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Pseudo-subarachnoid hemorrhage in a patient with hypoxic encephalopathy
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Clinical case
Pseudo-subarachnoid hemorrhage in a patient with hypoxic encephalopathy Hémorragie sous-arachnoïdienne chez une patiente présentant une encéphalopathie hypoxique J. Zhang 1 , Q. Li 1 , Z. Zhang ∗ , X. Sun Department of Neurology, The Third Central Hospital of Tianjin, 83, Jintang Road Hedong, Tianjin 300170, China
a r t i c l e
i n f o
Article history: Received 25 April 2014 Received in revised form 1st August 2014 Accepted 28 August 2014 Available online xxx Keywords: Pseudo-subarachnoid hemorrhage Hyperdensity Cerebral edema Pseudo-subarachnoid hemorrhage signs High-density sign Encephaledema
a b s t r a c t The authors report an unusual case of diffuse subarachnoid hemorrhage on brain computed tomography (CT) scan in a patient with post-resuscitation anoxic encephalopathy. A 42-year-old woman suffered both respiratory and cardiac arrest, associated with hypoxic encephalopathy, which occurred during a visit to our gynecology clinic. CT examination was performed the next day, which revealed a hyperdensity in the basal cisterns with a diffuse cerebral edema. Lumbar puncture was applied for diagnosis. No yellow coloration or red cells were observed in the cerebrospinal fluid. Nineteen days after treatment, the CT examination revealed features of a subarachnoid hemorrhage with a significantly increased cerebral edema. The patient died two months later. This clinical case illustrates that hypoxic encephalopathy can mimic diffuse subarachnoid hemorrhage on CT scan. © 2015 Published by Elsevier Masson SAS.
r é s u m é Mots clés : Pseudo-hémorragie sous-arachnoïdienne Hyperdensité Œdème cérébral Signe de pseudo-hémorragie sous-arachnoïdienne Hyperdensité au scanner Œdème encéphalique
Les auteurs rapportent un cas inhabituel d’hémorragie sous-arachnoïdienne diffuse, diagnostiquée par scanner cérébral chez une patiente présentant une encéphalopathie anoxique après une période de réanimation. Il s’agit d’une femme de 42 ans qui présentait un arrêt cardio-respiratoire associé à une encéphalopathie hypoxique. Le lendemain, l’examen tomodensitométrique mettait en évidence une hyperdensité au niveau des citernes basales, ainsi qu’un œdème cérébral diffus. Une ponction lombaire à visée diagnostique était pratiquée. Aucune coloration jaune et aucune hématie n’étaient observées au niveau du liquide céphalorachidien. Dix-neuf jours plus tard, le scanner révélait la présence d’une hémorragie méningée associée à une augmentation significative de l’œdème cérébral. La patiente décédait deux mois plus tard. L’encéphalopathie hypoxique peut mimer une hémorragie méningée au scanner. © 2015 Publie´ par Elsevier Masson SAS.
1. Introduction Typical clinical presentations of subarachnoid hemorrhage (SAH) include a severe headache of rapid onset, vomiting,
∗ Corresponding author. E-mail address: [email protected] (Z. Zhang). 1 Co-first authors: Jing Zhang, Qian Li. These authors contributed equally to this work and should be considered co-first authors.
confusion, and occasional seizures. The diagnosis of SAH is generally confirmed with the presence of increased attenuation of the basal cisterns and subarachnoid space on brain computed tomography (CT) scan. In fact, hyperdensity in the subarachnoid space and basal cisterns are present in 95–98% of CT brain scans of SAH patients within 24 hours of onset [1]. It is well known that CT is a highly sensitive, non-invasive tool to diagnose SAH. However, in rare cases, other diffuse neurological conditions may also produce attenuation of basal cisterns on CT mimicking that of SAH. In 1998, Avrahami et al. [2] proposed that these CT mimicking SAH could
http://dx.doi.org/10.1016/j.neuchi.2014.08.003 0028-3770/© 2015 Published by Elsevier Masson SAS.
Please cite this article in press as: Zhang J, et al. Pseudo-subarachnoid hemorrhage in a patient with hypoxic encephalopathy. Neurochirurgie (2015), http://dx.doi.org/10.1016/j.neuchi.2014.08.003
G Model NEUCHI-677; No. of Pages 3
ARTICLE IN PRESS J. Zhang et al. / Neurochirurgie xxx (2015) xxx–xxx
2
be defined as pseudo-subarachnoid hemorrhage (pseudo-SAH). In this article, we report a case of pseudo-SAH associated with hypoxic encephalopathy, and explore the key findings for its differential diagnosis based on a true SAH.
after treatment, CT examination revealed features of SAH with significantly increased cerebral edema (Fig. 2). The patient died two months later. 3. Discussion
2. Case presentation A 42-year-old woman visited the clinic for ovarian cyst, and suddenly fell on the ground accompanied by a loss of consciousness. She was found to have respiratory and cardiac arrest. Detailed medical history was not obtained as we were unable to contact any of her relatives. She underwent emergency cardiopulmonary resuscitation in the intensive care unit with pressure support ventilation. Her vital signs were: temperature 36.8 ◦ C, pulse 158/min, blood pressure 156/79 mmHg. The physical examination showed: bilateral pupils with equal size (2.5 mm in diameter), negative light response, negative oculocephalogyric reflex, a supple neck, upper limbs flexion and lower limbs extension, lungs clear on auscultation, regular heart rhythm, no abdominal tenderness, extremities unremarkable. The patient’s Glasgow coma scale was 5. CT scan examination was performed the next day when her vital signs were stable, which revealed a hyperdensity in the basal cisterns and diffuse cerebral edema (Fig. 1). Lumbar puncture was applied for diagnosis due to the lack of detailed medical history and revealed: pressure 170 mmHg, white blood cells 0/mm3 , red blood cells 0/mm3. No yellow coloration was observed in the cerebrospinal fluid, and glucose, chlorides, and protein levels were within normal range. The patient was eventually diagnosed as having an hypoxic encephalopathy. Low-temperature treatment was performed to protect brain tissue, and dehydration was applied to reduce the intracranial pressure. Hemodynamic stability was maintained at the same time to ensure sufficient blood supply to the major organs. Nineteen days
Fig. 1. The CT shows slightly lower density of brain parenchyma with no clear corticomedullary boundaries; the densities of part of the sulci and split brain as well as the entorhinal edge increase. The CT features are consistent with either SAH or cerebral edema (higher density areas CT value 35 HU). Le scanner montre une hypodensité modérée du parenchyme cérébral sans limites cortico-médullaires clairement objectivées ; les densités d’une partie des sillons et d’une schizencéphalie (split brain), ainsi que de la région entorhinale, sont augmentées. Les caractéristiques du scanner sont compatibles soit avec une hémorragie arachnoïdienne, soit avec un œdème cérébral (densité : 35 HU).
It has been well accepted that the diagnosis of SAH is generally confirmed with the presence of increased attenuation of the basal cisterns and subarachnoid spaces on brain CT scan. However, in rare cases, other diffuse neurological conditions may produce attenuation of basal cisterns on CT and mimic characteristics of SAH, defined as pseudo-subarachnoid hemorrhage (pseudo-SAH). Therefore, without a clear disease history, lumbar puncture is usually needed to avoid misdiagnosis. As for the patient in this case, sulci, split brain, tentorium and interhemispheric tentorial density increased as shown in the CT scan. The patient’s clinical history was not clear. Diagnosis of pseudo-SAH was eventually made with the help of a lumbar puncture. In 1986, Spiegel et al. [3] first described this phenomenon in a patient with cerebral edema. In 1998, Avrahami et al. [2] proposed that the imaging change mimicking SAH could be defined as pseudo-SAH. Since then, further studies have been continuously performed as regards this phenomenon, and the several possible pathophysiological etiologies underlying it were proposed. The most popular theories include hypoxic-ischemic encephalopathy, reperfusion injury encephalopathy, massive cerebral infarction, viral meningoencephalitis, bilateral subdural hematoma, idiopathic intracranial hypertension, venous sinus thrombosis, and intrathecal or intravascular contrast agent injection [4–11]. These causes are excluded by detailed history, physical examination and laboratory data. Certainly, lumbar puncture is of particular importance for an accurate clinical diagnosis, especially when there is a lack of other relevant clinical information. Although the CT imaging of pseudo-SAH closely mimics SAH, there remains a slight difference between them. Based on the fact that most of the pseudo-SAHs are associated with cerebral edema,
Fig. 2. The CT shows features similar to Fig. 1, except that the extent of cerebral edema has increased significantly (higher density areas CT value 35 HU). Le scanner présente des caractéristiques similaires celles de la Fig. 1, hormis le fait que l’œdème cérébral a augmenté de manière significative (densité : 35 HU).
Please cite this article in press as: Zhang J, et al. Pseudo-subarachnoid hemorrhage in a patient with hypoxic encephalopathy. Neurochirurgie (2015), http://dx.doi.org/10.1016/j.neuchi.2014.08.003
G Model NEUCHI-677; No. of Pages 3
ARTICLE IN PRESS J. Zhang et al. / Neurochirurgie xxx (2015) xxx–xxx
the CT characteristics useful for differential diagnosis include the following: • pseudo-SAH CT image tends to show relatively symmetrical and diffused high-density distribution; whereas the distribution of CT high-density shadow is always associated with the area of aneurysm rupture in SAH patients; • in the enhanced CT scan, the high-density areas displayed in pseudo-SAH can be significantly enhanced compared to SAH [2]; • in pseudo-SAH, the CT value difference between cerebral gray matter and white matter is less than that in the true SAH patient; • ventricle sulci, split brain of pseudo-SAH patients become relatively narrow; while 35–70% of true SAH patients have enlarged ventricle sulci, split brain in the early days after onset; • the average CT values of the high-density area in pseudo-SAH patients are in the range of 29 to 33 Hounsfield units (HU), significantly lower than those in true SAH patients, which range from 60 to 70 HU [12,13]; • the CT retrieval rates are different: the SAH CT retrieval rate declines quickly, with 100% 2 days after onset, 50% 1 week after onset, 30% 2 weeks after onset and 0% 3 weeks after onset. In contrast, a pseudo-SAH patient will have a similar CT scan 2–3 days after onset, which usually lasts a much longer time [14]. In our case, the SAH phenomenon appeared on the second day after resuscitation. SAH and cerebral edema were considered (high-density area CT value is 35 HU). These findings persisted up to 19 days after resuscitation. Cerebral edema was more severe. The ventricle was not detectable on CT (high-density area CT value 30 HU). Therefore, the CT characteristics were consistent with pseudo-SAH. The mechanisms underlying pseudo-SAH still remain unclear. Excluding the effects of contrast agents causing high-density performance, this phenomenon is more likely related to cerebral edema based on our experience. Severe cerebral edema may compress venous sinuses, and then block cerebral venous return. This therefore leads to further expansion of the superficial veins, which can stand out in contrast to the background of attenuated density of the brain parenchyma on CT, mimicking the features of SAH [3,15]. It should be noted that the distribution on imaging is consistent with that of expanded veins, which can explain the diffused high-density distribution as well as the enhancement effects. It is also worth mentioning that, under these circumstances, the high-density shadow in sulci, the split brain shows a smooth linear presentation. Due to the presence of a cerebral edema, the boundaries between gray matter and white matter are unclear, and subsequent cerebral ventricle shrinkage is present at the early stage. This effect will not be weakened unless the insult of the cerebral edema is removed. Given et al. [8] also reported that partial or complete loss of cerebrospinal fluid space also contributes to the above observations. Therefore, the CT findings of pseudo-SAH are most likely the result of synergizing effects of both elevated intracranial pressure and severe cerebral edema. Other than the mechanisms mentioned above, Norman et al. [16] proposed that the proteinaceous materials from inflammatory reactions are responsible for increased density of basal cisterns and subarachnoid. However, their effects were minimal and probably
3
the negligible blood-brain barrier (BBB) was disrupted by toxins or a toxin-related autoimmune reaction causing SAH. The BBB was disrupted by ischemic intolerance during the cardiopulmonary arrest (CPA) and caused reperfusion injury, and as a result, the BBB was disrupted resulting in SAH [17]. It has been reported that the clinical prognosis of patients with cerebral edema accompanied by pseudo-SAH is significantly worse than the patients without it. The poor prognosis was likely due to the severity of cerebral edema associated with pseudo-SAH. Therefore, despite that it is a relatively rare finding, it is critical to accurately recognize this entity in a timely manner for the appropriate emergent treatment, hence an optimized patient’s outcome. Disclosure of interest The authors declare that they have no conflicts of interest concerning this article. References [1] Latchaw RE, Silva P, Falcone SF. The role of CT following aneurysmal rupture. Neuroimaging Clin N Am 1997;7:693–708. [2] Avrahami E, Katz R, Rabin A, Friedman V. CT diagnosis of non-traumatic subarachnoid haemorrhage in patients with brain edema. Eur J Radiol 1998;28:222–5. [3] Spiegel SM, Fox AJ, Vinuela F, Pelz DM. Increased density of tentorium and falx: a false positive CT sign of subarachnoid hemorrhage. J Can Assoc Radiol 1986;37:243–7. [4] Cucchiara B, Sinson G, Kasner SE, Chalela JA. Pseudo-subarachnoid hemorrhage. Report of three cases and review of the literature. Neurocrit Care 2004;1:371–4. [5] You JS, Park S, Park YS, Chung SP. Pseudo-subarachnoid hemorrhage. Am J Emerg Med 2008;26 [521.e1–2]. [6] Misra V, Hoque R, Gonzalez-Toledo E, Kelley RE, Minagar A. Pseudosubarachnoid hemorrhage in a patient with acute cerebellar infarction. Neurol Res 2008;30:813–5. [7] Mendelsohn DB, Moss ML, Chason DP, Muphree S, Casey S. Acute purulent leptomeningitis mimicking subarachnoid hemorrhage on CT. J Comput Assist Tomogr 1994;18:126–8. [8] Given 2nd CA, Burdette JH, Elster AD, Williams 3rd DW. Pseudosubarachnoid hemorrhage: a potential imaging pitfall associated with diffuse cerebral edema. AJNR Am J Neuroradiol 2003;24:254–6. [9] Min YG, Tse ML. Image in toxicology: pseudo-subarachnoid hemorrhage in a case of severe valproic acid poisoning. Clin Toxicol (Phila) 2011;49:699–700. [10] Koh E, Huang SH, Lai YJ, Hong CT. Spontaneous intracranial hypotension presenting as pseudo-subarachnoid hemorrhage on CT scan. J Clin Neurosci 2011;18:1264–5. [11] Lang JL, Leach PL, Emelifeonwu JA, Bukhari S. Meningitis presenting as spontaneous subarachnoid haemorrhage. Eur J Emerg Med 2013;20:140–1. [12] van Gijn J, van Dongen KJ. The time course of aneurysmal haemorrhage on computed tomograms. Neuroradiology 1982;23:153–6. [13] Senthilkumaran S, Balamurugan N, Menezes RG, Thirumalaikolundusubramanian P. Role of Hounsfield units to distinguish pseudo-subarachnoid hemorrhage. Clin Toxicol 2011;49:948. [14] Yuzawa H, Higano S, Mugikura S, Umetsu A, Murata T, Nakagawa A, et al. Pseudo-subarachnoid hemorrhage found in patients with postresuscitation encephalopathy: characteristics of CT findings and clinical importance. AJNR Am J Neuroradiol 2008;29:1544–9. [15] De La Cruz-Cosme C, Barbieri G, Vallejo-Baez A. Pseudo-subarachnoid haemorrhage. A need for clinical-radiological diagnostic criteria. Neurologia 2010;25:463–5. [16] Norman D, Price D, Boyd D, Fishman R, Newton TH. Quantitative aspects of computed tomography of the blood and cerebrospinal fluid. Radiology 1997;123:335–6. [17] Ogami R, Nakahara T, Hamasaki O, Araki H, Kurisu K. Cerebrospinal fluid enhancement on fluid attenuated inversion recovery images after carotid artery stenting with neuroprotective balloon occlusions: hemodynamic instability and blood-brain barrier disruption. Cardiovasc Intervent Radiol 2011;34:936–41.
Please cite this article in press as: Zhang J, et al. Pseudo-subarachnoid hemorrhage in a patient with hypoxic encephalopathy. Neurochirurgie (2015), http://dx.doi.org/10.1016/j.neuchi.2014.08.003
ARTICLE IN PRESS
NEUCHI-677; No. of Pages 3
Neurochirurgie xxx (2015) xxx–xxx
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Clinical case
Pseudo-subarachnoid hemorrhage in a patient with hypoxic encephalopathy Hémorragie sous-arachnoïdienne chez une patiente présentant une encéphalopathie hypoxique J. Zhang 1 , Q. Li 1 , Z. Zhang ∗ , X. Sun Department of Neurology, The Third Central Hospital of Tianjin, 83, Jintang Road Hedong, Tianjin 300170, China
a r t i c l e
i n f o
Article history: Received 25 April 2014 Received in revised form 1st August 2014 Accepted 28 August 2014 Available online xxx Keywords: Pseudo-subarachnoid hemorrhage Hyperdensity Cerebral edema Pseudo-subarachnoid hemorrhage signs High-density sign Encephaledema
a b s t r a c t The authors report an unusual case of diffuse subarachnoid hemorrhage on brain computed tomography (CT) scan in a patient with post-resuscitation anoxic encephalopathy. A 42-year-old woman suffered both respiratory and cardiac arrest, associated with hypoxic encephalopathy, which occurred during a visit to our gynecology clinic. CT examination was performed the next day, which revealed a hyperdensity in the basal cisterns with a diffuse cerebral edema. Lumbar puncture was applied for diagnosis. No yellow coloration or red cells were observed in the cerebrospinal fluid. Nineteen days after treatment, the CT examination revealed features of a subarachnoid hemorrhage with a significantly increased cerebral edema. The patient died two months later. This clinical case illustrates that hypoxic encephalopathy can mimic diffuse subarachnoid hemorrhage on CT scan. © 2015 Published by Elsevier Masson SAS.
r é s u m é Mots clés : Pseudo-hémorragie sous-arachnoïdienne Hyperdensité Œdème cérébral Signe de pseudo-hémorragie sous-arachnoïdienne Hyperdensité au scanner Œdème encéphalique
Les auteurs rapportent un cas inhabituel d’hémorragie sous-arachnoïdienne diffuse, diagnostiquée par scanner cérébral chez une patiente présentant une encéphalopathie anoxique après une période de réanimation. Il s’agit d’une femme de 42 ans qui présentait un arrêt cardio-respiratoire associé à une encéphalopathie hypoxique. Le lendemain, l’examen tomodensitométrique mettait en évidence une hyperdensité au niveau des citernes basales, ainsi qu’un œdème cérébral diffus. Une ponction lombaire à visée diagnostique était pratiquée. Aucune coloration jaune et aucune hématie n’étaient observées au niveau du liquide céphalorachidien. Dix-neuf jours plus tard, le scanner révélait la présence d’une hémorragie méningée associée à une augmentation significative de l’œdème cérébral. La patiente décédait deux mois plus tard. L’encéphalopathie hypoxique peut mimer une hémorragie méningée au scanner. © 2015 Publie´ par Elsevier Masson SAS.
1. Introduction Typical clinical presentations of subarachnoid hemorrhage (SAH) include a severe headache of rapid onset, vomiting,
∗ Corresponding author. E-mail address: [email protected] (Z. Zhang). 1 Co-first authors: Jing Zhang, Qian Li. These authors contributed equally to this work and should be considered co-first authors.
confusion, and occasional seizures. The diagnosis of SAH is generally confirmed with the presence of increased attenuation of the basal cisterns and subarachnoid space on brain computed tomography (CT) scan. In fact, hyperdensity in the subarachnoid space and basal cisterns are present in 95–98% of CT brain scans of SAH patients within 24 hours of onset [1]. It is well known that CT is a highly sensitive, non-invasive tool to diagnose SAH. However, in rare cases, other diffuse neurological conditions may also produce attenuation of basal cisterns on CT mimicking that of SAH. In 1998, Avrahami et al. [2] proposed that these CT mimicking SAH could
http://dx.doi.org/10.1016/j.neuchi.2014.08.003 0028-3770/© 2015 Published by Elsevier Masson SAS.
Please cite this article in press as: Zhang J, et al. Pseudo-subarachnoid hemorrhage in a patient with hypoxic encephalopathy. Neurochirurgie (2015), http://dx.doi.org/10.1016/j.neuchi.2014.08.003
G Model NEUCHI-677; No. of Pages 3
ARTICLE IN PRESS J. Zhang et al. / Neurochirurgie xxx (2015) xxx–xxx
2
be defined as pseudo-subarachnoid hemorrhage (pseudo-SAH). In this article, we report a case of pseudo-SAH associated with hypoxic encephalopathy, and explore the key findings for its differential diagnosis based on a true SAH.
after treatment, CT examination revealed features of SAH with significantly increased cerebral edema (Fig. 2). The patient died two months later. 3. Discussion
2. Case presentation A 42-year-old woman visited the clinic for ovarian cyst, and suddenly fell on the ground accompanied by a loss of consciousness. She was found to have respiratory and cardiac arrest. Detailed medical history was not obtained as we were unable to contact any of her relatives. She underwent emergency cardiopulmonary resuscitation in the intensive care unit with pressure support ventilation. Her vital signs were: temperature 36.8 ◦ C, pulse 158/min, blood pressure 156/79 mmHg. The physical examination showed: bilateral pupils with equal size (2.5 mm in diameter), negative light response, negative oculocephalogyric reflex, a supple neck, upper limbs flexion and lower limbs extension, lungs clear on auscultation, regular heart rhythm, no abdominal tenderness, extremities unremarkable. The patient’s Glasgow coma scale was 5. CT scan examination was performed the next day when her vital signs were stable, which revealed a hyperdensity in the basal cisterns and diffuse cerebral edema (Fig. 1). Lumbar puncture was applied for diagnosis due to the lack of detailed medical history and revealed: pressure 170 mmHg, white blood cells 0/mm3 , red blood cells 0/mm3. No yellow coloration was observed in the cerebrospinal fluid, and glucose, chlorides, and protein levels were within normal range. The patient was eventually diagnosed as having an hypoxic encephalopathy. Low-temperature treatment was performed to protect brain tissue, and dehydration was applied to reduce the intracranial pressure. Hemodynamic stability was maintained at the same time to ensure sufficient blood supply to the major organs. Nineteen days
Fig. 1. The CT shows slightly lower density of brain parenchyma with no clear corticomedullary boundaries; the densities of part of the sulci and split brain as well as the entorhinal edge increase. The CT features are consistent with either SAH or cerebral edema (higher density areas CT value 35 HU). Le scanner montre une hypodensité modérée du parenchyme cérébral sans limites cortico-médullaires clairement objectivées ; les densités d’une partie des sillons et d’une schizencéphalie (split brain), ainsi que de la région entorhinale, sont augmentées. Les caractéristiques du scanner sont compatibles soit avec une hémorragie arachnoïdienne, soit avec un œdème cérébral (densité : 35 HU).
It has been well accepted that the diagnosis of SAH is generally confirmed with the presence of increased attenuation of the basal cisterns and subarachnoid spaces on brain CT scan. However, in rare cases, other diffuse neurological conditions may produce attenuation of basal cisterns on CT and mimic characteristics of SAH, defined as pseudo-subarachnoid hemorrhage (pseudo-SAH). Therefore, without a clear disease history, lumbar puncture is usually needed to avoid misdiagnosis. As for the patient in this case, sulci, split brain, tentorium and interhemispheric tentorial density increased as shown in the CT scan. The patient’s clinical history was not clear. Diagnosis of pseudo-SAH was eventually made with the help of a lumbar puncture. In 1986, Spiegel et al. [3] first described this phenomenon in a patient with cerebral edema. In 1998, Avrahami et al. [2] proposed that the imaging change mimicking SAH could be defined as pseudo-SAH. Since then, further studies have been continuously performed as regards this phenomenon, and the several possible pathophysiological etiologies underlying it were proposed. The most popular theories include hypoxic-ischemic encephalopathy, reperfusion injury encephalopathy, massive cerebral infarction, viral meningoencephalitis, bilateral subdural hematoma, idiopathic intracranial hypertension, venous sinus thrombosis, and intrathecal or intravascular contrast agent injection [4–11]. These causes are excluded by detailed history, physical examination and laboratory data. Certainly, lumbar puncture is of particular importance for an accurate clinical diagnosis, especially when there is a lack of other relevant clinical information. Although the CT imaging of pseudo-SAH closely mimics SAH, there remains a slight difference between them. Based on the fact that most of the pseudo-SAHs are associated with cerebral edema,
Fig. 2. The CT shows features similar to Fig. 1, except that the extent of cerebral edema has increased significantly (higher density areas CT value 35 HU). Le scanner présente des caractéristiques similaires celles de la Fig. 1, hormis le fait que l’œdème cérébral a augmenté de manière significative (densité : 35 HU).
Please cite this article in press as: Zhang J, et al. Pseudo-subarachnoid hemorrhage in a patient with hypoxic encephalopathy. Neurochirurgie (2015), http://dx.doi.org/10.1016/j.neuchi.2014.08.003
G Model NEUCHI-677; No. of Pages 3
ARTICLE IN PRESS J. Zhang et al. / Neurochirurgie xxx (2015) xxx–xxx
the CT characteristics useful for differential diagnosis include the following: • pseudo-SAH CT image tends to show relatively symmetrical and diffused high-density distribution; whereas the distribution of CT high-density shadow is always associated with the area of aneurysm rupture in SAH patients; • in the enhanced CT scan, the high-density areas displayed in pseudo-SAH can be significantly enhanced compared to SAH [2]; • in pseudo-SAH, the CT value difference between cerebral gray matter and white matter is less than that in the true SAH patient; • ventricle sulci, split brain of pseudo-SAH patients become relatively narrow; while 35–70% of true SAH patients have enlarged ventricle sulci, split brain in the early days after onset; • the average CT values of the high-density area in pseudo-SAH patients are in the range of 29 to 33 Hounsfield units (HU), significantly lower than those in true SAH patients, which range from 60 to 70 HU [12,13]; • the CT retrieval rates are different: the SAH CT retrieval rate declines quickly, with 100% 2 days after onset, 50% 1 week after onset, 30% 2 weeks after onset and 0% 3 weeks after onset. In contrast, a pseudo-SAH patient will have a similar CT scan 2–3 days after onset, which usually lasts a much longer time [14]. In our case, the SAH phenomenon appeared on the second day after resuscitation. SAH and cerebral edema were considered (high-density area CT value is 35 HU). These findings persisted up to 19 days after resuscitation. Cerebral edema was more severe. The ventricle was not detectable on CT (high-density area CT value 30 HU). Therefore, the CT characteristics were consistent with pseudo-SAH. The mechanisms underlying pseudo-SAH still remain unclear. Excluding the effects of contrast agents causing high-density performance, this phenomenon is more likely related to cerebral edema based on our experience. Severe cerebral edema may compress venous sinuses, and then block cerebral venous return. This therefore leads to further expansion of the superficial veins, which can stand out in contrast to the background of attenuated density of the brain parenchyma on CT, mimicking the features of SAH [3,15]. It should be noted that the distribution on imaging is consistent with that of expanded veins, which can explain the diffused high-density distribution as well as the enhancement effects. It is also worth mentioning that, under these circumstances, the high-density shadow in sulci, the split brain shows a smooth linear presentation. Due to the presence of a cerebral edema, the boundaries between gray matter and white matter are unclear, and subsequent cerebral ventricle shrinkage is present at the early stage. This effect will not be weakened unless the insult of the cerebral edema is removed. Given et al. [8] also reported that partial or complete loss of cerebrospinal fluid space also contributes to the above observations. Therefore, the CT findings of pseudo-SAH are most likely the result of synergizing effects of both elevated intracranial pressure and severe cerebral edema. Other than the mechanisms mentioned above, Norman et al. [16] proposed that the proteinaceous materials from inflammatory reactions are responsible for increased density of basal cisterns and subarachnoid. However, their effects were minimal and probably
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the negligible blood-brain barrier (BBB) was disrupted by toxins or a toxin-related autoimmune reaction causing SAH. The BBB was disrupted by ischemic intolerance during the cardiopulmonary arrest (CPA) and caused reperfusion injury, and as a result, the BBB was disrupted resulting in SAH [17]. It has been reported that the clinical prognosis of patients with cerebral edema accompanied by pseudo-SAH is significantly worse than the patients without it. The poor prognosis was likely due to the severity of cerebral edema associated with pseudo-SAH. Therefore, despite that it is a relatively rare finding, it is critical to accurately recognize this entity in a timely manner for the appropriate emergent treatment, hence an optimized patient’s outcome. Disclosure of interest The authors declare that they have no conflicts of interest concerning this article. References [1] Latchaw RE, Silva P, Falcone SF. The role of CT following aneurysmal rupture. Neuroimaging Clin N Am 1997;7:693–708. [2] Avrahami E, Katz R, Rabin A, Friedman V. CT diagnosis of non-traumatic subarachnoid haemorrhage in patients with brain edema. Eur J Radiol 1998;28:222–5. [3] Spiegel SM, Fox AJ, Vinuela F, Pelz DM. Increased density of tentorium and falx: a false positive CT sign of subarachnoid hemorrhage. J Can Assoc Radiol 1986;37:243–7. [4] Cucchiara B, Sinson G, Kasner SE, Chalela JA. Pseudo-subarachnoid hemorrhage. Report of three cases and review of the literature. Neurocrit Care 2004;1:371–4. [5] You JS, Park S, Park YS, Chung SP. Pseudo-subarachnoid hemorrhage. Am J Emerg Med 2008;26 [521.e1–2]. [6] Misra V, Hoque R, Gonzalez-Toledo E, Kelley RE, Minagar A. Pseudosubarachnoid hemorrhage in a patient with acute cerebellar infarction. Neurol Res 2008;30:813–5. [7] Mendelsohn DB, Moss ML, Chason DP, Muphree S, Casey S. Acute purulent leptomeningitis mimicking subarachnoid hemorrhage on CT. J Comput Assist Tomogr 1994;18:126–8. [8] Given 2nd CA, Burdette JH, Elster AD, Williams 3rd DW. Pseudosubarachnoid hemorrhage: a potential imaging pitfall associated with diffuse cerebral edema. AJNR Am J Neuroradiol 2003;24:254–6. [9] Min YG, Tse ML. Image in toxicology: pseudo-subarachnoid hemorrhage in a case of severe valproic acid poisoning. Clin Toxicol (Phila) 2011;49:699–700. [10] Koh E, Huang SH, Lai YJ, Hong CT. Spontaneous intracranial hypotension presenting as pseudo-subarachnoid hemorrhage on CT scan. J Clin Neurosci 2011;18:1264–5. [11] Lang JL, Leach PL, Emelifeonwu JA, Bukhari S. Meningitis presenting as spontaneous subarachnoid haemorrhage. Eur J Emerg Med 2013;20:140–1. [12] van Gijn J, van Dongen KJ. The time course of aneurysmal haemorrhage on computed tomograms. Neuroradiology 1982;23:153–6. [13] Senthilkumaran S, Balamurugan N, Menezes RG, Thirumalaikolundusubramanian P. Role of Hounsfield units to distinguish pseudo-subarachnoid hemorrhage. Clin Toxicol 2011;49:948. [14] Yuzawa H, Higano S, Mugikura S, Umetsu A, Murata T, Nakagawa A, et al. Pseudo-subarachnoid hemorrhage found in patients with postresuscitation encephalopathy: characteristics of CT findings and clinical importance. AJNR Am J Neuroradiol 2008;29:1544–9. [15] De La Cruz-Cosme C, Barbieri G, Vallejo-Baez A. Pseudo-subarachnoid haemorrhage. A need for clinical-radiological diagnostic criteria. Neurologia 2010;25:463–5. [16] Norman D, Price D, Boyd D, Fishman R, Newton TH. Quantitative aspects of computed tomography of the blood and cerebrospinal fluid. Radiology 1997;123:335–6. [17] Ogami R, Nakahara T, Hamasaki O, Araki H, Kurisu K. Cerebrospinal fluid enhancement on fluid attenuated inversion recovery images after carotid artery stenting with neuroprotective balloon occlusions: hemodynamic instability and blood-brain barrier disruption. Cardiovasc Intervent Radiol 2011;34:936–41.
Please cite this article in press as: Zhang J, et al. Pseudo-subarachnoid hemorrhage in a patient with hypoxic encephalopathy. Neurochirurgie (2015), http://dx.doi.org/10.1016/j.neuchi.2014.08.003