Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter March 13, 2014

Coefficient of energy balance, a new parameter for basic investigation of the cerebrospinal fluid

  • Petr Kelbich EMAIL logo , Aleš Hejčl , Iva Selke Krulichová , Jan Procházka , Eva Hanuljaková , Jitka Peruthová , Martina Koudelková , Martin Sameš and Jan Krejsek


Background: The concentrations of glucose and lactate in cerebrospinal fluid (CSF) provide important information about energy metabolism in the CSF compartment. To improve our understanding of this information we introduced a new parameter resulting from a formula for calculating the fictitious production of adenosine triphosphate, i.e., the coefficient of energy balance (KEB).

Methods: We evaluated cytology, the concentrations of glucose and lactate and the KEB in the CSF of 948 patients, who were divided into five groups. For statistical analysis we used the Kruskal-Wallis test with post-hoc analysis using the Dunn method and multinomial regression analysis. We determined the specificities and sensitivities of the cytological pictures and the KEB.

Results: A KEB>28.0 corresponded to normal energy metabolism in the CSF. A KEB<28.0 corresponded to an increased level of anaerobic metabolism in the CSF during inflammation in the CNS. A KEB<10.0 corresponded to a high level of anaerobic metabolism in the CSF during severe inflammation with an oxidative burst of professional phagocytes in the CNS. The KEB parameter increased the specificities of cytological examinations of the CSF in all cases.

Conclusions: The KEB represents an equation for calculating the fictitious average number of ATP molecules produced in the CSF compartment from one molecule of glucose, and we used it successfully as a new parameter for evaluating energy metabolism status in the CSF.

Corresponding author: Petr Kelbich, Hospital Kadaň, Department of Clinical Biochemistry, Haematology and Immunology, Golovinova 1559. Kadaň. 432 01, Czech Republic, E-mail: ; Charles University in Prague, Faculty of Medicine in Hradec Králové, Department of Clinical Immunology and Allergology, Hradec Králové, Czech Republic; Masaryk Hospital in Ústí nad Labem, Department of Clinical Biochemistry, Ústí nad Labem, Czech Republic; and Laboratory for Liquorology and Neuroimmunology Topelex, Prague, Czech Republic


We thank James Dutt for critical reading of the article. This work was supported by Charles University in Prague, Faculty of Medicine in Hradec Králové, Czech Republic, the projects “PRVOUK” P37/09 and P37/10, by the European Regional Development Fund – Project FNUSA-ICRC (No. CZ.1.05/1.1.00/02.0123), by the Grant of the Ministry of Health of the Czech Republic IGA NT 13883/4-2012 and Human Resources for Neurosciences in the Hradec Králové and Ústí Regions, CZ.1.07/2.3.00/20.0274. This project is co-financed by the European social fund and the state budget of the Czech Republic.

Conflict of interest statement

Authors’ conflict of interest disclosure: The authors stated that there are no conflicts of interest regarding the publication of this article. Research support played no role in thestudy design; in the collection, analysis, and interpretationof data; in the writing of the report; or in the decision tosubmit the report for publication.

Research funding: None declared.

Employment or leadership: None declared.

Honorarium: None declared.


1. Deisenhammer F, Bartos A, Egg R, Gilhus NE, Giovannoni G, Rauer S, et al. Routine cerebrospinal fluid (CSF) analysis. In: Gilhus NE, Barnes MP, Brainin M, editors. European handbook of neurological management, 2nd ed. Oxford: Blackwell Publishing Ltd., 2010:5–17.Search in Google Scholar

2. Leen WG, Willemsen MA, Wevers RA, Verbeek MM. Cerebrospinal fluid glucose and lactate: age-specific reference values and implications for clinical practice. PLoS One 2012;7:e42745.10.1371/journal.pone.0042745Search in Google Scholar PubMed PubMed Central

3. Sobek O, Adam P, Koudelková M, Štourač P, Mareš J. The algorithm of CSF examination according to the recommendation of the Committee of CSF and Neuroimmunology of the Czech Neurological Society. Cesk Slov Neurol N 2012;75:159–63.Search in Google Scholar

4. Adam P, Táborský L, Sobek O, Hildebrand T, Kelbich P, Průcha M, et al. Cerebrospinal fluid. In: Spiegel HE, Nowacki G, Hsiao K-J, editors. Advances in clinical chemistry. San Diego, San Francisco, New York, Boston, London, Sydney, Tokyo: Academic Press, 2001:1–62.Search in Google Scholar

5. Beer R, Pfausler B, Schmutzhard E. Infectious intracranial complications in the neuro-ICU patient population. Curr Opin Crit Care 2010;16:117–22.10.1097/MCC.0b013e328338cb5fSearch in Google Scholar PubMed

6. Felgenhauer K. Laboratory diagnosis of neurological diseases. In: Thomas L, editor. Clinical laboratory diagnostics. Use and assessment of clinical laboratory results. Frankfurt/Main: TH-Books Verlagsgessellschaft mbH, 1998:1308–26.Search in Google Scholar

7. Huy NT, Thao NT, Diep DT, Kikuchi M, Zamora J, Hirayama K. Cerebrospinal fluid lactate concentration to distinguish bacterial from aseptic meningitis: a systemic review and meta-analysis. Crit Care 2010;14:R240.10.1186/cc9395Search in Google Scholar PubMed PubMed Central

8. Logan SA, MacMahon E. Viral meningitis. Br Med J 2008;336:36–40.10.1136/bmj.39409.673657.AESearch in Google Scholar PubMed PubMed Central

9. Prasad K, Sahu JK. Cerebrospinal fluid lactate: is it a reliable and valid marker to distinguish between acute bacterial meningitis and aseptic meningitis? Crit Care 2011;15:104.10.1186/cc9396Search in Google Scholar PubMed PubMed Central

10. Viallon A, Desseigne N, Marjollet O, Birynczyk A, Belin M, Guyomarch S, et al. Meningitis in adult patients with a negative direct cerebrospinal fluid examination: value of cytochemical markers for differential diagnosis. Crit Care 2011;15:R136.10.1186/cc10254Search in Google Scholar PubMed PubMed Central

11. Hořejší V, Bartůňková J, editors. Základy imunologie, 4th ed. Prague: Triton, 2009.Search in Google Scholar

12. Krejsek J, Kopecký O, editors. Klinická imunologie, 1st ed. NUCLEUS HK, 2004.Search in Google Scholar

13. Kelbich P, Slavík S, Jasanská J, Adam P, Hanuljaková E, Jermanová K, et al. Evaluations of the energy relations in the CSF compartment by investigation of selected parameters of the glucose metabolism in the CSF. Klin Biochem Metab 1998;6:213–25.Search in Google Scholar

14. Kelbich P, Koudelková M, Machová H, Tomaškovič M, Vachata P, Kotalíková P, et al. Importance of urgent cerebrospinal fluid examination for early diagnosis of central nervous system infections. Klin Mikrobiol Inf Lék 2007;13:9–20.Search in Google Scholar

15. Kelbich P, Adam P, Sobek O, Koudelková M, Procházka J, Hanuljaková E, et al. Basic cerebrospinal fluid test in diagnosing central nervous system involvement. Neurol Pro Praxi 2009;10:285–9.Search in Google Scholar

16. Kelbich P, Hejčl A, Procházka J, Hanuljaková E, Peruthová J, Špička J. Cerebrospinal fluid cytology and energy balance as important attributes of cerebrospinal fluid examination. Klin Biochem Metab 2012;20:17–24.Search in Google Scholar

17. Kelbich P, Hejčl A, Procházka J, Selke Krulichová I, Peruthová J, Hanuljaková E, et al. Number of cells in the cerebrospinal fluid, energy relation in the cerebrospinal fluid compartment and intensity of inflammatory response in the central nervous system. Klin Biochem Metab 2013;21:4–10.Search in Google Scholar

18. Hejčl A, Kelbich P, Bolcha M, Procházka J, Hušková E, Peruthová J, et al. Importance and possibilities of brain metabolism inquiry in neurointensive care using microdialysis. Klin Biochem Metab 2013;21:11–8.Search in Google Scholar

19. Bořecká K, Adam P, Sobek O, Hajduková L, Lánská V, Nekola P. Coefficient of energy balance: effective tool for early differential diagnosis of CNS diseases. Bio Med Res Int 2013; article ID 745943.10.1155/2013/745943Search in Google Scholar PubMed PubMed Central

20. Nejedlý B, Chyská A, Kazda A, Lemon V, editors. Vnitřní prostředí, klinická biochemie a praxe, 2nd ed. Praha: Avicenum, 1981:276.Search in Google Scholar

21. Chehtane M, Khaled AR. Interleukin-7 mediates glucose utilization in lymphocytes through transcriptional regulation of the hexokinase II gene. Am J Physiol Cell Physiol 2010;298:C1560–71.10.1152/ajpcell.00506.2009Search in Google Scholar PubMed PubMed Central

22. Maciver NJ, Jacobs SR, Wieman HL, Wofford JA, Coloff JL, Rathmell JC. Glucose metabolism in lymphocytes is a regulated process with significant effects on immune cell function and survival. J Leukoc Biol 2008;84:949–57.10.1189/jlb.0108024Search in Google Scholar PubMed PubMed Central

23. Marko AJ, Miller RA, Kelman A, Frauwirth KA. Induction of glucose metabolism in stimulated T lymphocytes is regulated by mitogen-activated protein kinase signaling. PLoS One 2010;5:e15425.10.1371/journal.pone.0015425Search in Google Scholar PubMed PubMed Central

24. Mathioudakis D, Engel J, Welters ID, Dehne MG, Matejec R, Harbach H, et al. Pyruvate: immunonutritional effects on neutrophil intracellular amino or alpha-keto acid profiles and reactive oxygen species production. J Amino Acids 2011;40:1077–90.10.1007/s00726-010-0731-zSearch in Google Scholar

25. Michalek RD, Rathmell JC. The metabolic life and times of a T-cell. Immunol Rev 2010;236:190–202.10.1111/j.1600-065X.2010.00911.xSearch in Google Scholar

26. Karlson P, editor. Kurzes Lehrbuch der Biochemie für Mediziner und Naturwissenschaftler. 10th ed. Stuttgart: Georg Thieme Verlag, 1977.Search in Google Scholar

27. Murray RK, Granner DK, Mayes PA, Rodwell VW, editors. Harper’s biochemistry, 23th ed. Prague: H&H, 1998.Search in Google Scholar

28. Hintze J, editor. NCSS, PASS, and GESS. NCSS. Kaysville, Utah, 2007.Search in Google Scholar

29. Adam P, Andrýs C, Friedecký B, Kalla K, Kelbich P, Král V, et al. Doporučení k vyšetřování mozkomíšního moku České společnosti klinické biochemie ČLS JEP, Referenční laboratoře MZ pro klinickou biochemii, Sekce pro neuroimunologii a likvorologii České neurologické společnosti ČLS JEP a Sekce laboratorní imunologie České společnosti pro alergologii a klinickou imunologii ČLS JEP. (Recommendations for cerebrospinal fluid examination by the Czech Society of Clinical Biochemistry of the Czech Medical Society, Referential Laboratory for Clinical Biochemistry of the Ministry of Health, Committee of Neuroimmunology and CSF investigation of the Czech Neurological Society of the Czech Medical Society and the Section of Laboratory Immunology of the Czech Society for Allergology and Clinical Immunology of the Czech Medical Society). Klin Biochem Metab 2006;14:125–7.Search in Google Scholar

30. Reinstrup P, Ståhl N, Mellergård P, Uski T, Ungerstedt U, Nordstöm C-H. Intracerebral microdialysis in clinical practice: baseline values for chemical markers during wakefulness, anesthesia, and neurosurgery. Neurosurgery 2000;47:701–9.Search in Google Scholar

31. Hejčl A, Bolcha M, Procházka J, Hušková E, Sameš M. Elevated intracranial pressure, and impaired brain metabolism correlate with fatal outcome after severe brain injury. Cen Eur Neurosurg 2011;72:1–6.10.1055/s-0031-1295452Search in Google Scholar

32. Van Cappellen van Walsum A-M, editor. Cerebral metabolism of hypoxic fetal sheep investigated by NMR spectrofotoscopy. Drukkerij SSN Nijmegen, 2000.Search in Google Scholar

33. Magistretti PJ, Pellerin L. Astrocytes couple synaptic activity to glucose utilization in the brain. News Physiol Sci 1999;14: 177–82.Search in Google Scholar

34. Adam P, Táborský L, Sobek O, Kelbich P, editors. Cytology of cerebrospinal fluid, 1st ed. Prague: Medica News Publishers, 2003.10.1016/S0065-2423(01)36024-9Search in Google Scholar

35. Hauser SL. Multiple sclerosis and other demyelinating diseases. In: Isselbacher KJ, Braunwald E, Wilson JD, Martin JB, Fauci AS, Kasper DL, editors. Harrison’s principles of internal medicine, 13th ed. New York: McGraw-Hill, 1994:2287–95.Search in Google Scholar

36. Zeman D, Hradílek P, Švagera Z, Mojžíšková E, Woznicová I, Zapletalová O. Detection of oligoclonal IgG kappa and IgG lambda bands in cerebrospinal fluid and serum with Hevylite™ antibodies comparison with the free light chain oligoclonal pattern. Fluids Barriers CNS 2012;9:5.10.1186/2045-8118-9-5Search in Google Scholar PubMed PubMed Central

37. Lukaszewicz A-C, Gontier G, Faivre V, Ouanounou I, Payen D. Elevated production of radical oxygen species by polymorphonuclear neutrophils in cerebrospinal fluid infection. Ann Intensive Care 2012;2:10.10.1186/2110-5820-2-10Search in Google Scholar PubMed PubMed Central

38. McCloskey PS, Salo RJ. Flow cytometric analysis of group B streptococci phagocytosis and oxidative burst in human neutrophils and monocytes. FEMS Immunol Med Microbiol 2000;27:59–65.10.1111/j.1574-695X.2000.tb01412.xSearch in Google Scholar PubMed

39. Musset B, Cherny VV, DeCoursey TE. Strong glucose dependence of electron current in human monocytes. Am J Physiol Cell Physiol 2012;302:C286–95.10.1152/ajpcell.00335.2011Search in Google Scholar PubMed PubMed Central

40. Remer KA, Reimer T, Brcic M, Jungi TW. Evidence for involvement of peptidoglycan in the triggering of an oxidative burst by Listeria monocytogenes in phagocytes. Clin Exp Immunol 2005;140:73–80.10.1111/j.1365-2249.2005.02740.xSearch in Google Scholar PubMed PubMed Central

Received: 2013-11-4
Accepted: 2014-2-12
Published Online: 2014-3-13
Published in Print: 2014-7-1

©2014 by Walter de Gruyter Berlin/Boston

Downloaded on 5.3.2024 from
Scroll to top button