Cerebral Digital Subtraction Angiographic Findings in Computed Tomography Angiography Negative Spontaneous Subarachnoid Hemorrhage

Raihan Ahmad 1, F M Monjur Hasan2, Ahsan Habib 3, Kaniz Farhana Bithi 4, Richmond Ronald Gomes 5*, Shafiqul Islam 6.

1Resident, Neurology, National Institute of Neurosciences and Hospital, Dhaka Bangladesh.

2 Associate Professor, Ad din Sakina Women’s Medical College, Jashore, Bangladesh.

3 Registrar, Neurology, Rajshahi Medical College Hospital, Rajshahi, Bangladesh.

4 Junior Consultant, Medicine, National Institute of Neurosciences and Hospital, Dhaka, Bangladesh.

5 Professor, Medicine, Ad din Women’s Medical College Hospital, Dhaka, Bangladesh.

6 Resident, Rheumatology, Bangabandhu Sheikh Mujib Medical University, Dhaka, Bangladesh.

*Corresponding Author:Richmond Ronald Gomes, Professor of Medicine, Ad-din Women’s Medical College Hospital, 2 Bara Maghbazar, Dhaka Bangladesh, Tel: 00(212)614134817, Fax: 00(212)614134817.

Citation: Raihan Ahmad, F M Monjur Hasan, Ahsan Habib, Kaniz Farhana Bithi, Richmond Ronald Gomes, et al. (2024) Cerebral Digital Subtraction Angiographic Findings in Computed Tomography Angiography Negative Spontaneous Subarachnoid Hemorrhage. Medcina Intern 6: 224.

Received: March 09, 2024; Accepted: March 16, 2024; Published: March 21, 2024.

Copyright: © 2024 Richmond Ronald Gomes, et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Abstract

Background: Ruptured aneurysm is the cause of spontaneous subarachnoid hemorrhage (SAH). Computed tomographic angiography (CTA) is commonly used to detect vascular lesion but in about 15-20% of SAH patients no aneurysm is found. In these CTA negative cases, Digital subtraction angiography (DSA) is performed for the detection of causative vascular lesions.

Aim: The purpose of this study was to observe the cerebral DSA findings in CTA negative cases. Materials and Methods: This descriptive type of cross-sectional study was conducted at National Institute of Neurosciences & Hospital (NINS&H), Dhaka, from January 2022 to June 2023. inclusion and exclusion criteria, total 90 patients were enrolled by purposive sampling technique and undergone DSA. Non-contrast head CT, CTA, DSA were viewed by 1 neurointerventionalist and 1 radiologist.

Results: Among ninety patients, mean age was 50.4 years with male predominance (64.4%). hypertension (58.9%) and smoking habit (33.3%) were the most common risk factors. All participants (100%) had headache while 95.6% had history of vomiting. 19% cases were found in altered level of consciousness. Sign of meningeal irritation, ptosis and hemiplegia were present in 74.4%, 3.3% and 1.1% cases respectively. After DSA causative vascular lesion were found in 14% (13 cases) of patients, including 13% (12) aneurysms and 1% (1) micro-AVM. Ruptured aneurysm (17.7%, 11/62) and micro-AVM (1.6%,1/62) were found as source of hemorrhage in nPM-SAH where ruptured aneurysm was also found as cause of hemorrhage in 3.6% (1/28) cases PM-SAH. All causative lesions were small predominantly saccular aneurysm 7(54%,7/13). Remaining were 1 micro-AVM and aneurysm with atypical morphology (3 blisters, 1 dissecting, 1 fusiform). Most of the causative lesion (total 11cases) were found in anterior circulation predominantly in anterior communicating artery (4cases) after DSA in these CTA negative cases.

Conclusion: DSA identified causative vascular lesions in 14% of cases. Vascular lesions mostly were found in nPM but ruptured aneurysm was also found in 3.6% cases of PM pattern of CTA negative.

Keywords

:Spontaneous Subarachnoid Hemorrhage, Negative Computed Tomography Angiography, Aneurysm, Non-Aneurysmal SAH, Non-Perimesencephalic SAH, Perimesencephalic SAH, Digital Subtraction Angiography.

Introduction

Subarachnoid hemorrhage (SAH) is a devastating clinical condition affecting a significant number of the population. The worldwide SAH incidence was 7.9 per 100 000 person-years. For Asia overall, the incidence was estimated to be 10.4 per 100 000 person-years.[1] It accounts for 5% of all strokes and approximately 45% mortality rate within one month after SAH. [2,3]

 Excluding head trauma, ruptured cerebral aneurysm (85%) is the most common aetiology for spontaneous SAH. [4,5] Patients with aneurysmal SAH (ASAH) experience high rates of morbidity and mortality. [6] So prompt aneurysm diagnosis is very much essential. Once SAH has been confirmed by Non-contrast CT (NCCT Computed tomography angiograph (CTA) is usually done to detect causative vascular lesion as because it is noninvasive, less expensive, widely available [2,7]. But prior studies reported that CTA fails to identify causative lesion in 15% (5-30%) cases, these are termed as angio-negative SAH (AN-SAH) or non-aneurysmal SAH (NASAH). [2,8-10] These AN-SAH cases are also at risk of rebleeding (0-5%), vasospasm and even death (0-15%). [11,12] Digital subtraction angiography (DSA) is the gold standard method with a reported sensitivity 99-99.9% and specificity 100% for the detection of intracranial aneurysm.[13,14] Prior studies suggested that DSA can identify causative vascular causative lesion about 4-14% in patients with initial CTA negative SAH and repeat DSA can detect the source of bleeding in 4-16% of initial DSA negative findings.2 CTA negative SAH, based pattern of hemorrhage on initial CT scan, can be divided into perimesenchalic SAH (PM-SAH) and non-perimesencephalic SAH (nPM-SAH), as because it may predict the probability of identifying a causative vascular lesion. [8,9,16] PM-SAH is typically benign in nature, having venous source of bleeding but clinical course of nPM-SAH is considered as similar to ASAH at onset, but have less severity than it. [17,18] Though some prior studies [9,19] recommended that no need to perform DSA in PM-SAH but other studies suggested that source of hemorrhage may be found about 0-5% in patient with PM-SAH after DSA and DSA should be done in both pattern of CTA negative SAH. [2,3,16, 20] The aim of this study was to observe the cerebral DSA findings in CTA negative SAH.

Materials and Methods

This descriptive type of cross-sectional study was conducted in the department of Neurology, National Institute of Neurosciences and Hospital (NINS&H) Dhaka, Bangladesh from January 2022 to June 2023. Total 90 patients (age ≥ 18years of both gender) of spontaneous SAH, after fulfilling the inclusion and exclusion criteria were enrolled by purposive sampling technique.

Inclusion criteria: a) Patients with CTA-negative spontaneous SAH b) CTA has done within first 72 hours of ictus c) Age ≥18 years of both male and female d) Patient or patients guardian who had given consent to enroll into this study.

Exclusion criteria: a) Patients with traumatic SAH b) CT negative SAH but positive lumber puncture c) Patients with bleeding diathesis d) SAH secondary to intracerebral hemorrhage e) Patients unwilling to undergo DSA. Statistical analysis was performed by using SPSS (Statistical Package for Social Science) software (IBM SPSS Statistics for Windows, Version 27.0). Continuous data that were normally distributed, expressed as mean and standard deviation. Continuous but not normally distributed data were expressed as median & Interquartile range (IQR). Categorical data were expressed as frequency and percentage where applicable.

Results

Total 90 participants underwent DSA and were included in this study. Among all, mean age of the study participants was 50.4±10.5 years (mean±SD) ranging from 27 to 70 years. Majority of the participants were within 41-50 years of aged group with male predominance (64.4%) (Table-1).

 Table1: Demographical profile of the Study participants (n=90).

Demographic profile

Frequency (n)

Percentage (%)

Age group (years)

 

 

   ≤30

4

 4.4

   31 to 40

16

17.8 

   41 to 50

   51 to 60

28

27

31.1

30

    ≥61

15

16.7 

Mean±SD

Range (27-70)

 50.4±10.5

 

 

Gender

 

 

   Male

58

 64.4

   Female

32

35.6 

Values were presented with frequency (%) and mean±SD; mean ± standard deviation

The most common risk factors were HTN (58.9%) followed by smoking (33.3%), diabetes mellitus (22.2%) and history of first-degree relatives with SAH was also found in 4.4% cases. All participants (100%) had headache among them 50% experienced severe headache. While 95.6% had history of vomiting, 19% were found in altered level of consciousness. Nuchal rigidity 67 (74.4%), ptosis 3 (3.3%) and hemiplegia 1(1.1%) were present among the study participants.

On the basis of pattern of hemorrhage on NCCT, nPM-SAH and PM-SAH were 62(68.9%) and 28(31.1%) respectively. All participants underwent DSA and the time interval median & (IQR) was 6 (5-8) days. DSA identified a causative vascular lesion 14% (13) of patients including 13% (12) aneurysm and 1% (1) AVM. No causative lesion was found in 86% (77) of the participants (Figure-1).

Figure1: Distribution of morphology of causative vascular lesion with size found on DSA in patients with CTA negative spontaneous SAH.

 

Aneurysms 17.7% (11) and AVM 1.6% (1) were identified in patients with nPM-SAH (62 patients) whereas aneurysm was also found in 3.6% (1) cases of PM-SAH (28 patients) (Table-2).

 Table 2: Distribution of participants by vascular lesions found on DSA in different pattern of SAH on CT findings.

 

Type of vascular lesion

           Pattern of SAH on CT findings

 

Total participants (n=90)

Non-perimesencephalic 

(nPM) (n=62)     

Perimesencephalic (PM)(n=28)

 No causative    vascular lesion

50 (80.6%)

27(96.4%)

77(86%)

Aneurysm

11(17.7%)

1(3.6%)

12(13%)

Arteriovenous malformation (AVM)

1(1.6%)

0(0%)

1(1%)

 Most common causative lesion was saccular aneurysms 7(54%), all were small (≤4mm in diameter). Second most common source of hemorrhage was blister aneurysms 3(23%) with ≤2.2mm in diameter. Others vascular lesions were 1(3.3mm) dissecting, 1(3.8mm) fusiform aneurysm and 1 micro-AVM, these were the source hemorrhage of spontaneous SAH, but not detected on CTA (Figure-2).

Figure 2: DSA findings in CTA negative spontaneous SAH.

 

Of these 12 aneurysms including 7 saccular were located in different territory (3 in ACom artery, 3 in PCom artery, 1 in basilar top). Others 3 blister (2 in supraclinoid part of ICA, 1 in ACom Artery), 1 dissecting (MCA), 1 fusiform aneurysm (cavernous part of ICA), 1 micro AVM (in perforators of PCA draining into superficial venous system). Most common location of vascular lesion (cerebral aneurysm) was anterior circulation (11cases) and ACom artery was the most frequent single location. Here 4 aneurysms were identified, followed by 3 in ICA, 3 in PCom artery, 1 in MCA. Remaining 2 vascular lesions were identified on DSA in posterior circulation including 1 AVM where feeding artery was PCA and 1 aneurysm at basilar top.

Discussion

CTA is noninvasive, less time consuming, widely available, it has emerged as a first line measure to detect causative vascular lesion. [2,7] Though CTA is effective screening tool, it fails to detect causative vascular lesion in 15(5–30%) cases of spontaneous SAH. [2,8] Due to the devastating effects of a false-negative findings, these patients are later assessed by DSA in the diagnosis of a ruptured causative vascular lesion. [22] In this study, amomg 90 participants, the majority (31.1%) of the patients were in the age group 41-50 years and the mean (±SD) age was 50.4±10.5 years with male preponderance (64.4%). In a previous study by Catapano et al, mean age of the patients was 56 years where 52% were male.6 In the study by Hasan et al, 80% of the patients were 50 or younger than 50 years of old with a mean (±SD) age was 45.0 ± 9.4 years with a male preponderance (60%). [23] de Rooij et al, reported that in the age group of 25–45 years, incidence of SAH was significantly higher in male than female but occurrence of SAH was higher in 5th to 6th decades with female predominance (1.6 times higher). [5] In this current study, of the risk factors, hypertension, smoking habit and diabetes demonstrated their significant presence (58.9%, 33.3% and 22.2% respectively). Hasan et al, reported that major modifiable risk factors were hypertension (46.7%), h/o smoking habit (44%). Diabetes (10-16%), family history SAH (6.7%) were also reported as contributory risk factor in previous studies. [23-25] Gupta SK et al, reported that the presence of diabetes and alcohol intake was also higher in patients with negative angiogram cases. [26] all the participants had headache (100%). Vomiting was invariably complained by most of the participants (95.5%). Signs of meningeal irritation which was found in 74.4% cases in this study. Previous studies also reported similar findings. [22,26].  In this current study, based on pattern of hemorrhage on NCCT findings, nPM-SAH 62 (68.9%) and PM-SAH 28(31%) were identified which was similar to authors in prior studies. [27,28] In this study, among all study participants, DSA determined the cause of hemorrhage in 14% (13/90) cases of SAH who were initially CTA negative. Delgado Almandoz et al, Heit et al, and Jung et al, reported similar results 11%, 13% and 18% respectively. [2,15,29] But results of this study were higher than that in previous study by Agid et al, where causative lesions were 4.2% detected on DSA in patient with CTA negative SAH. The difference in overall DSA findings between our study and that of Agid et al, is likely explained by the larger proportion of patients with PM-SAH in their study participants (48.2%) compared to with this study (31.1%). [16] Indeed, the most common identified cause in this study was ruptured intracranial aneurysm detected on cerebral DSA in CTA negative spontaneous SAH. Causative vascular lesion was 13% (12/90), aneurysms and 1.1% (1/90) arteriovenous malformation (AVM). This study result was similar to the previous retrospective analyses in which ruptured intracranial aneurysms were the primary causative vascular lesion.16 In this study, among the causative vascular lesions, 17.7% aneurysms (11/62) and 1.6% (1/62) AVM were identified on DSA in patients with nPM-SAH. On the other hand, 3.6% (1/28) aneurysm was found on DSA in patient with PM-SAH. Previous studies Delgado Almandoz et al, westerlaan et al, Bashir et al, reported that causative lesions were only found in 18%, 29%, 12.5% cases of nPM-SAH respectively.9,29,30 They also reported that no source of bleeding was dectected on repeat angiography in case of PM-SAH. Rinkel et al, suggested that the cause of PM-SAH is not aneurysm but may be venous source, no risk of rebleeding no need to do DSA at all in patients with PM-SAH who had negative CTA findings.31 But some studies by Delgado Almandoz et al, and Heit et al, reported that aneurysm (3.4% and 4.5% respectively) as a source of hemorrhage was also found on DSA in patients with PM-SAH.2,20 The results of the these studies were similar to the result of this current study. In this study, among 13 vascular lesions, 1microAVM and 12 aneurysms were detected on DSA where most of them 7 (54%) were saccular aneurysm with a diameter <4mm. Second most common source of hemorrhage was atypical aneurysm like 3(23%) blister aneurysms with ≤2.2mm diameter in size. Others were 1(3.3mm) dissecting, 1(3.8mm) fusiform aneurysm. In this study all the vascular lesions were small and some were with atypical morphology.32 These were the main reason for negative CTA findings in this study. Previous study by Catapano et al, reported similar findings to this study, where most of the causative lesion 7 (87.5%) were small saccular and atypical aneurysm (blisters, dissecting, fusiform) and 1(12.5%) was cervical arteriovenous fistula (AVF). All aneurysms were small <3mm with atypical features ((blisters, dissecting, fusiform). [6] In this study most of the vascular lesions were present in the anterior circulation (11 cases) and ACom artery was the most common location for causative lesion (4 cases). Remaining 2 vascular lesion were located at posterior circulation, detected on DSA, similar results in previous studies by Jafar, weiner, Gharib-Salehi et al, and Jung et al, also reported that anterior circulation, most commonly ACom artery was the most frequent location and small aneurysm was the most common lesion. [15,33,34] by agid et al, had suggested that widespread aneurysmal pattern of angio-negative SAH must need to do DSA and aneurysm must also be excluded in the posterior circulation in patient with PM-SAH. [16] In this study, 1 saccular aneurysm was detected in posterior circulation (basilar top) on cerebral DSA which was missed on CTA where pattern of haemorrhage on NCCT was perimesencephalic (PM-SAH). Some figures regarding vascular lesion found in DSA in CTA negative cases are given below (Figure-A, B, C, D).

Figure A: A 40 years old service holder male presented with the history of sudden severe headache, vomiting and neck rigidity. He was a smoker and hypertensive. His SAH was confirmed by (a) NCCT (nPM) but initial (b) CTA was negative. But small saccular aneurysm (arrow) was detected following (c)DSA.

Figure B: A 27 years old male student presented with the history of sudden severe headache, vomiting, ptosis. He was a smoker. His SAH was confirmed by (a) NCCT (nPM) but initial (b) CTA there was no causative lesion. But after (c) DSA small saccular aneurysm (arrow) was detected at right ICA and at the origin of right PCom artery.

Figure C: A 57 years old diabetic, hypertensive housewife presented with the history of sudden severe thunderclap headache, vomiting, and sign of meningeal irritation. She was also gave the history of SAH in her 1st degree relatives. Her SAH was confirmed by (a) NCCT (nPM) but in initial (b) CTA no causative lesion was found. But after (c) DSA a blister aneurysm (arrow) was detected at supraclinoid segment left ICA measuring about 1.54×1.60mm.

 

Conclusion

Causative lesions were identified after DSA as a cause of hemorrhage in 14% cases of study participants. Though after DSA, most of the causative lesions were identified in case of nPM-SAH, but aneurysm also found in 3.6% cases of PM-SAH. These results give the emphasis to do DSA for the patients with CTA negative spontaneous SAH of both pattern of hemorrhage including nPM-SAH and PM-SAH to detect primarily aneurysm or other causative vascular lesions. These findings can help for taking decision in further treatment plan in CTA negative SAH.

Limitations

The study was based on a single center, so result may vary with other institutional study and may not reflect the population. In this study sample size was small due to time constraint and repeat DSA was not done.

Recommendations

A large-scale study involving greater number of patients in multiple centers is recommended to make final comment regarding this issue. DSA must be done in CTA negative cases. Repeat DSA should also be done.

Conflict of interest

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

References

  1. Etminan N, Chang HS, Hackenberg K, De Rooij, et al. (2019) Worldwide incidence of aneurysmal subarachnoid hemorrhage according to region, time period, blood pressure, and smoking prevalence in the population: a systematic review and meta-analysis. JAMA neurology 76: 588-597.
  2. Heit JJ, Pastena GT, Nogueira RG, Yoo AJ, Leslie-Mazwi TM, et al. (2016) Cerebral angiography for evaluation of patients with CT angiogram-negative subarachnoid hemorrhage:an11-year experience. American Journal of Neuroradiology 37: 297-304.
  3. Haider AS, Gottlich C, Khahera A, Vayalumkal S, Khan U, et al. (2017) The importance of catheter angiography in computed tomography angiography-negative subarachnoid hemorrhage. Cureus 9: 1-7.
  4. Macdonald RL, Schweizer TA (2017) Spontaneous subarachnoid hemorrhage. The Lancet 389: 655-666.
  5. de Rooij NK, Linn FH, van der Plas JA, Algra A, Rinkel GJ, et al. (2007) Incidence of subarachnoid hemorrhage: a systematic review with emphasis on region, age, gender and time trends. Journal of Neurology, Neurosurgery & Psychiatry 78:1365-1372.
  6. Catapano JS, Lang MJ, Koester SW, Wang DJ, DiDomenico JD, et al. (2020) Digital subtraction cerebral angiography after negative computed tomography angiography findings in non-traumatic subarachnoid hemorrhage. Journal of Neuro Interventional Surgery 12: 526-530.
  7. Hoh BL, Cheung AC, Rabinov JD, Pryor JC, Carter BS et al. (2004) Results of a prospective protocol of computed tomographic angiography in place of catheter angiography as the only diagnostic and pretreatment planning study for cerebral aneurysms by a combined neurovascular team. Neurosurgery 54: 1329-1342.
  8. Ali mohammadi E, Ahadi P, Karbas foroushan A, Rahmani S, Bagheri SR et al. (2020) Nontraumatic nonaneurysmal subarachnoid hemorrhage: Risk factors, complications, and clinical outcomes. Indian Journal of Neurosurgery 10: 037-041.
  9. Bashir A, Mikkelsen R, Sørensen L, Sunde N (2018) Non-aneurysmal subarachnoid hemorrhage: when is a second angiography indicated? The Neuroradiology Journal 3: 244-252.
  10. Boswell S, Thorell W, Gogela S, Lyden E, Surdell D, et al. (2013) Angiogram-negative subarachnoid hemorrhage: outcomes data and review of the literature. Journal of Stroke and Cerebrovascular Diseases 22: 750-757.
  11. Kumar R, Das KK, Sahu RK, Sharma P, Mehrotra A, et al. (2014) Angio negative spontaneous subarachnoid hemorrhage: Is repeat angiogram required in all cases. Surgical neurology international 5.
  12. Pyysalo LM, Niskakangas TT, Keski-Nisula LH, Kähärä VJ, Öhman, JE (2011) Long term outcome after subarachnoid hemorrhage of unknown aetiology. Journal of Neurology, Neurosurgery & Psychiatry 82: 1264-1266.
  13. Yeung R, Ahmad T, Aviv RI, et al. (2009) Comparison of CTA to DSA in determining the etiology of spontaneous ICH. Can J Neurol Sci 36: 176–180
  14. Luo Z, Wang D, Sun X, Zhang T, Liu F, et al. (2012) Comparison of the accuracy of subtraction CT angiography performed on 320-detector row volume CT with conventional CT angiography for diagnosis of intracranial aneurysms. European journal of radiology 81: 118–122.
  15. Jung JY, Kim YB, Lee JW, Huh SK, Lee KC, et al. (2006) Spontaneous subarachnoid hemorrhage with negative initial angiography: a review of 143 cases. Journal of Clinical Neuroscience 13: 1011-1017.
  16. Agid R, Andersson T, Almqvist H, Willinsky RA, Lee SK, et al. (2010) Negative CT angiography findings in patients with spontaneous subarachnoid hemorrhage: When is digital subtraction angiography still needed? American Journal of Neuroradiology 31: 696–705.
  17. Andaluz N, Zuccarello M (2008) Yield of further diagnostic work-up of cryptogenic subarachnoid hemorrhage based on bleeding patterns on computed tomographic scans. Neurosurgery 62: 1040-1047.
  18. Akcakaya MO, Aydoseli A, Aras Y, Sabanci PA, Barburoglu M, et al. (2017) Clinical course of nontraumatic non-aneurysmal subarachnoid hemorrhage: A single institution experience over 10 years and review of the contemporary literature. Turk Neurosurg 27: 732-742.
  19. Rinkel GJE, Wijdicks EFM, van Gijn J, Hasan D, Vermeulen M, et al. (1991) Outcome in patients with subarachnoid hemorrhage and negative angiography according to pattern of hemorrhage on computed tomography. The Lancet 338: 964-968.
  20. Almandoz JED, Jagadeesan BD, Refai D, Moran CJ, Cross III DT, et al. (2012) Diagnostic yield of repeat catheter angiography in patients with catheter and computed tomography angiography negative subarachnoid hemorrhage. Neurosurgery 70: 1135-1142.
  21. Mohan M, Islim AI, Rasul FT, Rominiyi O, deSouza RM, et al. (2019) Subarachnoid hemorrhage with negative initial neurovascular imaging: a systematic review and meta-analysis. Acta neurochirurgica 161: 2013-2026.
  22. Van Gijn J, Rinkel GJE (2001) Subarachnoid hemorrhage: diagnosis, causes and management. Brain 124: 249-278.
  23. Hasan MN, Hoque MA, Rahman KM, Hoque MH, Amin MR, et al. (2015) Clinical and digital subtraction angiographic (DSA) evaluation of patients of subarachnoid hemorrhage (SAH) in a tertiary level hospital. Bangladesh Medical Journal 44: 125-129.
  24. Moscovici S, Fraifeld S, Ramirez-de-Noriega F, Rosenthal G, Leker RR, et al. (2013) Clinical relevance of negative initial angiogram in spontaneous subarachnoid hemorrhage. Neurological Research 35: 117-122.
  25. Gupta SK, Gupta R, Khosla VK, Mohindra S, Chhabra R, et al. (2009) non-aneurysmal non-perimesencephalic subarachnoid hemorrhage: is it a benign entity? Surgical neurology 71: 566-571.
  26. Islam M, Hasan M, Hakim M Khan SU, Rahman KM, Mohammad QD, et al. (2016) Digital Subtraction Angiography Findings in Aneurysmal Subarachnoid Hemorrhage: Experience of 30 Cases in Bangladesh. Journal of National Institute of Neurosciences Bangladesh 2: 51-54.
  27. Sadigh G, Menon, RK Bhojak, M Aladi, A Mossa-Basha, et al. (2019) Radiological management of angiographically negative, spontaneous intracranial subarachnoid hemorrhage: a multicenter study of utilization and diagnostic yield. Neurosurgery 85: 126-133.
  28. Achrén A, Raj R, Siironen J, Laakso A, Marjamaa, J, et al. (2022) Spontaneous angiogram-negative subarachnoid hemorrhage: a retrospective single center cohort study. Acta Neurochirurgica 1-12.
  29. Almandoz JD, Crandall BM, Fease JL, Scholz JM, Anderson RE, et al.  (2013) Diagnostic yield of catheter angiography in patients with subarachnoid hemorrhage and negative initial noninvasive neurovascular examinations. American Journal of Neuroradiology 34: 833-839.
  30. Westerlaan HE, Gravendeel J, Fiore D, Metzemaekers JDM, Groen RJM, et al. (2007) Multislice CT angiography in the selection of patients with ruptured intracranial aneurysms suitable for clipping or coiling. Neuroradiology 49: 997-1007.
  31. Rinkel GJ, Van Gijn J, Wijdicks EF (1993) Subarachnoid hemorrhage without detectable aneurysm. A review of the causes. Stroke 24: 1403-1409.
  32. Teksam M, McKinney A, Casey S, Asis M, Kieffer S, et al. (2004) Multi-section CT angiography for detection of cerebral aneurysms. American journal of neuroradiology 25: 1485-1492.
  33. Jafar JJ, Weiner HL (1993) Surgery for angiographically occult cerebral aneurysms. Journal of neurosurgery 79: 674-679.
  34. Gharib-Salehi M, Ali mohammadi E, Bagheri SR, Saeidi-Brojeni H, Abdi A, et al. (2017) Cerebral Angiographic Findings in Non-Traumatic Intracranial Hemorrhage: A Single Center Experience in the West of Iran. Iranian Journal of Neurosurgery 3: 95–102.