Lacunair Syndromes: An Updated Review Download PDF

Journal Name : SunText Review of Neuroscience & Psychology

DOI : 10.51737/2766-4503.2021.029

Article Type : Review Article

Authors : De Reuck JL

Keywords : Lacunar syndromes; Lacunar infarcts; Pure motor stroke; Pure sensory stroke; Sensorimotor stroke; Ataxic hemiparesis; Dysarthria-clumsy hand; Prevention; Treatment

Abstract

Cortical small vessel disease (CSVD) is the main cause of vascular dementia. However occlusion of a single perforating branch can lead to a lacunar syndrome (LS). Miller Fisher described 5 types of LSs: a pure motor stroke, a pure sensory stroke, a sensorimotor stroke and, the ataxic hemiparesis, and the dysarthria-clumsy hand types. Only the pure motor stroke had a favourable outcome. LSs are frequently progressive due to the extension of the occlusion to nearby branches. LSs can also be due to territorial infarcts in a minority of cases. Treatment modalities are not successful. Only prevention of the cardiovascular risk factors can slow down the occurrence of LSs. Mainly early treatment of arterial hypertension is important. Only acute Intravenous alteplase treatment seems to reduce the severity of the LS.


Introduction

Lacunar syndromes (LSs) are due to small deep cerebral infarcts within the territory of a single perforating artery with a maximum diameter of less than 25 millimetres on neuro-imaging [1]. Cerebral small vessel disease (CSVD) causes 25% of the overall number of strokes [2]. The occurrence rate of vascular dementia due to lacunar strokes is 37% [3]. With an incidence of 15%, it is the second most important cause of dementia after Alzheimer’s disease [4]. Asymptomatic lacunar infarcts (LIs) are 5 times more common than symptomatic ones. However, they must be considered as preceding risk factors for a stroke and cognitive impairment leading to dementia [5].

In the 1960s, C Miller Fisher performed autopsy studies showing that vessels supplying LIs display segmental arteriolar disorganization, characterized by vessel enlargement, haemorrhage and fibrinoid deposition, that he called “lipohyalinosis” [6]. However, still a minority of LIs is suspected to be due to a cardiac embolic source or to a symptomatic carotid stenosis [7-9].

CSVD is not only responsible for LIs but also for ischemic white matter changes [10,11]. Magnetic resonance imaging (MRI) shows very well the hyperintensive white matter changes, but probably underestimate the number of LIs [12]. Cerebral micro-infarcts are overall considered as the invisible lesions on MRI [13]. The present review will only discuss the LSs due to involvement of a single deep perforating branch as vascular dementia due to CSVD has been already extensively been discussed previously [14,15]. 


Vascular supply of lacunar infarcts

On post-mortem examination LIs, due to CSVD, are most observed in the lentiform nucleus (100%), followed by the thalamus (70%) and the internal capsule (55%). In the periventriclar white matter the incidence is 51% and in the caudate nucleus 41%. The lowest frequency is observed in the brainstem (19%) [16]. The lenticulo-striatal arteries, issued from the middle cerebral artery, supply the superolateral part of the caudate nucleus, the superior part of the internal capsule, most of the putamen and partly the globus pallidus. The perforating branches from the anterior cerebral artery perfuse the medial segment of the globus pallidus and the inferior part of the internal capsule [17]. The periventricular white matter is supplied in the fronto-central part of the brain by ventriculofugal end-branches of the lateral lenticulo-striatal arteries, while in the parieto-occipital regions it is supplied by ventriculofugal branches issued from the choroidal arteries [18]. The thalamus is mainly supplied by performing branches, issued from the basilar artery, and from the posterior communicating and posterior cerebral arteries [19]. On post-mortem angiograms the deep perforating arteries are poorly filled and show several narrowing’s and post-stenotic dilatations in brains with LIs. A responsible occlusion is observed in 80% of the lesions [20].


Risk Factors

CSVD is predominantly observed in aged patients with a strong previous history of early occurring adulthood vascular risks [21]. Arterial hypertension is the most established vascular risk factor for the occurrence of CSVD [22]. The incidence of white matter lesions is less severe in hypertensive adults with well-treated arterial hypertension compared to those in which the treatment was less severe and less well followed up [22]. Increased body mass index, cardiovascular disease, lack of physical activity, heavy alcohol consumption, smoking, hypercholesterolemia and diabetes are considered as additional risk factors when already occurring in young adulthood [23]. Atrial fibrillation and carotid stenosis are associated more with non-lacunar than with lacunar infarction [24]. Hyperhomocysteinemia has also been considered as an increased risk of LIs in the basal ganglia [25].


Clinical Syndromes

Miller Fisher described five types of classical clinical syndromes: pure motor stroke, pure sensory stroke, sensorimotor stroke, ataxic hemiparesis, and dysarthria-clumsy hand [26]. On MRI with diffusion-weighted imaging performed within 5 days after the appearance of the LS, only pure motor stroke correlated with the presence of the LI in the controlateral posterior limb of the internal capsule. In the other syndromes no clinico-neuroimaging correlation was observed [27]. Pure motor hemiparesis is observed in 57% of the LSs. Sensorimotor syndrome in 20%, ataxic hemiparesis in 10%, pure sensory syndrome in 7% and dysarthria-clumsy hand syndrome in 6% are the incidences in the remaining types [28]. The pure motor stroke involves to the same degree the face, the arm and the leg. Although the main location is the internal capsule, a minority is due to a pontine lacuna. The long-term prognosis is excellent with in the majority of cases a complete recovery within six months [29].

The pure sensory stroke syndrome is difficult to delineate because the symptoms are mainly subjective, linked to the thalamus [30]. Also cases of pure sensory stroke due to a pontine lacunes have been described [31,32]. Sensorimotor stroke is the most difficult defined LS as additional cortical signs cannot always been excluded clinically. Both equal sensory and motor involvement of the face, the arm and the leg with exclusion of cortical participation have to be confirmed mainly by neuroimaging techniques [33]. The atactic hemiparesis syndrome presents with cerebellar ataxia and with pyramidal signs involving the limbs at the same side [34]. The LI is limited to the basis pontis, opposed to the clinical symptoms [35]. Dysarthria-clumsy hand syndrome has similarities with the atactic hemiparese syndrome: moderate weakness of the face, and upper and lower limbs, moderate dysarthria and dysmetria, Babinski sign and, slight dragging and imbalance of the leg on the right side. Fisher found a 5 mm lesion in the pons on the side opposed the clinical deficit [36]. Also other sides have been observed [37,38]. Pseudo-lacunar syndromes have as well been described. However the extreme variety of the symptoms makes their inclusion as LSs highly improbable [39].


Outcome

When comparing visible symptomatic LIs on CT scans the average size of the lesions is smaller in the independent patients compared to in those with a remaining handicap. The LI decreases in average size from day 3 to 10 in the former group but remains unchanged in the group of still disabled patients [40]. LSs are a major cause of progressive motor deficits, probably because of stepwise occlusion of the branches of small perforating arteries [41]. LIs are more frequently progressive than large artery disease and cardio-embolism. Their pattern varies according to the location of the LI [42]. However, the main risk in patients with LIs is the progressive cognitive impairment, eventually leading to vascular dementia [43]. From the onset on LIs are associated with a moderately increased overall mortality compared to the normal general population. Post-stroke mortality risks from LIs associated to atherothrombotic and cardio-embolic strokes are significantly higher [44]. The mortality rate after a mean follow-up of 3.6 years is 1.78% [45].

Prevention and Treatment

The most widely accepted approach to prevention and treatment is to intensively control of the well-established vascular risk factors, of which arterial hypertension is the most important [2]. Antithrombotic treatment with aspirin has not been effective in the long-term lacunar stroke prevention and treatment [46]. Addition of clopidogrel did not reduce the risk of recurrent LS [47]. However, it significantly increases the risk of bleeding and death [48]. Aspirin plus extended–release dipyridamole also is not found to be very effective [49]. On the other end, an effective treatment with intravenous alteplase in patients with imaging-defined acute LAs is observed, similar to those experienced in other subtypes [50]. Oral anticoagulants and left atrial appendage closure do not prevent recurrence of single LIs [51].


Discussion

Lis not due to CSVD represent between 16 and 20% of patients with a LS history. They are mainly the result of embolism due to atrial fibrillation [52,53]. Seizures are not observed in patients with pure LSs [54, 55]. When occurring they only reflect the existence of an underlying neurodegenerative process that is responsible for mental deterioration [56]. Another disease with LIs and severe white matter changes is the cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy (CADASIL) due to Notch3 mutation [57]. However, in this disease only mild gait disturbances are associated to the vascular cognitive deterioration [58].

Positron emission tomography (PET) can already demonstrate a global decrease of cerebral blood flow in patients with silent LIs [59]. No PET studies are available in patients presenting a solitaty LS. However, cerebral blood flow is lower in the cerebral cortex and the white matter of subjects with intensive white matter hyper-intensities on MRI [60]. In our study LSs due to LIs only represent 11% of the whole stroke population [27] instead of the 25% observed in a more recent study [27]. 


Disclosure

The authors have nothing to declare in relation to this article. No funding was received for the publication of this article.


References

  1. Micheli S, Corea F. Lacunar versus non-lacunar syndromes. Front Neurol Neurosci. 2012; 30: 94-98.
  2. Cannistraro RJ, Badi M, Eidelman BH, Dickson DW, Middelbrooks EH, Meschia JF. CNS small vessel disease: a clinical review. Neurology. 2019; 92: 1146-1156.
  3. Makin SDJ, Turpin S, Dennis MS, Wardlaw JM. Cognitive impairment after lacunar stroke: systematic review and meta-analysis of incidence, prevalence and comparison with other strokes subtypes. J Neurol Neurosurg Psychiatry. 2013; 84: 893-900.
  4. O’Brien JT, Thomas A. Vascular dementia. Lancet. 2015; 366: 1698-1706.
  5. Vermeer S, Longstreth Jr WT, Koudstaal PJ. Silent brain infarcts: a systematic review. Lancet Neurol. 2007; 6: 611-619.
  6. Regenhardt RW, Das AS, LO EH, Caplan LR. Advances in understanding the pathophysiology of lacunar stroke: a review. JAMA Neurol. 2018; 75: 1273-1281.
  7. Kappelle LJ, Van Gijn J. Carotid angiography in patients with subcortical ischaemia. In: Lacunar and other subcortical infarcts (Eds: Donnan GA, Norrving B, Bamford J, Bogouslavsky J). London: Oxford University Press. 1995: 56-69.
  8. Boiten J, Lodder J. Risk factors for lacunar infarction. In: Lacunar and other subcortical infarcts (Eds: Donnan GA, Norrving B, Bamford J, Bogouslavsky J). London: Oxford University Press. 1995: 80-86
  9. Wessels T, Rottger C, Jauss M, Kaps M, Traupe H, Stolz E. Identification of embolic stroke pattern by diffusion-weighted MRI in clinically defined lacunar stroke syndromes. Stroke. 2005; 36: 757-761.
  10. Leys D, Englund E, Del Ser T, Inzitari D, Fazekas F, Bornstein N, et al. White matter changes in stroke patients. Relationship with stroke subtypes and outcome. Eur Neurol. 1999; 42: 67-75.
  11. Wardlaw JM, Smith C, Dichgans M. Small vessel disease: mechanisms and clinical implications. Lancet Neurol. 2019; 18: 684-696.
  12. De Reuck J, Auger F, Durieux N, Cordonnier C, Deramecourt V, Pasquier F, et al. Topographic distribution of white matter changes and lacunar infarcts in neurodegenerative and vascular dementia syndromes: a post-mortem 7.0-tesla magnetic resonance imaging study. Eur Stroke J. 2016; 1: 122-129.
  13. Smith EE, Schneider JA, Wardlaw JM, Greenberg SM. Cerebral microinfarcts: the invisible lesions. Lancet Neurol. 2012; 11: 272-282.
  14. McAleese KE, Alafuzoff I, Charidimou A, De Reuck J, Grimberg LT, Hainsworth AH, et al. Post-mortem assessment in vascular dementia: advances and aspirations. BMC Med. 2016; 14: 129.
  15. Heiss WD, Rosenberg GA, Thiel A, Berlot R, De Reuck J. Neuroimaging in vascular cognitive impairment: a state-of-the art review. BMC Med. 2016; 14: 174.
  16. De Reuck J, vander Eecken H. Topography of infarcts in the lacunar state. Cerebral vascular disease 7th international conference Salzburg, 1974 (Eds: Meyer JS, Lechner H, Reivich M). Stuttgart, George Thieme Publishers. 1976; 162-165.
  17. DjuLejic V, Marinkovic S, Georgievski B, Stijlak L, Aksic M, Puskas L, et al. Clinical significance of blood supply to the internal capsule and basal ganglia. J Clin Neurosci. 2016; 25: 19-26.
  18. De Reuck J. The human periventricular arterial blood supply and the anatomy of cerebral infarctions. Eur Neurol. 1971; 5: 321-334.
  19. Plets C, De Reuck J, Vander Eecken H, Van den Bergh R. The vascularization of the human thalamus. Acta Neurol Belg. 1970; 70: 687-770.
  20. De Reuck J, vander Eecken H. The arterial angioarchitecture in lacunar state. Acta Neurol Belg. 1976; 76: 142-149.
  21. Lane CA, Barnes J, Nicholas JM, Sudre CH, Cash DM, Malone IB, et al. Associations between vascular risk across adulthood and brain pathology in late life: evidence from a British Birth Cohort. JAMA Neurol. 2020; 77: 175-183.
  22. SPRINT MIND Investigators for the SPRINT Research Group et al. Association of intensive vs standard blood pressure control with cerebral white matter lesions. JAMA. 2019; 322: 524-534.
  23. Williamson W, Lewandowski AJ, Forkert NS, Griffanti L, Okell TW, Betts J, et al. Association of cardiovascular risk factors with MRI Indices of cerebrovascular structure and function and white matter hyperintensities in young adults. JAMA. 2018; 320: 665-673.
  24. Jackson C, Sudlow C. Are lacunar strokes really different? A systematic review of differences in risk factor profiles between lacunar and nonlacunar infarcts. Stroke. 2005; 36: 891-901.
  25. Kloppenborg RP, Nederkoorn PJ, Grool AM, De Cocker LJL, Mali WPTM, van der Graaf Y, et al. Do lacunar infarcts have different aetiologies? Risk factors profiles of lacunar infarcts in deep white matter and basal ganglia: the second manifestations of arterial disease-magnetic resonance study. Cerebrovasc Dis. 2017; 43: 161-168.
  26. Lastilla M. Lacunar infarct. Clin Exp Hypertens. 2006; 28: 205-215.
  27. De Reuck J, De Groote L, Van Maele G. The classical lacunar syndromes: clinical and neuroimaging correlates. Eur J Neurol. 2008; 15: 681-684.
  28. Chamorro A, Sacco RL, Mohr JP, Foulkes MA, Kase CS, Tatemichi TK, et al. Clinical-computed tomographic correlations of lacunar infarction in the Stroke Data Bank. 1991; 22: 175-181.
  29. Fisher CM, Curry B. Pure motor hemiplegia of vascular origin. Arch Neurol. 1965; 13: 30-44.
  30. Fisher CM. Pure sensory stroke and allied conditions. Stroke. 1982; 13: 434-447.
  31. Klein IF, Lavallée PC, Mazighi M, Schouman-Claeys E, Labreuche J, Amarenco P. Basilar artery artherosclerotic plaques in paramedian and lacunar pontine infarctions: a high-resolution MRI study. Stroke. 2010; 41: 1405-1409.
  32. Field TS, Benavente OR. Penetrating artery territory pontine infarction. Rev Neurol Dis. 2011; 8: 30-38.
  33. Staaf G, Samuelsson M, Lindgren A, Norrving B. Sensorimotor stroke; clinical features, MRI findings, and cardiac and vascular concomitants in 32 patients. Acta Neurol Scand. 1998; 97: 93-98.
  34. Fisher CM. Homolateral ataxia and crural parese: a vascular syndrome. J Neurol Neurosurg Psychiatry. 1965; 28: 48-55.
  35. Fisher CM. Ataxic hemiparesis. Arch Neurol. 1978; 35: 126-128.
  36. Fisher CM. A lacunar stroke: the dysarthria-clumsy hand syndrome. Neurology. 1967; 17: 614-617.
  37. Spertell RB, Ransom BR. Dysarthria-clumsy hand syndrome by capsular infarct. Ann Neurol. 1979; 6: 263-265.
  38. Iguchi Y, Kimura K, Ueno Y, Inoue T, Matusmoto N, Sunada. Dysarthria-clumsy hand syndrome originating in the corona radiata. Eur J Neurol. 2006; 13: 6.
  39. Besson G, Hommel M. Lacunar syndromes. In: Advances in Neurology (vol 62): cerebral small vessel disease (Eds: Pullicino PM, Caplan LR, Hommel M). New York. Raven. 1993; 141-160.
  40. De Reuck J, Hemelsoet D, Nieuwenhuis L, Van Maele G. Computed tomographic changes in lacunar syndromes. Clin Neurol Neurosurg. 2005; 108: 18-24.
  41. Steinke W, Ley SC. Lacunar stroke is the major cause of progressive motor deficits. Stroke. 2002. 33: 1510-1516.
  42. Kim YB, Moon HS, Sah BC, Park KY, Lee YT, Chung PW. Topographic patterns and stroke subtypes according to progressive deficits in lacunair syndrome. J Stroke Cerebrovasc Dis. 2011; 20: 352-356.
  43. Makin SDJ, Turpin S, Dennis MS, Wardlaw JM. Cognitive impairment after lacunar stroke: systematic review and meta-analysis of Incidence, prevalence and comparison with other stroke subtypes. J Neurol Neursurg Psychiatry. 2013; 84: 893-900.
  44. Lund RW. Lacunar infarction, mortality over time and mortality relative to other ischemic strokes. J Insur Med. 2014; 44: 32-37.
  45. Sharma M, Pearce LA, Benavente OR, Anderson DC, Connolly SJ, Palacio S, et al. Predictors of mortality in patients with lacunar stroke in seconday prevention of small subcortical strokes trial. Stroke. 2014; 45: 2989-2994.
  46. Das AS, Regenhardt RW, Feske SK, Gurol ME. Treatment approaches to lacunar stroke. J Stroke Cerebrovasc Dis. 2019; 28: 2055-2078.
  47. Cote R, Zhang Y, Hart RG, McClure LA, Anderson DC, Talbert RL, et al. ASA failure: does the combination ASA/clopidogrel confer better long-term vascular protection?. Neurology. 2014; 82: 382-389.
  48. SPS3 investigators, Benavene OR, Hart RG, McClure LA, Szychowski JM, Coffey CS, Pearce LA. Effect of clopidogrel added to aspirin in patients with recent lacunar stroke. N Eng J Med. 2012; 367: 817-825.
  49. Biller J. Antiplatelet therapy in ischemic stroke: variability in clinical trials and on choosing the appropriate therapy. Neurol Sci. 2009; 1: 1-9.
  50. Barow E, Boutitie F, Cheng R, Cho TH, Ebinger M, Endres M, et al. Functional outcome of intravenous thrombolysis in patients with lacunar infarcts in the WAKE-Up trial. JAMA Neurol. 2019; 76: 641-649.
  51. Das AS, Regenhardt RW, Feske SK, Gurol ME. Treatment approaches to lacunar stroke. J Stroke Cerebrovasc Dis. 2019; 28: 2055-2078.
  52. Arbois A, Massons J, Garcia-Eroles L, Targa C, Comes E, Parra O. Clinical predictors of lacunar syndrome not due to lacunar infarction. Neurol. 2010; 10.
  53. Giacomozzi S, Caso V, Agnelli G, Acciarresi M, Allberti A, Venti M, et al. Lacunar stroke syndromes as predictors of lacunar and non-lacunar infarcts on neuroimaging: a hospital-based study. Intern Emerg Med. 2020; 15: 429-436.
  54. Bladin CF, Alexandrov AV, Bellavence A, Borenstein N, Chambers B, Colé R, et al. Seizures after stroke: a prospective multicenter study. Arch Neurol. 2000; 57: 1617-1622.
  55. De Reuck J, Nagy E, Van Maele G. Seizures and epilepsy in patients with lacunar strokes. J Neurol Sci. 2007; 263: 75-78.
  56. De Reuck J, Van Maele G. Cognitive impairment and seizures in patients with lacunar strokes. Eur Neurol. 2009; 61: 159-163.
  57. Chabriat H, Joutel A, Dichgans, Tournier-Lasserve E, Bousser MG. Cadasil. Lancet Neurol. 2009; 8: 643-653.
  58. Finsterwalder S, Wuehr M, Gesierich B, Dietze A, Konieczny MJ, Schmidt R, et al; Minor gait impairment despite white matter damage in pure small vessel disease. Ann Clin Trans Neurol. 2019; 6: 2026-2036.
  59. Kobayashi S, Okeda K, Yamashita K. Incidence of silent lacunar lesion in normal adults and its relation to cerebral blood flow and risk factors. Stroke. 1991; 22: 1379-1383.
  60. Shi Y, Trippleton MJ, Makin SD, Marshall I, Geerlings MI, de Craen AJM, et al. Cerebral blood flow in small vessel disease: a systematic review and meta-analysis. J Cereb Blood Flow Metab. 2016; 36: 1653-1667.