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Acta Neurochirurgica

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Open Access 01-12-2024 | Central Nervous System Trauma | Original Article

The effects of cerebral pressure autoregulation status and CPP levels on cerebral metabolism in pediatric traumatic brain injury

Authors: Fartein Velle, Anders Lewén, Tim Howells, Anders Hånell, Pelle Nilsson, Per Enblad

Published in: Acta Neurochirurgica | Issue 1/2024

Abstract

Background

Cerebral perfusion pressure (CPP) management in the developing child with traumatic brain injury (TBI) is challenging. The pressure reactivity index (PRx) may serve as marker of cerebral pressure autoregulation (CPA) and optimal CPP (CPPopt) may be assessed by identifying the CPP level with best (lowest) PRx. To evaluate the potential of CPPopt guided management in children with severe TBI, cerebral microdialysis (CMD) monitoring levels of lactate and the lactate/pyruvate ratio (LPR) (indicators of ischemia) were related to actual CPP levels, autoregulatory state (PRx) and deviations from CPPopt (ΔCPPopt).

Methods

Retrospective study of 21 children ≤ 17 years with severe TBI who had both ICP and CMD monitoring were included. CPP, PRx, CPPopt and ΔCPPopt where calculated, dichotomized and compared with CMD lactate and lactate-pyruvate ratio.

Results

Median age was 16 years (range 8–17) and median Glasgow coma scale motor score 5 (range 2–5). Both lactate (p = 0.010) and LPR (p = < 0.001) were higher when CPP ≥ 70 mmHg than when CPP < 70. When PRx ≥ 0.1 both lactate and LPR were higher than when PRx < 0.1 (p = < 0.001). LPR was lower (p = 0.012) when CPPopt ≥ 70 mmHg than when CPPopt < 70, but there were no differences in lactate levels. When ΔCPPopt > 10 both lactate (p = 0.026) and LPR (p = 0.002) were higher than when ΔCPPopt < –10.

Conclusions

Increased levels of CMD lactate and LPR in children with severe TBI appears to be related to disturbed CPA (PRx). Increased lactate and LPR also seems to be associated with actual CPP levels ≥ 70 mmHg. However, higher lactate and LPR values were also seen when actual CPP was above CPPopt. Higher CPP appears harmful when CPP is above the upper limit of pressure autoregulation. The findings indicate that CPPopt guided CPP management may have potential in pediatric TBI.

Agrawal S, Placek MM, White D, Daubney E, Cabeleira M, Smielewski P, Czosnyka M, Young A, Watson S, Maw A, Hutchinson PJ (2023) Studying Trends of Auto-Regulation in Severe Head Injury in Paediatrics (STARSHIP): protocol to study cerebral autoregulation in a prospective multicentre observational research database study. BMJ Open 13:e071800. https://doi.org/10.1136/bmjopen-2023-071800CrossRefPubMedPubMedCentral

Aries MJ, Czosnyka M, Budohoski KP, Steiner LA, Lavinio A, Kolias AG, Hutchinson PJ, Brady KM, Menon DK, Pickard JD, Smielewski P (2012) Continuous determination of optimal cerebral perfusion pressure in traumatic brain injury. Crit Care Med 40:2456–2463. https://doi.org/10.1097/CCM.0b013e3182514eb6CrossRefPubMed

Balestreri M, Czosnyka M, Steiner LA, Schmidt E, Smielewski P, Matta B, Pickard JD (2004) Intracranial hypertension: what additional information can be derived from ICP waveform after head injury? Acta Neurochir 146:131–141. https://doi.org/10.1007/s00701-003-0187-y. (Wien)CrossRefPubMed

Bellander BM, Cantais E, Enblad P, Hutchinson P, Nordstrom CH, Robertson C, Sahuquillo J, Smith M, Stocchetti N, Ungerstedt U, Unterberg A, Olsen NV (2004) Consensus meeting on microdialysis in neurointensive care. Intensive Care Med 30:2166–2169. https://doi.org/10.1007/s00134-004-2461-8CrossRefPubMed

Brady KM, Shaffner DH, Lee JK, Easley RB, Smielewski P, Czosnyka M, Jallo GI, Guerguerian AM (2009) Continuous monitoring of cerebrovascular pressure reactivity after traumatic brain injury in children. Pediatrics 124:e1205-1212. https://doi.org/10.1542/peds.2009-0550CrossRefPubMed

Charalambides C, Sgouros S, Sakas D (2010) Intracerebral microdialysis in children. Childs Nerv Syst 26:215–220. https://doi.org/10.1007/s00381-009-1031-3CrossRefPubMed

Czosnyka M, Guazzo E, Whitehouse M, Smielewski P, Czosnyka Z, Kirkpatrick P, Piechnik S, Pickard JD (1996) Significance of intracranial pressure waveform analysis after head injury. Acta Neurochir 138:531–541; discussion 541–532. https://doi.org/10.1007/bf01411173. (Wien)

Czosnyka M, Smielewski P, Kirkpatrick P, Laing RJ, Menon D, Pickard JD (1997) Continuous assessment of the cerebral vasomotor reactivity in head injury. Neurosurgery 41:11–17; discussion 17–19. https://doi.org/10.1097/00006123-199707000-00005

Czosnyka M, Smielewski P, Piechnik S, Steiner LA, Pickard JD (2001) Cerebral autoregulation following head injury. J Neurosurg 95:756–763. https://doi.org/10.3171/jns.2001.95.5.0756CrossRefPubMed

10.

Czosnyka M, Steiner L, Balestreri M, Schmidt E, Smielewski P, Hutchinson PJ, Pickard JD (2005) Concept of “true ICP” in monitoring and prognostication in head trauma. Acta Neurochir Suppl 95:341–344. https://doi.org/10.1007/3-211-32318-x_70CrossRefPubMed

11.

Dewan MC, Mummareddy N, Wellons JC 3rd, Bonfield CM (2016) Epidemiology of global pediatric traumatic brain injury: qualitative review. World Neurosurg 91(497–509):e491. https://doi.org/10.1016/j.wneu.2016.03.045CrossRef

12.

Elf K, Nilsson P, Enblad P (2002) Outcome after traumatic brain injury improved by an organized secondary insult program and standardized neurointensive care. Crit Care Med 30:2129–2134. https://doi.org/10.1097/00003246-200209000-00029CrossRefPubMed

13.

Elf K, Nilsson P, Ronne-Engstrom E, Howells T, Enblad P (2005) Cerebral perfusion pressure between 50 and 60 mm Hg may be beneficial in head-injured patients: a computerized secondary insult monitoring study. Neurosurgery 56:962–971; discussion 962–971

14.

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. https://doi.org/10.1097/00004647-199607000-00014CrossRefPubMed

15.

Figaji AA (2017) Anatomical and physiological differences between children and adults relevant to traumatic brain injury and the implications for clinical assessment and care. Front Neurol 8:685. https://doi.org/10.3389/fneur.2017.00685CrossRefPubMedPubMedCentral

16.

Flechet M, Meyfroidt G, Piper I, Citerio G, Chambers I, Jones PA, Lo TM, Enblad P, Nilsson P, Feyen B, Jorens P, Maas A, Schuhmann MU, Donald R, Moss L, Van den Berghe G, Depreitere B, Guiza F (2018) Visualizing cerebrovascular autoregulation insults and their association with outcome in adult and paediatric traumatic brain injury. Acta Neurochir Suppl 126:291–295. https://doi.org/10.1007/978-3-319-65798-1_57CrossRefPubMed

17.

Guilfoyle MR, Helmy A, Donnelly J, Stovell MG, Timofeev I, Pickard JD, Czosnyka M, Smielewski P, Menon DK, Carpenter KLH, Hutchinson PJ (2021) Characterising the dynamics of cerebral metabolic dysfunction following traumatic brain injury: a microdialysis study in 619 patients. PLoS ONE 16:e0260291. https://doi.org/10.1371/journal.pone.0260291CrossRefPubMedPubMedCentral

18.

Hillered L, Persson L, Nilsson P, Ronne-Engstrom E, Enblad P (2006) Continuous monitoring of cerebral metabolism in traumatic brain injury: a focus on cerebral microdialysis. Curr Opin Crit Care 12:112–118. https://doi.org/10.1097/01.ccx.0000216576.11439.dfCrossRefPubMed

19.

Hockel K, Diedler J, Neunhoeffer F, Heimberg E, Nagel C, Schuhmann MU (2017) Time spent with impaired autoregulation is linked with outcome in severe infant/paediatric traumatic brain injury. Acta Neurochir 159:2053–2061. https://doi.org/10.1007/s00701-017-3308-8. (Wien)CrossRefPubMed

20.

Howells T, Elf K, Jones PA, Ronne-Engstrom E, Piper I, Nilsson P, Andrews P, Enblad P (2005) Pressure reactivity as a guide in the treatment of cerebral perfusion pressure in patients with brain trauma. J Neurosurg 102:311–317. https://doi.org/10.3171/jns.2005.102.2.0311CrossRefPubMed

21.

Howells T, Johnson U, McKelvey T, Enblad P (2015) An optimal frequency range for assessing the pressure reactivity index in patients with traumatic brain injury. J Clin Monit Comput 29:97–105. https://doi.org/10.1007/s10877-014-9573-7CrossRefPubMed

22.

Jennett B, Bond M (1975) Assessment of outcome after severe brain damage. Lancet 1:480–484. https://doi.org/10.1016/s0140-6736(75)92830-5CrossRefPubMed

23.

Kochanek PM, Tasker RC, Carney N, Totten AM, Adelson PD, Selden NR, Davis-O’Reilly C, Hart EL, Bell MJ, Bratton SL, Grant GA, Kissoon N, Reuter-Rice KE, Vavilala MS, Wainwright MS (2019) Guidelines for the management of pediatric severe traumatic brain injury, third edition: update of the brain trauma foundation guidelines. Pediatr Crit Care Med 20:S1-s82. https://doi.org/10.1097/pcc.0000000000001735CrossRefPubMed

24.

Lewis PM, Czosnyka M, Carter BG, Rosenfeld JV, Paul E, Singhal N, Butt W (2015) Cerebrovascular pressure reactivity in children with traumatic brain injury. Pediatr Crit Care Med 16:739–749. https://doi.org/10.1097/PCC.0000000000000471CrossRefPubMed

25.

Liesemer K, Riva-Cambrin J, Bennett KS, Bratton SL, Tran H, Metzger RR, Bennett TD (2014) Use of Rotterdam CT scores for mortality risk stratification in children with traumatic brain injury. Pediatr Crit Care Med 15:554–562. https://doi.org/10.1097/pcc.0000000000000150CrossRefPubMedPubMedCentral

26.

Lo T, Piper I, Depreitere B, Meyfroidt G, Poca M, Sahuquillo J, Durduran T, Enblad P, Nilsson P, Ragauskas A, Kiening K, Morris K, Agbeko R, Levin R, Weitz J, Park C, Davis P (2018) KidsBrainIT: a new multi-centre, multi-disciplinary, multi-national paediatric brain monitoring collaboration. Acta Neurochir Suppl 126:39–45. https://doi.org/10.1007/978-3-319-65798-1_9CrossRefPubMed

27.

Nagel C, Diedler J, Gerbig I, Heimberg E, Schuhmann MU, Hockel K (2016) State of cerebrovascular autoregulation correlates with outcome in severe infant/pediatric traumatic brain injury. Acta Neurochir Suppl 122:239–244. https://doi.org/10.1007/978-3-319-22533-3_48CrossRefPubMed

28.

Nordstrom CH (2010) Cerebral energy metabolism and microdialysis in neurocritical care. Childs Nerv Syst 26:465–472. https://doi.org/10.1007/s00381-009-1035-zCrossRefPubMed

29.

Nordstrom CH, Reinstrup P, Xu W, Gardenfors A, Ungerstedt U (2003) Assessment of the lower limit for cerebral perfusion pressure in severe head injuries by bedside monitoring of regional energy metabolism. Anesthesiology 98:809–814. https://doi.org/10.1097/00000542-200304000-00004CrossRefPubMed

30.

Nyholm L, Howells T, Enblad P, Lewen A (2013) Introduction of the Uppsala Traumatic Brain Injury register for regular surveillance of patient characteristics and neurointensive care management including secondary insult quantification and clinical outcome. Ups J Med Sci 118:169–180. https://doi.org/10.3109/03009734.2013.806616CrossRefPubMedPubMedCentral

31.

Persson L, Hillered L (1992) Chemical monitoring of neurosurgical intensive care patients using intracerebral microdialysis. J Neurosurg 76:72–80. https://doi.org/10.3171/jns.1992.76.1.0072CrossRefPubMed

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. https://doi.org/10.1097/00006123-200009000-00035

33.

Signorini DF, Piper IR, Jones PA, Howells TP (1997) Importance of textual data in multimodality monitoring. Crit Care Med 25:2048–2050. https://doi.org/10.1097/00003246-199712000-00024CrossRefPubMed

34.

Smith CA, Rohlwink UK, Mauff K, Thango NS, Hina TS, Salie S, Enslin JMN, Figaji AA (2023) Cerebrovascular pressure reactivity has a strong and independent association with outcome in children with severe traumatic brain injury. Crit Care Med. https://doi.org/10.1097/CCM.0000000000005815CrossRefPubMedPubMedCentral

35.

Sorrentino E, Diedler J, Kasprowicz M, Budohoski KP, Haubrich C, Smielewski P, Outtrim JG, Manktelow A, Hutchinson PJ, Pickard JD, Menon DK, Czosnyka M (2012) Critical thresholds for cerebrovascular reactivity after traumatic brain injury. Neurocrit Care 16:258–266. https://doi.org/10.1007/s12028-011-9630-8CrossRefPubMed

36.

Stahl N, Mellergard P, Hallstrom A, Ungerstedt U, Nordstrom CH (2001) Intracerebral microdialysis and bedside biochemical analysis in patients with fatal traumatic brain lesions. Acta Anaesthesiol Scand 45:977–985. https://doi.org/10.1034/j.1399-6576.2001.450810.xCrossRefPubMed

37.

Steiner LA, Czosnyka M, Piechnik SK, Smielewski P, Chatfield D, Menon DK, Pickard JD (2002) Continuous monitoring of cerebrovascular pressure reactivity allows determination of optimal cerebral perfusion pressure in patients with traumatic brain injury. Crit Care Med 30:733–738. https://doi.org/10.1097/00003246-200204000-00002CrossRefPubMed

38.

Svedung Wettervik T, Howells T, Hillered L, Rostami E, Lewen A, Enblad P (2021) Autoregulatory or fixed cerebral perfusion pressure targets in traumatic brain injury: determining which is better in an energy metabolic perspective. J Neurotrauma 38:1969–1978. https://doi.org/10.1089/neu.2020.7290CrossRefPubMed

39.

Thango NS, Rohlwink UK, Dlamini L, Tshavhungwe MP, Banderker E, Salie S, Enslin JMN, Figaji AA (2021) Brain interstitial glycerol correlates with evolving brain injury in paediatric traumatic brain injury. Childs Nerv Syst 37:1713–1721. https://doi.org/10.1007/s00381-021-05058-2CrossRefPubMed

40.

Tolias CM, Richards DA, Bowery NG, Sgouros S (2002) Extracellular glutamate in the brains of children with severe head injuries: a pilot microdialysis study. Childs Nerv Syst 18:368–374. https://doi.org/10.1007/s00381-002-0623-yCrossRefPubMed

41.

Velle F, Lewen A, Howells T, Enblad P, Nilsson P (2019) Intracranial pressure-based barbiturate coma treatment in children with refractory intracranial hypertension due to traumatic brain injury. J Neurosurg Pediatr 1–9. https://doi.org/10.3171/2019.10.PEDS19268

42.

Velle F, Lewen A, Howells T, Hanell A, Nilsson P, Enblad P (2023) Cerebral pressure autoregulation and optimal cerebral perfusion pressure during neurocritical care of children with traumatic brain injury. J Neurosurg Pediatr 1–11. https://doi.org/10.3171/2023.1.PEDS22352

43.

Velle F, Lewen A, Howells T, Nilsson P, Enblad P (2021) Temporal effects of barbiturate coma on intracranial pressure and compensatory reserve in children with traumatic brain injury. Acta Neurochir 163:489–498. https://doi.org/10.1007/s00701-020-04677-z. (Wien)CrossRefPubMed

44.

Wettervik TS, Lenell S, Nyholm L, Howells T, Lewen A, Enblad P (2018) Decompressive craniectomy in traumatic brain injury: usage and clinical outcome in a single centre. Acta Neurochir 160:229–237. https://doi.org/10.1007/s00701-017-3418-3. (Wien)CrossRefPubMed

45.

Young AM, Donnelly J, Czosnyka M, Jalloh I, Liu X, Aries MJ, Fernandes HM, Garnett MR, Smielewski P, Hutchinson PJ, Agrawal S (2016) Continuous multimodality monitoring in children after traumatic brain injury-preliminary experience. PLoS ONE 11:e0148817. https://doi.org/10.1371/journal.pone.0148817CrossRefPubMedPubMedCentral

Title: The effects of cerebral pressure autoregulation status and CPP levels on cerebral metabolism in pediatric traumatic brain injury
Authors: Fartein Velle
Anders Lewén
Tim Howells
Anders Hånell
Pelle Nilsson
Per Enblad
Publication date: 01-12-2024
Publisher: Springer Vienna
Keywords: Central Nervous System Trauma
Intracranial Hypertension
Neurointensive Care
Published in: Acta Neurochirurgica / Issue 1/2024
Print ISSN: 0001-6268
Electronic ISSN: 0942-0940
DOI: https://doi.org/10.1007/s00701-024-06085-z

Keynote webinar | Spotlight on medication adherence

Springer Medicine

The effects of cerebral pressure autoregulation status and CPP levels on cerebral metabolism in pediatric traumatic brain injury

Abstract

Background

Methods

Results

Conclusions

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

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