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Review Articles

Monitoring cognition during awake brain surgery in adults: A systematic review

Carla RuisDepartment of Neurology and Neurosurgery, University Medical Center Utrecht, Utrecht, The Netherlands;Experimental Psychology, Utrecht University, Utrecht, The NetherlandsCorrespondence[email protected]
Pages 1081-1104 | Received 05 Feb 2018, Accepted 18 Apr 2018, Published online: 01 Aug 2018

ABSTRACT

Introduction: Historically, most studies about awake brain surgery have focused on language or motor functions. More recently, other cognitive functions have also been assessed. However, a clear overview of the neuropsychological tests or test paradigms that are used during such procedures is missing. The primary research question of this review is: What neuropsychological tests or paradigms are used during awake brain surgery? This review aims to give an extensive overview about the assessment of cognition during awake brain surgery.

Method: A systematic search was performed in PubMed and Embase. Studies about awake surgery that mentioned a specific test or test paradigm for assessing cognition were included in this review.

Results: The search yielded 4,052 articles. A manual selection for cognition in title and abstract resulted in 360 studies. Those were evaluated in full text; 212 articles described a cognitive task or paradigm. Further reference-list search yielded 20 more studies. In 207 of 232 studies, a test for assessment of language is reported. Tests for the visuospatial domain and motor and sensory functions are described in, respectively, only 23 and 20 studies. Tests for memory, calculation, emotions, or other cognitive functions are reported only in a minority of the included studies.

Conclusions: Tests for assessment of language functions during awake brain surgery are widely reported. Other cognitive functions are underexposed. There is a need for development of tests or paradigms for assessment of other cognitive functions so that the broad spectrum of cognition can be monitored during awake brain surgery.

Awake brain surgery has been performed frequently in the past several years, especially in patients suffering from epilepsy or a brain tumor in an eloquent area. Literature shows that awake brain surgery results in a more extensive resection (De Benedictis, Moritz-Gasser, & Duffau, Citation2010) and fewer neurological deficits (Hamer, Robles, Zwinderman, Duffau, & Berger, Citation2012).

Table 1. Studies included in the review, with cognitive domains monitored during surgery and test/paradigm used to assess the domain.

Table 2. Overview of described tests or paradigms used for measurement of different cognitive functions during awake brain surgery.

Figure 1. Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) flow diagram of the systematic literature search.

Figure 1. Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) flow diagram of the systematic literature search.

Figure 2. Number of studies reporting tests or paradigms per cognitive domain during awake brain surgery (total number of studies included in review = 232). *Other: executive functions, face recognition, musical skills, finger gnosis.

Figure 2. Number of studies reporting tests or paradigms per cognitive domain during awake brain surgery (total number of studies included in review = 232). *Other: executive functions, face recognition, musical skills, finger gnosis.

During awake brain surgery, cognitive functions are monitored. The use of neuropsychological tests during awake brain surgery is not comparable to a standard neuropsychological assessment. Such tests have to meet specific criteria. Administration has to be done during electrical stimulation, and consequently presentation time of stimuli has to be short. Furthermore, repeated measurements are usually necessary within one operation, so a test must have many stimuli, and possible learning effects should be minimalized.

Traditionally, awake surgery was usually done when a tumor was in a language area in the dominant hemisphere (Coello et al., Citation2013), or when motor functions needed to be monitored. There was much attention paid to preservation of language and motor functions (Grossman & Ram, Citation2013). Several reviews are available specifically addressing language mapping (e.g., De Witte & Mariën, Citation2013; Rofes & Miceli, Citation2014).

More recently, awake brain surgery has also been done in patients with lesions in different areas than language areas in the dominant hemisphere. This asks for other cognitive tasks or neuropsychological test paradigms. More and more often, tests for monitoring other cognitive functions are described: for example, visuospatial functions (Conner et al., Citation2016) or calculation (Kurimoto et al., Citation2006). However, an overview of different neuropsychological tests used during awake surgery is missing. A review of Duffau (Citation2010) gives an overview of mapping of nonlanguage functions during awake surgery. However, instead of tests, cognitive domains are described. More recently, Coello and colleagues (Citation2013) presented an overview of different tasks that can be used intraoperatively. In this study, specific parameters such as tumor location and functional networks were used to create a personalized protocol for a patient. However, both studies are not based on a systematic review of the literature, and the cognitive domains or tests are not described from a neuropsychological perspective.

The primary research question for this systematic research is therefore: What neuropsychological tests or paradigms are used during awake brain surgery in brain tumor or epilepsy patients? In contrast to the study of Coello (Citation2013), we include not only studies that describe brain tumor patients but also studies concerning epilepsy patients, so that we can review a wide range of tests used in awake surgeries. This overview will help clinicians in selecting tasks for monitoring cognition during awake brain surgery, taking into account the patient’s lesion and cognitive complaints. We hope to make clear which cognitive domains are best covered by different neuropsychological tests and which cognitive domains are not yet covered. Subsequently, this overview can be helpful in clarifying which domains are most in need of new test development so that cognition can be monitored in the most optimal way.

Method

A systematic literature search was conducted using PubMed and Embase up to February 2017.

We designed a framework for the search strategy, wherein we searched for diseases in combination with awake brain surgery (disease [e.g., tumor] AND procedure [e.g., neurosurgery]) AND (awake [e.g., local anesthesia]). For exact search strategies for PubMed and Embase, see Appendix.

A pilot search made clear that when adding a factor “cognition” to the search strategy, too many relevant articles were not found. Therefore, the author has chosen not to include this factor in our search, but screen for cognition manually in the first results.

Title and abstract screening and full-text reviews were based on the following inclusion criteria:

  • English language.

  • Original article (no review, letter to editor, etc.).

  • Intraoperative measurement of cognition during awake brain surgery.

  • Clear description of test or paradigm used during awake brain surgery.

  • Age of patients ≥18.

When there was any doubt about whether an article met the inclusion criteria (for example about intra- or extraoperatively measurement of cognition), the original author of the study was contacted, when possible.

After papers were selected from the literature search in PubMed and Embase, reference list searching was used to identify possible missing papers.

From each paper included in this review, a description of the cognitive domain that was monitored during awake brain surgery and a description of the test or neuropsychological test paradigm used was abstracted.

Results

The PubMed search yielded 3,792 results, and a second search in Embase resulted in 578 additional articles (see ). After removing duplicates, the author manually screened 4,052 articles for the factor cognition in title or abstract, and 360 papers were potentially relevant. Those 360 papers were assessed in full text for eligibility. This study included 212 papers. By reference list searching, another 20 papers were added.

As can be seen in , papers were excluded from this review because of multiple reasons (another language than English, type of article, content not about cognition or awake brain surgery, etc.). Some issues are worth mentioning regarding the process of exclusion. The majority of studies about awake surgery describe that the procedure starts with mapping sensory and motor areas, because these areas tend to have lower thresholds. This kind of mapping is not included in this review. Moreover, when somatosensory functions are assessed more extensively, this is frequently done by sensations described by patients themself, and no specific test is described (e.g., Duffau et al., Citation1999). Comparably, patients can be instructed to report any contractions, movements, or loss of control of voluntary movements (e.g., Kumar et al., Citation2014). Only studies that described a specific test or standardized procedure for measurement of somatosensory and motor functions were included. In addition, mapping of motor functions is also often done by motor-evoked potentials under general anesthesia. Those studies were also excluded from this review.

In addition, many studies report that mapping of a cognitive function (e.g., language) was done, but no description of the test or test paradigm was given (see, e.g., Almairac, Herbet, Moritz-Gasser, & Duffau, Citation2014). Those studies were also excluded. Studies that made use of extraoperative cortical mapping (e.g., by use of a grid) are likewise excluded. During extraoperative mapping there is usually much more time to administer cognitive tests. Therefore, this procedure is not comparable to intraoperative direct electrical stimulation. Studies that describe mapping under awake conditions but resection under general anesthesia could be included (e.g., Ojemann & Schoenfield-McNeill, Citation1999; Weber & Ojemann, Citation1995; Zamora, Corina, & Ojemann, Citation2016), but mapping and resection had to be done in the same operation.

The studies included in this review are presented in . For each study, the cognitive domains that were monitored during surgery are presented in the second column, followed by a description of the tests used to assess this cognitive domain in the third column. The description of the tests or test paradigms is as detailed as possible but is dependent on how much information is given in the original articles. If specific standardized neuropsychological tests are mentioned, those are presented in italic.

Naming famous faces is described as a test for language (naming test) but also as a test for face recognition. Therefore, the author assigned this test to both the language domain and the face-recognition domain.

In , the total number of studies that describe tests or paradigms per cognitive domain are presented. From the 232 studies included in this review, 207 studies describe one or more tests/paradigms for assessment of language functions. Only a minority of the included studies describe tests for other cognitive domains, whereby visuospatial and sensory or motor functions are best represented, followed by tests for memory and calculation. Tests for assessment of executive functions, face recognition, musical skills, and finger gnosis are reported only sporadically.

summaries the tests/paradigms used per cognitive function during awake brain surgery.

Discussion

In this review the author provides an overview of the neuropsychological tests or paradigms that are used during awake brain surgery for brain tumors or epilepsy. Results of this study show that language is by far the most tested cognitive domain in awake brain surgery. Almost 90% of the studies included in this review describe a test or test paradigm for the assessment of language functions. Monitoring of this function is done by very simple tasks such as counting, to more complex or specific tasks such as semantic associations or translating skills. In addition to more experimental paradigms, a variety of standardized neuropsychological tests, such as the Test de Dénomination Orale D’Images (DO80; Deloche & Hannequin, Citation1997), Boston Naming Test (Kaplan, Goodglass, & Weintraub, Citation2001), and Pyramid and Palmtree Test (Howard & Patterson, Citation1992), are used in monitoring language functions.

Tests for motor or sensory functions are less frequently mentioned. This does not automatically mean that those functions are only rarely monitored during awake brain surgery. Actually, many studies report that they monitor those functions, but this is mostly done by asking a patient to report any sensations or movements, and no specific task or paradigm is administered. Moreover, as mentioned earlier in the Method section, motor functions are also often monitored by motor-evoked potentials. So, unless the fact that motor and sensory functions are frequently monitored during awake brain surgery, only a few studies describe a specific test or paradigm for the measurement of these domains.

Tests for visuospatial functions are also reported in just a few studies, followed by tests for memory, calculation, and emotions. Tests for the measurement of other cognitive functions such as face recognition, executive functions, musical skills, and finger gnosis are rare.

Only four studies included in this review describe a complete test battery that can be used during awake brain surgery. Two of them assess multiple cognitive domains (De Witte et al. Citation2015; Skrap, Marin, Ius, Fabbro, & Tomasino, Citation2016); the others focus on language (De Witte et al., Citation2015) and motor/sensory functions (Becker et al., Citation2016).

It is remarkable that in many studies only one cognitive domain is tested, sometimes with just one test (for example, only object naming). The minority of the studies included in this review describe monitoring of multiple cognitive functions and usage of different cognitive tests in an awake brain surgery.

It is also remarkable that language takes such an important part of the monitoring of cognition during awake brain surgery, while other cognitive functions are clearly underexposed. Of course, impairment in language functions can cause numerous participation problems in daily life, and preservation of this function is very important. On the other hand, deficits in, for example, executive functions may also have a great impact on daily life (Chan, Shum, Toulopoulou, & Chen, Citation2008), and preserved executive functions are important for self-regulation (Hofmann, Schmeichel, & Baddeley, Citation2012). A recent systematic review about neurocognitive functioning prior to antitumor treatment shows that the majority of patients have impairment in any cognitive domain. Especially executive functioning is frequently impaired (Van Kessel, Baumfalk, Van Zandvoort, Robe, & Snijders, Citation2017). While many patients have executive impairments prior to surgery, it is paradoxical that the monitoring of executive functions is only reported in such a small number of studies included in this review (Plaza, Du Boullay, Perrault, Chaby, & Capelle, Citation2014; Wager et al., Citation2013). Possibly, the fact that executive functions are less concrete than, for example, language and motor functions makes it more difficult to imagine the consequenses of deficits in this cognitive domain. Permanent deficits in language and motor functions are clearly not acceptable for patients, surgeons, and society. However, deficits in executive functions may have an impact on daily functioning and communication with others that is at least as big as the problems deriving from language disorders. Although assessment of executive functions seems difficult, some aspects of this cognitive domain such as inhibition can be perfectly tested intraoperatively by administration of, for example, an (adjusted) Stroop Color Word Test (Wager et al., Citation2013).

The majority of the studies included in this review describe experimental tasks or paradigms, and just a minority of the studies make use of well-known standardized tests (example DO80, line bisection task) or modification of those tests. This is not surprising, given that tests that are used during awake brain surgery must meet specific criteria. Because of the short simulation time, items of the test should have a short presentation time. Furthermore, because of the sometimes-long duration of the surgery, many comparable stimuli with a comparable level of difficulty are needed.On the other hand, learning effects should be limited as much as possible. It is also important that the responses on the test items are simple and clear and do not have a high chance level. Tests that require a yes/no answer are therefore unsuitable. Rofes and Miceli (Citation2014) give a detailed description of the design of intraoperative tasks specific for language mapping. Besides language-specific recommendations, they also state that tasks should be short (both in presentation of stimuli and in response from patients) and that the tasks should be sensitive enough to detect subtle changes. While specificity is important during regular neuropsychological assessment, sensitivity is most important in monitoring cognition during the intraoperative phase, so that changes in cognitive functioning can be detected. It is important to realize that intraoperative cognitive functioning is always compared to preoperative functioning, and therefore an extensive preoperative neuropsychological assessment is indispensable. It is clear that most standardized neuropsychological tests cannot be simply used during awake brain surgery. Keeping the abovementioned criteria in our minds, there is a need for development of new tests or paradigms (or modifications of existing tests) for the cognitive domains that are underexposed up to this point.

A limitation of this study may be the exclusion of studies that do not give a description of the tests or paradigms used for monitoring cognition during awake brain surgery. Although it was the specific goal of this study to include only studies that gave a description of how different cognitive functions are measured during awake brain surgery, this may distort the overall picture of measurement of cognition in such procedures. Many studies do mention that cognition is monitored, but because of a lack of further explanation of the way this was done, those studies were excluded from this review. For example, this review makes clear that only a few formalized tests for monitoring motor and sensory functions are described in different studies. On the other hand, this does not mean that these functions are also monitored only in a small proportion of the surgeries. Furthermore, it is plausible that in clinical practice, more specific tests are administered during awake brain surgery, but that those groups have not yet published about their procedures.

A strength of this study is the extensive systematic search of the literature. This is the first systematic review about monitoring cognition during awake brain surgery at test or neuropsychological paradigm level. Furthermore, the full width of cognition instead of a specific cognitive function, such as language, is studied.

Monitoring cognition during awake brain surgery is done more and more, and can usually not be captured in a strict protocol because of different locations of lesions and, as a result, different (possible) cognitive deficits. Individual patient care is needed, and most standardized neuropsychological tests cannot be used. This review can help clinicians in selecting tests that can be used during such a procedure so that optimal cognitive monitoring can be achieved. Sharing knowledge about this specific topic is important, and there is a need for scientific publications about new methods that are used in clinical care.

In summary, monitoring of language functions during awake brain surgery has been studied extensively, and many different tests or paradigms for assessing language functions have been described. Although there is no doubt about the importance of preserving language functions, it is remarkable that tests for other cognitive domains receive much less attention. The results of this review make clear that development of new tests for several cognitive domains is needed, so that cognition can be comprehensively monitored in awake brain surgeries.

Acknowledgments

The author would like to thank Paulien Wiersma for her support in constructing a search strategy.

Disclosure statement

No potential conflict of interest was reported by the author.

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Appendix

Search strategy used for Pubmed and Embase

PubMed

(“Brain Neoplasms”[MeSH:noexp] OR brain neoplasm*[Title/Abstract] OR brain tumor*[Title/Abstract] OR brain tumour*[Title/Abstract] OR “Glioma”[Mesh] OR glioma*[Title/Abstract] OR glioblastoma*[Title/Abstract] OR “Epilepsy”[MAJR] OR epilepsy[Title/Abstract] OR epilepsies[Title/Abstract]) AND (“Neurosurgical Procedures”[Mesh] OR “Cytoreduction Surgical Procedures”[Mesh] OR Cytoreduction Surgical Procedure*[Title/Abstract] OR reduction[Title/Abstract] OR debulking[Title/Abstract] OR remove[Title/Abstract] OR removal[Title/Abstract] OR surgery[Title/Abstract] OR craniotomy[Title/Abstract]) AND (“Anesthesia, Local”[Mesh] OR local anesthesia[Title/Abstract] OR local anaesthesia[Title/Abstract] OR “Transcranial Direct Current Stimulation”[Mesh] OR stimulat*[Title/Abstract] OR awake[Title/Abstract] OR penfield[Title/Abstract] OR “Monitoring, Intraoperative”[Mesh] OR intraoperative monitoring[Title/Abstract])

Embase

“brain tumor”/de OR brain AND neoplasm*:ti,ab OR brain AND tumour*:ti,ab OR “glioma”/exp OR glioma*:ti,ab OR glioblastoma*:ti,ab OR “epilepsy”/mj OR “epilepsy”:ti,ab OR epilepsies:ti,ab AND “cytoreductive surgery”/exp OR “neurosurgery”/exp OR cytoreductive AND surgery:ti,ab OR reduction:ti,ab OR debulking:ti,ab OR remove:ti,ab OR removal:ti,ab OR surgery:ti,ab OR craniotomy:ti,ab AND “local anesthesia”/exp OR “local anaesthesia”:ti,ab OR “transcranial direct current stimulation”/exp OR stimulat*:ti,ab OR awake:ti,ab OR penfield:ti,ab OR “neuromonitoring”/exp OR intraoperative AND monitoring:ti,ab AND [embase]/lim NOT [medline]/lim AND (“article”/it OR “article in press”/it OR “review”/it) AND [english]/lim

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