trephination of the skull but also penetration of the cerebral parenchyma. As a result, intracranial EEG monitoring is associated with morbidity and mortality (11, 27, 34, 42). Minor complications such as headache, nausea, and transiently increased temperature and more serious complications such as infections, postoperative epidural or subdural hematoma, cerebrospinal fluid (CSF) collection, increased intracranial pressure, cortical contusion, CSF leakage, and brain herniation have been previously reported (7). Among these complications, postoperative infection is one of the most severe (15, 18, 24). The development of central nervous system infection after a neurosurgical procedure represents a significant threat and requires immediate medical and possibly surgical intervention (20). Postoperative nosocomial infection was associated with increased postoperative length of stay, increased costs, and increased hospital readmission rate (14). Clarifying the risk factors directly associated with these infective complications is essential. We conducted a clinical study of infective complications with the goals to reduce further complications from long-term intracranial electrode implantation and to improve the safety of invasive evaluation of epilepsy surgery. MATERIALS AND METHODS This study was approved by the Ethics Committee at Kyoto University Graduate School and Faculty of Medicine (E2102). We
Neurosurgery, Sapporo Medical University Graduate School of Medicine, Hokkaido; and Center for iPS Cell Research and Application, Kyoto University, Kyoto, Japan
Key words Epilepsy - Implanted electrode - Infection - Risk factors
5
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To whom correspondence should be addressed: Takeharu Kunieda, M.D., Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2015) 84, 2:320-326. http://dx.doi.org/10.1016/j.wneu.2015.03.048
Abbreviations and Acronyms CSF: Cerebrospinal fluid EEG: Electroencephalography
Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2015 Elsevier Inc. All rights reserved.
From the Departments of 1Neurosurgery, 2Epilepsy, Movement Disorders and Physiology, and 3 Neurology, Kyoto University Graduate School of Medicine, Kyoto; 4Department of
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performed a retrospective review of a database of patients who had undergone epilepsy surgery at Kyoto University Hospital between May 1992 and March 2012. We identified 49 patients who had undergone 53 invasive monitoring sessions. One patient died 2 days after the resection surgery of acute myocardial infarction. Because the death was unrelated to the neurosurgical procedure, this patient was excluded from the analysis. All patients required intracranial monitoring because they were candidates for epilepsy surgery, and results of noninvasive monitoring did not reveal sufficient localizing information to delineate a resection procedure. The number and location of the intracranial electrodes to be implanted were carefully determined for each individual with reference to the noninvasive evaluation. For electrode implantation, 2 different types of platinum subdural strip and grid electrodes provided by 2 different manufacturers (Ad-Tech Medical Instrument Corporation, Racine, Wisconsin, USA, and Unique Medical Co., Ltd., Tokyo, Japan) were used. In 5 of the monitoring sessions, depth electrodes were used in addition to either subdural electrodes or cavernous sinus electrodes (16, 23). In 1 other monitoring session, only epidural electrodes were used. These 6 sessions using other types of electrodes together with or instead of the subdural type were excluded from the analysis because of the small number of cases. The monitoring sessions with depth electrodes, epidural electrodes, or cavernous sinus electrodes had no infective complications at all. The analysis included 46 monitoring sessions (26 of which involved male patients). All patients underwent general anesthesia for the subdural grid or strip electrode implantation surgery. In the first stage of surgery, a skin incision and wide craniotomy and cranioplasty were performed to create an operative field large enough to expose the appropriate cortical areas for electrode coverage. Most subdural electrodes were placed under direct visualization to avoid any damage to bridging veins or other cerebral cortex and vascular structures. In some cases, additional smaller grid or strip electrodes were slid over the brain without direct visualization. The cables of the electrodes were kept in a bundle. The dura mater was closed with an artificial dural patch in 25 sessions and primarily or with an autograft (without an artificial dura mater) in 19 sessions (data were unavailable in 2 sessions). When the electrode leads were exfiltrated through the dura mater to the outside, 2 techniques were used to fix the leads tightly to the dura mater and to prevent any damage (kinking, direct injury) to them. In some cases, small lateral slits were made off of the main incision (with suturing between the electrode leads and the main incision). In other cases, a small section of the dura mater along the main incision was raised slightly or pinched, creating a “tunnel” through which the electrode lead was fed and sutured in place. The bone flap was fixed back temporarily. The cables were tunneled >1 cm away from the initial skin incision line for each lead. Data on the use of prophylactic antibiotics were available in 45 of 46 analyzed monitoring sessions. In 35 of the monitoring sessions, prophylactic antibiotics were administered intravenously not only during the operation but also throughout the monitoring period. In 10 of the monitoring sessions, prophylactic intravenous administration of antibiotics was interrupted, with prophylactic antibiotics discontinued completely in 5 of these monitoring sessions and administered orally for some period in the other 5 sessions.
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INFECTIVE COMPLICATIONS WITH INTRACRANIAL EEG RECORDING
After sufficient EEG monitoring, data were obtained along with determination of the regions of epileptogenesis and functional mapping of eloquent cortical areas, the subdural electrodes were removed, and the planned resection was performed as the second surgical treatment. The following demographic data and monitoring variables were recorded (Table 1): age at surgery, sex, duration of invasive monitoring, season of monitoring, side of electrode implantation, number of electrode contacts, cumulative number of electrode contacts (number of electrode contacts multiplied by days of invasive monitoring), intravenous administration of antibiotics throughout the invasive monitoring period, pathologic diagnosis (hippocampal sclerosis was diagnosed with preoperative magnetic resonance imaging in some cases), state of associated infections, and seizure outcome. Because 1 patient had 40 contacts in the first 2 days and 60 contacts in the last 5 days, his number of electrode contacts was calculated as 54 [(40 2 þ 60 5)/7]. Seizure outcome data were obtained from clinical visits. These data were obtained 13e243 months after surgery (mean 100 months). The outcomes of postoperative seizure control were categorized as either “good” (class I) or “not good” (classes
Table 1. Demographic Data and Monitoring Variables Sex (monitoring sessions): male/female Age at surgery (years) (mean SD)
26/20 26.5 7.2
Side of electrode implantation (monitoring sessions): right/left/bilateral
20/25/1
Number of electrode contacts (mean SD)
50 20
Duration of invasive monitoring (days) (mean SD) Cumulated number of electrode contacts (contacts $ days) (mean SD)
11 4 567 329
Season of monitoring (monitoring sessions) MarcheMay (spring)
12
JuneeAugust (summer)
14
SeptembereNovember (autumn) DecembereFebruary (winter)
9 11
Pathologic diagnosis (monitoring sessions)* BT
6
CD
24
HS
7
Others
14
Seizure outcome (patients) I
21
II
4
III
18
IV
0
BT, brain tumor; CD, cortical dysplasia; HS, hippocampal sclerosis. *Some patients had >1 pathologic finding. The pathologic finding of 1 patient was unknown.
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IIeIV) according to the Engel classification system (6). An exception to the Engel classification system was our minimum follow-up period of 13 months rather than 24 months. All the analyses but the calculation of q value were conducted by JMP Pro 11.0 (SAS Institute, Cary, North Carolina, USA). Pearson c2 or Fisher exact test as appropriate was used to test for association between categorical variables and the presence of complications. Wilcoxon test was used to assess associations between continuous variables and the presence of complications. To correct for multiple comparisons and false discovery rate (3), q value was calculated. Statistical significance was adopted as P value < 0.05 and q value < 0.3. Because the number of events was small (4 sessions with infective complications) and 1 of the sessions with infective complications had no data on the administration of antibiotics, we did not perform multivariate analysis.
RESULTS The present analysis included 46 monitoring sessions (26 of which involved male patients) (Table 1). The mean age of the patients at surgery was 26.5 years 7.2 (mean SD). Electrodes were placed over the right hemisphere in 20 monitoring sessions, the left hemisphere in 25 monitoring sessions, and both hemispheres in 1 monitoring session. The mean number of electrode contacts per monitoring session was 50 contacts 20. The mean length of intracranial recording was 11 days 4. The seasonal breakdown of the invasive monitoring procedures was 12 in spring, 14 in summer, 9 in autumn, and 11 in winter. The pathologic findings were brain tumor in 6 cases, cortical dysplasia in 24 cases, hippocampal sclerosis in 7 cases, and “other” in 14 cases. Seizure outcomes were classified as “good” (Engel classification class I) in 21 patients and “not good” (Engel classes IIeIV) in 22 patients. Infective complications related to intracranial electrodes occurred in 4 monitoring sessions (8.7%) (3 of which involved male patients) (Table 2). These 4 cases resulted in removal of the bone flap. Wound cultures revealed Staphylococcus aureus infection in 3 monitoring sessions and Staphylococcus epidermidis infection in 1 monitoring session. These 4 patients were treated with antibiotics and subsequently underwent reconstructive cranioplasty 259, 231, 259, and 197 days after the removal of the bone flap. After cranioplasty, infective complications recurred in 2 cases (Cases 2 and 3). S aureus was isolated in these 2 cases.
Table 2. Clinical Characteristics of 4 Patients Who Had Infective Complications Age at Surgery (years)/Sex
Duration from Surgery to Appearance of Infection (days)
Isolated Microorganisms
1
26/male
33
Staphylococcus aureus
2
25/male
10
S aureus
3
18/male
40
S aureus
4
23/female
45
Staphylococcus epidermidis
Case Number
322
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Table 3 shows the risk factors for infective complication related to intracranial electrodes. In univariate analysis, the only identified risk factor was season of monitoring. More infective complications occurred when monitoring took place in autumn. More infective complications tended to occur in the patients who had implantation in the right side or discontinuation of intravenously administered prophylactic antibiotics, although these factors were not statistically significant. Age, sex, duration of monitoring, number of electrodes, and pathologic diagnosis did not seem to be associated with an increased risk of infective complications. Infective complications had no significant influence on seizure outcome. DISCUSSION In our study, more infective complications occurred when the monitoring took place in autumn (from September to November). S aureus was the most common pathogen identified. S aureus is a human commensal and a frequent cause of clinically important infections. Several past studies showed seasonal variation of S aureus infections with peak occurrences in summer and autumn (10, 17, 22). These studies suggested several factors that explained the seasonality of the infections. The first possible factor is the level of provider training (“the July effect”). The inexperience of new residents could result in worse patient outcomes at the beginning of the academic year (29). However, in Japan, new residents start in April, and so this factor would not explain our finding. The second possible factor is the survival of pathogens (9). Pathogen survival depends partly on the characteristics of the weather such as temperature and humidity. A high-temperature, high-humidity environment promoted bacterial growth on the human skin (19). Nasal carriers of S aureus were shown to have an increased risk of acquiring an infection with this pathogen (40). Because patients are colonized with large numbers of S aureus in seasons with high temperatures and humidity, infections would develop more frequently during hospitalization of patients in that season. However, the influence of this meteorologic element may not be apparent in a hospital with central air conditioning. Our study found higher infection rates during autumn than summer, although generally in Kyoto summer has the highest temperature and humidity in a year. A previous study of nasopharyngeal bacterial flora (12) revealed that S aureus tended to be more common in the autumn and winter months. This trend correlated with the peak of viral respiratory infections. Another study in Japan (32), which investigated the bacterial dispersion from the surface of the human body, determined that the sum of airborne S aureus and coagulasenegative staphylococci in an operating room in a year was the largest in autumn, although the total number of airborne bacteria was the largest in summer in a year. From the results of these 2 studies, airborne transmission of S aureus may increase during autumn. S aureus acquired from an external source could cause infection (17). The infection by airborne S aureus could partially explain our result. We also found that there were more infective complications in the patients who had implantation in the right side or discontinuation of intravenously administered prophylactic antibiotics,
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Table 3. Risk Factors for Infective Complications
Sex (male/female) (monitoring sessions) Age at surgery (years) (mean SD)
No Infection
Infection
23/19
3/1
P Value
q Value
0.44
0.87
26.8 7.4
23.0 3.6
0.27
0.66
Side of electrode implantation (right/left/bilateral) (monitoring sessions)
16/25/1
4/0/0
0.08*
0.32*
Number of electrode contacts (mean SD)
50 20
47 20
0.70
11 4
12 4
> 0.99
> 0.99
566 330
580 375
0.86
> 0.99
Duration of invasive monitoring (days) (mean SD) Cumulated number of electrode contacts (contacts $ days) (mean SD) Season of monitoring (monitoring sessions) MarcheMay (spring)
11
1
JuneeAugust (summer)
14
0
SeptembereNovember (autumn)
6
3
11
0
34
1
8
2
BT
3
1
CD
17
2
BT and CD
2
0
CD and HS
1
0
CD and others
2
0
HS
5
0
HS and others
1
0
10
1
DecembereFebruary (winter) z
Antibiotics intravenously administered (monitoring sessions) Full coverage Partial coverage x
Pathologic findings (monitoring sessions)
Others Outcome of epilepsy surgery (patients)k I
18
3
IIeIV
21
1
> 0.99
0.02y
0.29y
0.06*
0.32*
0.80
> 0.99
0.27
0.66
The values noted in the footnotes y are significant. Those noted in the footnotes * are insignificant but close to the significance level. BT, brain tumor; CD, cortical dysplasia; HS, hippocampal sclerosis. *< 0.1 for P values; < 0.5 for q values. y< 0.05 for P values; < 0.3 for q values. zIn 1 monitoring session, there were no data on the use of prophylactic antibiotics. xThe pathologic findings of 1 patient were unknown. k1 patient who had an infective complication in 1 of 3 monitoring sessions was counted as an “infection” patient.
although these factors were not statistically significant. Few studies reported the site of implantation as a risk factor for complications. Hamer et al. (11) reported that left-sided grid insertion was associated with neurologic deficits. They suggested that the dominant left hemisphere might be more sensitive to neurologic deficits compared with the nondominant right hemisphere. Wong et al. (42) reported that right central surface implantation was associated with neurologic deficits. They suggested that the central region is responsible for important motor and sensory function and might be sensitive to trauma.
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They did not indicate why right-side implantation should increase risk. The use of antibiotics to prevent postoperative infection is a matter of debate (18). Wyler et al. (43) reported that the absence of antibiotics during monitoring did not correlate with the infection rate. In their series, only strip electrodes were implanted through burr holes, without any craniotomies (7). Barker (1) reviewed 6 prospective randomized trials in general neurosurgery and showed that prophylactic antibiotics reduced the rate of postoperative meningitis. The duration of antibiotic prophylaxis is
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also a matter of debate. The prolonged use of antibiotics could increase the likelihood of colonization or infection with antibioticresistant bacteria (21). Blauwblomme et al. (4) reported the infection rate (14.9%) related to invasive recording when they gave prophylactic antibiotics only at the induction of anesthesia. Because the centers using antibiotics throughout the EEG recording period had lower infection rates (2.4%e8.57%) than Blauwblomme et al. (4), they discussed the duration of antibiotic prophylaxis with their infectious disease team. The use of antibiotic prophylaxis should be studied further, especially in neurosurgical procedures in which a foreign body communicating outside the body, such as an electrode, is inserted. In our study, age, sex, duration of monitoring, number of electrode contacts, cumulative number of electrode contacts, and pathologic diagnosis did not seem to be associated with an increased risk of infective complications. In several previous studies, complications occurred in association with a larger number of electrodes (11, 33, 41, 42), longer duration of monitoring (11, 41), and older patient age (11). This difference might be explained by the difference in analytic methodology. First, we evaluated only infective complications. Previously cited studies evaluated all complications, including neurologic deficit, infection, bleeding, CSF leakage, and cerebral edema (11, 27, 33, 41, 42). Because subdural electrodes cause a mass effect on the brain (13), a larger number of electrodes might increase the intracranial pressure and cause several neurologic symptoms. Mild neurologic disturbances could be noticed more reliably in self-reporting adults compared with children (11). Musleh et al. (25) reported that duration of grid placement, number of electrodes, and number of exit wires did not increase the risk of infective complications. The results of other past studies might be influenced by complications other than infection. Second, we excluded depth electrodes because only 5 monitoring sessions used those electrodes. Intracranial hemorrhage was the most significant complication associated with the placement of stereotactic intracerebral electrodes (31). The results of past studies also might be influenced by complications related to depth electrodes. As another risk factor, Musleh et al. (25) suggested an increase in the rate of infection with grid reimplantation. Case 4 in our study underwent subdural electrode reimplantation, and the delay in wound healing caused postoperative infections. Although we did not perform a statistical analysis with respect to the reimplantation and infective complications because of the limited number of patients undergoing reimplantation, this procedure might influence the prevalence of postoperative infections caused by delayed wound healing. Careful postoperative wound management should be required in the case of reimplantation. Hydrocolloid dressings that maintain a moist environment might be useful in promoting wound healing (8). In general, CSF leakage is a risk factor associated with infections in neurosurgery (18). Watertight closure of the dura mater without tension is not always possible because of the additional intracranial volume of electrodes themselves and the cables of the electrodes passing through the dural closure, which might lead to CSF leakage. In our series, Cases 2 and 3 had CSF leakage. To minimize CSF leakage, it is necessary to close the incision of the dura mater with great care and to tunnel electrodes far away from the point of pial entrance. A previous
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study reported the insertion of a lumbar drain and drainage of CSF as an additional method for preventing CSF leakage (39). However, the efficacy of drainage of CSF in reducing the infective complication remains to be studied. In the present series, S aureus was isolated in 3 cases (75%). Staphylococcus is a common pathogen found in intracranial electrode implantation (11, 37, 43) and in other types of neurosurgery (15, 18). Our results from wound culture were similar to past reports. The mean time between surgery and the onset of infection was 32 days 15. Past studies reported the mean time was 21 days 31 for electrode implantation (37) and 18 days 25 for all types of neurosurgery (15). In the present study, osteomyelitis was identified in 2 cases (Cases 1 and 3), and meningoencephalitis was identified in 2 cases (Cases 2 and 4). These were deep wound infections. Superficial scalp infections tend to occur earlier than deep wound infections (15), and this may explain why the mean time between surgery and the onset of infection in our study was longer than that of other studies. In the present study, 2 reinfections occurred after cranioplasty. A previous study showed that undergoing multiple procedures before cranioplasty increased the risk of infection (5) suggesting the infection may be related to the disruption of wound healing. Our patients underwent at least 2 craniotomies (at the implantation and removal of electrodes) before cranioplasty; this could explain why our infection rate after cranioplasty was high. The cranioplasties were performed 231 days and 259 days after the removal of the bone flap in the reinfection cases. Thavarajah et al. (35) demonstrated cranioplasty carried out within 6 months after craniectomy increased the infection rate significantly. All patients reported by these authors had a single procedure before cranioplasty. Longer time intervals may be required in cases with multiple prior procedures until the wound heals completely. The present study has some limitations. One limitation is the small sample size. The finding in this study should not discourage neurosurgeons from performing electrode implantation in autumn. Nevertheless, it may suggest that neurosurgeons should have increased awareness of infection risk, especially infections by airborne S aureus, when implantations are performed in autumn. There may be some criticisms that our inexperience in this particular surgery is a contributing factor to the infection rate. However, if that is the case, postoperative infections would have been randomly distributed over the seasons. The fact that postoperative infections occurred more frequently in autumn could not be explained only by inexperience. In addition, our infection rate was within the acceptable range of the infection rates reported so far. The infection rate related to electrode implantation was shown to be between 1.1% and 14.9% (2, 4, 7, 11, 28, 33, 37, 42). Another limitation that could have affected our results was the variation in surgical techniques. An artificial dural patch was used to close the dura mater in 25 sessions, whereas an autograft was used in 19 sessions. The advantage of duraplasty with an artificial dura mater was the prevention of adhesion formations (36) after the implantation of electrodes, facilitating subsequent surgery. In addition, dural expansion with an artificial dura could decrease the mass effect on the brain caused by subdural electrodes. The disadvantage was the relationship between duraplasty with an artificial dura mater and the postoperative infection caused by foreign body reaction to the duraplasty (26). An autograft was
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nontoxic and did not induce immunologic or inflammatory reactions (30). In our series, the dura mater was closed with an artificial dural patch in all cases with infective complications. Further studies are required to clarify the influence of an artificial dural patch on the occurrence of infection. CONCLUSIONS According to the analysis of our surgical series, age, sex, duration of monitoring, side of electrode implantation, number of
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34. Tebo CC, Evins AI, Christos PJ, Kwon J, Schwartz TH: Evolution of cranial epilepsy surgery complication rates: a 32-year systematic review and meta-analysis. J Neurosurg 120:1415-1427, 2014. 35. Thavarajah D, Lacy PD, Hussien A, Sugar A: The minimum time for cranioplasty insertion from craniectomy is six months to reduce risk of infection—a case series of 82 patients. Br J Neurosurg 26:78-80, 2012. 36. Vakis A, Koutentakis D, Karabetsos D, Kalostos G: Use of polytetrafluoroethylene dural substitute as adhesion preventive material during craniectomies. Clin Neurol Neurosurg 108: 798-802, 2006. 37. Van Gompel JJ, Worrell GA, Bell ML, Patrick TA, Cascino GD, Raffel C, Marsh WR, Meyer FB: Intracranial electroencephalography with subdural grid electrodes: techniques, complications, and outcomes. Neurosurgery 63:498-505; discussion 505-506, 2008. 38. Vulliemoz S, Carmichael DW, Rosenkranz K, Diehl B, Rodionov R, Walker MC, McEvoy AW,
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Lemieux L: Simultaneous intracranial EEG and fMRI of interictal epileptic discharges in humans. Neuroimage 54:182-190, 2011. 39. Weinand ME, Oommen K: Lumbar cerebral spinal fluid drainage during long-term electrocorticographic monitoring with subdural strip electrodes: elimination of cerebral spinal fluid leak. Seizure 2: 133-136, 1993. 40. Wertheim HF, Melles DC, Vos MC, van Leeuwen W, van Belkum A, Verbrugh HA, Nouwen JL: The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis 5: 751-762, 2005. 41. Wiggins GC, Elisevich K, Smith BJ: Morbidity and infection in combined subdural grid and strip electrode investigation for intractable epilepsy. Epilepsy Res 37:73-80, 1999. 42. Wong CH, Birkett J, Byth K, Dexter M, Somerville E, Gill D, Chaseling R, Fearnside M, Bleasel A: Risk factors for complications during intracranial electrode recording in presurgical evaluation of drug resistant partial epilepsy. Acta Neurochir (Wien) 151:37-50, 2009.
43. Wyler AR, Walker G, Somes G: The morbidity of long-term seizure monitoring using subdural strip electrodes. J Neurosurg 74:734-737, 1991. Conflict of interest statement: This research was partly supported by the Japan Society for the Promotion of Science (Grant-in-Aid for Young Scientists B [Grant No. 25861273] and Scientific Research C [Grant No. 24592159]). The Department of Epilepsy, Movement Disorders and Physiology of Kyoto University Graduate School of Medicine is an endowment department, supported by grants from GlaxoSmithKline K.K., Nihon Kohden, Otsuka Pharmaceutical Co., Ltd., and UCB Japan Co., Ltd. The funding sources had no involvement in the study design; in the collection, analysis, and interpretation of data; in the writing of the article; or in the decision to submit the article for publication. Received 14 July 2014; accepted 16 March 2015 Citation: World Neurosurg. (2015) 84, 2:320-326. http://dx.doi.org/10.1016/j.wneu.2015.03.048 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2015 Elsevier Inc. All rights reserved.
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Risk Factors for Infective Complications with Long-Term Subdural Electrode Implantation in Patients with Medically Intractable Partial Epilepsy Sumiya Shibata1, Takeharu Kunieda1, Rika Inano1, Masahiro Sawada1, Yukihiro Yamao1, Takayuki Kikuchi1, Riki Matsumoto2, Akio Ikeda2, Ryosuke Takahashi3, Nobuhiro Mikuni4, Jun Takahashi5, Susumu Miyamoto1
OBJECTIVE: To evaluate infective complications with intracranial electroencephalography (EEG) recording so as to lessen them.
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METHODS: A database of intracranial monitoring cases with subdural electrodes at Kyoto University Hospital between May 1992 and March 2012 was retrospectively reviewed.
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RESULTS: This analysis included 46 EEG monitoring sessions. Infective complications related to intracranial electrodes occurred in 4 monitoring sessions (8.7%; 3 male patients). Causative agents were identified as Staphylococcus aureus in 3 monitoring sessions and Staphylococcus epidermidis in 1 session. In univariate analysis, the season of monitoring was identified as the sole significant risk factor. More infective complications occurred when monitoring occurred in autumn. More infective complications tended to occur in patients who had implantation in the right side or discontinuation of intravenously administered prophylactic antibiotics, although these factors were not statistically significant. Age, sex, duration of monitoring, number of electrodes, and pathologic diagnosis did not seem to be associated with an increased risk of infective complications. Infective complications had no significant influence on seizure outcome.
-
CONCLUSIONS: Invasive EEG monitoring during autumn might be a risk factor in terms of infective complications. S aureus was a common pathogen.
-
INTRODUCTION
A
lthough intracranial electroencephalography (EEG) monitoring has greater sensitivity and spatial specificity than scalp EEG, it also has some shortcomings (38). One shortcoming is that intracranial EEG monitoring is associated with neurosurgical procedures. Implantation of subdural grid electrodes inevitably accompanies a craniotomy. Insertion of depth electrodes requires not only trephination of the skull but also penetration of the cerebral parenchyma. As a result, intracranial EEG monitoring is associated with morbidity and mortality (11, 27, 34, 42). Minor complications such as headache, nausea, and transiently increased temperature and more serious complications such as infections, postoperative epidural or subdural hematoma, cerebrospinal fluid (CSF) collection, increased intracranial pressure, cortical contusion, CSF leakage, and brain herniation have been previously reported (7). Among these complications, postoperative infection is one of the most severe (15, 18, 24). The development of central nervous system infection after a neurosurgical procedure represents a significant threat and requires immediate medical and possibly surgical intervention (20). Postoperative nosocomial infection was associated with increased postoperative length of stay, increased costs, and increased hospital readmission rate (14). Clarifying the risk factors directly associated with these infective complications is essential. We conducted a clinical study of infective complications with the goals to reduce further complications from long-term intracranial electrode implantation and to improve the safety of invasive evaluation of epilepsy surgery. MATERIALS AND METHODS This study was approved by the Ethics Committee at Kyoto University Graduate School and Faculty of Medicine (E2102). We
Neurosurgery, Sapporo Medical University Graduate School of Medicine, Hokkaido; and Center for iPS Cell Research and Application, Kyoto University, Kyoto, Japan
Key words Epilepsy - Implanted electrode - Infection - Risk factors
5
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To whom correspondence should be addressed: Takeharu Kunieda, M.D., Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2015) 84, 2:320-326. http://dx.doi.org/10.1016/j.wneu.2015.03.048
Abbreviations and Acronyms CSF: Cerebrospinal fluid EEG: Electroencephalography
Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2015 Elsevier Inc. All rights reserved.
From the Departments of 1Neurosurgery, 2Epilepsy, Movement Disorders and Physiology, and 3 Neurology, Kyoto University Graduate School of Medicine, Kyoto; 4Department of
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performed a retrospective review of a database of patients who had undergone epilepsy surgery at Kyoto University Hospital between May 1992 and March 2012. We identified 49 patients who had undergone 53 invasive monitoring sessions. One patient died 2 days after the resection surgery of acute myocardial infarction. Because the death was unrelated to the neurosurgical procedure, this patient was excluded from the analysis. All patients required intracranial monitoring because they were candidates for epilepsy surgery, and results of noninvasive monitoring did not reveal sufficient localizing information to delineate a resection procedure. The number and location of the intracranial electrodes to be implanted were carefully determined for each individual with reference to the noninvasive evaluation. For electrode implantation, 2 different types of platinum subdural strip and grid electrodes provided by 2 different manufacturers (Ad-Tech Medical Instrument Corporation, Racine, Wisconsin, USA, and Unique Medical Co., Ltd., Tokyo, Japan) were used. In 5 of the monitoring sessions, depth electrodes were used in addition to either subdural electrodes or cavernous sinus electrodes (16, 23). In 1 other monitoring session, only epidural electrodes were used. These 6 sessions using other types of electrodes together with or instead of the subdural type were excluded from the analysis because of the small number of cases. The monitoring sessions with depth electrodes, epidural electrodes, or cavernous sinus electrodes had no infective complications at all. The analysis included 46 monitoring sessions (26 of which involved male patients). All patients underwent general anesthesia for the subdural grid or strip electrode implantation surgery. In the first stage of surgery, a skin incision and wide craniotomy and cranioplasty were performed to create an operative field large enough to expose the appropriate cortical areas for electrode coverage. Most subdural electrodes were placed under direct visualization to avoid any damage to bridging veins or other cerebral cortex and vascular structures. In some cases, additional smaller grid or strip electrodes were slid over the brain without direct visualization. The cables of the electrodes were kept in a bundle. The dura mater was closed with an artificial dural patch in 25 sessions and primarily or with an autograft (without an artificial dura mater) in 19 sessions (data were unavailable in 2 sessions). When the electrode leads were exfiltrated through the dura mater to the outside, 2 techniques were used to fix the leads tightly to the dura mater and to prevent any damage (kinking, direct injury) to them. In some cases, small lateral slits were made off of the main incision (with suturing between the electrode leads and the main incision). In other cases, a small section of the dura mater along the main incision was raised slightly or pinched, creating a “tunnel” through which the electrode lead was fed and sutured in place. The bone flap was fixed back temporarily. The cables were tunneled >1 cm away from the initial skin incision line for each lead. Data on the use of prophylactic antibiotics were available in 45 of 46 analyzed monitoring sessions. In 35 of the monitoring sessions, prophylactic antibiotics were administered intravenously not only during the operation but also throughout the monitoring period. In 10 of the monitoring sessions, prophylactic intravenous administration of antibiotics was interrupted, with prophylactic antibiotics discontinued completely in 5 of these monitoring sessions and administered orally for some period in the other 5 sessions.
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INFECTIVE COMPLICATIONS WITH INTRACRANIAL EEG RECORDING
After sufficient EEG monitoring, data were obtained along with determination of the regions of epileptogenesis and functional mapping of eloquent cortical areas, the subdural electrodes were removed, and the planned resection was performed as the second surgical treatment. The following demographic data and monitoring variables were recorded (Table 1): age at surgery, sex, duration of invasive monitoring, season of monitoring, side of electrode implantation, number of electrode contacts, cumulative number of electrode contacts (number of electrode contacts multiplied by days of invasive monitoring), intravenous administration of antibiotics throughout the invasive monitoring period, pathologic diagnosis (hippocampal sclerosis was diagnosed with preoperative magnetic resonance imaging in some cases), state of associated infections, and seizure outcome. Because 1 patient had 40 contacts in the first 2 days and 60 contacts in the last 5 days, his number of electrode contacts was calculated as 54 [(40 2 þ 60 5)/7]. Seizure outcome data were obtained from clinical visits. These data were obtained 13e243 months after surgery (mean 100 months). The outcomes of postoperative seizure control were categorized as either “good” (class I) or “not good” (classes
Table 1. Demographic Data and Monitoring Variables Sex (monitoring sessions): male/female Age at surgery (years) (mean SD)
26/20 26.5 7.2
Side of electrode implantation (monitoring sessions): right/left/bilateral
20/25/1
Number of electrode contacts (mean SD)
50 20
Duration of invasive monitoring (days) (mean SD) Cumulated number of electrode contacts (contacts $ days) (mean SD)
11 4 567 329
Season of monitoring (monitoring sessions) MarcheMay (spring)
12
JuneeAugust (summer)
14
SeptembereNovember (autumn) DecembereFebruary (winter)
9 11
Pathologic diagnosis (monitoring sessions)* BT
6
CD
24
HS
7
Others
14
Seizure outcome (patients) I
21
II
4
III
18
IV
0
BT, brain tumor; CD, cortical dysplasia; HS, hippocampal sclerosis. *Some patients had >1 pathologic finding. The pathologic finding of 1 patient was unknown.
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IIeIV) according to the Engel classification system (6). An exception to the Engel classification system was our minimum follow-up period of 13 months rather than 24 months. All the analyses but the calculation of q value were conducted by JMP Pro 11.0 (SAS Institute, Cary, North Carolina, USA). Pearson c2 or Fisher exact test as appropriate was used to test for association between categorical variables and the presence of complications. Wilcoxon test was used to assess associations between continuous variables and the presence of complications. To correct for multiple comparisons and false discovery rate (3), q value was calculated. Statistical significance was adopted as P value < 0.05 and q value < 0.3. Because the number of events was small (4 sessions with infective complications) and 1 of the sessions with infective complications had no data on the administration of antibiotics, we did not perform multivariate analysis.
RESULTS The present analysis included 46 monitoring sessions (26 of which involved male patients) (Table 1). The mean age of the patients at surgery was 26.5 years 7.2 (mean SD). Electrodes were placed over the right hemisphere in 20 monitoring sessions, the left hemisphere in 25 monitoring sessions, and both hemispheres in 1 monitoring session. The mean number of electrode contacts per monitoring session was 50 contacts 20. The mean length of intracranial recording was 11 days 4. The seasonal breakdown of the invasive monitoring procedures was 12 in spring, 14 in summer, 9 in autumn, and 11 in winter. The pathologic findings were brain tumor in 6 cases, cortical dysplasia in 24 cases, hippocampal sclerosis in 7 cases, and “other” in 14 cases. Seizure outcomes were classified as “good” (Engel classification class I) in 21 patients and “not good” (Engel classes IIeIV) in 22 patients. Infective complications related to intracranial electrodes occurred in 4 monitoring sessions (8.7%) (3 of which involved male patients) (Table 2). These 4 cases resulted in removal of the bone flap. Wound cultures revealed Staphylococcus aureus infection in 3 monitoring sessions and Staphylococcus epidermidis infection in 1 monitoring session. These 4 patients were treated with antibiotics and subsequently underwent reconstructive cranioplasty 259, 231, 259, and 197 days after the removal of the bone flap. After cranioplasty, infective complications recurred in 2 cases (Cases 2 and 3). S aureus was isolated in these 2 cases.
Table 2. Clinical Characteristics of 4 Patients Who Had Infective Complications Age at Surgery (years)/Sex
Duration from Surgery to Appearance of Infection (days)
Isolated Microorganisms
1
26/male
33
Staphylococcus aureus
2
25/male
10
S aureus
3
18/male
40
S aureus
4
23/female
45
Staphylococcus epidermidis
Case Number
322
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Table 3 shows the risk factors for infective complication related to intracranial electrodes. In univariate analysis, the only identified risk factor was season of monitoring. More infective complications occurred when monitoring took place in autumn. More infective complications tended to occur in the patients who had implantation in the right side or discontinuation of intravenously administered prophylactic antibiotics, although these factors were not statistically significant. Age, sex, duration of monitoring, number of electrodes, and pathologic diagnosis did not seem to be associated with an increased risk of infective complications. Infective complications had no significant influence on seizure outcome. DISCUSSION In our study, more infective complications occurred when the monitoring took place in autumn (from September to November). S aureus was the most common pathogen identified. S aureus is a human commensal and a frequent cause of clinically important infections. Several past studies showed seasonal variation of S aureus infections with peak occurrences in summer and autumn (10, 17, 22). These studies suggested several factors that explained the seasonality of the infections. The first possible factor is the level of provider training (“the July effect”). The inexperience of new residents could result in worse patient outcomes at the beginning of the academic year (29). However, in Japan, new residents start in April, and so this factor would not explain our finding. The second possible factor is the survival of pathogens (9). Pathogen survival depends partly on the characteristics of the weather such as temperature and humidity. A high-temperature, high-humidity environment promoted bacterial growth on the human skin (19). Nasal carriers of S aureus were shown to have an increased risk of acquiring an infection with this pathogen (40). Because patients are colonized with large numbers of S aureus in seasons with high temperatures and humidity, infections would develop more frequently during hospitalization of patients in that season. However, the influence of this meteorologic element may not be apparent in a hospital with central air conditioning. Our study found higher infection rates during autumn than summer, although generally in Kyoto summer has the highest temperature and humidity in a year. A previous study of nasopharyngeal bacterial flora (12) revealed that S aureus tended to be more common in the autumn and winter months. This trend correlated with the peak of viral respiratory infections. Another study in Japan (32), which investigated the bacterial dispersion from the surface of the human body, determined that the sum of airborne S aureus and coagulasenegative staphylococci in an operating room in a year was the largest in autumn, although the total number of airborne bacteria was the largest in summer in a year. From the results of these 2 studies, airborne transmission of S aureus may increase during autumn. S aureus acquired from an external source could cause infection (17). The infection by airborne S aureus could partially explain our result. We also found that there were more infective complications in the patients who had implantation in the right side or discontinuation of intravenously administered prophylactic antibiotics,
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Table 3. Risk Factors for Infective Complications
Sex (male/female) (monitoring sessions) Age at surgery (years) (mean SD)
No Infection
Infection
23/19
3/1
P Value
q Value
0.44
0.87
26.8 7.4
23.0 3.6
0.27
0.66
Side of electrode implantation (right/left/bilateral) (monitoring sessions)
16/25/1
4/0/0
0.08*
0.32*
Number of electrode contacts (mean SD)
50 20
47 20
0.70
11 4
12 4
> 0.99
> 0.99
566 330
580 375
0.86
> 0.99
Duration of invasive monitoring (days) (mean SD) Cumulated number of electrode contacts (contacts $ days) (mean SD) Season of monitoring (monitoring sessions) MarcheMay (spring)
11
1
JuneeAugust (summer)
14
0
SeptembereNovember (autumn)
6
3
11
0
34
1
8
2
BT
3
1
CD
17
2
BT and CD
2
0
CD and HS
1
0
CD and others
2
0
HS
5
0
HS and others
1
0
10
1
DecembereFebruary (winter) z
Antibiotics intravenously administered (monitoring sessions) Full coverage Partial coverage x
Pathologic findings (monitoring sessions)
Others Outcome of epilepsy surgery (patients)k I
18
3
IIeIV
21
1
> 0.99
0.02y
0.29y
0.06*
0.32*
0.80
> 0.99
0.27
0.66
The values noted in the footnotes y are significant. Those noted in the footnotes * are insignificant but close to the significance level. BT, brain tumor; CD, cortical dysplasia; HS, hippocampal sclerosis. *< 0.1 for P values; < 0.5 for q values. y< 0.05 for P values; < 0.3 for q values. zIn 1 monitoring session, there were no data on the use of prophylactic antibiotics. xThe pathologic findings of 1 patient were unknown. k1 patient who had an infective complication in 1 of 3 monitoring sessions was counted as an “infection” patient.
although these factors were not statistically significant. Few studies reported the site of implantation as a risk factor for complications. Hamer et al. (11) reported that left-sided grid insertion was associated with neurologic deficits. They suggested that the dominant left hemisphere might be more sensitive to neurologic deficits compared with the nondominant right hemisphere. Wong et al. (42) reported that right central surface implantation was associated with neurologic deficits. They suggested that the central region is responsible for important motor and sensory function and might be sensitive to trauma.
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They did not indicate why right-side implantation should increase risk. The use of antibiotics to prevent postoperative infection is a matter of debate (18). Wyler et al. (43) reported that the absence of antibiotics during monitoring did not correlate with the infection rate. In their series, only strip electrodes were implanted through burr holes, without any craniotomies (7). Barker (1) reviewed 6 prospective randomized trials in general neurosurgery and showed that prophylactic antibiotics reduced the rate of postoperative meningitis. The duration of antibiotic prophylaxis is
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also a matter of debate. The prolonged use of antibiotics could increase the likelihood of colonization or infection with antibioticresistant bacteria (21). Blauwblomme et al. (4) reported the infection rate (14.9%) related to invasive recording when they gave prophylactic antibiotics only at the induction of anesthesia. Because the centers using antibiotics throughout the EEG recording period had lower infection rates (2.4%e8.57%) than Blauwblomme et al. (4), they discussed the duration of antibiotic prophylaxis with their infectious disease team. The use of antibiotic prophylaxis should be studied further, especially in neurosurgical procedures in which a foreign body communicating outside the body, such as an electrode, is inserted. In our study, age, sex, duration of monitoring, number of electrode contacts, cumulative number of electrode contacts, and pathologic diagnosis did not seem to be associated with an increased risk of infective complications. In several previous studies, complications occurred in association with a larger number of electrodes (11, 33, 41, 42), longer duration of monitoring (11, 41), and older patient age (11). This difference might be explained by the difference in analytic methodology. First, we evaluated only infective complications. Previously cited studies evaluated all complications, including neurologic deficit, infection, bleeding, CSF leakage, and cerebral edema (11, 27, 33, 41, 42). Because subdural electrodes cause a mass effect on the brain (13), a larger number of electrodes might increase the intracranial pressure and cause several neurologic symptoms. Mild neurologic disturbances could be noticed more reliably in self-reporting adults compared with children (11). Musleh et al. (25) reported that duration of grid placement, number of electrodes, and number of exit wires did not increase the risk of infective complications. The results of other past studies might be influenced by complications other than infection. Second, we excluded depth electrodes because only 5 monitoring sessions used those electrodes. Intracranial hemorrhage was the most significant complication associated with the placement of stereotactic intracerebral electrodes (31). The results of past studies also might be influenced by complications related to depth electrodes. As another risk factor, Musleh et al. (25) suggested an increase in the rate of infection with grid reimplantation. Case 4 in our study underwent subdural electrode reimplantation, and the delay in wound healing caused postoperative infections. Although we did not perform a statistical analysis with respect to the reimplantation and infective complications because of the limited number of patients undergoing reimplantation, this procedure might influence the prevalence of postoperative infections caused by delayed wound healing. Careful postoperative wound management should be required in the case of reimplantation. Hydrocolloid dressings that maintain a moist environment might be useful in promoting wound healing (8). In general, CSF leakage is a risk factor associated with infections in neurosurgery (18). Watertight closure of the dura mater without tension is not always possible because of the additional intracranial volume of electrodes themselves and the cables of the electrodes passing through the dural closure, which might lead to CSF leakage. In our series, Cases 2 and 3 had CSF leakage. To minimize CSF leakage, it is necessary to close the incision of the dura mater with great care and to tunnel electrodes far away from the point of pial entrance. A previous
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study reported the insertion of a lumbar drain and drainage of CSF as an additional method for preventing CSF leakage (39). However, the efficacy of drainage of CSF in reducing the infective complication remains to be studied. In the present series, S aureus was isolated in 3 cases (75%). Staphylococcus is a common pathogen found in intracranial electrode implantation (11, 37, 43) and in other types of neurosurgery (15, 18). Our results from wound culture were similar to past reports. The mean time between surgery and the onset of infection was 32 days 15. Past studies reported the mean time was 21 days 31 for electrode implantation (37) and 18 days 25 for all types of neurosurgery (15). In the present study, osteomyelitis was identified in 2 cases (Cases 1 and 3), and meningoencephalitis was identified in 2 cases (Cases 2 and 4). These were deep wound infections. Superficial scalp infections tend to occur earlier than deep wound infections (15), and this may explain why the mean time between surgery and the onset of infection in our study was longer than that of other studies. In the present study, 2 reinfections occurred after cranioplasty. A previous study showed that undergoing multiple procedures before cranioplasty increased the risk of infection (5) suggesting the infection may be related to the disruption of wound healing. Our patients underwent at least 2 craniotomies (at the implantation and removal of electrodes) before cranioplasty; this could explain why our infection rate after cranioplasty was high. The cranioplasties were performed 231 days and 259 days after the removal of the bone flap in the reinfection cases. Thavarajah et al. (35) demonstrated cranioplasty carried out within 6 months after craniectomy increased the infection rate significantly. All patients reported by these authors had a single procedure before cranioplasty. Longer time intervals may be required in cases with multiple prior procedures until the wound heals completely. The present study has some limitations. One limitation is the small sample size. The finding in this study should not discourage neurosurgeons from performing electrode implantation in autumn. Nevertheless, it may suggest that neurosurgeons should have increased awareness of infection risk, especially infections by airborne S aureus, when implantations are performed in autumn. There may be some criticisms that our inexperience in this particular surgery is a contributing factor to the infection rate. However, if that is the case, postoperative infections would have been randomly distributed over the seasons. The fact that postoperative infections occurred more frequently in autumn could not be explained only by inexperience. In addition, our infection rate was within the acceptable range of the infection rates reported so far. The infection rate related to electrode implantation was shown to be between 1.1% and 14.9% (2, 4, 7, 11, 28, 33, 37, 42). Another limitation that could have affected our results was the variation in surgical techniques. An artificial dural patch was used to close the dura mater in 25 sessions, whereas an autograft was used in 19 sessions. The advantage of duraplasty with an artificial dura mater was the prevention of adhesion formations (36) after the implantation of electrodes, facilitating subsequent surgery. In addition, dural expansion with an artificial dura could decrease the mass effect on the brain caused by subdural electrodes. The disadvantage was the relationship between duraplasty with an artificial dura mater and the postoperative infection caused by foreign body reaction to the duraplasty (26). An autograft was
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nontoxic and did not induce immunologic or inflammatory reactions (30). In our series, the dura mater was closed with an artificial dural patch in all cases with infective complications. Further studies are required to clarify the influence of an artificial dural patch on the occurrence of infection. CONCLUSIONS According to the analysis of our surgical series, age, sex, duration of monitoring, side of electrode implantation, number of
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43. Wyler AR, Walker G, Somes G: The morbidity of long-term seizure monitoring using subdural strip electrodes. J Neurosurg 74:734-737, 1991. Conflict of interest statement: This research was partly supported by the Japan Society for the Promotion of Science (Grant-in-Aid for Young Scientists B [Grant No. 25861273] and Scientific Research C [Grant No. 24592159]). The Department of Epilepsy, Movement Disorders and Physiology of Kyoto University Graduate School of Medicine is an endowment department, supported by grants from GlaxoSmithKline K.K., Nihon Kohden, Otsuka Pharmaceutical Co., Ltd., and UCB Japan Co., Ltd. The funding sources had no involvement in the study design; in the collection, analysis, and interpretation of data; in the writing of the article; or in the decision to submit the article for publication. Received 14 July 2014; accepted 16 March 2015 Citation: World Neurosurg. (2015) 84, 2:320-326. http://dx.doi.org/10.1016/j.wneu.2015.03.048 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2015 Elsevier Inc. All rights reserved.
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