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Perioperative microdialysis in meningioma surgery: correlation of cerebral metabolites with clinical outcome

  • Clinical Article - Brain Tumors
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Abstract

Background

Brain tumour resection requires surgical manoeuvres that may cause an ischaemic injury to peritumoral tissue. The aim of the present study was to examine whether putative alterations in peritumoral tissue biochemistry, monitored by microdialysis, correlate with clinical outcome in patients undergoing craniotomy for meningioma resection.

Methods

In 34 patients undergoing meningioma resection (35 % male; mean age ± SD: 54.3 ± 12.1 years), microdialysis measurements were taken perioperatively from peritumoral brain parenchyma. Standard metabolites (glucose, lactate, pyruvate, glycerol and the lactate:pyruvate ratio) were quantified in relation to clinical outcome assessed by the Glasgow Coma Scale (GCS) and the Karnofsky Performance Status scale.

Results

Higher postoperative glucose and pyruvate levels were found in patients with a favourable outcome (GCS not deteriorated or Karnofsky score >80). Multiple logistic regression analysis (age, preoperative physical status, metabolite levels as independent variables) showed that lower postoperative glucose and pyruvate levels as well as higher lactate:pyruvate ratio values were independently associated with an unfavourable outcome as defined by Karnofsky score <80 [(OR: 0.084, 95 % CI: 0.01–0.98, p = 0.049), (OR: 0.97, 95 % CI: 0.95–0.99, p = 0.050), (OR: 1.21, 95 % CI: 1.04–1.42, p = 0.015) respectively], as well as with death [(OR: 0.08, 95 % CI: 0.01–0.97, p = 0.046), (OR: 0.94, 95 % CI: 0.89–0.99, p = 0.016), (OR: 1.07, 95 % CI: 1.00–1.15, p = 0.05) respectively].

Conclusions

Postoperative levels of glucose and pyruvate and the lactate:pyruvate ratio appear to correlate with clinical outcome in patients undergoing meningioma resection. The present findings provide support for the utility of microdialysis as a prognostic tool in brain tumour surgery.

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References

  1. Bergenheim AT, Roslin M, Ungerstedt U, Waldenstrom A, Henriksson R, Ronquist G (2006) Metabolic manipulation of glioblastoma in vivo by retrograde microdialysis of L-2, 4 diaminobutyric acid (DAB). J Neuro-Oncol 80:285–293

    Article  CAS  Google Scholar 

  2. Black PM, Morokoff AP, Zauberman J (2008) Surgery for extra-axial tumors of the cerebral convexity and midline. Neurosurgery 62:1115–1121, discussion 1121–1113

    Article  PubMed  Google Scholar 

  3. Blakeley JO, Olson J, Grossman SA, He X, Weingart J, Supko JG (2009) Effect of blood brain barrier permeability in recurrent high grade gliomas on the intratumoral pharmacokinetics of methotrexate: a microdialysis study. J Neuro-Oncol 91:51–58

    Article  CAS  Google Scholar 

  4. Chefer VI, Thompson AC, Zapata A, Shippenberg TS (2009) Overview of brain microdialysis. Curr Protoc Neurosci Chapter 7: Unit7 1

  5. De Micheli E, Alfieri A, Pinna G, Bianchi L, Colivicchi MA, Melani A, Pedata F, Della Corte L, Bricolo A (2000) Extracellular levels of taurine in tumoral, peritumoral and normal brain tissue in patients with malignant glioma: an intraoperative microdialysis study. Adv Exp Med Biol 483:621–625

    Article  PubMed  Google Scholar 

  6. De Micheli E, Pinna G, Alfieri A, Caramia G, Bianchi L, Colivicchi MA, Della Corte L, Bricolo A (2000) Post-operative monitoring of cortical taurine in patients with subarachnoid hemorrhage: a microdialysis study. Adv Exp Med Biol 483:595–603

    Article  PubMed  Google Scholar 

  7. Dutzmann S, Gessler F, Bink A, Quick J, Franz K, Seifert V, Senft C (2012) Risk of ischemia in glioma surgery: comparison of first and repeat procedures. J Neuro-Oncol 107:599–607

    Article  Google Scholar 

  8. El-Bahy K (2009) Validity of the frontolateral approach as a minimally invasive corridor for olfactory groove meningiomas. Acta Neurochir (Wien) 151:1197–1205

    Article  Google Scholar 

  9. Enblad P, Valtysson J, Andersson J, Lilja A, Valind S, Antoni G, Langstrom B, Hillered L, Persson L (1996) Simultaneous intracerebral microdialysis and positron emission tomography in the detection of ischemia in patients with subarachnoid hemorrhage. J Cereb Blood Flow Metab 16:637–644

    Article  CAS  PubMed  Google Scholar 

  10. Gempt J, Forschler A, Buchmann N, Pape H, Ryang YM, Krieg SM, Zimmer C, Meyer B, Ringel F (2013) Postoperative ischemic changes following resection of newly diagnosed and recurrent gliomas and their clinical relevance. J Neurosurg 118:801–808

    Article  PubMed  Google Scholar 

  11. Goodman JC (2011) Clinical microdialysis in neuro-oncology: principles and applications. Chin J Cancer 30:173–181

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  12. Hillered L, Persson L, Ponten U, Ungerstedt U (1990) Neurometabolic monitoring of the ischaemic human brain using microdialysis. Acta Neurochir (Wien) 102:91–97

    Article  CAS  Google Scholar 

  13. Hillered L, Valtysson J, Enblad P, Persson L (1998) Interstitial glycerol as a marker for membrane phospholipid degradation in the acutely injured human brain. J Neurol Neurosurg Psychiatry 64:486–491

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  14. Hutchinson PJ, O’Connell MT, Al-Rawi PG, Maskell LB, Kett-White R, Gupta AK, Richards HK, Hutchinson DB, Kirkpatrick PJ, Pickard JD (2000) Clinical cerebral microdialysis: a methodological study. J Neurosurg 93:37–43

    Article  CAS  PubMed  Google Scholar 

  15. Johnston AJ, Gupta AK (2002) Advanced monitoring in the neurology intensive care unit: microdialysis. Curr Opin Crit Care 8:121–127

    Article  PubMed  Google Scholar 

  16. Kett-White R, Hutchinson PJ, Al-Rawi PG, Gupta AK, Pickard JD, Kirkpatrick PJ (2002) Adverse cerebral events detected after subarachnoid hemorrhage using brain oxygen and microdialysis probes. Neurosurgery 50:1213–1221, discussion 1221–1212

    PubMed  Google Scholar 

  17. Konglund A, Rogne SG, Lund-Johansen M, Scheie D, Helseth E, Meling TR (2013) Outcome following surgery for intracranial meningiomas in the aging. Acta Neurol Scand 127:161–169

    Article  CAS  PubMed  Google Scholar 

  18. Landolt H, Langemann H (1996) Cerebral microdialysis as a diagnostic tool in acute brain injury. Eur J Anaesthesiol 13:269–278

    Article  CAS  PubMed  Google Scholar 

  19. Marcoux J, McArthur DA, Miller C, Glenn TC, Villablanca P, Martin NA, Hovda DA, Alger JR, Vespa PM (2008) Persistent metabolic crisis as measured by elevated cerebral microdialysis lactate-pyruvate ratio predicts chronic frontal lobe brain atrophy after traumatic brain injury. Crit Care Med 36:2871–2877

    Article  CAS  PubMed  Google Scholar 

  20. Marcus HJ, Carpenter KL, Price SJ, Hutchinson PJ (2010) In vivo assessment of high-grade glioma biochemistry using microdialysis: a study of energy-related molecules, growth factors and cytokines. J Neuro-Oncol 97:11–23

    Article  CAS  Google Scholar 

  21. Melani A, Corti F, Stephan H, Muller CE, Donati C, Bruni P, Vannucchi MG, Pedata F (2012) Ecto-ATPase inhibition: ATP and adenosine release under physiological and ischemic in vivo conditions in the rat striatum. Exp Neurol 233:193–204

    Article  CAS  PubMed  Google Scholar 

  22. Melani A, De Micheli E, Pinna G, Alfieri A, Corte LD, Pedata F (2003) Adenosine extracellular levels in human brain gliomas: an intraoperative microdialysis study. Neurosci Lett 346:93–96

    Article  CAS  PubMed  Google Scholar 

  23. Melani A, Turchi D, Vannucchi MG, Cipriani S, Gianfriddo M, Pedata F (2005) ATP extracellular concentrations are increased in the rat striatum during in vivo ischemia. Neurochem Int 47:442–448

    Article  CAS  PubMed  Google Scholar 

  24. Meyerson BA, Linderoth B, Karlsson H, Ungerstedt U (1990) Microdialysis in the human brain: extracellular measurements in the thalamus of parkinsonian patients. Life Sci 46:301–308

    Article  CAS  PubMed  Google Scholar 

  25. Mindermann T, Zimmerli W, Gratzl O (1998) Rifampin concentrations in various compartments of the human brain: a novel method for determining drug levels in the cerebral extracellular space. Antimicrob Agents Chemother 42:2626–2629

    CAS  PubMed Central  PubMed  Google Scholar 

  26. Nordstrom CH (2008) Insulin, intracerebral glucose and bedside biochemical monitoring utilizing microdialysis. Crit Care 12:124

    Article  PubMed Central  PubMed  Google Scholar 

  27. Nordstrom CH (2010) Cerebral energy metabolism and microdialysis in neurocritical care. Childs Nerv Syst 26:465–472

    Article  PubMed  Google Scholar 

  28. Persson L, Hillered L (1992) Chemical monitoring of neurosurgical intensive care patients using intracerebral microdialysis. J Neurosurg 76:72–80

    Article  CAS  PubMed  Google Scholar 

  29. Persson L, Valtysson J, Enblad P, Warme PE, Cesarini K, Lewen A, Hillered L (1996) Neurochemical monitoring using intracerebral microdialysis in patients with subarachnoid hemorrhage. J Neurosurg 84:606–616

    Article  CAS  PubMed  Google Scholar 

  30. Plock N, Kloft C (2005) Microdialysis–theoretical background and recent implementation in applied life-sciences. Eur J Pharm Sci 25:1–24

    Article  CAS  PubMed  Google Scholar 

  31. Rachinger W, Grau S, Tonn JC (2010) Different microsurgical approaches to meningiomas of the anterior cranial base. Acta Neurochir (Wien) 152:931–939

    Article  Google Scholar 

  32. Reinstrup P, Stahl N, Mellergard P, Uski T, Ungerstedt U, Nordstrom CH (2000) Intracerebral microdialysis in clinical practice: baseline values for chemical markers during wakefulness, anesthesia, and neurosurgery. Neurosurgery 47:701–709, discussion 709–710

    CAS  PubMed  Google Scholar 

  33. Roslin M, Henriksson R, Bergstrom P, Ungerstedt U, Bergenheim AT (2003) Baseline levels of glucose metabolites, glutamate and glycerol in malignant glioma assessed by stereotactic microdialysis. J Neuro-Oncol 61:151–160

    Article  Google Scholar 

  34. Sahuquillo J, Merino MA, Sanchez-Guerrero A, Arikan F, Vidal-Jorge M, Martinez-Valverde T, Rey A, Riveiro M, Poca MA (2014) Lactate and the lactate-to-pyruvate molar ratio cannot be used as independent biomarkers for monitoring brain energetic metabolism: a microdialysis study in patients with traumatic brain injuries. PLoS One 9:e102540

    Article  PubMed Central  PubMed  Google Scholar 

  35. Sarrafzadeh A, Haux D, Kuchler I, Lanksch WR, Unterberg AW (2004) Poor-grade aneurysmal subarachnoid hemorrhage: relationship of cerebral metabolism to outcome. J Neurosurg 100:400–406

    Article  PubMed  Google Scholar 

  36. Sarrafzadeh AS, Haux D, Ludemann L, Amthauer H, Plotkin M, Kuchler I, Unterberg AW (2004) Cerebral ischemia in aneurysmal subarachnoid hemorrhage: a correlative microdialysis-PET study. Stroke 35:638–643

    Article  PubMed  Google Scholar 

  37. Schlenk F, Graetz D, Nagel A, Schmidt M, Sarrafzadeh AS (2008) Insulin-related decrease in cerebral glucose despite normoglycemia in aneurysmal subarachnoid hemorrhage. Crit Care 12:R9

    Article  PubMed Central  PubMed  Google Scholar 

  38. Smith JS, Cha S, Mayo MC, McDermott MW, Parsa AT, Chang SM, Dillon WP, Berger MS (2005) Serial diffusion-weighted magnetic resonance imaging in cases of glioma: distinguishing tumor recurrence from postresection injury. J Neurosurg 103:428–438

    Article  PubMed  Google Scholar 

  39. Staub F, Graf R, Gabel P, Kochling M, Klug N, Heiss WD (2000) Multiple interstitial substances measured by microdialysis in patients with subarachnoid hemorrhage. Neurosurgery 47:1106–1115, discussion 1115–1106

    Article  CAS  PubMed  Google Scholar 

  40. Tisdall MM, Smith M (2006) Cerebral microdialysis: research technique or clinical tool. Br J Anaesth 97:18–25

    Article  CAS  PubMed  Google Scholar 

  41. Ulmer S, Braga TA, Barker FG 2nd, Lev MH, Gonzalez RG, Henson JW (2006) Clinical and radiographic features of peritumoral infarction following resection of glioblastoma. Neurology 67:1668–1670

    Article  CAS  PubMed  Google Scholar 

  42. Ungerstedt U (1997) Microdialysis in normal and injured human brain. In: Kinney JM, Tucker HN (eds) Physiology, stress and malnutrition: functional correlates, nutritional intervention. Lippincott-Raven Publishers, Philadelphia, pp 361–374

    Google Scholar 

  43. Valtysson J, Persson L, Hillered L (1998) Extracellular ischaemia markers in repeated global ischaemia and secondary hypoxaemia monitored by microdialysis in rat brain. Acta Neurochir (Wien) 140:387–395

    Article  CAS  Google Scholar 

  44. Vespa PM, McArthur D, O’Phelan K, Glenn T, Etchepare M, Kelly D, Bergsneider M, Martin NA, Hovda DA (2003) Persistently low extracellular glucose correlates with poor outcome 6 months after human traumatic brain injury despite a lack of increased lactate: a microdialysis study. J Cereb Blood Flow Metab 23:865–877

    Article  CAS  PubMed  Google Scholar 

  45. Wartenberg KE, Schmidt JM, Mayer SA (2007) Multimodality monitoring in neurocritical care. Crit Care Clin 23:507–538

    Article  CAS  PubMed  Google Scholar 

  46. Wrobel G, Roerig P, Kokocinski F, Neben K, Hahn M, Reifenberger G, Lichter P (2005) Microarray-based gene expression profiling of benign, atypical and anaplastic meningiomas identifies novel genes associated with meningioma progression. Int J Cancer 114:249–256

    Article  CAS  PubMed  Google Scholar 

  47. Xu W, Mellergard P, Ungerstedt U, Nordstrom CH (2002) Local changes in cerebral energy metabolism due to brain retraction during routine neurosurgical procedures. Acta Neurochir (Wien) 144:679–683

    Article  CAS  Google Scholar 

  48. Zetterling M, Hillered L, Samuelsson C, Karlsson T, Enblad P, Ronne-Engstrom E (2009) Temporal patterns of interstitial pyruvate and amino acids after subarachnoid haemorrhage are related to the level of consciousness–a clinical microdialysis study. Acta Neurochir (Wien) 151:771–780, discussion 780

    Article  Google Scholar 

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Statement of human and animal rights

This study was approved by the Research Ethics Committee of “Evangelismos” General Hospital of Athens, Greece, and all procedures were performed in accordance with the revised Declaration of Helsinki (2000).

Conflict of interest

None.

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All persons gave their informed consent prior to the inclusion in the study.

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Authors and Affiliations

  1. Department of Anaesthesiology, Evangelismos Hospital, 66 Kosta Varnali Str., 15233, Athens, Greece

    Christina Balaka

  2. Hellenic Center for Neurosurgical Research “Prof. Petros Kokkalis”, Athens, Greece

    George Stranjalis, Theodosis Kalamatianos & Damianos E. Sakas

  3. Department of Neurosurgery, University of Athens, Evangelismos Hospital, Athens, Greece

    George Stranjalis, Christos Koutsarnakis, Triantafyllos Bouras, Efstathios Boviatsis & Damianos E. Sakas

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  1. Christina Balaka
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  2. George Stranjalis
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Correspondence to Christina Balaka.

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Comment

The authors present pioneering work regarding postoperative monitoring of patients undergoing craniotomy for meningioma surgery. It seems that the authors were able to determine a pivotal time point in the early postoperative course separating worse from better outcomes by the means of intra- and postoperative microdialysis of the cerebral extracellular space. At 8 h postoperatively, the authors found significant metabolic changes indicative of problems that could not be detected by early postoperative CT scans at 24 h postoperatively. If those findings can be reproduced, several questions need to be addressed. What is the exact pathophysiological nature of the early postoperative changes in cerebral metabolism in patients with an unfavourable postoperative outcome? What can be done clinically to intervene once those changes become evident? Should patients undergo an MRI at the time such diagnostic metabolic changes are detected? It seems that microdialysis may bridge the neurological monitoring gap that lies between skin closure and an early postoperative CT scan or MRI performed at 24–48 h postoperatively. This time gap is usually bridged clinically by monitoring the patients’ Glasgow Coma Score. Judging from the authors’ data, it also seems that events in the early postoperative course that are not yet understood seem to play a decisive role in the postoperative outcome following craniotomy for tumour surgery. The authors have opened a new avenue of research in the early postoperative phase in such patients.

Thomas Mindermann

Zurich, Switzerland

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Balaka, C., Stranjalis, G., Kalamatianos, T. et al. Perioperative microdialysis in meningioma surgery: correlation of cerebral metabolites with clinical outcome. Acta Neurochir 156, 2275–2282 (2014). https://doi.org/10.1007/s00701-014-2242-2

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  • DOI: https://doi.org/10.1007/s00701-014-2242-2

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