Gadolinium-enhanced magnetic resonance angiography in brain death

ABSTRACT Confirmatory tests for the diagnosis of brain death in addition to clinical findings may shorten observation time required in some countries and may add certainty to the diagnosis

under specific circumstances. The practicability of Gadolinium-enhanced magnetic resonance angiography to confirm cerebral circulatory arrest was assessed after the diagnosis of brain death

in 15 patients using a 1.5 Tesla MRI scanner. In all 15 patients extracranial blood flow distal to the external carotid arteries was undisturbed. In 14 patients no contrast medium was noted

within intracerebral vessels above the proximal level of the intracerebral arteries. In one patient more distal segments of the anterior and middle cerebral arteries (A3 and M3) were filled

with contrast medium. Gadolinium-enhanced MRA may be considered conclusive evidence of cerebral circulatory arrest, when major intracranial vessels fail to fill with contrast medium while

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SIMPLE PRACTICAL PREDICTIVE MODEL FOR SAH MORTALITY AND OUTCOMES Article Open access 28 December 2024 INTRODUCTION Death is the irreversible loss of all functions. The diagnosis of brain

death in most countries is based on the evidence of the loss of brain function and confirmation of the irreversibility of that loss of function1,2,3,4. The clinical criteria giving evidence

of the loss of brain function (coma, cranial nerve areflexia and apnea) are universally accepted. “_Most physicians recognize that the diagnosis of death based upon clinical judgement alone

is subject to human error_”5. The evidence for the irreversibility of loss of function, a waiting period and/or a confirmatory test, is viewed variably and reflects different concepts of

safety6,7. Two main groups of confirmatory tests focus either on the demonstration of the cessation of cerebral blood flow or the absence of cerebral bioelectrical brain activity.

Conventional angiography and electroencephalography (EEG) have frequently been recommended4. As the complete arrest of cerebral blood flow will result in a global brain infarction after a

short interval8 Bernat1 considered the registration of the absence of intracranial blood flow the most reliable finding to demonstrate an irreversible loss of all brain functions.

Identification of cerebral circulatory arrest has been reported using a number of techniques: computed tomography (CT) angiography, four-vessel angiography, cerebral digital subtraction

angiography, intravenous radionuclide angiography, single photon emission computed tomography (SPECT) and transcranial Doppler ultrasonography (TCD)9,10,11,12,13,14. All these techniques

have their limitations and their availability is variable. While TCD depends on the expertise of the investigator and requires a high degree of experience, CT angiography (CTA) involves

contrast media with a possibly harmful side effect on the donor or the transplantable organs. We consider contrast-enhanced MR-angiography (MRA) particularly suitable to identify cerebral

circulatory arrest. Subsequently we report our MRA findings, which we obtained in 15 patients after brain death had been diagnosed. RESULTS The clinical data and the MR findings of all brain

dead patients are presented in Table 1. Common MRI findings were diffuse gyral swelling, parenchymal hemorrhage; diffuse cerebral white matter injury and tonsilar herniation. In 14 of 15

patients the Gadolinium-enhanced MRA showed no evidence of arterial blood flow in the intracranial circulation above the level of the proximal A2-segment of the anterior cerebral artery

(ACA) and the M1-segment of the middle cerebral artery (MCA) as depicted in Figure 1. One patient exhibited some extremely slow cerebral blood flow of contrast medium into the A3 and M3

segments after the diagnosis of brain death (Figure 2). DISCUSSION Confirmatory tests for the diagnosis of BD in addition to the clinical findings of coma and apnoeic cranial nerve areflexia

are not required in many countries4. It may be mandatory in some countries under specific clinical conditions6. Confirmatory tests are used in cases of unreliable clinical examinations, to

shorten the time of observation and in some countries in primary brain lesions of the posterior fossa. The treatment with CNS depressant medication (e.g. barbiturates) is the most frequent

reason for the delay of the diagnosis of brain death based on clinical criteria. As long as CNS depressant drugs have not been eliminated to a neglectable level or until other confounding

factors such as metabolic or endocrine disorders have not been excluded, brain death cannot be diagnosed on clinical criteria alone. A delay of the diagnosis of brain death has been linked

to an increased risk of organ failure in transplant recipients15 as timing has proved to be an important factor for successful transplantation. In order to preserve the integrity of the

donor organs and to decrease the rate of transplant failures some authors therefore call for a regular use of reliable confirmatory tests to shorten the time needed to diagnose brain

death16. Confirmatory tests may be divided into two groups: in those that demonstrate the cessation of cerebral blood flow (CBF) and those, which prove the absence of bioelectrical activity.

In the countries in which confirmatory tests are recommended or eventually even required, the most often used ancillary test is electroencephalography (EEG), which has been reported to have

a 90% sensitivity2. Other accepted electrophysiological tests rely on the evidence of the loss of evoked potentials17. A reliable confirmatory test would be most helpful particularly in

cases when cranial nerve areflexia cannot be verified because of lesions to the midface and the eyes or in concomitant drug intoxication. In recent years great efforts have been made to

develop new confirmatory tests for the reliable diagnosis of brain death. Magnetic resonance imaging (MRI) is believed to offer several sophisticated techniques that may improve the

diagnostics of BD. Aichner et al.18 observed uniform patterns of diffuse brain swelling and tonsilar herniation in patients with clinical signs of brain death. Kumada et al.19 found

decreased ADC values up to 40% as compared to a healthy control group emphasizing that DWI and ADC mapping show areas that correspond to edema of cytotoxic nature and ischemic tissue.

Several other authors confirmed these results20,21,22,23. In a recent study we evaluated the reliability of diffusion weighted imaging in the diagnosis of brain death. We concluded that the

unpredictable effects of pseudonormalization and possible susceptibility artifacts due to micro hemorrhages preclude a leading role of DWI in the diagnosis of brain death22. It is widely

accepted that the cessation of cerebral blood flow for about 30 minutes results in a global brain infarction and subsequently in brain death8. Hence, Bernat1 argued that the proof of a

complete cerebral circulatory arrest is the most reliable confirmation of an irreversible loss of all brain functions. The precise pathophysiology of the cessation of cerebral blood flow may

still be discussed, but several mechanisms have been proposed to explain the arrest of brain circulation in BD. A massively increased intracerebral pressure (ICP) leads to an increased

vascular resistance of the brain. When the ICP exceeds the systolic blood pressure, the brain cannot be perfused. As the tolerance of brain tissue to withdrawal of oxygen is very short, thus

irreversible destruction of brain tissue will ensue within minutes, leading to further swelling of the brain. Undoubtedly, a total cerebral circulatory arrest documents the “death of all

intracranial neurons”1,24. Various techniques have been used to demonstrate this arrest: four-vessel angiography12, cerebral intravenous digital subtraction angiography9, radionuclide

angiography10, single photon emission tomography25, MRI angiography26,27,28,29, CT angiography13 and a few more2. Transcranial Doppler sonography (TCD) is a non-invasive technique and is

independent from any contrast media. It is cost-effective and additionally fast and easy to use on the intensive care unit (ICU)30. Some authors have investigated the reliability of MR

angiography26,27,29. Ishii et al.26 suggested first that absence of the cerebral blood flow above the supraclinoid portions of ICA and their intracranial branches on MR angiograms is

specific to brain death. Karantanas et al.27 and Sohn et al.29 confirmed these findings using sophisticated time-of-flight (TOF) imaging techniques. TOF imaging has been increasingly

accepted as a technique for the examination of the intracranial circulation. The advantages of time-of-flight imaging include high spatial resolution, relative short imaging time, high

signal-to-noise ratio and the independence from any contrast agents31. It is based on the flow-related signal enhancement of the blood entering into the volume-of-interest32. TOF imaging,

however, underlies some technical limitations and potential pitfalls. Large intracranial hematomas excite high signal intensities leading to an extremely difficult and unreliable

interpretation of the intracranial circulation33. The dependence on adequate flow enhancement imposes certain constraints on time-of-flight imaging. Thus, slowed circulation causes dephasing

and saturation leading to signal losses. Furthermore, when vessels run parallel to the imaging slice orientation, the signal may become saturated with a subsequently undetectable blood

flow, even when the blood flow is not severely impaired31. As we are not aware of any preceding study examining the diagnostic value of gadolinium-enhanced MR angiography (MRA) for the

detection of brain death we examined its practicability to confirm cerebral circulatory arrest. In 14 patients the MRA showed no intracranial contrast signal media above the level of the

proximal A2-segment of the ACA and the M1-segment of the MCA indicating an irreversible loss of all brain functions (Figure 1). These results are consistent with the findings of several

other authors who investigated the intracranial circulation using TOF-based MR angiography26,27,29. No blood flow above the level of the supraclinoid portions of the ICA was found. One brain

dead patient presented with contrast medium in the A3 and M3 segments (Figure 2). Such findings are not unusual, as “_total cessation of circulation is less common than reduced cerebral

blood flow in the early phases of brain death_”5. Flower and Patel34 observed some markedly reduced residual intracranial arterial flow in 6 patients who were brain dead using radionuclide

angiography. Shah et al.35 evaluated the reliability of cerebral perfusion scintigraphy (CPS) in the diagnosis of brain death. They reported the case of a patient who suffered brain death as

a result of a ruptured giant aneurysm and following subarachnoid hemorrhage. A partially persistent intracranial perfusion was detected by using CPS. Several authors presented persistent

but reduced CBF in patients after diagnosis of brain death using various imaging techniques36,37 in up to 2–3%38. Decreased intracranial pressure e.g. after decompressive craniectomy,

extensive decompressing fractures or ventricular shunts may lead to preserved but markedly decreased cerebral blood flow or some reperfusion after the onset of complete and irreversible loss

of brain function38. In the present study patient #10 exhibited a markedly reduced intracranial circulation after unilateral decompressive craniectomy and subsequent diagnosis of brain

death (Figure 2). These observations from angiography have led to the concept that the documentation of cerebral circulatory arrest is conclusive evidence of brain death. Some residual blood

flow is compatible with brain death but less conclusive than large vessels failing to fill with contrast medium while extracranial vessels exhibit normal circulation39. In the case of

residual cerebral blood the diagnosis of brain death cannot be ruled out and diagnosis should be based either on the duration of observation time or other confirmatory tests. An ideal

confirmatory test for the diagnosis of brain death is safe, extremely sensitive, reliable and widely available. None of the existing ancillary tests fulfill all these criteria. Validities

and sensitivities of 90% and more were reported for the widely accepted ancillary tests that confirm brain death by either demonstrating the absence of cerebral bioelectrical activity or

cerebral circulation2,14. Bedside examinations are more practicable on the intensive care unit (ICU) and MRI of ventilated patients is quite a burden in terms of time and personnel required.

All confirmatory tests, however, have their limitations. TCD is investigator-dependent and requires a high degree of experience. Four-vessel and CT angiography are based on contrast media

with a potentially harmful impact on the possibly alive patients and on possible donor organs. Direct arterial angiography is hardly performed in Germany because of legal concerns, since

adverse effects of iodine contrast media and arterial infarction are a rare but realistic risk40. EEG is useless in hypothermia, CNS depressants and hypotonic conditions2. Angiographic

methods that demonstrate the absence of cerebral blood flow are independent from confounders like drug-intoxication or metabolic disturbances that preclude the BD diagnosis on clinical

criteria solely. The presented preliminary results of gadolinium-enhanced MRA likewise show highest sensitivity and validity. To date, now study compared the validity and reliability between

contrast-enhanced (CE-MRA) and non-contrast-enhanced magnetic resonance angiography (NCA-MRA) and its practicability in the diagnosis of BD. Both methods showed sensitivities and

specificities up to 100%. The substantial differences, however, are based on the methodical issues26,27,29. Thus, CE-MRA relies on the paramagnetic properties of the applied contrast agents

like Gadolinium (Gd) that shorten the T1 relaxation time. In contrast, NCE-MRA techniques, such as TOF, are based on the suppression of the background signal by slice-selective

radiofrequency pulses that saturate the signal from the stationary tissue. NCE-MRA techniques fully refrain from the use of contrast agents. Advantages of CE-MRA relative to NCE-MRA

techniques include considerably shorter acquisition times, improved anatomical coverage and decreased susceptibility artifacts caused by hemorrhages or other pathological conditions like

increased intracranial pressure and reduced intracranial blood flow41. The major drawback of CE-MRA is the dependence on contrast agents such as Gd that is known to induce nephrogenic

systemic fibrosis (NSF); a very rare syndrome however, which appears to occur exclusively in patients with renal impairment. Severe, life-threatening anaphylactoid or nonallergic

anaphylactic reactions are exceedingly rare with a likelihood of about 1:1,000,000 patients42. No case of NSF has been reported in patients with unimpaired renal function as of yet43. The

effect of contrast media on organ transplants is unknown as of yet. The unwanted side effects of invasive arterial angiography with iodine contrast media have raised generally accepted legal

concerns. The likelihood of severe unwanted side effects of iodine contrast media is 1:170,00044. Thus, MR angiography with Gd appears to pose a tenfold lower risk to the patient than CT

angiography with iodine contrast media. We concluded that contrast-enhanced MRA techniques may be useful to confirm brain death and that its inherent risk is acceptably low. A comparison of

CE- and NCE-MRA in future studies may be interesting. METHODS The present study was approved by the Local Ethics Committee of the University of Magdeburg in compliance with national

legislation and the Code of Ethical Principles for Medical Research Involving Human Subjects of the World Medical Association (Declaration of Helsinki). PATIENTS Gadolinium-enhanced MRA of

the brain was prospectively obtained in fifteen patients (13 males and 2 females; mean age 58.20±19.6 years; age ranged between 20 and 80 years). The primary underlying brain lesion was

caused by: traumatic brain injury (n = 6), intracerebral hemorrhage (n = 7) and subarachnoid hemorrhage (n = 2). Brain death was diagnosed according to the guidelines of the

Bundesärztekammer [Richtlinien zur Feststellung des Hirntodes, Deutsches Ärzteblatt 95, Heft 30, 24.07.1998]. Clinical tests included the confirmation of coma, cranial nerve areflexia, apnea

and the loss of cerebral bioelectrical activity using EEG for at least 30 minutes as a sign of irreversible bioelectrical silence. The presence of a brain lesion and exclusion of other

factors that can cause coma was a prerequisite (e.g. CNS-depressant drugs, hypothermia, imbalance of electrolytes, metabolic or endocrine disturbances). IMAGING All patients were examined

within the first 24 hours after the clinical diagnosis of brain death. MR imaging was conducted on a 1.5 Tesla Intera scanner (Philips Medical Systems, Best, Netherlands) using a 16-channel

head coil. Details of the MRA protocol are listed in Table 2. The MR angiography was visualized by a maximum intensity projection (MIP). DATA ANALYSIS Image data of all observed brain dead

patients were pseudonymized and transferred to a separate workstation running Osirix [Version 5.5.2, http://www.osirix-viewer.com/]. The MRA findings were evaluated by neuroradiologists.

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1267–1275 (2001). Article  CAS  Google Scholar  Download references AUTHOR INFORMATION AUTHORS AND AFFILIATIONS * Department of Neurosurgery, Otto-von-Guericke-University Magdeburg, M.

Luchtmann, J. Kohl & R. Firsching * Institute of Neuroradiology, Otto-von-Guericke-University Magdeburg, O. Beuing, M. Skalej & S. Serowy * Institute of Biometry and Medical

Informatics, Otto-von-Guericke-University Magdeburg, J. Bernarding Authors * M. Luchtmann View author publications You can also search for this author inPubMed Google Scholar * O. Beuing

View author publications You can also search for this author inPubMed Google Scholar * M. Skalej View author publications You can also search for this author inPubMed Google Scholar * J.

Kohl View author publications You can also search for this author inPubMed Google Scholar * S. Serowy View author publications You can also search for this author inPubMed Google Scholar *

J. Bernarding View author publications You can also search for this author inPubMed Google Scholar * R. Firsching View author publications You can also search for this author inPubMed Google

Scholar CONTRIBUTIONS M.L. prepared the manuscript including all figures/tables and was responsible for the clinical part of the data collection and analysis. O.B. and M.S. were responsible

for the technical part of the data collection. J.K. was responsible for the clinical part of the data collection. S.S. analysed the collected data especially the maximum intensity

projections (MIP) of the MRA. J.B. prepared parts of the manuscript and analyzed the collected data. R.F. designed the study and was responsible for manuscript preparation and data analysis.

All authors reviewed the manuscript. ETHICS DECLARATIONS COMPETING INTERESTS The authors declare no competing financial interests. RIGHTS AND PERMISSIONS This work is licensed under a

Creative Commons Attribution-NonCommercial-NoDerivs 3.0 Unported License. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-nd/3.0/ Reprints and permissions

ABOUT THIS ARTICLE CITE THIS ARTICLE Luchtmann, M., Beuing, O., Skalej, M. _et al._ Gadolinium-enhanced magnetic resonance angiography in brain death. _Sci Rep_ 4, 3659 (2014).

https://doi.org/10.1038/srep03659 Download citation * Received: 08 October 2013 * Accepted: 16 December 2013 * Published: 13 January 2014 * DOI: https://doi.org/10.1038/srep03659 SHARE THIS

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