Acta Neurochirurgica

, Volume 159, Issue 11, pp 2089–2097 | Cite as

Intracerebral hemorrhage as a manifestation of cerebral hyperperfusion syndrome after carotid revascularization: systematic review and meta-analysis

  • Pedro Abreu
  • Jerina Nogueira
  • Filipe Brogueira Rodrigues
  • Ana Nascimento
  • Mariana Carvalho
  • Ana Marreiros
  • Hipólito Nzwalo
Review Article - Vascular



Intracerebral hemorrhage (ICH) in the context of cerebral hyperperfusion syndrome (CHS) is an uncommon but potentially lethal complication after carotid revascularization for carotid occlusive disease. Information about its incidence, risk factors and fatality is scarce. Therefore, we aimed to perform a systematic review and meta-analysis focusing on the incidence, risk factors and outcomes of ICH in the context of CHS after carotid revascularization.


We searched the PubMed and EBSCO hosts for all studies published in English about CHS in the context of carotid revascularization. Two reviewers independently assessed each study for eligibility based on predefined criteria. Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines were followed, and the PROSPERO register was made (register no. CRD42016033190), including the pre-specified protocol.


Forty-one studies involving 28,956 participants were deemed eligible and included in our analysis. The overall quality of the included studies was fair. The pooled frequency of ICH in the context of CHS was 38% (95% CI: 26% to 51%, I2 = 84%, 24 studies), and the pooled case fatality of ICH after CHS was 51% (95% CI: 32% to 71%, I2 = 77%, 17 studies). When comparing carotid angioplasty with stenting (CAS) with carotid endarterectomy (CEA), post-procedural ICH in the context of CHS was less frequent in CEA. ICH following CHS occurred less often in large series and was rare in asymptomatic patients. The most common risk factors were periprocedural hypertension and ipsilateral severe stenosis.


ICH as a manifestation of CHS is rare, more frequent after CAS and associated with poor prognosis. Periprocedural control of hypertension can reduce its occurrence.


Cerebral hyperperfusion syndrome Intracerebral hemorrhage Carotid endarterectomy Carotid angioplasty Carotid revascularization 


Ischemic stroke is a major cause of morbidity and mortality worldwide [12, 33, 53]. Carotid artery disease contributes to 18–29% of all cases [59, 66]. Carotid invasive interventions such as carotid endarterectomy (CEA) and carotid angioplasty with stenting (CAS) are widely used to treat carotid artery disease [6, 26, 62]. One potentially severe complication is intracerebral hemorrhage (ICH) in the context of cerebral hyperperfusion syndrome (CHS) [37]. Clinical manifestations of CHS are diverse and include symptoms such as throbbing headaches, confusion, focal neurological deficits, partial or generalized seizures, among others [25, 27, 60]. Diagnostic examinations such computerized tomography scans (CT), magnetic resonance imaging (MRI), transcranial Doppler (TCD), single-photon emission computerized tomography (SPECT) and positron emission tomography (PET) can be used to confirm or exclude this diagnosis [3, 11, 24, 60]. The pathophysiology behind CHS is still poorly understood [41]. Three mechanisms have been associated with the syndrome: failure of brain vessels’ autoregulatory mechanisms to adapt to the sudden and deregulated increase in cerebral blood flow after carotid revascularization in long-standing hypoperfused brains due to severe stenosis/obstruction [2, 36, 48, 54, 60]; baroreflex disturbances secondary to carotid revascularization [58]; disturbances in the trigeminovascular reflex [35, 60]. Despite its severity, the knowledge about the frequency, risk factors and prognosis of ICH in the context of CHS is scarce. Previous reviews did not specifically address the occurrence of ICH in the context of CHS [32, 41]. Therefore, we performed a systematic review of the existent studies and meta-analytically estimated the frequency of ICH after CHS and its case fatality.

Materials and methods

Protocol and registration

This systematic review was registered at the PROSPERO database (CRD42016033190) and written in accordance with the PRISMA guidelines [31].

Eligibility criteria

Primary studies involving patients submitted to carotid revascularization (CAS or CEA) due to carotid occlusive disease were included. Studies with CEA/CAS performed for other specific conditions, case reports and animal studies, and studies in which the definition and frequency of ICH related CHS were not described were excluded.

Information sources

The search process was performed using the search engines PubMed and EBSCOHost (1986 to January 2016). Databases accessed via EBSCOhost include MEDLINE, sciencedirect, academic one file, J-stage, general one file, OAlster, expanded academic ASAP, China/Asia on demand, SciELO, Scitech conect, MedicLatina and Korean studies information study system. Only full-text English-written publications were included.

Search strategy and study selection

The Mesh terms “cerebral hyperperfusion syndrome,” “complications,” “carotid revascularization,” “endarterectomy” and “carotid angioplasty” were used to retrieve relevant literature. Studies were selected by two independent investigators. A consensus between the authors was used to resolve any disagreements about the inclusion of specific studies.

Data collection process

Studies were analyzed by two independent investigators. A consensus between the authors was used to resolve any disagreements about the inclusion of specific studies.

Data items

The following items were extracted: type of surgical procedure, frequency of CHS with ICH, associated risk factors and outcome (case fatality, morbidity rates).

Studies' risk of bias

The National Institutes of Health (NIH) tools were used [15] for quality assessment (supplement). Two reviewers performed the assessment independently. Discrepancies in the classifications were discussed and agreement achieved.

Planned methods of analysis

Qualitative analysis with quantitative description including all selected studies was performed whenever applicable. To address the risk factors, and for the meta-analysis of frequency and case fatality of ICH after CHS, only large studies (≥ 100 patients) were considered. This arbitrary threshold was selected to minimize the effects of substantial variability in the diagnostic criteria, time of evaluation and populations included in our study. We used Stata/SE 14.0 software for conducting the analysis and to derive forest plots. Random-effects meta-analysis weighted by the inverse-variance method was performed to estimate pooled frequency and 95% confidence intervals (CI). Heterogeneity was assessed with the I2 test. We used a random-effects model as substantial heterogeneity between studies results was expected. The limit for statistical significance was established at 0.05.


Study selection

The initial search yielded a total of 545 manuscripts (423 publications at EBSCOhost and 122 publications at PubMed) (Fig. 1). After extraction removal of duplicates and studies not fulfilling our eligibility criteria, 41 studies were included in the final analysis (Fig. 1). Reasons for study exclusions are documented in supplement 1.
Fig. 1

Flowchart of the article inclusion process in the systematic review

Study characteristics

A total of 28,956 participants were included, with study sample sizes ranging from 26 to 4494 participants (Table 1). Eighteen studies (44%) defined both CHS and ICH in the Methods section [1, 2, 7, 8, 9, 16, 19, 20, 22, 24, 29, 34, 42, 44, 46, 47, 61, 65]. The frequency of ICH after carotid intervention in studies with fewer than 100 participants ranged from 0% to 4.44% [4, 8, 14, 17, 18, 21, 22, 24, 40, 46, 48, 64]. In studies with 101 to 1000 participants, the range was from 0% to 2.21% [1, 2, 5, 7, 9, 10, 13, 19, 20, 23, 29, 30, 34, 39, 42, 43, 51, 55, 57, 65]. In studies that included 1001 or more participants, a range from 0.09% to 0.6% was found [16, 44, 45, 47, 49, 50, 52, 61, 63]. With regard to the quality evaluation, the majority were rated as “good” [1, 2, 5, 7, 8, 18, 22, 29, 30, 34, 50, 65] or fair [4, 9, 10, 13, 16, 17, 19, 20, 21, 23, 24, 39, 40, 42, 43, 44, 45, 46, 47, 48, 49, 51, 55, 56, 57, 63, 64], and three were “poor” [14, 52, 61]. The risk of bias was considerable in most studies (Supplement 2) [4, 9, 10, 13, 16, 17, 19, 20, 21, 23, 24, 39, 42, 43, 44, 45, 47, 49, 55, 64]. The pooled frequency of ICH in the context of CHS was 38% (95% CI: 26% to 51%, I2 = 84%) (Fig. 2).
Table 1

Frequency and case fatality of intracerebral hemorrhage in large and small studies in the context of hyperperfusion syndrome

Line with large studies (≥100 patients) in gray: ABREVIATIONS: NA-Not applicable; NS-Not specified; ICH-Intracerebral; CEA-carotid endarterectomy; CAS-carotid angioplasty with stenting

Fig. 2

Forest plot showing the frequency of intracerebral hemorrhage in the context of cerebral hyperperfusion syndrome in studies including at least 100 patients (point estimates and 95% CIs are shown along with pooled estimates)

Risk factors

Table 2 summarizes the risk factors found in larger studies (≥ 100 patients). Table 1 shows that when comparing CEA and CAS, the frequency of ICH in the context of CHS in large studies was higher after CAS, ranging from 0.28% to 4.05% [1, 7, 9, 19, 30, 39, 42, 47, 49, 55, 57, 65]. In CEA, it varied from 0% to 2.15% [2, 5, 9, 10, 13, 16, 18, 20, 23, 29, 34, 43, 44, 45, 47, 61]. Also, 73% of the studies involving CAS had a frequency of ICH in the context of CHS above 0.5% [1, 7, 9, 19, 30, 39, 42, 47, 49, 55, 57, 65]. In CEA, these frequencies occurred in only 26% of the cases [2, 5, 9, 10, 13, 16, 18, 20, 23, 29, 34, 43, 44, 45, 47, 61]. The “ICH to CHS proportion” was higher after CAS in comparison to CES: 7 out of 11 CAS studies (63.6%) had 50% or more hemorrhagic CHS (range 0–100%) [2, 5, 9, 10, 13, 16, 18, 20, 23, 29, 34, 43, 44, 45, 47, 61]. In CEA, 5 out of 12 studies (41.6%) had 50% or more cases of hemorrhagic CHS (range 0–80%) [2, 5, 9, 10, 13, 16, 18, 20, 23, 29, 34, 43, 44, 45, 47, 61]. Post-procedure ICH in asymptomatic patients was addressed in nine large studies [1, 7, 10, 13, 47, 49, 55, 57, 61] and occurred in three [47, 57, 61]. Overall, periprocedural hypertension is the most frequent risk factor, being documented in four studies [16, 20, 47, 50]. Three studies mention severe ipsilateral stenosis as a risk factor [50, 51, 63]. Younger age was considered a risk factor in two studies but denied as a risk factor in another two studies [16, 47, 51, 63].
Table 2

Risk factors for ICH in the context of CHS


Risk factor









Periprocedural hypertension


OR = 4.5




Ipsilateral severe stenosis






Younger age





Contralateral occlusion/high stenosis



Periprocedural anticoagulation


OR = 7.3


Postoperative headache


Neuro-imaging findings

Yes, cerebral circulation time variation pre- to post-procedure (ΔCCT) greater than 2.7 s

Yes, silence brain lesions

Posoperative antiplatelets

No (without supporting statistical data)

OR, Odds ratio


The mortality from ICH related to CHS ranged from 0% to 100% [1, 8, 9, 16, 20, 21, 23, 30, 39, 40, 42, 45, 47, 49, 51, 55, 57, 61, 63, 64, 65]. In large studies the mortality was ≥ 50% in more than half of the studies (range 0 to 100%) [1, 10, 17, 21, 24, 31, 39, 42, 45, 47, 49, 51, 55, 57, 61, 63, 65]. The pooled case fatality of ICH after CHS was 51% (95% CI: 32% to 71%, I2 = 77%) (Fig. 3).
Fig. 3

Forest plot showing the case-fatality rates from intracerebral hemorrhage in the context of cerebral hyperperfusion syndrome in studies including at least 100 patients (point estimates and 95% CIs are shown along with pooled estimates)


This is the first systematic review and meta-analysis addressing the frequency, risk factors and outcome of ICH in the context of CHS. Despite being discussed since 1981 [54], no consensual definition exists for CHS, and its pathophysiology is still to be elucidated [28, 60]. We found a high variation in the frequency of ICH in the context of CHS, with a range of 0% to 4.44% [1, 2, 4, 5, 7, 8, 9, 10, 13, 14, 16, 17, 18, 19, 20, 21, 22, 23, 24, 29, 30, 34, 39, 40, 42, 43, 44, 45, 46, 47, 48, 49, 50, 51, 52, 55, 57, 61, 63, 64, 65]. The overall case fatality associated with ICH in the context of CHS was high [1, 8, 10, 17, 21, 22, 24, 31, 39, 40, 42, 45, 47, 49, 51, 55, 57, 61, 63, 64, 65]. Of note, the two larger studies reported associated mortality varying from 25.93% to 57.14% [16, 47]. Important variation exists regarding mortality rates when considering all studies' information (0 to 100%). However, this may be explained by the inclusion of different study designs, sample sizes and the classification criteria used for ICH in the context of CHS . In large studies, the frequency of ICH was higher after CAS in comparison to CEA and was rare after asymptomatic carotid disease. The higher “ICH to CHS proportion” post-CAS CHS further supports the notion that patients with CHS after CAS are at increased risk of ICH [38]. The mandatory use of double antiplatelet therapy in CAS could contribute to this finding. Indeed, the use of antithrombotics was associated with the occurrence of post-CAS ICH in two small studies and in one large study based on administrative data [16]. Periprocedural hypertension and ipsilateral severe stenosis were the most common risk factors described [16, 20, 47, 50, 51, 63]. These data are relevant and stress the importance of pre- and post-carotid revascularization blood pressure control, particularly in patients with severe stenosis. One frequent bias found in the included studies was the lack of definition for CHS with ICH. However, the requirement of brain imaging for ICH diagnosis may minimize the impact of this bias for the overall comparison. The use of different methodologies and size discrepancies between the studies can also explain the variation in the frequency of ICH in the context of CHS [1, 2, 4, 5, 7, 8, 9, 10, 13, 14, 16, 17, 18, 19, 20, 21, 22, 23, 24, 29, 30, 34, 39, 40, 42, 43, 44, 45, 46, 47, 48, 49, 50, 51, 52, 55, 57, 61, 63, 64, 65]. The lack of information regarding associated factors such as use of antithrombotics, time interval from the ischemic event to revascularization procedure and severity of chronic white matter disease represents a limitation when evaluating the occurrence of ICH in the context of CHS.


This systematic review and meta-analysis showed that ICH in the context of CHS is rare in large series, occurs more frequently after CHS secondary to CAS and than post CAS, and is generally associated with high case-fatality rates. The main risk factors are periprocedural hypertension and ipsilateral severe stenosis. Further studies to better describe the contribution of other risk factors are needed.


Compliance with ethical standards

Conflict of interest

FBR is supported by the CHDI Foundation and EHDN. All authors certify that they have no affiliations with or involvement in any organization or entity with any financial interest (such as honoraria; educational grants; participation in speakers’ bureaus; membership, employment, consultancies, stock ownership, or other equity interest; and expert testimony or patent-licensing arrangements), or non-financial interest (such as personal or professional relationships, affiliations, knowledge or beliefs) in the subject matter or materials discussed in this manuscript.

This article does not contain any studies with human participants performed by any of the authors.

Supplementary material

701_2017_3328_MOESM1_ESM.docx (20 kb)
ESM 1(DOCX 19 kb)
701_2017_3328_MOESM2_ESM.docx (23 kb)
ESM 2(DOCX 22 kb)


  1. 1.
    Abou-Chebl A, Yadav JS, Reginelli JP, Bajzer C, Bhatt D, Krieger DW (2004) Intracranial hemorrhage and hyperperfusion syndrome following carotid artery stenting. J Am Coll Cardiol 43:6CrossRefGoogle Scholar
  2. 2.
    Ascher E, Markevich N, Schutzer RW, Kallakuri S, Jacob T, Hingorani AP (2003) Cerebral hyperperfusion syndrome after carotid endarterectomy: predictive factors and hemodynamic changes. J Vasc Surg 37:9CrossRefGoogle Scholar
  3. 3.
    Benzel EC, Hoppens KD (1991) Factors associated with postoperative hypertension complicating carotid endarterectomy. Acta Neurochir 112:5Google Scholar
  4. 4.
    Bonaldi G, Aiazzi L, Baruzzi F, Biroli F, Facchinetti A, Fachinetti P, Lunghi A, Terraneo F (2005) Angioplasty and stenting of the cervical carotid bifurcation under filter protection: a prospective study in a series of 53 patients. J Neuroradiol 32(2):109–117Google Scholar
  5. 5.
    Borst GJ, Moll FL, Van de Pavoordt HD, Mauser HW, Kelder JC, Ackerstaff RG (2001) Stroke from carotid endarterectomy: when and how to reduce perioperative stroke rate? Eur J Vasc Endovasc Surg 21(6):484–489Google Scholar
  6. 6.
    Bradac O, Mohapl M, Kramar F, Netuka D, Ostry S, Charvat F, Lacman J, Benes V (2014) Carotid endarterectomy and carotid artery stenting: changing paradigm during 10 years in a high-volume centre. Acta Neurochir 156:8CrossRefGoogle Scholar
  7. 7.
    Brantley HP, Kiessling JL, Milteer HB Jr, Mendelsohn FO (2009) Hyperperfusion syndrome following carotid artery stenting: the largest single-operator series to date. J Invasive Cardiol 21(1):27–30Google Scholar
  8. 8.
    Buczek J, Karliński M, Kobayashi A, Bialek P, Czlonkowska A (2013) Hyperperfusion syndrome after carotid endarterectomy and carotid stenting. Cerebrovasc Dis 35(6):531–537Google Scholar
  9. 9.
    Coutts SB, Hill MD, Hu W (2003) Hyperperfusion syndrome: toward a stricter definition. Neurosurgery 53(5):1053–1058Google Scholar
  10. 10.
    Dalman JE, Beenakkers IC, Moll FL, Leusink JA, Ackerstaff RG (1999) Transcranial doppler monitoring during carotid endarterectomy helps to identify patients at risk of postoperative hyperperfusion. Eur J Vasc Endovasc Surg 18(3):222–227Google Scholar
  11. 11.
    Deruty R, Mottolese C, Pelissou-Guyotat I, Lapras C (1991) The carotid endarterectomy: experience with 260 cases and discussion of the indications. Acta Neurochir 112:7CrossRefGoogle Scholar
  12. 12.
    Go AS, Mozaffarian D, Roger VL, Benjamin EJ, Berry JD, Blaha MJ (2014) Heart disease and stroke statistics and 2014 update: a report from the American Heart Association. Circulation 129:28CrossRefGoogle Scholar
  13. 13.
    Gosseti B, Martinelli O, Guerricchio R, Irace L, Benedetti-Valentini F (1997) Transcranial doppler in 178 patients before, during and after carotid endarterectomy. J Neuroimaging 7(4):213–216Google Scholar
  14. 14.
    Gupta AK, Purkayastha S, Unnikrishnan M, Vattoth S, Krishnamoorthy T, Kesavadas C (2005) Hyperperfusion syndrome after supraaortic vessel interventions and bypass surgery. J Neuroradiol 32:7CrossRefGoogle Scholar
  15. 15.
    National Institute of Health. Study quality assessment Tools [] Last Updated April 2014
  16. 16.
    Henderson RD, Phan TG, Piepgras DG, Wijdicks EFM (2001) Mechanisms of intracerebral hemorrhage after carotid endarterectomy. J Neurosurg 95:6Google Scholar
  17. 17.
    Henry M, Gopalakrishnan L, Rjagopal S, Rath PC, Henry I, Hugel M (2005) Bilateral carotid angioplasty and stenting. Catheter Cardiovasc Interv 64:8CrossRefGoogle Scholar
  18. 18.
    Hosoda K, Kawaguchi T, Shibata Y, Kamei M, Kidoguchi K, Koyama J, Fujita S, Tamaki N (2001) Cerebral vasoreactivity and internal carotid artery flow help to identify patients at risk for hyperperfusion after carotid endarterectomy. Stroke 32(7):1567–1573Google Scholar
  19. 19.
    Iko M, Aikawa H, Go Y, Nakai K, Tsutsumi M, Yu I, Mizokami T, Sakamoto K, Inoue R, Mitsutake T, Eto A, Hanada H, Kazekawa K (2014) Treatment outcomes of carotid artery stenting with two types of distal protection filter device. Springerplus 3:7CrossRefGoogle Scholar
  20. 20.
    Jansen C, Sprengers AM, Moll FL, Vermeulen FEE, Hamerlijnck RPHM, van Gijin J, Ackerstaff RGA (1994) Prediction of intracerebral hemorrhage after carotid endarterectomy by clinical criteria and intraoperative transcranial doppler monitoring: results of 233 operations. Eur J Vasc Surg 8(2):220–225Google Scholar
  21. 21.
    Kablak-Ziembicka A, Przewlocki T, Pieniazek P, Musialek P, Motyl R, Moczulski Z, Tracz W (2006) Assessment of flow changes in the circle of Willis after stenting for severe internal carotid artery stenosis. J Endovasc Ther 13:10CrossRefGoogle Scholar
  22. 22.
    Kaku Y, Yoshimura S, Kokuzawa J (2004) Factors predictive of cerebral hyperperfusion after carotid angioplasty and stent placement. AJNR Am J Neuroradiol 25(8):1403–1408Google Scholar
  23. 23.
    Karapanayiotides T, Meuli R, Devuyst G, Piechowski-Jozwiak B, Dewarrat A, Ruchat P, Segesser LV, Bogousslavsky (2004) Postcarotid endarterectomy hyperperfusion or reperfusion syndrome. Stroke 36:7Google Scholar
  24. 24.
    Katano H, Mase M, Sakurai K, Miyachi S, Yamada K (2012) Revaluation of collateral pathways as escape routes from hyperemia/hyperperfusion following surgical treatment for carotid stenosis. Acta Neurochir 154:12CrossRefGoogle Scholar
  25. 25.
    Kayahara T, Takeda R, Kikkawa Y, Take Y, Kurita H (2015) Hyperperfusion syndrome after aneurysm surgery: a case report. Acta Neurochir 157:3CrossRefGoogle Scholar
  26. 26.
    Khattar NK, Friedlander RM, Chaer RA, Avgerinos ED, Kretz ES, Balzer JR, Crammond DJ, Habeych MH, Thirumala PD (2016) Perioperative stroke after carotid endarterectomy: etiology and implications. Acta Neurochir 158:7CrossRefGoogle Scholar
  27. 27.
    Kim DYK, Kim BM, Park H, Chung J (2012) Retinal hemorrhage as an initial sign of cerebral hyperperfusion syndrome after carotid stenting. Acta Neurochir 154:3Google Scholar
  28. 28.
    Kozar S, Jeromel M (2014) Hyperperfusion and intracranial haemorrhage after carotid angioplasty with stenting—latest review. Signa Vitae 9:6CrossRefGoogle Scholar
  29. 29.
    Lai Z, Liu B, Chen Y, Ni L, Liu C (2015) Prediction of cerebral hyperperfusion syndrome with velocity blood pressure index. Chin Med J 128:7CrossRefGoogle Scholar
  30. 30.
    Li SM, Li D, Ling F, Miao ZR, Wang ML (2005) Carotid artery stenting: experience of a single Institute in China. Interv Neuroradiol 11:8CrossRefGoogle Scholar
  31. 31.
    Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gotzsche PC, Ionannidis JPA, Clarke M, Devereaux PJ, Kleijnen J, Moher D (2009) The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. Ann Intern Med 151:30CrossRefGoogle Scholar
  32. 32.
    Lieb M, Shah U, Hines GL (2012) Cerebral hyperperfusion syndrome after carotid intervention: a review. Cardiol Rev 20(2):84–89Google Scholar
  33. 33.
    Luengo-Fernandez R, Gray AM, Bull L, Cuthbertson F, Rothwell PM (2013) Oxford vascular study. Quality of life after TIA and stroke: ten-year results of the oxford vascular study. Neurology 81:95CrossRefGoogle Scholar
  34. 34.
    Maas MBK, Kwolek CJ, Hirsch JA, Jaff MR, Rordorf GA (2013) Clinical risk predictors for cerebral hyperperfusion syndrome after carotid endarterectomy. J Neurol Neurosurg Psychiatry 84:5CrossRefGoogle Scholar
  35. 35.
    Macfarlane R, Moskowitz MA, Sakas DE, Tasdemiroglu E, Wei EP, Kontos HA (1991) The role of neuroeffector mechanisms in cerebral hyperperfusion syndromes. J Neurosurg 1991:11Google Scholar
  36. 36.
    Magee TR, Davies AH, Baird RN, Horrocks M (1992) Transcranial Doppler measurement before and after carotid endarterectomy. J R Coll Surg Edinb 37:2Google Scholar
  37. 37.
    McCabe D, Brown MM, Clifton A (1999) Fatal cerebral reperfusion hemorrhage after carotid stenting. Stroke 30:4CrossRefGoogle Scholar
  38. 38.
    McDonald RJ, Cloft HJ, Kallmes DF (2011) Intracraneal hemorrhage is much more common after carotid stenting than after endarterectomy. Evidence from the national inpatient sample. Stroke 42(10):2782–2787Google Scholar
  39. 39.
    Mohammadian R, Sohrabi B, Mansourizadeh R, Mohammadian F, Nasiri B, Haririan S (2012) Unprotected carotid artery stenting: complications in 6 months follow-up. J Neuroradiol 54:7CrossRefGoogle Scholar
  40. 40.
    Morrish W, Grahovac S, Douen A, Cheung G, Hu W, Farb R, Kalapos P, Wee R, Hudon M, Agbi C, Richard M (2000) Intracranial hemorrhage after stenting and angioplasty of extracranial carotid stenosis. AJNR Am J Neuroradiol 21(10):1911–1916Google Scholar
  41. 41.
    Moulakakis KG, Mylonas SN, Sfyroeras GS, Andrikopoulos V (2009) Hyperperfusion syndrome after carotid revascularization. J Vasc Surg 49:9CrossRefGoogle Scholar
  42. 42.
    Narita S, Aikawa H, Nagata S, Tstutsumi M, Kouhei N, Yoshida H, Matsumoto Y, Hamaguchi S, Etoh H, Sakamoto K, Inoue R, Kazekawa K (2013) Intraprocedural prediction of hemorrhagic cerebral Hyperperfusion syndrome after carotid artery stenting. J Stroke Cerebrovasc Dis 22:5CrossRefGoogle Scholar
  43. 43.
    Naylor AR, Evans J, Thompson MM, London NJM, Abbott RJ, Cherryman G, Bell PRF (2003) Seizures after carotid endarterectomy: hyperperfusion, dysautoregulation or hypertensive encephalopathy? Eur J Vasc Endovasc Surg 26:6Google Scholar
  44. 44.
    Newman JE, Ali M, Sharpe R, Bown MJ, Sayers RD, Naylor AR (2013) Changes in middle cerebral artery velocity after carotid endarterectomy do not identify patients at high-risk of suffering intracranial haemorrhage or stroke due to hyperperfusion syndrome. Eur Soc Vasc Surg 45(6):562–571Google Scholar
  45. 45.
    Nicholas GG, Hashemi H, Gee W, Reed JF (1993) The cerebral hyperperfusion syndrome: diagnostic value of ocular pneumoplethysmography. J Vasc Surg 17:6CrossRefGoogle Scholar
  46. 46.
    Ogasawara K, Inoue T, Kobayashi M, Endo H, Yoshida K, Fukuda T, Terasaki K, Ogawa A (2005) Cerebral hyperperfusion following carotid endarterectomy: diagnostic utility of intraoperative transcranial Doppler ultrasonography compared with single-photon emission computed tomography study. AJNR Am J Neuroradiol 26(2):252–257Google Scholar
  47. 47.
    Ogasawara K, Sakai N, Kuroiwa T, Hosoda K, Iihara K, Toyoda K, Sakai C, Nagata I, Ogawa A (2007) Intracranial hemorrhage associated with cerebral hyperperfusion syndrome following carotid endarterectomy and carotid artery stenting: retrospective review of 4494 patients. J Neurosurg 107(6):1130–1136Google Scholar
  48. 48.
    Ogasawara K, Yukawa H, Kobayashi M et al (2003) Prediction and monitoring of cerebral hyperperfusion after carotid endarterectomy by using single-photon emission computerized tomography scanning. J Neurosurg 99:7CrossRefGoogle Scholar
  49. 49.
    Pieniazek PT, Tekieli L, Musialek P, Kablak-Ziembicka A, Przewlocki T, Motyl R, Dzierwa K, Paluszek P, Hlawaty M, Zmudka K, Podolec P (2012) Carotid artery stenting according to the ‘tailored-CAS’ algorithm is associated with a low complication rate at 30 days: data from the TARGET-CAS study. Kardiol Pol 70:9Google Scholar
  50. 50.
    Piepgras D, Morgan MK, Sundt T, Yanagiihara T, Mussman LM (1988) Intracerebral hemorrhage after carotid endarterectomy. J Neurosurg 68:5CrossRefGoogle Scholar
  51. 51.
    Schroeder T, Sillesen H, Boesen J, Laursen H, Sorensen P (1987) Intracerebral hemorrhage after carotid endarterectomy. Eur J Vasc Surg 1(1):51–60Google Scholar
  52. 52.
    Solomon RA, Loftus CM, Quest DO, Correll JW (1986) Incidence and etiology of intracerebral hemorrhage following carotid endarterectomy. J Neurosurg 64(1):29–34Google Scholar
  53. 53.
    Sprigg NS, Selby J, Fox L, Berge E, Whynes D, Bath PM (2013) Efficacy of nitric oxide in stroke investigators. Very low quality of life after acute stroke: data from the efficacy of nitric oxide in stroke trial. Stroke 44:62CrossRefGoogle Scholar
  54. 54.
    Sundt TM Jr, Sharbrough FW, Piepgras DG, Kearns TP, Messick JM Jr, O’Fallon WM (1981) Correlation of cerebral blood flow and electroencephalographic changes during carotid endarterectomy: with results of surgery and hemodynamics of cerebral ischemia. Mayo Clin Proc 56:11Google Scholar
  55. 55.
    Tan GS, Phatouros CC (2009) Cerebral hyperperfusion syndrome post-carotid artery stenting. J Med Imaging Radiat Oncol 53:7CrossRefGoogle Scholar
  56. 56.
    Terada T, Tsuura M, Matsumoto H, Masuo O, Tsumoto T, Yamaga H, Ohura Y, Itakura T (2006) Hemorrhagic complications after endovascular therapy for atherosclerotic intracranial arterial stenoses. Neurosurgery 59:9Google Scholar
  57. 57.
    Tietke MW, Kerby T, Alfke K, Riedel C, Rohr A, Jensen U, Zimmermann P, Stingele R, Jansen O (2009) Complication rate in unprotected carotid artery stenting with closed-cell stents. Neuroradiology 52(7):611–618Google Scholar
  58. 58.
    Timmers HJLM, Wieling W, Karemaker JM, Lenders JWM (2004) Baroreflex failure: a neglected type of secondary hypertension. Neth J Med 62:5Google Scholar
  59. 59.
    Urbach DR (2005) Measuring quality of life after surgery. Surg Innov 12:5CrossRefGoogle Scholar
  60. 60.
    van Mook WN, Rennenberg RJ, Schurink GW, van Oostenbrugge RJ, Mess WH, Hofman PAM, de Leeuw PW (2005) Cerebral hyperperfusion syndrome. Lancet Neurol 4:12CrossRefGoogle Scholar
  61. 61.
    Wagner WH, Cossman DV, Farber A, Levin PM, Cohen JL (2005) Hyperperfusion syndrome after carotid endarterectomy. Ann Vasc Surg 19(4):479–486Google Scholar
  62. 62.
    Wallaert JB, Nolan BW, Stone DH, Powell RJ, Brown JR, Cronenwett JL, Googney PP (2016) Physician specialty and variation in carotid revascularization technique selected for Medicare patients. J Vasc Surg 63:9CrossRefGoogle Scholar
  63. 63.
    Wilson PV, Ammar AD (2005) The incidence of ischaemic stroke versus intracerebral hemorrhage after carotid endarterectomy: a review of 2452 cases. Ann Vasc Surg 19(1):1–4Google Scholar
  64. 64.
    Wu YM, Wong HF, Chen Y-L, Wong M-C, Toh C-H (2011) Carotid stenting of asymptomatic and symptomatic carotid artery stenoses with and without the use of a distal embolic protection device. Acta Cardiol 66:6CrossRefGoogle Scholar
  65. 65.
    Yoshie T, Ueda T, Takada T, Nogoshi S, Fukano T, Hasegawa Y (2016) Prediction of cerebral hyperperfusion syndrome after carotid artery stenting by CT perfusion imaging with acetazolamide challenge. Neuroradiology 58:7CrossRefGoogle Scholar
  66. 66.
    Zhu CZ, Norris JW (1990) Role of carotid stenosis in ischemic stroke. Stroke 21:4CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria 2017

Authors and Affiliations

  • Pedro Abreu
    • 1
  • Jerina Nogueira
    • 1
  • Filipe Brogueira Rodrigues
    • 2
    • 3
    • 4
  • Ana Nascimento
    • 5
  • Mariana Carvalho
    • 5
  • Ana Marreiros
    • 1
  • Hipólito Nzwalo
    • 1
  1. 1.Department of Biomedical Sciences and MedicineUniversity of AlgarveFaroPortugal
  2. 2.Clinical Pharmacology UnitInstituto de Medicina MolecularLisbonPortugal
  3. 3.Laboratory of Clinical Pharmacology and Therapeutics, Faculty of MedicineUniversity of LisbonLisbonPortugal
  4. 4.Huntington’s Disease Centre, Institute of NeurologyUniversity College LondonLondonUK
  5. 5.Department of NeurologyCentro Hospitalar do AlgarveFaroPortugal

Personalised recommendations