Patterns in neurosurgical adverse events: intracranial neoplasm surgery

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Object

Neurosurgery is a high-risk specialty currently undertaking the pursuit of systematic approaches to measuring and improving outcomes. As part of a project to devise evidence-based safety interventions for specialty surgery, the authors sought to review current evidence in cranial tumor resection concerning the frequency of adverse events in practice, their patterns, and current methods of reducing the occurrence of these events. This review represents part of a series of papers written to consolidate information about these events and preventive measures as part of an ongoing effort to ascertain the utility of devising system-wide policies and safety tools to improve neurosurgical practice.

Methods

The authors performed a PubMed search using search terms “intracranial neoplasm,” “cerebral tumor,” “cerebral meningioma,” “glioma,” and “complications” or “adverse events.” Only papers that specifically discussed the relevant complication rates were included. Papers were chosen to maximize the range of rates of occurrence for the reported adverse events.

Results

Review of the tumor neurosurgery literature showed that documented overall complication rates ranged from 9% to 40%, with overall mortality rates of 1.5%–16%. There was a wide range of types of adverse events overall. Deep venous thromboembolism (DVT) was the most common adverse event, with a reported incidence of 3%–26%. The presence of new or worsened neurological deficit was the second most common adverse event found in this review, with reported rates ranging from 0% for the series of meningioma cases with the lowest reported rate to 20% as the highest reported rate for treatment of eloquent glioma. Benign tumor recurrence was found to be a commonly reported adverse event following surgery for intracranial neoplasms. Rates varied depending on tumor type, tumor location, patient demographics, surgical technique, the surgeon's level of experience, degree of specialization, and changes in technology, but these effects remain unmeasured. The incidence on our review ranged from 2% for convexity meningiomas to 36% for basal meningiomas. Other relatively common complications were dural closure–related complications (1%–24%), postoperative peritumoral edema (2%–10%), early postoperative seizure (1%–12%), medical complications (6%–7%), wound infection (0%–4%), surgery-related hematoma (1%–2%), and wrong-site surgery.

Strategies to minimize risk of these events were evaluated. Prophylactic techniques for DVT have been widely demonstrated and confirmed, but adherence remains unstudied. The use of image guidance, intraoperative functional mapping, and real-time intraoperative MRI guidance can allow surgeons to maximize resection while preserving neurological function. Whether the extent of resection significantly correlates with improved overall outcomes remains controversial.

Discussion

A significant proportion of adverse events in intracranial neoplasm surgery may be avoidable by use of practices to encourage use of standardized protocols for DVT, seizure, and infection prophylaxis; intraoperative navigation among other steps; improved teamwork and communication; and concentrated volume and specialization. Systematic efforts to bundle such strategies may significantly improve patient outcomes.

Abbreviations used in this paper:5-ALA = 5-aminolevulinic acid; DVT = deep venous thromboembolism; ICU = intensive care unit; SCD = sequential intermittent compression device.

Object

Neurosurgery is a high-risk specialty currently undertaking the pursuit of systematic approaches to measuring and improving outcomes. As part of a project to devise evidence-based safety interventions for specialty surgery, the authors sought to review current evidence in cranial tumor resection concerning the frequency of adverse events in practice, their patterns, and current methods of reducing the occurrence of these events. This review represents part of a series of papers written to consolidate information about these events and preventive measures as part of an ongoing effort to ascertain the utility of devising system-wide policies and safety tools to improve neurosurgical practice.

Methods

The authors performed a PubMed search using search terms “intracranial neoplasm,” “cerebral tumor,” “cerebral meningioma,” “glioma,” and “complications” or “adverse events.” Only papers that specifically discussed the relevant complication rates were included. Papers were chosen to maximize the range of rates of occurrence for the reported adverse events.

Results

Review of the tumor neurosurgery literature showed that documented overall complication rates ranged from 9% to 40%, with overall mortality rates of 1.5%–16%. There was a wide range of types of adverse events overall. Deep venous thromboembolism (DVT) was the most common adverse event, with a reported incidence of 3%–26%. The presence of new or worsened neurological deficit was the second most common adverse event found in this review, with reported rates ranging from 0% for the series of meningioma cases with the lowest reported rate to 20% as the highest reported rate for treatment of eloquent glioma. Benign tumor recurrence was found to be a commonly reported adverse event following surgery for intracranial neoplasms. Rates varied depending on tumor type, tumor location, patient demographics, surgical technique, the surgeon's level of experience, degree of specialization, and changes in technology, but these effects remain unmeasured. The incidence on our review ranged from 2% for convexity meningiomas to 36% for basal meningiomas. Other relatively common complications were dural closure–related complications (1%–24%), postoperative peritumoral edema (2%–10%), early postoperative seizure (1%–12%), medical complications (6%–7%), wound infection (0%–4%), surgery-related hematoma (1%–2%), and wrong-site surgery.

Strategies to minimize risk of these events were evaluated. Prophylactic techniques for DVT have been widely demonstrated and confirmed, but adherence remains unstudied. The use of image guidance, intraoperative functional mapping, and real-time intraoperative MRI guidance can allow surgeons to maximize resection while preserving neurological function. Whether the extent of resection significantly correlates with improved overall outcomes remains controversial.

Discussion

A significant proportion of adverse events in intracranial neoplasm surgery may be avoidable by use of practices to encourage use of standardized protocols for DVT, seizure, and infection prophylaxis; intraoperative navigation among other steps; improved teamwork and communication; and concentrated volume and specialization. Systematic efforts to bundle such strategies may significantly improve patient outcomes.

Progress in the science of improving surgical safety has been notable in recent years. Methods for evaluating outcomes have been developed and deployed,30,45,46,61,72,81,113 and the data have been used to research patterns of errors and complications. From these findings, solutions have been designed and tested with sometimes striking improvements, whether using simple process tools like checklists30,31,51,112 or technological changes.48,85,111 Neurosurgery is a high-risk surgical specialty that is beginning to pursue systematic, nationwide approaches to measuring and improving outcomes. As part of a project funded by the US Agency for Healthcare Research and Quality to devise evidence-based checklists and protocols for specialty surgery, we sought to review current evidence in neurosurgery concerning the frequency of adverse events in practice, their patterns, and the state of knowledge about how to improve them. We hypothesized that this consolidation of existing data, even if commonly known to neurosurgeons, will not only highlight the need for devising system-wide policies and safety tools to improve neurosurgical practice but also inform future efforts to develop and implement these tools and policies. This paper reviews the patterns of neurosurgical adverse events in tumor neurosurgery.

Scope of the Problem

According to the Healthcare Cost and Utilization Project, 40,788 procedures were performed for the treatment of benign and malignant intracranial neoplasms in 2009 (http://hcupnet.ahrq.gov). Studies focusing on complications specifically related to surgery for intracranial neoplasms are largely single-provider or single-institution series. Documented overall complication rates range from 9.0% to 40% with overall mortality rates of 1.5% to 16%.12,17,21,22,32,39,84,94,96,106 Existing data capture outcomes primarily from a limited set of academic institutions presenting selective findings on particular tumor types; they therefore hold inherently uncertain value as an indicator of patient experiences with neurosurgery on a larger scale.

Table 1 summarizes what is known from these data about the types and frequencies of commonly seen adverse events, in order of descending estimated frequency. Results are bound to vary according to the tumor type prevalent at a given institution and patient and surgeon preferences regarding the aggressiveness of the planned resection. Unlike cardiac bypass surgery,36 bariatric surgery,59 or other high-risk specialty procedures,61,102 there is no national database or registry of outcomes for neurosurgery. Although data from the Surveillance, Epidemiology and End Results national registry have proven useful for analysis of the epidemiology and survival rates of brain tumors,23,33,54,83,86 these data do not address surgery-specific outcomes. The National Inpatient Sample has borne several studies relating to neurosurgical outcomes8,25,26 but may not be as useful for detailed risk stratification and granular outcomes such as degree of neurological deficit given that the data were not collected specifically for the field.

TABLE 1:

Frequency of adverse events reported in intracranial neoplasm surgery*

AE w/ Author & YearSample Size (no. of pts)Lesion CharacteristicsAE Frequency (%)
venous thromboembolism
 Brandes et al., 199777glioma26
 Agnelli et al., 1998307mixed25
 Chan et al., 1999497mixed10
 Chang et al., 2003499glioma5 (1st), 8 (repeat)
 Auguste et al., 2003180glioma3
new or worsened neurological deficit
 Talacchi et al., 2010171eloquent glioma20
 Fadul et al., 1988213glioma20
 Sawaya et al., 1998400mixed9
 Chang et al., 2003499glioma8 (1st), 18 (repeat)
 Ciric et al., 198742glioma7
 Black et al., 199857meningioma5
 Cabantog & Bernstein, 1994207mixed3
 Sanai et al., 2010141meningioma0
benign tumor recurrence
 Oya et al., 201139sphenoorbital meningioma18
 Simpson, 195750basal13 (Grade II), 36 (Grade I)
 Simpson, 1957154convexity/parasagittal/intraventricular17 (Grade II), 3–5 (Grade I)
 Nakamura et al., 200782olfactory groove meningioma5
 Sanai et al., 2010141convexity meningioma4
 Morokoff et al., 2008163convexity meningioma2
 Obeid & Al-Mefty, 200315olfactory groove meningioma0
dural closure-related complications
 Duz et al., 200893transphenoidal24
 Laws et al., 1985158transphenoidal6
 Sade et al., 2011439meningioma3
 Fatemi et al., 2008881transphenoidal2
 Barker et al., 20035497transphenoidal1
 Sanai et al., 2010141meningioma1
postop peritumoral edema
 Ciric et al., 198742glioma10
 Cabantog & Bernstein, 1994207mixed8
 Black et al., 199857meningioma2
early postop seizure
 De Santis et al., 2002200mixed12
 De Santis et al., 199649mixed11
 Zachenhofer et al., 201178mixed3
 Sughrue et al., 2011104180meningioma1
medical complications
 Sughrue et al., 2011105834meningioma7
 Sawaya et al., 1998400mixed7
 Black et al., 199857meningioma6
wound infection
 Sanai et al., 2010141meningioma4
 Hardy et al., 20102485mixed2
 Sawaya et al., 1998400mixed1
 Chang et al., 2003499glioma0.5 (1st), 1 (repeat)
surgery-related hematoma
 Chang et al., 2003499glioma2 (1st), 4 (repeat)
 Taylor et al., 19952305mixed2
 Romani et al., 2009656meningioma2
 Sanai et al., 2010141meningioma1
 Palmer et al., 19946668tumor & other1
wrong-site surgery
 Cohen et al., 201035 casesNANA

* AE = adverse event; NA = not applicable; pts = patients.

† Case reports.

Nonetheless, among the existing series reviewed, the most commonly reported adverse events are: venous thromboembolism, benign tumor recurrence, new or worsened neurological deficit, dural closure–related complications, postoperative peritumoral edema, early postoperative seizure, medical complications, wound infection, surgery-related hematoma, and wrong-site surgery. Many of these complications are interrelated, and some, particularly benign tumor recurrence, may be considered adverse events rather than preventable complications.

Methods

We performed a PubMed search of the English literature using the search terms “intracranial neoplasm,” “cerebral tumor,” “cerebral meningioma,” “glioma,” AND “complications” OR “adverse events.” Only papers that specifically discussed the relevant complication rates were included. Papers were chosen to maximize the range of rates of occurrence for the reported adverse events rather than to include all possible studies. We did not impose any threshold of minimum patients or publication year; however, we attempted to choose series that were representative of the most common complications. We focused this review on primary brain tumors only.

Venous Thromboembolism

Few studies have carefully assessed occurrences of venous thromboembolism. As malignancy itself is a hypercoagulable state,42 thromboembolism rates in tumor neurosurgery are significant, ranging from 3% to 26% even with DVT prophylaxis.2,6,14,19,21 Randomized trials have shown significant benefit from use of sequential intermittent compression devices (SCDs) in this patient population.99 There is also benefit from low-dose anticoagulation, but guidance is unclear for balancing against increased bleeding risk following surgery for intraaxial lesions.14,18,73 Adherence to guidelines for SCD use is unmeasured but likely inconsistent.

New or Worsened Neurological Deficit

Neurological deficit after tumor resection is clearly related to tumor type. Patients with malignant gliomas have a higher rate of new or worsened deficit than those with benign tumors.12,17,21,39,94,96,106 For all tumors, more recent studies appear to show improved rates compared with earlier ones, but the source of improvement, whether technological or experiential, is unclear.

Single-institution series suggest that the use of image guidance,9,15 intraoperative functional mapping,20,27,62,78,92 and real-time intraoperative MRI guidance23,74,75,101 can allow surgeons to maximize resection while preserving neurological function and perhaps prolonging survival. In recent years, use of these technologies has increased.

Findings in other surgical fields indicate that greater hospital and/or surgeon volume of experience are associated with better clinical outcomes.10,11,49,116 Three studies using the National Inpatient Sample database suggest the same for intracranial tumor surgery.8,25,26 There has been a shift in recent decades to encourage subspecialization in training and practice.

Controversy remains regarding the impact of extent of resection on neurological and functional outcome and overall survival, in the treatment of gliomas.91,93 For a given glioma, it remains unclear if maximizing extent of resection or minimizing risk to functional tissue should be the optimal goal. Recent data, however, support maximizing resection. In the only randomized controlled trial addressing this issue, Stummer et al.103 compared 5-ALA–aided resection to conventional white light microscopic resection in 322 patients with malignant glioma, finding greater radiographically confirmed resection and higher 6-month progression-free survival in the 5-ALA group. Of note, the 5-ALA group experienced greater immediate postoperative neurological decline, but this difference became nonsignificant at 7 days. Multiple other series support maximization of resection for better perioperative neurological outcome, longer overall survival, or both.22,57,65,109 However, there are also data suggesting that extent of resection is not correlated with neurological outcome.96,106

Benign Tumor Recurrence

The recurrence of tumors with benign histology is not avoidable even in the best of hands. Nonetheless, it is a commonly occurring adverse event with various causes worthy of discussion.

Recurrence rates vary depending on tumor location, patient demographics, and surgical technique. McDermott's group reported on 141 convexity meningioma patients having 4% radiographical evidence for recurrence with 2% proceeding to repeat resection,94 correlating with Simpson's results in 1957.98 Meningiomas in more difficult locations such as those at the skull base have higher and more varied rates of recurrence, depending on the surgeon, tumor location, and Simpson grade. For example Al-Mefty, Samii, and Lee report rates of 0% (with short duration of follow-up) to 18%.71,77,79 Like rates of postoperative neurological deficit, recurrence rates are affected by surgical technique, surgeon's level of experience, specialization, and changes in technology such as adjunctive stereotactic radiosurgery, but these effects remain unmeasured.

Dural Closure–Related Complications

Dural closure–related complications are rare but serious. Cerebrospinal fluid leak occurs with the highest frequency following transsphenoidal operations, with rates ranging from 1% to 24%,8,35,40,66 and is also a significant concern after tumor resection at the skull base where dural repair can be technically challenging. This complication occurs with lower frequency in other neurosurgical procedures. A series of 439 meningioma cases was reviewed by Lee and colleagues, who reported rates of 0.4% for CSF leak; 2.3% for graft-related complications such as chemical meningitis, cerebritis, and accumulation of extraaxial fluid; and 0.9% for infectious complications.90 Similarly, Sanai et al.94 found a 1.4% rate of CSF leak following convexity meningioma resection. Different strategies, including use of autologous versus nonautologous graft types, and variation with respect to suture type, postclosure sealants, and use of postoperative lumbar drainage to reduce these complications are debated but are nonetheless advocated by various authors.1

Postoperative Peritumoral Edema

Rates of postoperative peritumoral edema appear significant, particularly in patients with intraaxial tumors, but no dedicated studies quantify such risk. Retrospective series show rates ranging from 7.7% to 9.5% for the percentage of patients experiencing symptomatic postoperative edema. Most of these patients underwent resection for glioma.17,22 In patients undergoing meningioma resection, postoperative edema rates are lower.12

Steroids are routinely given perioperatively to reduce peritumoral edema, as first described by Galicich in 1961.44 Indeed, in Cabantog and Bernstein's 1994 series, the neurological deficits improved after addition of postoperative steroids to their protocol.17 Serious steroid medication errors have been observed, however, although the frequency has not been measured. These errors include inadvertent failure to begin steroids, failure to cease or taper the dose of the steroids, and failure to protect against their well-recognized complications.37,68,69 Methods for reduction of complications or errors may include use of electronic physician order entry, decision-support, and pharmacist review.55

Intraoperatively, the surgeon must optimize patient head and body positioning to maximize venous drainage from the brain, thereby minimizing tumor edema.60 Positioning also holds important implications for the anesthesiologist.89

Other strategies are less well established or proven but commonly include elevation of the head of the patient's bed, maintaining expired carbon dioxide in a low-normal range postoperatively,110 and/or intraoperative3,53 and perioperative56 CSF drainage. Adherence to these practices is variable. Unintended compromise of the brain's arterial or venous supply also exacerbates postoperative edema and is surgeon dependent.

Early Postoperative Seizure

Early postoperative seizures are thought to occur at a frequency between 1% and 12% for all intracranial tumors, with the greatest risk in the first 48 hours after surgery.29,64 Although the use of postoperative antiepileptic agents has not been definitively shown to prevent postoperative seizures, the majority of neurosurgeons routinely use them in the immediate perioperative period. Using perioperative levetiracetam for patients undergoing resection of supratentorial intraaxial tumors, Zachenhofer et al.117 observed a reduction in the percentage of patients with seizures from 38.5% preoperatively to 2.6% in the early postoperative period. With use of phenytoin in 49 patients with various tumors, a postoperative seizure rate of 10.6% was observed, which appeared to be an improvement over previous experience.28 Conversely, Sughrue et al.104 retrospectively analyzed 180 cases involving patients who underwent convexity meningioma resection and found no difference in seizure rates between those who received prophylactic anticonvulsant medication and those who did not. A randomized trial has not been published.

The one clear error associated with prophylactic anticonvulsant use is prescribing these agents for prolonged periods, due to risk of myelosuppression and drug interactions.47 One single-center study reveals, however, that despite national practice guidelines recommending restriction of prophylactic antiepileptic drugs to a 1-week course, 68% of patients were erroneously prescribed antiepileptic drugs for extended periods—in some cases, indefinitely.67

Use of increasingly popular minimally invasive techniques, including the endoscopic endonasal approach, will likely reduce the incidence of early postoperative seizures in patients whose tumors can be treated with these techniques,63 though randomized studies may not be feasible.

Medical Complications

The most common medical complications observed in large series are pneumonia, followed by renal dysfunction and arrhythmia, and the incidence rates do not appear to vary according to tumor histology.4,12,17,21,32,96,105,106 Neurological deficit is strongly associated with the development of medical complications.105

Common strategies recommended in the surgical literature include use of intraoperative checklists,51 perioperative screening protocols and medical optimization,41 ICU quality improvement interventions,97 and hospitalist consultation,88 but these strategies remain unexplored specifically in the neurosurgical literature.

Wound Infection

Patients with tumors are particularly susceptible to surgical-site infection, because many are immunosuppressed from steroid use and/or chemotherapy and because many have extensive soft-tissue changes from radiation therapy.5,52,76 Overall surgical-site infection rates in tumor resection are not documented in the literature but appear to be significant. Rates of infection range from 0.5% to 4% in removal of intra- and extraaxial lesions.21,50,94,96 Although the role of prophylactic antibiotics in cranial neurosurgery was debated after its initial use by Cairns in 1947,82 more recent data strongly support timely prophylactic antibiotic use in this patient population.7,13,16,34,43,95,108 Additionally, broader surgical guidelines support methods such as maintaining intraoperative normothermia, appropriate methods of hair removal, confirmation of proper asepsis, and antisepsis of skin and instruments.115 The Surgical Care Improvement Project has been implemented and has reported on specific procedural groupings with good effect,102 but the results have not yet been incorporated into neurosurgical data. In neurosurgery, use of an endoscopic approach for certain lesions may be beneficial63 but has not been evaluated prospectively.

Surgery-Related Hematoma

Postoperative hemorrhage is a significant and potentially devastating concern. Overall rates range from 1.1% to 4.4%.21,80,87,94,107 Eighty-eight percent of these hemorrhages occurred within the first 6 hours after surgery.107

Options commonly employed to minimize the risk of postoperative hematoma include meticulous intraoperative hemostasis, use of absorbable topical hemostatic agents,38 technical maneuvers including peripheral and central tack-up stitches,53 minimization of postoperative hypertension and fluid shifts,100 and judicious use of perioperative antithrombotic prophylaxis. No convincing randomized studies have been done on this topic, however. One of the most important preventive measures for this event is correction of coagulopathy and early discontinuation of antiplatelet and anticoagulation therapy preoperatively. There are also strategies to recognize bleeding early enough to avert mortality or new deficit, including vigilant neurological monitoring and routine postoperative imaging for high-risk patients.58

Wrong-Site Surgery

Cohen et al.24 described wrong-site surgery as perhaps “the most regrettable and egregious error a surgeon can commit.” These cases are persistent and often highly publicized. Their analysis of 35 cases of wrong site operations suggested that operating at the incorrect site in neurosurgery most frequently results from communication breakdown, failure to follow standard checks, and technical factors such as mislabeled imaging.24

Conclusions

Surgery for intracranial neoplasms carries a high risk of adverse events. A significant proportion may be avoidable using practices to encourage standardized protocols, improved teamwork and communication, increased use of beneficial technologies, and concentrated experiences and specializations. Compared with other surgical fields, however, these strategies have been sparingly used in cranial tumor surgery. Concerted efforts aimed at large-scale monitoring of neurosurgical complications and consistent quality improvement within these highlighted realms may significantly improve patient outcomes. These ideas are discussed in more detail in the summary paper of this series.114

Disclosure

This work is funded by a US Agency for Healthcare Quality and Research grant (1R18 HS018537-01). Dr. Gawande receives royalties on his publications and books about patient safety.

Author contributions to the study and manuscript preparation include the following. Conception and design: Gawande, Bader. Acquisition of data: Wong, Panchmatia. Analysis and interpretation of data: Wong, Panchmatia. Drafting the article: Wong, Panchmatia, Ziewacz. Critically revising the article: all authors. Reviewed submitted version of manuscript: Gawande, Wong, Dunn, Laws. Approved the final version of the manuscript on behalf of all authors: Gawande. Study supervision: Gawande, Bader.

Portions of this work were presented in oral abstract form at the New England Neurosurgical Society annual meeting in Chatham Bars, Massachusetts, in June 2011.

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Article Information

Address correspondence to: Atul A. Gawande, M.D., M.P.H., Department of Surgery, Brigham and Women's Hospital, 75 Francis Street, Boston, Massachusetts 02115. email: agawande@partners.org.

Please include this information when citing this paper: DOI: 10.3171/2012.7.FOCUS12183.

© AANS, except where prohibited by US copyright law.

Headings

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