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Ruptured intracranial aneurysm in patients with osteogenesis imperfecta: 2 familial cases and a systematic review of the literature
Neurochirurgie 62 (2016) 317–320
Disponible en ligne sur
ScienceDirect www.sciencedirect.com
Original article
Ruptured intracranial aneurysm in patients with osteogenesis imperfecta: 2 familial cases and a systematic review of the literature T. Gaberel a,b,∗ , A. Rochey a , C. di Palma a,b , F. Lucas a , E. Touze b,c , E. Emery a,b a
Department of neurosurgery, university hospital of Caen, avenue de la Côte-de-Nacre, 14000 Caen, France Inserm, Inserm U919, serine protease and pathophysiology of the neurovascular unit, SP2U, UMR CNRS 6232, centre d’imagerie et de neurosciences appliquées aux pathologies, GIP Cyceron, university of Caen Lower Normandy, boulevard Henri-Becquerel, 14000 Caen, France c Department of neurology, university hospital of Caen, avenue de la Côte-de-Nacre, 14000 Caen, France b
a r t i c l e
i n f o
Article history: Received 4 May 2016 Received in revised form 6 June 2016 Accepted 3 July 2016 Available online 26 October 2016 Keywords: Microsurgery Endovascular procedure Osteogenesis imperfecta Intracranial aneurysm Subarachnoid hemorrhage
a b s t r a c t Objective. – Osteogenesis imperfecta is an inherited connective tissue disorder that causes bone fragility. Vascular complications have been described, but only few cases of ruptured intracranial aneurysm have been reported. Materials and methods. – We first described 2 familial cases of ruptured intracranial aneurysm and then conducted a systematic review of the literature. Results. – A mother and her daughter with a typical history of osteogenesis imperfecta presented with subarachnoid hemorrhage, which was related to a posterior communicating artery aneurysm in both cases. The mother had early rebleeding and died. The aneurysm was excluded by coiling in the daughter. Despite occurrence of hydrocephalus and delayed cerebral ischemia, she had an excellent functional outcome. A systematic review of the literature identified seven additional cases. None of the cases were in fact familial. All patients had a previous medical history of multiple fractures. Seven aneurysms were resolved, three by surgical clipping and four by endovascular procedure. No periprocedural complication was reported. One patient died prematurely and 6 experienced good functional outcome. Conclusions. – We report the first familial cases of aneurysmal subarachnoid hemorrhage in osteogenesis imperfecta patients. Intracranial aneurysms are probably linked to a collagen pathology, which is at the origin of osteogenesis imperfecta. In cases of aneurysmal subarachnoid hemorrhage in an osteogenesis imperfecta family, intracranial aneurysm screenings in the relatives showing osteogenesis imperfecta should be considered. © 2016 Elsevier Masson SAS. All rights reserved.
1. Introduction Osteogenesis imperfecta (OI) is a phenotypically and molecularly heterogeneous group of inherited connective tissue disorders that share similar skeletal abnormalities causing bone fragility and deformity [1]. These skeletal abnormalities can be variably associated with the following manifestations: hearing loss, blue sclerae, dentinogenesis imperfecta, and hyperlaxity of ligaments and skin. Several genetic abnormalities could be involved in OI, but they are all related to collagen pathophysiology [1]. Like most of the collagen-related diseases, vascular complications have been described, such as aortic and cervical artery dissection, carotid cavernous fistula, ulnar and coronary artery aneurysms [1–3]. The
∗ Corresponding author. Service de neurochirurgie, CHU de Caen, avenue de la Côte-de-Nacre, 14000 Caen, France. E-mail address: [email protected] (T. Gaberel). http://dx.doi.org/10.1016/j.neuchi.2016.07.004 0028-3770/© 2016 Elsevier Masson SAS. All rights reserved.
cerebrovascular system could also be involved in OI [4], but less frequently, and only few cases of ruptured intracranial aneurysm (IA) have been reported in the literature [5]. In this study we report 2 familial cases of ruptured IA associated with OI, which to our knowledge has never been previously described, and also present a systematic review of the literature. 2. Materials and methods 2.1. Cases report A 50-year-old woman presented in our department with a ruptured IA and suffering from OI (Case 1). Her family history revealed that her mother had previously experienced a subarachnoid hemorrhage (SAH) at 50 (Case 2). We retrospectively collected the medical history of her mother and obtained written informed consent from the patient for publication of this case report and any accompanying images.
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2.2. Systematic review of the literature 2.2.1. Study selection and data collection Relevant studies were identified based on a systematic PubMed search of the scientific literature for all reported case of aneurysmal SAH in patients with OI. OI and aneurysmal SAH in the studies included had to be defined according to the World Health Organization criteria. However, studies that gave no explicit definition were also included. All studies reporting aneurysmal SAH in OI patients were included. The search was not restricted to Englishlanguage articles and included all articles published up to October 2015. The search strategy used both key words and MeSH term searches for cerebral aneurysm, subarachnoid hemorrhage, osteogenesis imperfecta, which were combined with the appropriate Boolean connectors. To identify additional studies, we used the “related citations in PubMed” link of retrieved articles and screened reference lists of retrieved articles. Two reviewers (T.G. and C.d.P.) independently assessed the studies to determine eligibility and independently carried out data extraction using a standardized form. Any discrepancy was resolved by consensus. 2.2.2. Baseline characteristics and outcome measures For each case, the data collected were: sex, age, already diagnosed OI, signs of OI, World Federation of Neurosurgery (WFNS) score, Fisher grade on initial computed tomography (CT) scan, aneurysm location and type, aneurysm exclusion modalities, hydrocephalus requiring shunting, delayed cerebral ischemia, functional outcome at end of follow-up. 3. Results 3.1. Case reports 3.1.1. Case no. 1 A 50-year-old woman was admitted to our hospital for a sudden-onset headache with loss of consciousness. Her medical history revealed chronic high blood pressure (HBP), but she never smoked. Moreover, she had an obvious history of OI: several fractures related to minor trauma, blue sclera, bilateral hearing loss and a splenectomy related to a splenic artery aneurysm. In fact, her mother exhibited the same OI signs, and died from a ruptured IA (Case 2, Fig. 1A). She was an only child, and had one daughter who did not exhibit any signs of OI. Neurological examination evidenced a left hemiparesis with a Glasgow coma scale (GCS) of 12 on admission, which declined to 3 during the
CT-scan. She was then intubated and sedated. We considered that her WFNS score was V. CT-scan revealed a typical SAH, with a small amount of blood within the fourth ventricle, corresponding to a Fisher grade IV (Fig. 1B), with an acute hydrocephalus. An external ventricular drainage (EVD) was inserted. Angiography performed subsequently showed a saccular posterior communicating (PCom) artery aneurysm, which we considered responsible for the hemorrhage (Fig. 1C). This aneurysm was excluded in emergency by simple coiling (Fig. 1D). We also identified a left middle cerebral artery (MCA) aneurysm, which was located away from the hemorrhage. We considered it unruptured, and decided to treat it few months later. The patient was admitted to the intensive care unit, where the sedation was stopped, allowing to obtained a normal level of consciousness three days after admission. Six days later, the patient showed a decrease in consciousness, related to an arterial vasospasm in the right MCA territory. Despite general and local treatment of this vasospasm, including repeated in situ milrinone infusion, a new CT-scan revealed a delayed cerebral ischemia in the right MCA territory (Fig. 1G). Moreover, ablation of the EVD was not possible, so a ventriculo-peritoneal shunt was inserted (Fig. 1G). Fortunately, the neurological evolution was favorable, and she had a normal neurological and psychological examination at discharge. Three months later the left unruptured MCA aneurysm was excluded by clipping without any complication (Fig. 1F). 3.1.2. Case no. 2 In 1980, a 50-year-old woman was admitted to our hospital for a sudden-onset headache, nausea and loss of consciousness. She had typical signs of OI, with several fractures, blue sclera, hearing loss and arterial hypertension. Except for her daughter, no other relative exhibited any signs of OI. She had chronic HBP, but she never smoked. Neurological examination revealed left hemiparesis and loss of consciousness. The GCS score was not reported, but the WFNS score was probably more than III. Lumbar puncture was hemorrhagic, confirming the diagnosis of SAH. Cerebral arteriography revealed a right PCom artery saccular aneurysm (Fig. 1A). Unfortunately, she showed a rapid neurological deterioration, leading to death. 3.2. Systematic literature review Of the 17 articles screened, 10 were considered in-depth for inclusion, but 3 were excluded as they did not meet inclusion criteria [6–8]. Seven reported cases met all inclusion criteria and had
Fig. 1. Radiographic findings of the 2 cases described. A. Angiography of the right carotid artery performed in Case 2 for which SAH was confirmed by lumbar puncture, showing a PCom artery aneurysm. B. CT-Scan performed in Case 1, where the patient was admitted for headaches and decrease level of consciousness, showing a Fisher III grade SAH. C and D. Right carotid angiography performed in Case 1, revealing a PCom artery aneurysm (C), which was successfully excluded in emergency by coil embolization (D). E and F. An unruptured left MCA aneurysm was also diagnosed (E), and was successfully excluded by surgical clipping four months after its discovery (F). G. Final CT-scan performed in Case 1, showing ischemia relative to DCI in the right temporal lobe, and the presence of a shunt catheter inserted because of chronic hydrocephalus.
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Table 1 Literature review of 9 cases of aneurysmal SAH associated with osteogenesis imperfecta. Sex, age (years)
Already diagnosed OI Associated signs of OI
WFNS score
Fisher grade
Aneurysm location and type
Treatment modalities
Hydrocephalus requiring shunting
Delayed cerebral ischemia
Functional outcome
Okamura et al., 1995 [9]
F, 33
No NA
NA
ACom artery, Saccular
Surgical clipping
No
No
Good
Narvaez et al., 1996 [10]
F, 22
I
ACom artery, Saccular
Surgical clipping
No
No
Good
Havlik et al., 2006 [11] Petruzzel1is et al., 2007 [12]
M, 38
NA
NA
NA
Death
Endovascular: coiling
No
No
Good
M, 49
IV
Unclear, probably II or III III
ACom artery, saccular Basilar artery, Saccular
Matouk et al., 2011 [3]
Yes Fractures, blue sclera, short stature Yes Fractures, blue sclera No Fractures, hearing loss, DI Yes Fractures, short stature, hearing loss
Unclear, probably II or III Unclear, probably II or III NA
No
Good
M, 53
IV
IV
Yes
Yes
Hirohata et al., 2014 [5] Present study Case 1
F, 37
No Deformed long bones, blue sclera No Fractures
Endovascular: parent vessel sacrifice using coiling Endovascular: stent + coils
No
Kaliaperumal et al., 2011 [13]
Superior cerebellar artery, dissecting-type Vertebral artery, fusiform
II
III
MCA, Saccular
Surgical clipping
No
No
Severe disability (GOS = 3/5) Good
Yes Fractures, hearing loss, blue sclera Yes Fractures, hearing loss, blue sclera
V
IV
Pcom artery, saccular
Endovascular: coiling
Yes
Yes
Good
≥ III
NA
Pcom artery, saccular
NA
NA
Yes
Death
Case 2
M, 44
F, 50
F, 50
NA III
NA: non applicable; OI: osteogenesis imperfecta; WFNS: world federation of neurosurgery; F: female; M: male; ACom artery: anterior communicating artery; MCA: middle cerebral artery; PCom artery: posterior communicating artery; GOS: Glasgow outcome scale; DI: dentinogenesis imperfecta.
sufficient available data [3,5,9–13]. We also associated our 2 cases to these seven cases. One article was in Japanese [9], so we were able to extract data only on the basis of the abstract. Characteristics of the 9 patients reported are summarized in Table 1. Mean age was 41.7 years. In 5 patients, OI was known before the occurrence of SAH. All patients had a previous history of multiple fractures. Mean WFNS, available in 6 patients, was 3.2, and mean Fisher score, available in 4, was 3.5. Six aneurysms were located on the anterior and three in the posterior circulation. Seven aneurysms were saccular, two were fusiform. Seven aneurysms were excluded, three by surgical clipping, four by endovascular mean. No procedural complication was reported. Two patients died prematurely, one under unclear conditions, associating SAH and post-neurosurgical meningitis [11]. The other reported case concerned a patient who was admitted to our institution 30 years previously, at a time when exclusion of ruptured aneurysm was not performed in emergency. Death probably occurred due to rebleeding. Concerning the seven other cases, two patients experienced DCI, and two required permanent CSF shunting. Finally, 6/7 patients experienced good functional outcome, whereas only one was disabled, with a Glasgow Outcome Scale of 3. 4. Discussion To our knowledge, our 2 cases are the first familial cases of aneurysmal SAH in a patient with OI. It raises the question of the link between OI and intracranial aneurysm. In Case 1, in the daughter who exhibited typical signs of OI, there was clearly an associated vascular pathology, as she previously had one ruptured aneurysm on the splenic artery, and had 2 intracranial aneurysms. It is also interesting to note that in Case 2 the mother, who exhibited the same OI signs, had a PCom aneurysm similar to her daughter. However, it is always difficult to determine whether ruptured IAs are truly caused by OI or accidentally occur in OI patients, but three points may suggest a link between OI and IA/IA rupture:
• seven other patients have previously been described in the literature (Table 1); • vascular manifestations are classic manifestations of OI, particularly at the level of the heart and aorta [2]. However, other arteries can be involved, like intra-abdominal artery like in our Case 1, a phenomenon reported in the literature [3]. Intracranial artery pathology other than IA have also reported, mainly dissection [3,4,7,8]. OI is a collagen-related disease, and it is known that formation and rupture of IA is linked to collagen abnormalities. OI is now more fully understood as a predominantly collagenrelated disorder, with about 85–90% of cases caused by structural or quantitative mutations in the collagen genes themselves [1]. The classical mutations are mutations in COL1A1 and COL1A2, coding for the ␣1(I) and ␣2(I) chains of type I collagen [1]. Or the variant of COL1A2 is a genetic risk factor for IA patients with family history [14]. Moreover, rupture of IA is linked to collagen abnormalities in the aneurysm wall [15]. In addition to the potential link between OI and aneurysmal rupture, our two observations and systematic review of the literature permitted us to discuss the management of these patients. First, we note that the ruptured aneurysms in OI patients were excluded by clipping or by coiling. Due to bone fragility in OI, safety of cranial surgery could be considered. However, none of the reported cases treated by clipping had any complication due to bone fragility. In contrast, because of an increased risk of arterial dissection, we could hypothesize a higher procedural risk of endovascular coiling. Also, the complication did not occur in any of the reported cases. Therefore, it seems that both treatments could be used, which was also suggested by Case 1, which received both treatments for the two aneurysms, without any complication. It is important to note that this statement should not be considered a recommendation because of the very limited number of cases. It is noteworthy that Case 1 required the insertion of a ventriculo-peritoneal shunt. We feared a possible bony complication for this type of surgery, but that
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did not occur as in the case reported by Kaliaperumal et al. [13]. Lastly, the question of the aneurysmal screening in OI should be considered. IA in the OI patient remained rare, and we cannot propose that systematic screening is justified. However, in the event of a familial case of aneurysmal SAH in an OI family, we believe that a familial screening in the relative exhibiting OI signs have to be considered as in cases of genetic diseases associated with IA like autosomal dominant polycystic kidney disease [16]. 5. Conclusion We report the first familial cases of aneurysmal SAH in OI patients. IA is probably linked to the collagen pathology, which is at the origin of OI. In cases of aneurysmal SAH in an OI family, IA screenings for relatives with OI should be considered. Authors contribution T.G., A.R. and F.L. collected the clinical data. T.G. and C.d.P. performed the systematic review. T.G. and A.R. wrote the manuscript. E.T. and E.E. corrected the manuscript. Disclosure of interest The authors declare that they have no competing interest. Acknowledgements T.G. received funding from Zeiss and the French Society of Neurosurgery. References [1] Forlino A, Marini JC. Osteogenesis imperfecta. Lancet 2016;387(10028): 1657–71.
[2] Radunovic Z, Wekre LL, Diep LM, Steine K. Cardiovascular abnormalities in adults with osteogenesis imperfecta. Am Heart J 2011;161(3):523–9. [3] Matouk CC, Hanbidge A, Mandell DM, Terbrugge KG, Agid R. Osteogenesis imperfecta, multiple intra-abdominal arterial dissections and a ruptured dissecting-type intracranial aneurysm. Interv Neuroradiol 2011;17(3):371–5. [4] Albayram S, Kizilkilic O, Yilmaz H, Tuysuz B, Kocer N, Islak C. Abnormalities in the cerebral arterial system in osteogenesis imperfecta. AJNR Am J Neuroradiol 2003;24(4):748–50. [5] Hirohata T, Miyawaki S, Mizutani A, Iwakami T, Yamada S, Nishido H, et al. Subarachnoid hemorrhage secondary to a ruptured middle cerebral aneurysm in a patient with osteogenesis imperfecta: a case report. BMC Neurol 2014;14:150. [6] Fox A, Symons S, Aviv R. Cerebral aneurysms in a patient with osteogenesis imperfecta and exon 28 polymorphism of COL1A2. AJNR Am J Neuroradiol 2007;28(10):1840. [7] Coutouly X, Bibi R, Magni C. [Isolated basilar artery dissection in a case of osteogenesis imperfecta]. J Radiol 2005;86(1):86–8. [8] Gilbert GJ. Spontaneous dissections. Neurology 1997;48(5):1475. [9] Okamura T, Yamamoto M, Ohta K, Matsuoka T, Takahashi M, Uozumi T. [A case of ruptured cerebral aneurysm associated with fenestrated vertebral artery in osteogenesis imperfecta]. No Shinkei Geka 1995;23(5):451–5. [10] Narváez J, Narváez JA, Majós C, Clavaguera MT, Alegre-Sancho JJ. Subarachnoid haemorrhage secondary to ruptured cerebral aneurysm in a patient with osteogenesis imperfecta. Br J Rheumatol 1996;35(12):1332–3. [11] Havlik DM, Nashelsky MB. Ruptured cerebral artery aneurysm and bacterial meningitis in a man with osteogenesis imperfecta. Am J Forensic Med Pathol 2006;27(2):117–20. [12] Petruzzellis M, De Blasi R, Lucivero V, Sancilio M, Prontera M, Tinelli A, et al. Cerebral aneurysms in a patient with osteogenesis imperfecta and exon 28 polymorphism of COL1A2. AJNR Am J Neuroradiol 2007;28(3):397–8. [13] Kaliaperumal C, Walsh T, Balasubramanian C, Wyse G, Fanning N, Kaar G. Osteogenesis imperfecta presenting as aneurysmal subarachnoid haemorrhage in a 53-year-old man. BMJ Case Rep 2011:2011, http://dx.doi.org/10.1136/bcr.10.2011.4910 [pii: bcr1020114910]. [14] Yoneyama T, Kasuya H, Onda H, Akagawa H, Hashiguchi K, Nakajima T, et al. Collagen type I alpha2 (COL1A2) is the susceptible gene for intracranial aneurysms. Stroke 2004;35(2):443–8. [15] Kataoka K, Taneda M, Asai T, Kinoshita A, Ito M, Kuroda R. Structural fragility and inflammatory response of ruptured cerebral aneurysms. A comparative study between ruptured and unruptured cerebral aneurysms. Stroke 1999;30(7):1396–401. [16] Thompson BG, Brown Jr RD, Amin-Hanjani S, Broderick JP, Cockroft KM, Connolly Jr ES, et al. Guidelines for the management of patients with unruptured intracranial aneurysms: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 2015;46(8):2368–400.
Disponible en ligne sur
ScienceDirect www.sciencedirect.com
Original article
Ruptured intracranial aneurysm in patients with osteogenesis imperfecta: 2 familial cases and a systematic review of the literature T. Gaberel a,b,∗ , A. Rochey a , C. di Palma a,b , F. Lucas a , E. Touze b,c , E. Emery a,b a
Department of neurosurgery, university hospital of Caen, avenue de la Côte-de-Nacre, 14000 Caen, France Inserm, Inserm U919, serine protease and pathophysiology of the neurovascular unit, SP2U, UMR CNRS 6232, centre d’imagerie et de neurosciences appliquées aux pathologies, GIP Cyceron, university of Caen Lower Normandy, boulevard Henri-Becquerel, 14000 Caen, France c Department of neurology, university hospital of Caen, avenue de la Côte-de-Nacre, 14000 Caen, France b
a r t i c l e
i n f o
Article history: Received 4 May 2016 Received in revised form 6 June 2016 Accepted 3 July 2016 Available online 26 October 2016 Keywords: Microsurgery Endovascular procedure Osteogenesis imperfecta Intracranial aneurysm Subarachnoid hemorrhage
a b s t r a c t Objective. – Osteogenesis imperfecta is an inherited connective tissue disorder that causes bone fragility. Vascular complications have been described, but only few cases of ruptured intracranial aneurysm have been reported. Materials and methods. – We first described 2 familial cases of ruptured intracranial aneurysm and then conducted a systematic review of the literature. Results. – A mother and her daughter with a typical history of osteogenesis imperfecta presented with subarachnoid hemorrhage, which was related to a posterior communicating artery aneurysm in both cases. The mother had early rebleeding and died. The aneurysm was excluded by coiling in the daughter. Despite occurrence of hydrocephalus and delayed cerebral ischemia, she had an excellent functional outcome. A systematic review of the literature identified seven additional cases. None of the cases were in fact familial. All patients had a previous medical history of multiple fractures. Seven aneurysms were resolved, three by surgical clipping and four by endovascular procedure. No periprocedural complication was reported. One patient died prematurely and 6 experienced good functional outcome. Conclusions. – We report the first familial cases of aneurysmal subarachnoid hemorrhage in osteogenesis imperfecta patients. Intracranial aneurysms are probably linked to a collagen pathology, which is at the origin of osteogenesis imperfecta. In cases of aneurysmal subarachnoid hemorrhage in an osteogenesis imperfecta family, intracranial aneurysm screenings in the relatives showing osteogenesis imperfecta should be considered. © 2016 Elsevier Masson SAS. All rights reserved.
1. Introduction Osteogenesis imperfecta (OI) is a phenotypically and molecularly heterogeneous group of inherited connective tissue disorders that share similar skeletal abnormalities causing bone fragility and deformity [1]. These skeletal abnormalities can be variably associated with the following manifestations: hearing loss, blue sclerae, dentinogenesis imperfecta, and hyperlaxity of ligaments and skin. Several genetic abnormalities could be involved in OI, but they are all related to collagen pathophysiology [1]. Like most of the collagen-related diseases, vascular complications have been described, such as aortic and cervical artery dissection, carotid cavernous fistula, ulnar and coronary artery aneurysms [1–3]. The
∗ Corresponding author. Service de neurochirurgie, CHU de Caen, avenue de la Côte-de-Nacre, 14000 Caen, France. E-mail address: [email protected] (T. Gaberel). http://dx.doi.org/10.1016/j.neuchi.2016.07.004 0028-3770/© 2016 Elsevier Masson SAS. All rights reserved.
cerebrovascular system could also be involved in OI [4], but less frequently, and only few cases of ruptured intracranial aneurysm (IA) have been reported in the literature [5]. In this study we report 2 familial cases of ruptured IA associated with OI, which to our knowledge has never been previously described, and also present a systematic review of the literature. 2. Materials and methods 2.1. Cases report A 50-year-old woman presented in our department with a ruptured IA and suffering from OI (Case 1). Her family history revealed that her mother had previously experienced a subarachnoid hemorrhage (SAH) at 50 (Case 2). We retrospectively collected the medical history of her mother and obtained written informed consent from the patient for publication of this case report and any accompanying images.
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2.2. Systematic review of the literature 2.2.1. Study selection and data collection Relevant studies were identified based on a systematic PubMed search of the scientific literature for all reported case of aneurysmal SAH in patients with OI. OI and aneurysmal SAH in the studies included had to be defined according to the World Health Organization criteria. However, studies that gave no explicit definition were also included. All studies reporting aneurysmal SAH in OI patients were included. The search was not restricted to Englishlanguage articles and included all articles published up to October 2015. The search strategy used both key words and MeSH term searches for cerebral aneurysm, subarachnoid hemorrhage, osteogenesis imperfecta, which were combined with the appropriate Boolean connectors. To identify additional studies, we used the “related citations in PubMed” link of retrieved articles and screened reference lists of retrieved articles. Two reviewers (T.G. and C.d.P.) independently assessed the studies to determine eligibility and independently carried out data extraction using a standardized form. Any discrepancy was resolved by consensus. 2.2.2. Baseline characteristics and outcome measures For each case, the data collected were: sex, age, already diagnosed OI, signs of OI, World Federation of Neurosurgery (WFNS) score, Fisher grade on initial computed tomography (CT) scan, aneurysm location and type, aneurysm exclusion modalities, hydrocephalus requiring shunting, delayed cerebral ischemia, functional outcome at end of follow-up. 3. Results 3.1. Case reports 3.1.1. Case no. 1 A 50-year-old woman was admitted to our hospital for a sudden-onset headache with loss of consciousness. Her medical history revealed chronic high blood pressure (HBP), but she never smoked. Moreover, she had an obvious history of OI: several fractures related to minor trauma, blue sclera, bilateral hearing loss and a splenectomy related to a splenic artery aneurysm. In fact, her mother exhibited the same OI signs, and died from a ruptured IA (Case 2, Fig. 1A). She was an only child, and had one daughter who did not exhibit any signs of OI. Neurological examination evidenced a left hemiparesis with a Glasgow coma scale (GCS) of 12 on admission, which declined to 3 during the
CT-scan. She was then intubated and sedated. We considered that her WFNS score was V. CT-scan revealed a typical SAH, with a small amount of blood within the fourth ventricle, corresponding to a Fisher grade IV (Fig. 1B), with an acute hydrocephalus. An external ventricular drainage (EVD) was inserted. Angiography performed subsequently showed a saccular posterior communicating (PCom) artery aneurysm, which we considered responsible for the hemorrhage (Fig. 1C). This aneurysm was excluded in emergency by simple coiling (Fig. 1D). We also identified a left middle cerebral artery (MCA) aneurysm, which was located away from the hemorrhage. We considered it unruptured, and decided to treat it few months later. The patient was admitted to the intensive care unit, where the sedation was stopped, allowing to obtained a normal level of consciousness three days after admission. Six days later, the patient showed a decrease in consciousness, related to an arterial vasospasm in the right MCA territory. Despite general and local treatment of this vasospasm, including repeated in situ milrinone infusion, a new CT-scan revealed a delayed cerebral ischemia in the right MCA territory (Fig. 1G). Moreover, ablation of the EVD was not possible, so a ventriculo-peritoneal shunt was inserted (Fig. 1G). Fortunately, the neurological evolution was favorable, and she had a normal neurological and psychological examination at discharge. Three months later the left unruptured MCA aneurysm was excluded by clipping without any complication (Fig. 1F). 3.1.2. Case no. 2 In 1980, a 50-year-old woman was admitted to our hospital for a sudden-onset headache, nausea and loss of consciousness. She had typical signs of OI, with several fractures, blue sclera, hearing loss and arterial hypertension. Except for her daughter, no other relative exhibited any signs of OI. She had chronic HBP, but she never smoked. Neurological examination revealed left hemiparesis and loss of consciousness. The GCS score was not reported, but the WFNS score was probably more than III. Lumbar puncture was hemorrhagic, confirming the diagnosis of SAH. Cerebral arteriography revealed a right PCom artery saccular aneurysm (Fig. 1A). Unfortunately, she showed a rapid neurological deterioration, leading to death. 3.2. Systematic literature review Of the 17 articles screened, 10 were considered in-depth for inclusion, but 3 were excluded as they did not meet inclusion criteria [6–8]. Seven reported cases met all inclusion criteria and had
Fig. 1. Radiographic findings of the 2 cases described. A. Angiography of the right carotid artery performed in Case 2 for which SAH was confirmed by lumbar puncture, showing a PCom artery aneurysm. B. CT-Scan performed in Case 1, where the patient was admitted for headaches and decrease level of consciousness, showing a Fisher III grade SAH. C and D. Right carotid angiography performed in Case 1, revealing a PCom artery aneurysm (C), which was successfully excluded in emergency by coil embolization (D). E and F. An unruptured left MCA aneurysm was also diagnosed (E), and was successfully excluded by surgical clipping four months after its discovery (F). G. Final CT-scan performed in Case 1, showing ischemia relative to DCI in the right temporal lobe, and the presence of a shunt catheter inserted because of chronic hydrocephalus.
T. Gaberel et al. / Neurochirurgie 62 (2016) 317–320
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Table 1 Literature review of 9 cases of aneurysmal SAH associated with osteogenesis imperfecta. Sex, age (years)
Already diagnosed OI Associated signs of OI
WFNS score
Fisher grade
Aneurysm location and type
Treatment modalities
Hydrocephalus requiring shunting
Delayed cerebral ischemia
Functional outcome
Okamura et al., 1995 [9]
F, 33
No NA
NA
ACom artery, Saccular
Surgical clipping
No
No
Good
Narvaez et al., 1996 [10]
F, 22
I
ACom artery, Saccular
Surgical clipping
No
No
Good
Havlik et al., 2006 [11] Petruzzel1is et al., 2007 [12]
M, 38
NA
NA
NA
Death
Endovascular: coiling
No
No
Good
M, 49
IV
Unclear, probably II or III III
ACom artery, saccular Basilar artery, Saccular
Matouk et al., 2011 [3]
Yes Fractures, blue sclera, short stature Yes Fractures, blue sclera No Fractures, hearing loss, DI Yes Fractures, short stature, hearing loss
Unclear, probably II or III Unclear, probably II or III NA
No
Good
M, 53
IV
IV
Yes
Yes
Hirohata et al., 2014 [5] Present study Case 1
F, 37
No Deformed long bones, blue sclera No Fractures
Endovascular: parent vessel sacrifice using coiling Endovascular: stent + coils
No
Kaliaperumal et al., 2011 [13]
Superior cerebellar artery, dissecting-type Vertebral artery, fusiform
II
III
MCA, Saccular
Surgical clipping
No
No
Severe disability (GOS = 3/5) Good
Yes Fractures, hearing loss, blue sclera Yes Fractures, hearing loss, blue sclera
V
IV
Pcom artery, saccular
Endovascular: coiling
Yes
Yes
Good
≥ III
NA
Pcom artery, saccular
NA
NA
Yes
Death
Case 2
M, 44
F, 50
F, 50
NA III
NA: non applicable; OI: osteogenesis imperfecta; WFNS: world federation of neurosurgery; F: female; M: male; ACom artery: anterior communicating artery; MCA: middle cerebral artery; PCom artery: posterior communicating artery; GOS: Glasgow outcome scale; DI: dentinogenesis imperfecta.
sufficient available data [3,5,9–13]. We also associated our 2 cases to these seven cases. One article was in Japanese [9], so we were able to extract data only on the basis of the abstract. Characteristics of the 9 patients reported are summarized in Table 1. Mean age was 41.7 years. In 5 patients, OI was known before the occurrence of SAH. All patients had a previous history of multiple fractures. Mean WFNS, available in 6 patients, was 3.2, and mean Fisher score, available in 4, was 3.5. Six aneurysms were located on the anterior and three in the posterior circulation. Seven aneurysms were saccular, two were fusiform. Seven aneurysms were excluded, three by surgical clipping, four by endovascular mean. No procedural complication was reported. Two patients died prematurely, one under unclear conditions, associating SAH and post-neurosurgical meningitis [11]. The other reported case concerned a patient who was admitted to our institution 30 years previously, at a time when exclusion of ruptured aneurysm was not performed in emergency. Death probably occurred due to rebleeding. Concerning the seven other cases, two patients experienced DCI, and two required permanent CSF shunting. Finally, 6/7 patients experienced good functional outcome, whereas only one was disabled, with a Glasgow Outcome Scale of 3. 4. Discussion To our knowledge, our 2 cases are the first familial cases of aneurysmal SAH in a patient with OI. It raises the question of the link between OI and intracranial aneurysm. In Case 1, in the daughter who exhibited typical signs of OI, there was clearly an associated vascular pathology, as she previously had one ruptured aneurysm on the splenic artery, and had 2 intracranial aneurysms. It is also interesting to note that in Case 2 the mother, who exhibited the same OI signs, had a PCom aneurysm similar to her daughter. However, it is always difficult to determine whether ruptured IAs are truly caused by OI or accidentally occur in OI patients, but three points may suggest a link between OI and IA/IA rupture:
• seven other patients have previously been described in the literature (Table 1); • vascular manifestations are classic manifestations of OI, particularly at the level of the heart and aorta [2]. However, other arteries can be involved, like intra-abdominal artery like in our Case 1, a phenomenon reported in the literature [3]. Intracranial artery pathology other than IA have also reported, mainly dissection [3,4,7,8]. OI is a collagen-related disease, and it is known that formation and rupture of IA is linked to collagen abnormalities. OI is now more fully understood as a predominantly collagenrelated disorder, with about 85–90% of cases caused by structural or quantitative mutations in the collagen genes themselves [1]. The classical mutations are mutations in COL1A1 and COL1A2, coding for the ␣1(I) and ␣2(I) chains of type I collagen [1]. Or the variant of COL1A2 is a genetic risk factor for IA patients with family history [14]. Moreover, rupture of IA is linked to collagen abnormalities in the aneurysm wall [15]. In addition to the potential link between OI and aneurysmal rupture, our two observations and systematic review of the literature permitted us to discuss the management of these patients. First, we note that the ruptured aneurysms in OI patients were excluded by clipping or by coiling. Due to bone fragility in OI, safety of cranial surgery could be considered. However, none of the reported cases treated by clipping had any complication due to bone fragility. In contrast, because of an increased risk of arterial dissection, we could hypothesize a higher procedural risk of endovascular coiling. Also, the complication did not occur in any of the reported cases. Therefore, it seems that both treatments could be used, which was also suggested by Case 1, which received both treatments for the two aneurysms, without any complication. It is important to note that this statement should not be considered a recommendation because of the very limited number of cases. It is noteworthy that Case 1 required the insertion of a ventriculo-peritoneal shunt. We feared a possible bony complication for this type of surgery, but that
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did not occur as in the case reported by Kaliaperumal et al. [13]. Lastly, the question of the aneurysmal screening in OI should be considered. IA in the OI patient remained rare, and we cannot propose that systematic screening is justified. However, in the event of a familial case of aneurysmal SAH in an OI family, we believe that a familial screening in the relative exhibiting OI signs have to be considered as in cases of genetic diseases associated with IA like autosomal dominant polycystic kidney disease [16]. 5. Conclusion We report the first familial cases of aneurysmal SAH in OI patients. IA is probably linked to the collagen pathology, which is at the origin of OI. In cases of aneurysmal SAH in an OI family, IA screenings for relatives with OI should be considered. Authors contribution T.G., A.R. and F.L. collected the clinical data. T.G. and C.d.P. performed the systematic review. T.G. and A.R. wrote the manuscript. E.T. and E.E. corrected the manuscript. Disclosure of interest The authors declare that they have no competing interest. Acknowledgements T.G. received funding from Zeiss and the French Society of Neurosurgery. References [1] Forlino A, Marini JC. Osteogenesis imperfecta. Lancet 2016;387(10028): 1657–71.
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