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A Prospective Observational Feasibility Study of Jugular Bulb Microdialysis in Subarachnoid Hemorrhage

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Abstract

Background

Cerebral metabolic perturbations are common in aneurysmal subarachnoid hemorrhage (aSAH). Monitoring cerebral metabolism with intracerebral microdialysis (CMD) allows early detection of secondary injury and may guide decisions on neurocritical care interventions, affecting outcome. However, CMD is a regional measuring technique that is influenced by proximity to focal lesions. Continuous microdialysis of the cerebral venous drainage may provide information on global cerebral metabolism relevant for the care of aSAH patients. This observational study aimed to explore the feasibility of jugular bulb microdialysis (JBMD) in aSAH and describe the output characteristics in relation to conventional multimodal monitoring.

Methods

Patients with severe aSAH were included at admission or after in-house deterioration when local clinical guidelines prompted extended multimodal monitoring. Non-dominant frontal CMD, intracranial pressure (ICP), partial brain tissue oxygenation pressure (PbtO2), and cerebral perfusion pressure (CPP) were recorded every hour. The dominant jugular vein was accessed by retrograde insertion of a microdialysis catheter with the tip placed in the jugular bulb under ultrasound guidance. Glucose, lactate, pyruvate, lactate/pyruvate ratio, glycerol, and glutamate were studied for correlation to intracranial measurements. Modified Rankin scale was assessed at 6 months.

Results

Twelve adult aSAH patients were monitored during a mean 4.2 ± 2.6 days yielding 22,041 data points for analysis. No complications related to JBMD were observed. Moderate or strong significant monotonic CMD-to-JBMD correlations were observed most often for glucose (7 patients), followed by lactate (5 patients), and pyruvate, glycerol, and glutamate (3 patients). Moderate correlation for lactate/pyruvate ratio was only seen in one patient. Analysis of critical periods defined by ICP > 20, CPP < 65, or PbtO2 < 15 revealed a tendency toward stronger CMD-to-JBMD associations in patients with many or long critical periods. Possible time lags between CMD and JBMD measurements were only identified in 6 out of 60 patient variables. With the exception of pyruvate, a dichotomized outcome was associated with similar metabolite patterns in JBMD and CMD. A nonsignificant tendency toward greater differences between outcome groups was seen in JBMD.

Conclusions

Continuous microdialysis monitoring of the cerebral drainage in the jugular bulb is feasible and safe. JBMD-to-CMD correlation is influenced by the type of metabolite measured, with glucose and lactate displaying the strongest associations. JBMD lactate correlated more often than CMD lactate to CPP, implying utility for detection of global cerebral metabolic perturbations. Studies comparing JBMD to other global measures of cerebral metabolism, e.g., PET CT or Xenon CT, are warranted.

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Abbreviations

aSAH:

Aneurysmal subarachnoid hemorrhage

CMD:

Cerebral microdialysis

JBMD:

Jugular bulb microdialysis

LPR:

Lactate/pyruvate ratio

ICP:

Intracranial pressure

MAP:

Mean arterial pressure

CPP:

Cerebral perfusion pressure

PbtO2 :

Brain tissue oxygenation

BBB:

Blood–brain barrier

NCC:

Neurocritical care

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Acknowledgements

The authors thank the staff at the neurointensive care ward at Odense University Hospital for excellent assistance during data collection. We thank Ulrich Halekoh for statistical consults and Claire Gudex for language editing.

Funding

The Syddansk Universitet (Grant No. Department of clinical research faculty scholarship), Odense Universitetshospital (Grant No. PhD scholarship), Karen S Jensens legat (Grant No. 40-A1922), Læge Else Poulsens Mindelegat (Grant No. 53-A2626), Fonden til Lægevidenskabens Fremme (Grant No. 12-260), and Fonden for neurologisk forskning (Grant No. A1281).

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Authors and Affiliations

  1. Department of Neurosurgery, Odense University Hospital, Sønder Boulevard 29, 5000, Odense, Denmark

    Axel Forsse, Troels Halfeld Nielsen, Kevin Hebøll Nygaard, Sibel Yilmaz, Carl-Henrik Nordström & Frantz Rom Poulsen

  2. BRIDGE - Brain Research - Inter-Disciplinary Guided Excellence, Department of Clinical Research, University of Southern Denmark, Odense, Denmark

    Axel Forsse, Troels Halfeld Nielsen, Kevin Hebøll Nygaard, Carl-Henrik Nordström & Frantz Rom Poulsen

  3. Department of Anesthesiology and Intensive Care, Odense University Hospital, Odense, Denmark

    Simon Mølstrøm

  4. Department of Biostatistics and Epidemiology, University of Southern Denmark, Odense, Denmark

    Jacob Hjelmborg

  5. Department of Oral and Maxillofacial Surgery, Odense University Hospital, Odense, Denmark

    Kasper Stokbro Nielsen

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  1. Axel Forsse
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Contributions

CHN, THN, and AF contributed to conceptualization. THN, CHN, AF, and FRP provided methodology. AF, KSN, and JH performed formal analysis. AF, KHN, SY, and SM were involved in data acquisition. AF wrote the original draft. All authors reviewed and edited the manuscript. FRP and THN supervised the project. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Axel Forsse.

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The authors declare that they have no conflict of interest.

Ethical Approval/Informed Consent

The study was approved by the Ethical Committee of Southern Denmark under Project No. S-20150173 and by the Danish Data Protection Agency under Project No. 16/36969. Written informed consent has been obtained from all participants or next of kin and a trial guardian.

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Forsse, A., Nielsen, T.H., Mølstrøm, S. et al. A Prospective Observational Feasibility Study of Jugular Bulb Microdialysis in Subarachnoid Hemorrhage. Neurocrit Care 33, 241–255 (2020). https://doi.org/10.1007/s12028-019-00888-0

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