- Email: [email protected]
Conscious Experience and Psychological Consequences of Awake Craniotomy
Original Article
Conscious Experience and Psychological Consequences of Awake Craniotomy Nader Hejrati1,2, Derek Spieler3, Robin Samuel4, Luca Regli5, Astrid Weyerbrock1, Werner Surbeck6
BACKGROUND: Experiencing cranial surgery under awake conditions may expose patients to considerable psychological strain.
-
METHODS: This study aimed to investigate the occurrence and course of psychological sequelae following awake craniotomy (AC) for brain tumors in a series of 20 patients using a broad, validated psychological assessment preoperatively, intraoperatively, postoperatively and a standardized follow-up of 3 months. In addition, the association of the preoperative psychological condition (including, but not limited to, anxiety and fear) with perioperative pain perception and interference was assessed.
-
RESULTS: AC did not induce any shift in the median levels of anxiety, depression, and stress symptoms already present prior to the procedure. Furthermore, anxiety and depression were all moderately to strongly associated over time (all P < 0.05). Stress symptoms also correlated positively over all times of measurement. Stress 3 days after surgery was strongly associated with stress 3 months after surgery (P < 0.001), whereas the correlation between preoperative and immediate postoperative stress showed a statistical trend (P [ 0.07). Preoperative fear was not related to intraoperative pain, but to pain and its interference with daily activity on the third postoperative day (P < 0.001 and P < 0.01, respectively).
-
CONCLUSIONS: Postoperative psychological symptoms clearly correlated with their corresponding preoperative
-
symptoms. Thus, mental health was not negatively affected by the AC experience in our series. Intraoperative fear and pain were not related to the preoperative psychological condition. However, preoperative fear and anxiety were positively related with pain and its interference with daily activity in the immediate postoperative period.
INTRODUCTION
A
wake craniotomy (AC) for tumors within or adjacent to eloquent brain regions has become increasingly routine in today’s neurosurgical practice, allowing for maximal tumor resection, extending life expectancy, and, most importantly, minimizing the risk of postoperative neurologic deficits, thus preserving the patient’s quality of life.1-5 However, experiencing cranial surgery under awake conditions might expose patients to considerable psychological strain. This is all the more significant as patients suffering from brain tumors display higher rates of mental distress, and are more prone to experiencing anxiety and/or depression as compared with patients suffering from tumors at other cancer sites.6,7 Previous studies reported that AC is generally well tolerated and overall patient satisfaction is high,8-19 with anxiety being the most commonly reported psychological phenomenon.16,20,21 Nevertheless, only a few studies have assessed patient tolerance and psychological consequences of this exceptional experience using standardized and validated questionnaires.14,17 Psychological aspects going beyond perioperative anxiety and fear have been particularly
Key words Awake craniotomy - Brain tumor - Depression - Fear - Pain perception - Psychology - Stress
From the 1Department of Neurosurgery, Cantonal Hospital St. Gallen, St. Gallen, Switzerland; 2 Department of Neurosurgery, University Hospital Basel, Basel, Switzerland; 3Department of Psychosomatic Medicine and Psychotherapy, University Medical Center Freiburg, AlbertLudwigs University, Freiburg, Germany; 4Research Unit INSIDE, University of Luxembourg, Esch-sur-Alzette, Luxembourg; 5Department of Neurosurgery, University Hospital Zurich, Zurich, Switzerland; and 6Department of Psychiatry, Psychotherapy and Psychosomatics, Psychiatric Hospital of the University of Zurich, Zurich, Switzerland
Abbreviations and Acronyms AC: Awake craniotomy BPI: Brief Pain Inventory HADS-D: Hospital Anxiety and Depression Scale, German version LGG: Low-grade glioma NRS: Numeric Rating Scale PHQ-D: Patient Health Questionnaire, German version PTSD: Posttraumatic stress disorder
Citation: World Neurosurg. (2019) 129:e381-e386. https://doi.org/10.1016/j.wneu.2019.05.156
-
WORLD NEUROSURGERY 129: e381-e386, SEPTEMBER 2019
To whom correspondence should be addressed: Werner Surbeck, M.D., Ph.D. [E-mail: [email protected]]
Journal homepage: www.journals.elsevier.com/world-neurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
www.journals.elsevier.com/world-neurosurgery
e381
ORIGINAL ARTICLE NADER HEJRATI ET AL.
CONSEQUENCES OF AWAKE CRANIOTOMY
neglected. The little information available presents a diverse picture of postoperative sequelae ranging from psychiatric morbidity resembling posttraumatic stress disorder (PTSD) in some cases,17 to deep psychological change and maturation in others.22 Some of these studies lack preoperative psychological data,8-10,12,14-17,23 limiting the drawing of causal conclusions, with follow-up periods of a few days9-12,14,23 or over 12 months,15,17,22 with the latter limiting the ability to differentiate between psychological sequelae of the surgery and those of the underlying tumor disease and related psychosocial factors. The present study aimed to investigate the occurrence and course of psychological sequelae following AC in a series of 20 patients using a broad, validated psychological assessment, and a standardized follow-up of 3 months. In addition, the association of the preoperative psychological condition (fear, anxiety, depression, and stress) with perioperative pain perception was assessed. METHODS Study Design and Setting From December 2015 to January 2018, we conducted a prospective, single center, clinical study at the Cantonal Hospital St. Gallen, Switzerland. Data were collected using standardized and validated questionnaires. Written informed consent was obtained from every patient. Collection of patient data for scientific purposes were approved by the Cantonal ethics committee (reference number: EKSG 15/157).
either intubated and kept under general anesthesia for the rest of the procedure or kept under analgosedation without intubation. Procedures Pain and fear were evaluated on the day prior to surgery, intraoperatively, and on the third postoperative day using the Numeric Rating Scale (NRS).24,25 Stress and anxiety were evaluated on the day prior to surgery, on the third postoperative day, and during the 3-month postoperative outpatient visit using the Hospital Anxiety and Depression Scale (HADS-D [German version]),26 and the Patient Health Questionnaire (PHQ-D [German version]),27 whereas pain and its interference with daily activities was evaluated using the Brief Pain Inventory (BPI)28,29 (for a timeline, see Supplementary Table 1). The Questionnaires NRS. Preoperative assessment of fear and pain was evaluated using the NRS24,25 on a scale of 0e10. Intraoperatively, the NRS was used at 3 timepoints (before skin incision, after craniotomy, and after tumor resection) to assess for fear and pain. A score of 0 indicates the absence of pain or fear, whereas a score of 10 indicates the maximum possible pain or fear. HADS-D. The HADS-D26 (German version) serves as a tool to screen for fear and depression in patients with physical diseases or symptoms, while evaluating the characteristics of anxious and depressive symptoms of the past week. The overall sum can be considered as the general mental impairment with >9 points suggesting depression and >11 points suggesting fear.
Patient Selection Patients aged between 18 and 75 years, referred to the department of neurosurgery because of an intracerebral lesion and in whom AC was performed owing to the proximity or infiltration of eloquent brain regions by the pathology were included. Contraindications for AC such as developmental delay, a significant communication barrier, important reflux or obesity, as well as an inability to obtain patient consent constituted exclusion criteria. None of the patients had been under psychiatric treatment, and consequently no psychotropic drugs were taken. If antiseizure medication was given, then patients were in an already wellestablished steady state without any sedating effect. Pain medication was administered according to demand.
PHQ-D. PTSD-related symptoms of intrinsic sensory hyperactivity and disinhibition (irritability, outbursts of anger, hyper-vigilance, and an exaggerated startle response) as well as intrusive flash backs were recorded by means of corresponding items of the PHQ-D27 (German version).
Anesthesiologic Regimen A scalp block using 0.25% bupivacaine with clonidine 2 mg/mL to a maximum of 1.25 mg bupivacaine per kg body weight was performed in every patient before head fixation in a Mayfield clamp. The standard protocol in patients undergoing AC at our institution is the awake-awake-asleep protocol. Controlled conscious analgosedation is achieved using low doses of propofol and remifentanil. If patients complain of pain, local anesthesia is applied between the dural sheets before dural opening. Once the dura is opened, analgosedation is stopped to achieve optimal conditions for vigilance and compliance required for functional mapping. After the functionally relevant boundaries are defined, the tumor in or in close proximity to functional brain areas or pathways, or, in most cases, the whole tumor is resected under functional monitoring. After tumor resection, the patient is
Statistical Analysis To examine whether the procedure induced any change in psychological symptoms, we tested for 1) shifts in average levels in the metrics, and 2) their association over time. We used Wilcoxon matched-pairs signed-ranks tests for 1, and Spearman rank correlations were calculated to assess for 2. To analyze the relation of preoperative fear to intraoperative and postoperative pain, we employed Spearman rank correlations. In addition, we ran a random-effects ordered logistic model to assess the overall association of fear and pain over time, controlling for age and sex. A 2-sided P value of <0.05 was considered significant. No correction for multiple testing was applied. Statistical analyses were performed using Stata version 15.1 (StataCorp, College Station, Texas, USA).
e382
www.SCIENCEDIRECT.com
BPI. The BPI28,29 is a validated questionnaire to measure pain and its interference with 7 daily activities. It assesses pain at its “worst,” “least,” “average,” and “now” (current pain), on a scale from 0e10, in which 0 indicates no pain at all and 10 indicates the worst imaginable pain. A pain interference score is calculated as the mean of the 7 interference items, 0 indicating no interference and 10 indicating the worst possible interference.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.05.156
ORIGINAL ARTICLE NADER HEJRATI ET AL.
CONSEQUENCES OF AWAKE CRANIOTOMY
RESULTS The selection criteria resulted in a series of 20 surgical procedures in 20 patients (11 men, 9 women; median age 56 years, range 20e72 years). Of the 20 participants, 1 patient refused to answer the postoperative questionnaire due to bad health condition and 3 did not answer the outpatient questionnaires (1 died due to impetuous disease progression, and 1 refusal due to bad health condition). Patient characteristics and disease specifics are shown in Supplementary Table 2. Median fear (NRS) decreased over time, whereas pain (NRS) increased (Table 1). The maximum range for fear (NRS) was observed on the day before and 3 days after surgery. Relation of Psychological Symptoms Over Time A series of tests of all medians of differences of anxiety, depression, and stress over time suggested that the procedure did not induce any shift in the median levels of symptoms already present prior to the procedure (all P > 0.12). Anxiety and depression were moderately to strongly associated over time (all P < 0.05; Table 2). Stress symptoms also correlated positively over all timepoints of the study period. Stress 3 days after surgery was strongly associated with stress 3 months after surgery, whereas the correlation between preoperative and immediate postoperative stress showed a statistical trend (P ¼ 0.07). Relation of Preoperative Fear to Intraoperative and Postoperative Pain Preoperative fear and anxiety were not related to preoperative and intraoperative pain, but to pain reported 3 days after surgery
(Table 3). Depression and stress were not associated with pain. Analyzing the relation of fear (NRS) to pain (NRS) at each observational timepoint, however, revealed that they were related intraoperatively (after craniotomy: r ¼ 0.62, P ¼ 0.01). Preoperative fear and anxiety were related to postoperative pain intensity (Table 4). Furthermore, preoperative fear and anxiety were related to postoperative pain interference (Table 5). Depression and stress were not associated with pain interference. DISCUSSION AC has evolved into an essential adjunct in neurologic surgery for patients suffering from brain tumors within or adjacent to eloquent brain regions, helping the neurosurgeon to preserve the patient’s quality of life. However, newly diagnosed neoplastic processes, in particular brain tumors, put the patient into considerable psychological distress.6,7 Although AC is usually well tolerated,8-18 it may be regarded as an additional traumatic incidence with possible negative consequences on mental health. In this context, Milian et al.17 investigated the presence/absence of symptoms of PTSD in patients undergoing AC. Although they did not observe patients suffering from symptomatic PTSD based on a self-developed inventory related to the Diagnostic and Statistical Manual of Mental Disorders, 4th Edition criteria, distinct sequelae of PTSD, such as increased arousal, avoidance of stimuli, or intense fear occurred more frequently. However, because preoperative psychological data are lacking, a causal relation of the symptomatology with the intervention can only be surmised. In the present series, AC did not induce any shift in the median levels of anxiety, depression, and stress symptoms already present
Table 1. Median and Range of Key Measures Over Time
Fear (NRS)
Pain (NRS)
Anxiety (HADS-D)
Depression (HADS-D)
Stress (PHQ-D)
Pain intensity
Pain interference
Observations
Day Before Surgery
Intraoperative Before Skin Incision
Intraoperative After Craniotomy
Intraoperative After Tumor Resection
3 Days After Surgery
3 Months After Surgery
3
1
1
0.5
0.5
e
0e10
0e8
0e7
0e8
0e10
e
0
0
0.5
1.5
2
e
0e5
0e7
0e5
0e7
0e6
e
7
e
e
e
6
6
1e13
e
e
e
0e16
0e12
3
e
e
e
3
4
0e15
e
e
e
1e19
1e10
3
e
e
e
4
2.5
0e15
e
e
e
0e12
0e9
0.5
e
e
e
1.3
0.8
0e5
e
e
e
0e8.8
0e7.3
1.1
e
e
e
1.3
1
0e6
e
e
e
0e6.6
0e6.3
20
18
18
18
19
18
Note: e indicates that no measure was taken. NRS, Numeric Rating Scale; HADS-D, Hospital Anxiety and Depression Scale, German version; PHQ-D, Patient Health Questionnaire, German version.
WORLD NEUROSURGERY 129: e381-e386, SEPTEMBER 2019
www.journals.elsevier.com/world-neurosurgery
e383
ORIGINAL ARTICLE NADER HEJRATI ET AL.
CONSEQUENCES OF AWAKE CRANIOTOMY
Table 2. Spearman Rank Correlations of Psychological Symptoms Over Time Day Before Surgery
Table 4. Spearman Rank Correlations of Fear and Preoperative Psychological Symptoms with Pain Intensity
3 Days After Surgery
Pain Intensity
Anxiety (HADS-D) 3 days after surgery
0.80z
1
3 months after surgery
0.68y
0.82z
3 days after surgery
0.58y
1
3 months after surgery
0.65y
0.54*
3 Days After Surgery
3 Months After Surgery
0.05
0.47*
0.29
0.45*
0.52*
0.09
0.43
0.15
0.03
0.00
0.09
0.00
Fear (NRS) Day before surgery
Depression (HADS-D)
Day Before Surgery
Anxiety (HADS-D) Day before surgery Depression (HADS-D)
Stress (PHQ-D) 3 days after surgery
0.44
3 months after surgery
0.44
1 0.81z
Measures taken preoperatively (day before surgery, n ¼ 20), postoperatively (3 days after surgery, n ¼ 19), and as outpatients (3 months after surgery, n ¼ 18). HADS-D, Hospital Anxiety and Depression Scale, German version; PHQ-D, Patient Health Questionnaire, German version. *P <0.05. yP <0.01. zP <0.001.
prior to the procedure. Furthermore, anxiety, depression, and stress were positively associated over time. When taken together, these findings suggest that the procedure did not induce a systematic change in psychological symptoms at the individual level. One of the 20 patient in our series, however, reported intrusive flash backs 3 days after the procedure, which resolved over the subsequent observation period. Thus, patients with relevant psychological distress generally already displayed their symptoms
Day before surgery Stress (PHQ-D) Day before surgery
Measures taken preoperatively (day before surgery, n ¼ 20), postoperatively (3 days after surgery, n ¼ 19), and as outpatients (3 months after surgery, n ¼ 18). NRS, Numeric Rating Scale; HADS-D, Hospital Anxiety and Depression Scale, German version; PHQ-D, Patient Health Questionnaire, German version. *P <0.05.
before surgery and the AC experience did not adversely affect mental health. This finding is in line with the report by Goebel et al.,23 observing no significant changes in patients’ emotional well-being preoperatively to postoperatively. However, the latter excluded patients suffering from severe anxiety or depression from the study.23 Considering that anxiety is the most commonly reported psychological phenomenon associated with AC,16,20,21 and the patient’s attitude toward fear of pain is generally assumed to be
Table 3. Spearman Rank Correlations of Fear and Preoperative Psychological Symptoms with Pain Pain (NRS) Day Before Surgery
Intraoperative Before Skin Incision
Intraoperative After Craniotomy
Intraoperative After Tumor Resection
3 Days After Surgery
0.03
0.28
0.15
0.10
0.77z
0.34
0.02
0.02
0.07
0.49*
0.29
0.14
0.18
e0.15
0.18
0.13
0.17
0.15
0.37
0.10
Fear (NRS) Day before surgery Anxiety (HADS-D) Day before surgery Depression (HADS-D) Day before surgery Stress (PHQ-D) Day before surgery
Measures taken preoperatively (day before surgery, n ¼ 20), postoperatively (3 days after surgery, n ¼ 19), and as outpatients (3 months after surgery, n ¼ 18). NRS, Numeric Rating Scale; HADS-D, Hospital Anxiety and Depression Scale, German version; PHQ-D, Patient Health Questionnaire, German version. *P <0.05. zP <0.001.
e384
www.SCIENCEDIRECT.com
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.05.156
ORIGINAL ARTICLE NADER HEJRATI ET AL.
CONSEQUENCES OF AWAKE CRANIOTOMY
Table 5. Spearman Rank Correlations of Preoperative Psychological Symptoms with Pain Interference Pain Interference Day Before Surgery
3 Days After Surgery
3 Months After Surgery
0.10
0.69y
0.41
0.37
0.72*
0.26
0.34
0.28
0.20
0.20
0.06
0.17
Fear (NRS) Day before surgery Anxiety (HADS-D) Day before surgery Depression (HADS-D) Day before surgery Stress (PHQ-D) Day before surgery
Measures taken preoperatively (day before surgery, n ¼ 20), postoperatively (3 days after surgery, n ¼ 19), and as outpatients (3 months after surgery, n ¼ 18). NRS, Numeric Rating Scale; HADS-D, Hospital Anxiety and Depression Scale, German version; PHQ-D, Patient Health Questionnaire, German version. *P <0.05. yP <0.01.
related to the individual pain threshold,20 anxiety and pain has attracted some scientific interest in this context. This topic is all the more of interest considering that anxiety, discomfort, and pain might negatively affect concentration and cooperation of the patient during the procedure, and thereby directly influence surgical outcome.12 Data from previous studies indicated that in 10%-14% of the patients severe anxiety was present throughout the procedure.8,9,16 Significant pain and discomfort is reported in up to 20% of patients,8,9,12 and is generally related to patient positioning, the head clamp, and dural opening.11,30 Although preoperative fear and anxiety were not related to pain perception during surgery (or 3 months thereafter) in our series, such an association was found with regard to pain reported 3 days after the procedure (Tables 2,3, and 4). A concurrent relationship between preoperative fear and anxiety and the interference of pain with daily activities 3 days after the intervention, as measured by the BPI, may indicate the need for a longer hospitalization in patients fearing surgery. Preoperative depressive mood and stress symptoms were unrelated to perioperative pain, pain intensity, and pain interference. Nonetheless, as previously shown,20 intraoperative fear and pain were clearly related. The recent finding that women and younger patients reported higher intraoperative levels of anxiety16 can, however, only be partly supported by our data. Overall, fear (and pain) experienced before, during, or after surgery was independent of patient age and sex. However, intraoperative fear just after craniotomy was negatively correlated with age.
WORLD NEUROSURGERY 129: e381-e386, SEPTEMBER 2019
These results underline the importance of establishing a positive therapeutic relationship with the patient, wherever possible, in the presurgical outpatient setting as repeatedly stressed,9,15,16,18 to reduce uncertainty and anxiety and establish trust for the purpose of a comfortable and uneventful perioperative period. This study has several limitations. First, the associations reported do not permit causal interpretation. Because all patients underwent AC, we could not calculate an average treatment effect and could not exclude potential selection bias. However, randomized controlled trials are obviously not an option in this case. Second, heterogeneity of diagnosis and age are 2 limiting factors that may influence psychological burden. Comparing young (<35 years) with older patients (50 years) in our sample, revealed that, overall, young patients exhibited higher levels of fear (NRS) compared with older patients. However, there were no significant differences between young and older patients in relation to other psychological outcomes. Furthermore, there were no overall differences between the groups with high-grade pathologies (high-grade glioma and metastasis) versus the one with lowgrade pathologies (low-grade glioma [LGG] and cavernoma) in fear (NRS) and pain (NRS). However, the group with low-grade pathologies reported significantly higher levels of anxiety, depression, and stress as compared with the group with highgrade pathologies. Importantly, the overall patterns observed for correlations reproduced in the subgroup of high-grade and lowgrade pathologies. Given the small number of cases in the subgroups, however, most of the correlations did not attain conventional levels of significance. Further studies should attempt to collect more data to enable a detailed analysis of subgroups and to assess heterogeneity in associations of pain and psychological symptoms over time. Finally, we did not control for adjuvant treatment at the postoperative course. Although for patients with LGG, some degree of compromise in health-related quality of life was found at 7e15 months after radiotherapy,31 no such was seen in patients with high-grade glioma who had undergone adjuvant radiotherapy and chemotherapy with temozolomide.32,33 When it comes to adjuvant chemotherapy with temozolomide in LGG patients, no negative effects on health-related quality of life were observed.34
CONCLUSIONS The results of this study provide evidence that mental health is not put at risk by the AC experience. Interestingly, intraoperative pain was not related to the preoperative psychological condition. However, preoperative fear and anxiety were positively correlated with pain and its interference with daily activity in the immediate postoperative period.
ACKNOWLEDGMENTS The authors thank Tim Killeen for English editing.
www.journals.elsevier.com/world-neurosurgery
e385
ORIGINAL ARTICLE NADER HEJRATI ET AL.
REFERENCES 1. Sanai N, Berger MS. Glioma extent of resection and its impact on patient outcome. Neurosurgery. 2008;62:753-764. 2. De Benedictis A, Moritz-Gasser S, Duffau H. Awake mapping optimizes the extent of resection for low-grade gliomas in eloquent areas. Neurosurgery. 2010;66:1074-1084. 3. Brown T, Shah AH, Bregy A, et al. Awake craniotomy for brain tumor resection: the rule rather than the exception? J Neurosurg Anesthesiol. 2013;25: 240-247. 4. Grossman R, Nossek E, Sitt R, et al. Outcome of elderly patients undergoing awake-craniotomy for tumor resection. Ann Surg Oncol. 2013;20: 1722-1728.
CONSEQUENCES OF AWAKE CRANIOTOMY
undergoing awake craniotomy for intracranial masses: expectations, recall, satisfaction and functional outcome. Br J Neurosurg. 2011;25: 391-400.
26. Bjelland I, Dahl AA, Haug TT, Neckelmann D. The validity of the Hospital Anxiety and Depression Scale: an updated literature review. J Psychosom Res. 2002;52:69-77.
14. Wrede KH, Stieglitz LH, Fiferna A, et al. Patient acceptance of awake craniotomy. Clin Neurol Neurosurg. 2011;113:880-884.
27. Gräfe K, Zipfel S, Herzog W, Löwe B. Screening psychischer Störungen mit dem “Gesundheitsfragebogen für Patienten (PHQ-D)” Daignostica. 2004; 50:11.
15. Fletcher KJ, das Nair R, Macniven JAB, Basu S, Byrne P. An interpretative phenomenological analysis of the patient experience of awake craniotomy: brain tumour diagnosis to discharge. Br J Health Psychol. 2012;17:828-842.
28. Cleeland CS, Ryan KM. Pain assessment: global use of the brief pain inventory. Ann Acad Med Singapore. 1994;23:129-138.
16. Beez T, Boge K, Wager M, et al. Tolerance of awake surgery for glioma: a prospective European Low Grade Glioma Network multicenter study. Acta Neurochir (Wien). 2013;155:1301-1308.
29. Radbruch L, Loick G, Kiencke P, et al. Validation of the German version of the Brief Pain Inventory. J Pain Symptom Manag. 1999;18:180-187. 30. Joswig H, Bratelj D, Brunner T, Jacomet A, Hildebrandt G, Surbeck W. Awake craniotomy: first-year experiences and patient perception. World Neurosurg. 2016;90:588-596.
5. Surbeck W, Hildebrandt G, Duffau H. The evolution of brain surgery on awake patients. Acta Neurochir (Wien). 2015;157:77-84.
17. Milian M, Luerding R, Ploppa A, et al. “Imagine your neighbor mows the lawn”: a pilot study of psychological sequelae due to awake craniotomy: clinical article. J Neurosurg. 2013;118:1288-1295.
6. Zabora J, Brintzenhofeszoc K, Curbow B, Hooker C, Piantadosi S. The prevalence of psychological distress by cancer site. Psycho-oncology. 2001;10:19-28.
18. Khu KJ, Doglietto F, Radovanovic I, et al. Patients’ perceptions of awake and outpatient craniotomy for brain tumor: a qualitative study. J Neurosurg. 2010;112:1056-1060.
7. Goebel S, Stark AM, Kaup L, von Harscher M, Mehdorn HM. Distress in patients with newly diagnosed brain tumours. Psycho-oncology. 2011;20: 623-630.
19. Milian M, Tatagiba M, Feigl GC. Patient response to awake craniotomy: a summary overview. Acta Neurochir (Wien). 2014;156:1063-1070.
32. Osoba D, Brada M, Yung WKA, Prados M. Healthrelated quality of life in patients treated with temozolomide versus procarbazine for recurrent glioblastoma multiforme. J Clin Oncol. 2000;18: 1481-1491.
20. Santini B, Talacchi A, Casagrande F, et al. Eligibility criteria and psychological profiles in patient candidates for awake craniotomy: a pilot study. J Neurosurg Anesthesiol. 2012;24:209-216.
33. Taphoorn MJB, Stupp R, Coens C, et al. Healthrelated quality of life in patients with glioblastoma: a randomised controlled trial. Lancet Oncol. 2005;6:937-944.
21. Potters JW, Klimek M. Awake craniotomy: improving the patient’s experience. Curr Opin Anesthesiol. 2015;28:511-516.
34. Liu R, Solheim K, Polley MY, et al. Quality of life in low-grade glioma patients receiving temozolomide. Neuro Oncol. 2009;11:59-68.
8. Danks RA, Rogers M, Aglio LS, Gugino LD, Black PM. Patient tolerance of craniotomy performed with the patient under local anesthesia and monitored conscious sedation. Neurosurgery. 1998;42:28-34. 9. Whittle IR, Midgley S, Georges H, Pringle AM, Taylor R. Patient perceptions of “awake” brain tumour surgery. Acta Neurochir (Wien). 2005;147: 275-277. 10. Manninen PH, Balki M, Lukitto K, Bernstein M. Patient satisfaction with awake craniotomy for tumor surgery: a comparison of remifentanil and fentanyl in conjunction with propofol. Anesth Analg. 2006;102:237-242. 11. Palese A, Skrap M, Fachin M, Visioli S, Zannini L. The experience of patients undergoing awake craniotomy. Cancer Nurs. 2008;31:166-172. 12. Wahab SS, Grundy PL, Weidmann C. Patient experience and satisfaction with awake craniotomy for brain tumours. Br J Neurosurg. 2011;25: 606-613. 13. Manchella S, Khurana VG, Duke D, Brussel T, French J, Zuccherelli L. The experience of patients
e386
www.SCIENCEDIRECT.com
22. Campanella F, Palese A, Del Missier F, et al. Longterm cognitive functioning and psychological well-being in surgically treated patients with lowgrade glioma. World Neurosurg. 2017;103:799-808. 23. Goebel S, Nabavi A, Schubert S, Mehdorn HM. Patient perception of combined awake brain tumor surgery and intraoperative 1.5-T magnetic resonance imaging: the Kiel experience. Neurosurgery. 2010;67:594-600. 24. Kremer E, Atkinson JH, Ignelzi RJ. Measurement of pain: patient preference does not confound pain measurement. Pain. 1981;10:241-248. 25. Farrar JT, Portenoy RK, Berlin JA, Kinman JL, Strom BL. Defining the clinically important difference in pain outcome measures. Pain. 2000;88: 287-294.
31. Kiebert GM, Curran D, Aaronson NK, et al. Quality of life after radiation therapy of cerebral low-grade gliomas of the adult: results of a randomised phase III trial on dose response (EORTC trial 22844). Eur J Cancer. 1998;34:1902-1909.
Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 12 March 2019; accepted 17 May 2019 Citation: World Neurosurg. (2019) 129:e381-e386. https://doi.org/10.1016/j.wneu.2019.05.156 Journal homepage: www.journals.elsevier.com/worldneurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.05.156
Conscious Experience and Psychological Consequences of Awake Craniotomy Nader Hejrati1,2, Derek Spieler3, Robin Samuel4, Luca Regli5, Astrid Weyerbrock1, Werner Surbeck6
BACKGROUND: Experiencing cranial surgery under awake conditions may expose patients to considerable psychological strain.
-
METHODS: This study aimed to investigate the occurrence and course of psychological sequelae following awake craniotomy (AC) for brain tumors in a series of 20 patients using a broad, validated psychological assessment preoperatively, intraoperatively, postoperatively and a standardized follow-up of 3 months. In addition, the association of the preoperative psychological condition (including, but not limited to, anxiety and fear) with perioperative pain perception and interference was assessed.
-
RESULTS: AC did not induce any shift in the median levels of anxiety, depression, and stress symptoms already present prior to the procedure. Furthermore, anxiety and depression were all moderately to strongly associated over time (all P < 0.05). Stress symptoms also correlated positively over all times of measurement. Stress 3 days after surgery was strongly associated with stress 3 months after surgery (P < 0.001), whereas the correlation between preoperative and immediate postoperative stress showed a statistical trend (P [ 0.07). Preoperative fear was not related to intraoperative pain, but to pain and its interference with daily activity on the third postoperative day (P < 0.001 and P < 0.01, respectively).
-
CONCLUSIONS: Postoperative psychological symptoms clearly correlated with their corresponding preoperative
-
symptoms. Thus, mental health was not negatively affected by the AC experience in our series. Intraoperative fear and pain were not related to the preoperative psychological condition. However, preoperative fear and anxiety were positively related with pain and its interference with daily activity in the immediate postoperative period.
INTRODUCTION
A
wake craniotomy (AC) for tumors within or adjacent to eloquent brain regions has become increasingly routine in today’s neurosurgical practice, allowing for maximal tumor resection, extending life expectancy, and, most importantly, minimizing the risk of postoperative neurologic deficits, thus preserving the patient’s quality of life.1-5 However, experiencing cranial surgery under awake conditions might expose patients to considerable psychological strain. This is all the more significant as patients suffering from brain tumors display higher rates of mental distress, and are more prone to experiencing anxiety and/or depression as compared with patients suffering from tumors at other cancer sites.6,7 Previous studies reported that AC is generally well tolerated and overall patient satisfaction is high,8-19 with anxiety being the most commonly reported psychological phenomenon.16,20,21 Nevertheless, only a few studies have assessed patient tolerance and psychological consequences of this exceptional experience using standardized and validated questionnaires.14,17 Psychological aspects going beyond perioperative anxiety and fear have been particularly
Key words Awake craniotomy - Brain tumor - Depression - Fear - Pain perception - Psychology - Stress
From the 1Department of Neurosurgery, Cantonal Hospital St. Gallen, St. Gallen, Switzerland; 2 Department of Neurosurgery, University Hospital Basel, Basel, Switzerland; 3Department of Psychosomatic Medicine and Psychotherapy, University Medical Center Freiburg, AlbertLudwigs University, Freiburg, Germany; 4Research Unit INSIDE, University of Luxembourg, Esch-sur-Alzette, Luxembourg; 5Department of Neurosurgery, University Hospital Zurich, Zurich, Switzerland; and 6Department of Psychiatry, Psychotherapy and Psychosomatics, Psychiatric Hospital of the University of Zurich, Zurich, Switzerland
Abbreviations and Acronyms AC: Awake craniotomy BPI: Brief Pain Inventory HADS-D: Hospital Anxiety and Depression Scale, German version LGG: Low-grade glioma NRS: Numeric Rating Scale PHQ-D: Patient Health Questionnaire, German version PTSD: Posttraumatic stress disorder
Citation: World Neurosurg. (2019) 129:e381-e386. https://doi.org/10.1016/j.wneu.2019.05.156
-
WORLD NEUROSURGERY 129: e381-e386, SEPTEMBER 2019
To whom correspondence should be addressed: Werner Surbeck, M.D., Ph.D. [E-mail: [email protected]]
Journal homepage: www.journals.elsevier.com/world-neurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
www.journals.elsevier.com/world-neurosurgery
e381
ORIGINAL ARTICLE NADER HEJRATI ET AL.
CONSEQUENCES OF AWAKE CRANIOTOMY
neglected. The little information available presents a diverse picture of postoperative sequelae ranging from psychiatric morbidity resembling posttraumatic stress disorder (PTSD) in some cases,17 to deep psychological change and maturation in others.22 Some of these studies lack preoperative psychological data,8-10,12,14-17,23 limiting the drawing of causal conclusions, with follow-up periods of a few days9-12,14,23 or over 12 months,15,17,22 with the latter limiting the ability to differentiate between psychological sequelae of the surgery and those of the underlying tumor disease and related psychosocial factors. The present study aimed to investigate the occurrence and course of psychological sequelae following AC in a series of 20 patients using a broad, validated psychological assessment, and a standardized follow-up of 3 months. In addition, the association of the preoperative psychological condition (fear, anxiety, depression, and stress) with perioperative pain perception was assessed. METHODS Study Design and Setting From December 2015 to January 2018, we conducted a prospective, single center, clinical study at the Cantonal Hospital St. Gallen, Switzerland. Data were collected using standardized and validated questionnaires. Written informed consent was obtained from every patient. Collection of patient data for scientific purposes were approved by the Cantonal ethics committee (reference number: EKSG 15/157).
either intubated and kept under general anesthesia for the rest of the procedure or kept under analgosedation without intubation. Procedures Pain and fear were evaluated on the day prior to surgery, intraoperatively, and on the third postoperative day using the Numeric Rating Scale (NRS).24,25 Stress and anxiety were evaluated on the day prior to surgery, on the third postoperative day, and during the 3-month postoperative outpatient visit using the Hospital Anxiety and Depression Scale (HADS-D [German version]),26 and the Patient Health Questionnaire (PHQ-D [German version]),27 whereas pain and its interference with daily activities was evaluated using the Brief Pain Inventory (BPI)28,29 (for a timeline, see Supplementary Table 1). The Questionnaires NRS. Preoperative assessment of fear and pain was evaluated using the NRS24,25 on a scale of 0e10. Intraoperatively, the NRS was used at 3 timepoints (before skin incision, after craniotomy, and after tumor resection) to assess for fear and pain. A score of 0 indicates the absence of pain or fear, whereas a score of 10 indicates the maximum possible pain or fear. HADS-D. The HADS-D26 (German version) serves as a tool to screen for fear and depression in patients with physical diseases or symptoms, while evaluating the characteristics of anxious and depressive symptoms of the past week. The overall sum can be considered as the general mental impairment with >9 points suggesting depression and >11 points suggesting fear.
Patient Selection Patients aged between 18 and 75 years, referred to the department of neurosurgery because of an intracerebral lesion and in whom AC was performed owing to the proximity or infiltration of eloquent brain regions by the pathology were included. Contraindications for AC such as developmental delay, a significant communication barrier, important reflux or obesity, as well as an inability to obtain patient consent constituted exclusion criteria. None of the patients had been under psychiatric treatment, and consequently no psychotropic drugs were taken. If antiseizure medication was given, then patients were in an already wellestablished steady state without any sedating effect. Pain medication was administered according to demand.
PHQ-D. PTSD-related symptoms of intrinsic sensory hyperactivity and disinhibition (irritability, outbursts of anger, hyper-vigilance, and an exaggerated startle response) as well as intrusive flash backs were recorded by means of corresponding items of the PHQ-D27 (German version).
Anesthesiologic Regimen A scalp block using 0.25% bupivacaine with clonidine 2 mg/mL to a maximum of 1.25 mg bupivacaine per kg body weight was performed in every patient before head fixation in a Mayfield clamp. The standard protocol in patients undergoing AC at our institution is the awake-awake-asleep protocol. Controlled conscious analgosedation is achieved using low doses of propofol and remifentanil. If patients complain of pain, local anesthesia is applied between the dural sheets before dural opening. Once the dura is opened, analgosedation is stopped to achieve optimal conditions for vigilance and compliance required for functional mapping. After the functionally relevant boundaries are defined, the tumor in or in close proximity to functional brain areas or pathways, or, in most cases, the whole tumor is resected under functional monitoring. After tumor resection, the patient is
Statistical Analysis To examine whether the procedure induced any change in psychological symptoms, we tested for 1) shifts in average levels in the metrics, and 2) their association over time. We used Wilcoxon matched-pairs signed-ranks tests for 1, and Spearman rank correlations were calculated to assess for 2. To analyze the relation of preoperative fear to intraoperative and postoperative pain, we employed Spearman rank correlations. In addition, we ran a random-effects ordered logistic model to assess the overall association of fear and pain over time, controlling for age and sex. A 2-sided P value of <0.05 was considered significant. No correction for multiple testing was applied. Statistical analyses were performed using Stata version 15.1 (StataCorp, College Station, Texas, USA).
e382
www.SCIENCEDIRECT.com
BPI. The BPI28,29 is a validated questionnaire to measure pain and its interference with 7 daily activities. It assesses pain at its “worst,” “least,” “average,” and “now” (current pain), on a scale from 0e10, in which 0 indicates no pain at all and 10 indicates the worst imaginable pain. A pain interference score is calculated as the mean of the 7 interference items, 0 indicating no interference and 10 indicating the worst possible interference.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.05.156
ORIGINAL ARTICLE NADER HEJRATI ET AL.
CONSEQUENCES OF AWAKE CRANIOTOMY
RESULTS The selection criteria resulted in a series of 20 surgical procedures in 20 patients (11 men, 9 women; median age 56 years, range 20e72 years). Of the 20 participants, 1 patient refused to answer the postoperative questionnaire due to bad health condition and 3 did not answer the outpatient questionnaires (1 died due to impetuous disease progression, and 1 refusal due to bad health condition). Patient characteristics and disease specifics are shown in Supplementary Table 2. Median fear (NRS) decreased over time, whereas pain (NRS) increased (Table 1). The maximum range for fear (NRS) was observed on the day before and 3 days after surgery. Relation of Psychological Symptoms Over Time A series of tests of all medians of differences of anxiety, depression, and stress over time suggested that the procedure did not induce any shift in the median levels of symptoms already present prior to the procedure (all P > 0.12). Anxiety and depression were moderately to strongly associated over time (all P < 0.05; Table 2). Stress symptoms also correlated positively over all timepoints of the study period. Stress 3 days after surgery was strongly associated with stress 3 months after surgery, whereas the correlation between preoperative and immediate postoperative stress showed a statistical trend (P ¼ 0.07). Relation of Preoperative Fear to Intraoperative and Postoperative Pain Preoperative fear and anxiety were not related to preoperative and intraoperative pain, but to pain reported 3 days after surgery
(Table 3). Depression and stress were not associated with pain. Analyzing the relation of fear (NRS) to pain (NRS) at each observational timepoint, however, revealed that they were related intraoperatively (after craniotomy: r ¼ 0.62, P ¼ 0.01). Preoperative fear and anxiety were related to postoperative pain intensity (Table 4). Furthermore, preoperative fear and anxiety were related to postoperative pain interference (Table 5). Depression and stress were not associated with pain interference. DISCUSSION AC has evolved into an essential adjunct in neurologic surgery for patients suffering from brain tumors within or adjacent to eloquent brain regions, helping the neurosurgeon to preserve the patient’s quality of life. However, newly diagnosed neoplastic processes, in particular brain tumors, put the patient into considerable psychological distress.6,7 Although AC is usually well tolerated,8-18 it may be regarded as an additional traumatic incidence with possible negative consequences on mental health. In this context, Milian et al.17 investigated the presence/absence of symptoms of PTSD in patients undergoing AC. Although they did not observe patients suffering from symptomatic PTSD based on a self-developed inventory related to the Diagnostic and Statistical Manual of Mental Disorders, 4th Edition criteria, distinct sequelae of PTSD, such as increased arousal, avoidance of stimuli, or intense fear occurred more frequently. However, because preoperative psychological data are lacking, a causal relation of the symptomatology with the intervention can only be surmised. In the present series, AC did not induce any shift in the median levels of anxiety, depression, and stress symptoms already present
Table 1. Median and Range of Key Measures Over Time
Fear (NRS)
Pain (NRS)
Anxiety (HADS-D)
Depression (HADS-D)
Stress (PHQ-D)
Pain intensity
Pain interference
Observations
Day Before Surgery
Intraoperative Before Skin Incision
Intraoperative After Craniotomy
Intraoperative After Tumor Resection
3 Days After Surgery
3 Months After Surgery
3
1
1
0.5
0.5
e
0e10
0e8
0e7
0e8
0e10
e
0
0
0.5
1.5
2
e
0e5
0e7
0e5
0e7
0e6
e
7
e
e
e
6
6
1e13
e
e
e
0e16
0e12
3
e
e
e
3
4
0e15
e
e
e
1e19
1e10
3
e
e
e
4
2.5
0e15
e
e
e
0e12
0e9
0.5
e
e
e
1.3
0.8
0e5
e
e
e
0e8.8
0e7.3
1.1
e
e
e
1.3
1
0e6
e
e
e
0e6.6
0e6.3
20
18
18
18
19
18
Note: e indicates that no measure was taken. NRS, Numeric Rating Scale; HADS-D, Hospital Anxiety and Depression Scale, German version; PHQ-D, Patient Health Questionnaire, German version.
WORLD NEUROSURGERY 129: e381-e386, SEPTEMBER 2019
www.journals.elsevier.com/world-neurosurgery
e383
ORIGINAL ARTICLE NADER HEJRATI ET AL.
CONSEQUENCES OF AWAKE CRANIOTOMY
Table 2. Spearman Rank Correlations of Psychological Symptoms Over Time Day Before Surgery
Table 4. Spearman Rank Correlations of Fear and Preoperative Psychological Symptoms with Pain Intensity
3 Days After Surgery
Pain Intensity
Anxiety (HADS-D) 3 days after surgery
0.80z
1
3 months after surgery
0.68y
0.82z
3 days after surgery
0.58y
1
3 months after surgery
0.65y
0.54*
3 Days After Surgery
3 Months After Surgery
0.05
0.47*
0.29
0.45*
0.52*
0.09
0.43
0.15
0.03
0.00
0.09
0.00
Fear (NRS) Day before surgery
Depression (HADS-D)
Day Before Surgery
Anxiety (HADS-D) Day before surgery Depression (HADS-D)
Stress (PHQ-D) 3 days after surgery
0.44
3 months after surgery
0.44
1 0.81z
Measures taken preoperatively (day before surgery, n ¼ 20), postoperatively (3 days after surgery, n ¼ 19), and as outpatients (3 months after surgery, n ¼ 18). HADS-D, Hospital Anxiety and Depression Scale, German version; PHQ-D, Patient Health Questionnaire, German version. *P <0.05. yP <0.01. zP <0.001.
prior to the procedure. Furthermore, anxiety, depression, and stress were positively associated over time. When taken together, these findings suggest that the procedure did not induce a systematic change in psychological symptoms at the individual level. One of the 20 patient in our series, however, reported intrusive flash backs 3 days after the procedure, which resolved over the subsequent observation period. Thus, patients with relevant psychological distress generally already displayed their symptoms
Day before surgery Stress (PHQ-D) Day before surgery
Measures taken preoperatively (day before surgery, n ¼ 20), postoperatively (3 days after surgery, n ¼ 19), and as outpatients (3 months after surgery, n ¼ 18). NRS, Numeric Rating Scale; HADS-D, Hospital Anxiety and Depression Scale, German version; PHQ-D, Patient Health Questionnaire, German version. *P <0.05.
before surgery and the AC experience did not adversely affect mental health. This finding is in line with the report by Goebel et al.,23 observing no significant changes in patients’ emotional well-being preoperatively to postoperatively. However, the latter excluded patients suffering from severe anxiety or depression from the study.23 Considering that anxiety is the most commonly reported psychological phenomenon associated with AC,16,20,21 and the patient’s attitude toward fear of pain is generally assumed to be
Table 3. Spearman Rank Correlations of Fear and Preoperative Psychological Symptoms with Pain Pain (NRS) Day Before Surgery
Intraoperative Before Skin Incision
Intraoperative After Craniotomy
Intraoperative After Tumor Resection
3 Days After Surgery
0.03
0.28
0.15
0.10
0.77z
0.34
0.02
0.02
0.07
0.49*
0.29
0.14
0.18
e0.15
0.18
0.13
0.17
0.15
0.37
0.10
Fear (NRS) Day before surgery Anxiety (HADS-D) Day before surgery Depression (HADS-D) Day before surgery Stress (PHQ-D) Day before surgery
Measures taken preoperatively (day before surgery, n ¼ 20), postoperatively (3 days after surgery, n ¼ 19), and as outpatients (3 months after surgery, n ¼ 18). NRS, Numeric Rating Scale; HADS-D, Hospital Anxiety and Depression Scale, German version; PHQ-D, Patient Health Questionnaire, German version. *P <0.05. zP <0.001.
e384
www.SCIENCEDIRECT.com
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.05.156
ORIGINAL ARTICLE NADER HEJRATI ET AL.
CONSEQUENCES OF AWAKE CRANIOTOMY
Table 5. Spearman Rank Correlations of Preoperative Psychological Symptoms with Pain Interference Pain Interference Day Before Surgery
3 Days After Surgery
3 Months After Surgery
0.10
0.69y
0.41
0.37
0.72*
0.26
0.34
0.28
0.20
0.20
0.06
0.17
Fear (NRS) Day before surgery Anxiety (HADS-D) Day before surgery Depression (HADS-D) Day before surgery Stress (PHQ-D) Day before surgery
Measures taken preoperatively (day before surgery, n ¼ 20), postoperatively (3 days after surgery, n ¼ 19), and as outpatients (3 months after surgery, n ¼ 18). NRS, Numeric Rating Scale; HADS-D, Hospital Anxiety and Depression Scale, German version; PHQ-D, Patient Health Questionnaire, German version. *P <0.05. yP <0.01.
related to the individual pain threshold,20 anxiety and pain has attracted some scientific interest in this context. This topic is all the more of interest considering that anxiety, discomfort, and pain might negatively affect concentration and cooperation of the patient during the procedure, and thereby directly influence surgical outcome.12 Data from previous studies indicated that in 10%-14% of the patients severe anxiety was present throughout the procedure.8,9,16 Significant pain and discomfort is reported in up to 20% of patients,8,9,12 and is generally related to patient positioning, the head clamp, and dural opening.11,30 Although preoperative fear and anxiety were not related to pain perception during surgery (or 3 months thereafter) in our series, such an association was found with regard to pain reported 3 days after the procedure (Tables 2,3, and 4). A concurrent relationship between preoperative fear and anxiety and the interference of pain with daily activities 3 days after the intervention, as measured by the BPI, may indicate the need for a longer hospitalization in patients fearing surgery. Preoperative depressive mood and stress symptoms were unrelated to perioperative pain, pain intensity, and pain interference. Nonetheless, as previously shown,20 intraoperative fear and pain were clearly related. The recent finding that women and younger patients reported higher intraoperative levels of anxiety16 can, however, only be partly supported by our data. Overall, fear (and pain) experienced before, during, or after surgery was independent of patient age and sex. However, intraoperative fear just after craniotomy was negatively correlated with age.
WORLD NEUROSURGERY 129: e381-e386, SEPTEMBER 2019
These results underline the importance of establishing a positive therapeutic relationship with the patient, wherever possible, in the presurgical outpatient setting as repeatedly stressed,9,15,16,18 to reduce uncertainty and anxiety and establish trust for the purpose of a comfortable and uneventful perioperative period. This study has several limitations. First, the associations reported do not permit causal interpretation. Because all patients underwent AC, we could not calculate an average treatment effect and could not exclude potential selection bias. However, randomized controlled trials are obviously not an option in this case. Second, heterogeneity of diagnosis and age are 2 limiting factors that may influence psychological burden. Comparing young (<35 years) with older patients (50 years) in our sample, revealed that, overall, young patients exhibited higher levels of fear (NRS) compared with older patients. However, there were no significant differences between young and older patients in relation to other psychological outcomes. Furthermore, there were no overall differences between the groups with high-grade pathologies (high-grade glioma and metastasis) versus the one with lowgrade pathologies (low-grade glioma [LGG] and cavernoma) in fear (NRS) and pain (NRS). However, the group with low-grade pathologies reported significantly higher levels of anxiety, depression, and stress as compared with the group with highgrade pathologies. Importantly, the overall patterns observed for correlations reproduced in the subgroup of high-grade and lowgrade pathologies. Given the small number of cases in the subgroups, however, most of the correlations did not attain conventional levels of significance. Further studies should attempt to collect more data to enable a detailed analysis of subgroups and to assess heterogeneity in associations of pain and psychological symptoms over time. Finally, we did not control for adjuvant treatment at the postoperative course. Although for patients with LGG, some degree of compromise in health-related quality of life was found at 7e15 months after radiotherapy,31 no such was seen in patients with high-grade glioma who had undergone adjuvant radiotherapy and chemotherapy with temozolomide.32,33 When it comes to adjuvant chemotherapy with temozolomide in LGG patients, no negative effects on health-related quality of life were observed.34
CONCLUSIONS The results of this study provide evidence that mental health is not put at risk by the AC experience. Interestingly, intraoperative pain was not related to the preoperative psychological condition. However, preoperative fear and anxiety were positively correlated with pain and its interference with daily activity in the immediate postoperative period.
ACKNOWLEDGMENTS The authors thank Tim Killeen for English editing.
www.journals.elsevier.com/world-neurosurgery
e385
ORIGINAL ARTICLE NADER HEJRATI ET AL.
REFERENCES 1. Sanai N, Berger MS. Glioma extent of resection and its impact on patient outcome. Neurosurgery. 2008;62:753-764. 2. De Benedictis A, Moritz-Gasser S, Duffau H. Awake mapping optimizes the extent of resection for low-grade gliomas in eloquent areas. Neurosurgery. 2010;66:1074-1084. 3. Brown T, Shah AH, Bregy A, et al. Awake craniotomy for brain tumor resection: the rule rather than the exception? J Neurosurg Anesthesiol. 2013;25: 240-247. 4. Grossman R, Nossek E, Sitt R, et al. Outcome of elderly patients undergoing awake-craniotomy for tumor resection. Ann Surg Oncol. 2013;20: 1722-1728.
CONSEQUENCES OF AWAKE CRANIOTOMY
undergoing awake craniotomy for intracranial masses: expectations, recall, satisfaction and functional outcome. Br J Neurosurg. 2011;25: 391-400.
26. Bjelland I, Dahl AA, Haug TT, Neckelmann D. The validity of the Hospital Anxiety and Depression Scale: an updated literature review. J Psychosom Res. 2002;52:69-77.
14. Wrede KH, Stieglitz LH, Fiferna A, et al. Patient acceptance of awake craniotomy. Clin Neurol Neurosurg. 2011;113:880-884.
27. Gräfe K, Zipfel S, Herzog W, Löwe B. Screening psychischer Störungen mit dem “Gesundheitsfragebogen für Patienten (PHQ-D)” Daignostica. 2004; 50:11.
15. Fletcher KJ, das Nair R, Macniven JAB, Basu S, Byrne P. An interpretative phenomenological analysis of the patient experience of awake craniotomy: brain tumour diagnosis to discharge. Br J Health Psychol. 2012;17:828-842.
28. Cleeland CS, Ryan KM. Pain assessment: global use of the brief pain inventory. Ann Acad Med Singapore. 1994;23:129-138.
16. Beez T, Boge K, Wager M, et al. Tolerance of awake surgery for glioma: a prospective European Low Grade Glioma Network multicenter study. Acta Neurochir (Wien). 2013;155:1301-1308.
29. Radbruch L, Loick G, Kiencke P, et al. Validation of the German version of the Brief Pain Inventory. J Pain Symptom Manag. 1999;18:180-187. 30. Joswig H, Bratelj D, Brunner T, Jacomet A, Hildebrandt G, Surbeck W. Awake craniotomy: first-year experiences and patient perception. World Neurosurg. 2016;90:588-596.
5. Surbeck W, Hildebrandt G, Duffau H. The evolution of brain surgery on awake patients. Acta Neurochir (Wien). 2015;157:77-84.
17. Milian M, Luerding R, Ploppa A, et al. “Imagine your neighbor mows the lawn”: a pilot study of psychological sequelae due to awake craniotomy: clinical article. J Neurosurg. 2013;118:1288-1295.
6. Zabora J, Brintzenhofeszoc K, Curbow B, Hooker C, Piantadosi S. The prevalence of psychological distress by cancer site. Psycho-oncology. 2001;10:19-28.
18. Khu KJ, Doglietto F, Radovanovic I, et al. Patients’ perceptions of awake and outpatient craniotomy for brain tumor: a qualitative study. J Neurosurg. 2010;112:1056-1060.
7. Goebel S, Stark AM, Kaup L, von Harscher M, Mehdorn HM. Distress in patients with newly diagnosed brain tumours. Psycho-oncology. 2011;20: 623-630.
19. Milian M, Tatagiba M, Feigl GC. Patient response to awake craniotomy: a summary overview. Acta Neurochir (Wien). 2014;156:1063-1070.
32. Osoba D, Brada M, Yung WKA, Prados M. Healthrelated quality of life in patients treated with temozolomide versus procarbazine for recurrent glioblastoma multiforme. J Clin Oncol. 2000;18: 1481-1491.
20. Santini B, Talacchi A, Casagrande F, et al. Eligibility criteria and psychological profiles in patient candidates for awake craniotomy: a pilot study. J Neurosurg Anesthesiol. 2012;24:209-216.
33. Taphoorn MJB, Stupp R, Coens C, et al. Healthrelated quality of life in patients with glioblastoma: a randomised controlled trial. Lancet Oncol. 2005;6:937-944.
21. Potters JW, Klimek M. Awake craniotomy: improving the patient’s experience. Curr Opin Anesthesiol. 2015;28:511-516.
34. Liu R, Solheim K, Polley MY, et al. Quality of life in low-grade glioma patients receiving temozolomide. Neuro Oncol. 2009;11:59-68.
8. Danks RA, Rogers M, Aglio LS, Gugino LD, Black PM. Patient tolerance of craniotomy performed with the patient under local anesthesia and monitored conscious sedation. Neurosurgery. 1998;42:28-34. 9. Whittle IR, Midgley S, Georges H, Pringle AM, Taylor R. Patient perceptions of “awake” brain tumour surgery. Acta Neurochir (Wien). 2005;147: 275-277. 10. Manninen PH, Balki M, Lukitto K, Bernstein M. Patient satisfaction with awake craniotomy for tumor surgery: a comparison of remifentanil and fentanyl in conjunction with propofol. Anesth Analg. 2006;102:237-242. 11. Palese A, Skrap M, Fachin M, Visioli S, Zannini L. The experience of patients undergoing awake craniotomy. Cancer Nurs. 2008;31:166-172. 12. Wahab SS, Grundy PL, Weidmann C. Patient experience and satisfaction with awake craniotomy for brain tumours. Br J Neurosurg. 2011;25: 606-613. 13. Manchella S, Khurana VG, Duke D, Brussel T, French J, Zuccherelli L. The experience of patients
e386
www.SCIENCEDIRECT.com
22. Campanella F, Palese A, Del Missier F, et al. Longterm cognitive functioning and psychological well-being in surgically treated patients with lowgrade glioma. World Neurosurg. 2017;103:799-808. 23. Goebel S, Nabavi A, Schubert S, Mehdorn HM. Patient perception of combined awake brain tumor surgery and intraoperative 1.5-T magnetic resonance imaging: the Kiel experience. Neurosurgery. 2010;67:594-600. 24. Kremer E, Atkinson JH, Ignelzi RJ. Measurement of pain: patient preference does not confound pain measurement. Pain. 1981;10:241-248. 25. Farrar JT, Portenoy RK, Berlin JA, Kinman JL, Strom BL. Defining the clinically important difference in pain outcome measures. Pain. 2000;88: 287-294.
31. Kiebert GM, Curran D, Aaronson NK, et al. Quality of life after radiation therapy of cerebral low-grade gliomas of the adult: results of a randomised phase III trial on dose response (EORTC trial 22844). Eur J Cancer. 1998;34:1902-1909.
Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 12 March 2019; accepted 17 May 2019 Citation: World Neurosurg. (2019) 129:e381-e386. https://doi.org/10.1016/j.wneu.2019.05.156 Journal homepage: www.journals.elsevier.com/worldneurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.05.156