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The study was funded by a Rosalind Franklin Fellowship by the University of Groningen DSV , Netherlands Organization for Health Research and Development ZonMw MAJT , Fonds Nuts-Ohra MAJT , Princes Beatrix Muscle fund MAJT , Gossweiler foundation MAJT , Science Foundation Dystonia Society MAJT , Funds Mental Health MAJT , Phelps Foundation MAJT , Beatrix Children Hospital Fund MAJT , Healthy Aging Fund UMCG MAJT.
Department of Neurology, University Medical Center Groningen, Hanzeplein 1, RB, Groningen, The Netherlands. Marlous C.
Department of Genetics, University Medical Center Groningen, Groningen, The Netherlands. Department of Radiology, University Medical Center Groningen, Groningen, The Netherlands.
Department of Radiology, Zorggroep Twente, Almelo and Hengelo, The Netherlands. Department of Cell Biology, University Medical Center Groningen, Groningen, The Netherlands.
Research project - Conception: MW, PL, MT Organization: MW Execution: MW, PL, DV, MT Statistical analysis - Design: MW, PL Execution: MW, PL Review and Critique: MW, PL, RL, DV, MT Manuscript preparation - Writing of the first draft: MW; Review and Critique: PL, RL, DV, MT.
All authors read and approved the final manuscript. Correspondence to Marlous C. The study was approved by the Medical Ethics Committee of the University Medical Center Groningen and participants or their parents gave written informed consent.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. NBIA patient demographics.
Figure S1. SWI with the positioning of the circular region-of-interest. Figure S2. Presence or absence of cortical pencil lining.
Open Access This article is distributed under the terms of the Creative Commons Attribution 4. Reprints and Permissions.
Cortical pencil lining on SWI MRI in NBIA and healthy aging. BMC Neurol 19, Download citation. Received : 25 May Accepted : 20 September Published : 14 October Skip to main content.
Search all BMC articles Search. Download PDF. A number of observations showing that the presence of AF is neither necessary nor sufficient for stroke, cast doubt on the causal role of AF as a villain in vascular brain injury VBI.
The requirement for additional risk factors before AF increases stroke risk; temporal disconnect of AF from a stroke in patients with no AF for months before stroke during continuous ECG monitoring but manifesting AF only after stroke; and increasing recognition of the role of atrial cardiomyopathy and atrial substrate in AF-related stroke, and also stroke without AF, have led to rethinking the pathogenetic model of cardioembolic stroke.
This is quite separate from recognition that in AF, shared cardiovascular risk factors can lead both to non-embolic stroke, or emboli from the aorta and carotid arteries.
Meanwhile, VBI is now expanded to include dementia and cognitive decline: research is required to see if reduced by OAC.
It could direct focus towards prevention of the atrial cardiomyopathy though much work is required to better define this entity before the balance between AF as villain or bystander can be determined.
At the population level, atrial fibrillation AF and stroke are inextricably intertwined. A significant world-wide increase in AF prevalence has been projected over the next decades.
In the context of the above changes in demographics and risk factor burden, the attributable proportion of AF-explained stroke will also increase in all age groups.
No right-shift towards older individuals on average is expected. Healthcare costs, in particular acute stroke care with AF are higher compared to other stroke entities.
Stroke has been the main focus of brain injury in AF, and recommendations for OAC to reduce stroke are well entrenched 19 with solid, consistent results indicating large treatment effects in relatively small randomized trials.
There is no specific effective therapy, providing an imperative to seek preventive measures. Because AF is similarly increasing, it is not surprising that associations have been made between AF presence and subsequent dementia, 21 independent of clinical stroke.
In the seminal Swiss-AF study, 25 MRI imaging showed multiple clinically known or silent infarcts, with large non-cortical or cortical infarcts related to lower cognitive function.
This also fuels the interesting proposition that OAC therapy might reduce cognitive decline and dementia. Observational studies suggest that OAC therapy for AF may prevent the onset of dementia, or slow cognitive decline.
Three Swedish registry studies showed those with AF given OAC therapy were less likely to develop dementia over a few years. Another approach compared to lower and higher time in therapeutic range TTR only in those on OAC: 29 reduced dementia was confined to those with TTR in the highest two quartiles.
Ultimately, randomized controlled trials will be required to settle the question. This will be examined in the BRAIN-AF study, 30 with results eagerly awaited.
The strong association between AF and VBI has long been thought directly caused by blood stasis in the fibrillating left atrium leading to thrombus formation and brain embolism.
In studies demonstrating association between subclinical device-detected AF and stroke, approximately one-third with AF and stroke had no evidence of AF before stroke and only manifested AF for the first time after stroke.
Therefore, some strokes before AF onset may result from large-artery atherosclerosis and artery-to-artery embolism, or hypertension-induced cerebral small-vessel occlusion.
Second, new AF after stroke may be a lagging marker of thrombogenic left atrial LA substrate. Further investigation is required to determine their relative role, but the strong link between AF and VBI cannot be explained by arrhythmia alone.
Links between risk factors, vascular dysfunction, cardiomyopathy, AF, and VBI. For AF to be the direct cause of atrial thromboembolism and VBI, AF should be necessary and sufficient for thromboembolism.
The evidence outlined above is inconsistent with AF being necessary for thromboembolism. If AF were sufficient for thromboembolism, then AF should be associated with thromboembolism regardless of systemic risk factors.
However, patients with clinical AF but no vascular risk factors do not have a higher ischaemic stroke risk than patients without AF.
The CHA 2 DS 2 -VASc score, summarizing systemic vascular risk factor burden, 56 modifies the association between AF and stroke.
One of the critical reasons for invoking a direct causal relationship between AF and VBI is the long-recognized association between AF cardioversion and cardioembolic stroke.
Observational studies showing OAC reduce thromboembolism from 2. Whatever the time window, conventional wisdom is that change from AF to sinus rhythm, with the return of atrial function, is the reason for cardioembolism and stroke.
This suggests risk factors and comorbidities may be more important than change in rhythm for cardioembolism.
While intriguing, further corroboration is required because cardioembolic event numbers were small: only four pre-cardioversion and nine post-cardioversion.
Left atrial enlargement has long been established as a risk factor for stroke in AF patients. Lower LA appendage flow velocity, and related spontaneous echo contrast, are associated with thromboembolism in AF.
Larger LA fibrosis extent detected by late gadolinium enhancement on cardiac MRI, is associated with AF stroke risk, 51 , 73 and also LA appendage thrombus, 74 lending further support for a causal relationship between atrial fibrosis, thrombo-embolic stroke, and VBI.
ECG markers of LA remodelling are also associated with AF-related stroke risk. Several MRI and ECG variables have been shown to improve stroke risk prediction beyond traditional clinical risk factors.
While atrial cardiomyopathy contribution to AF-related thromboembolism is well appreciated, 67 , 78 it now appears that atrial cardiomyopathy can be involved in atrial thromboembolism in the absence of AF.
There are conflicting reports on the relationship between LA size and VBI without AF or after adjustment for known AF, and more data are required to test this relationship.
After adjustment for AF, two early population-based studies found that echocardiographic LA size was associated with stroke risk, but only in men.
A small case—control study suggests LA fibrosis on MRI is more common in ESUS than controls. AF presence or absence. Whatever the relationship, one has to carefully consider whether AF burden, however defined, acting solely as an arrhythmia, is directly related to the likelihood of VBI, or whether high AF burden is in fact a surrogate measure of the presence or severity of an underlying atrial or general cardiomyopathy which determines the thrombo-embolic potential.
Lower burden short episodes with a benign prognosis, may be more driven by arrhythmic triggers. Much more work is required to answer these questions, though the ongoing ARTESIA and NOAH-AFNET6 studies will provide some answers.
Atrial cardiomyopathy results from progressive atrial remodelling due to aging and stretch. Due to underlying risk factors and comorbidities an overall cardiomyopathy develops, including ventricular involvement.
Risk factors, co-morbidities, and AF all involved in the development of an atrial cardiomyopathy modified from Kloosterman et al.
The available evidence suggests that AF is both an independent, causal risk factor for LA thromboembolism and a marker of an underlying, thrombogenic atrial substrate that can lead to LA thromboembolism independently of AF.
Patients in AF have lower LA appendage flow velocities than patients in sinus rhythm. Sinus rhythm restoration after AF ablation is associated with significant improvement in LA appendage flow velocity.
In addition to immediate LA hemodynamic effects, sustained AF leads to atrial contractile dysfunction and dilatation which in turn leads to atrial remodelling and fibrosis.
As outlined above, abnormal atrial substrate markers are associated with thrombo-embolic risk with or without clinically apparent AF.
Moreover, it is difficult to develop a model of AF-related thromboembolism that fully fits available data without accounting for thrombogenic atrial substrate.
Incorporating atrial substrate as an independent cause of thromboembolism results in a more satisfactory model in which age- and disease-related atrial remodelling result in atrial substrate prone to both AF and thromboembolism.
Usually, AF occurs first and thromboembolism later, but sometimes the order is reversed, and in either case, there is not necessarily a close temporal relationship between episodes of AF and thromboembolism.
This would explain the notable temporal disconnection between subclinical AF and stroke. This would explain the relationship between AF burden and stroke.
Recent experimental data show that the hypercoagulable state during AF causes pro-fibrotic and pro-inflammatory responses in adult atrial fibroblasts and the development of a substrate for AF in both transgenic mice and goats with persistent AF, illustrating the further complexity of the relationship.
Whether AF is a villain or bystander, OAC thromboprophylaxis of AF-related cardioembolic risk unquestionably reduces ischaemic stroke by a large margin.
While the prognosis untreated is unknown, it is likely the same as incidentally-detected asymptomatic AF discovered in primary care, which has a similar stroke rate as clinical AF.
The place of systematic screening using greater screening intensity, including continuous ECG recordings, is less certain, because stroke risk may be lower if the detected AF burden is lower.
There are a number of large ongoing trials set up to answer this question, , , and more have commenced SAFER ISRCTN, GUARD-AF NCT , so we will soon know whether such screening will reduce AF-related stroke burden.
It is also important to consider other VBI endpoints including dementia that might be impacted by OAC, but cognitive assessment is not part of most ongoing screening studies.
An important unmet need in patients with AF is improved long-term maintenance of sinus rhythm and prevention of cardiovascular events.
Larger prospective randomized trials, however, failed to show a significant reduction in AF recurrences or adverse cardiovascular outcomes, possibly because these studies addressed only one risk factor.
In contrast to this approach, the RACE 3 trial showed feasibility and efficacy of comprehensive cardiovascular risk reduction in patients with persistent AF and moderate heart failure.
A thrombogenic atrial myopathy leading to VBI independently of AF has important implications for the management of ESUS.
The term ESUS applies to ischaemic strokes that appear embolic but lack an identifiable embolic source. In this context, accumulating evidence linking atrial myopathy and thromboembolism suggests many ESUS cases may actually be cardioembolic strokes.
Two large randomized clinical trials found OAC therapy did not reduce stroke recurrence post-ESUS. Given the close connection between atrial myopathy and AF, and the proven benefit of anticoagulation for stroke prevention in AF, it is plausible that anticoagulation may also reduce stroke risk in atrial myopathy without AF.
Post hoc subgroup-analyses of two randomized clinical trials finding no overall benefit suggest that OACs reduce recurrent stroke in patients with markers of atrial myopathy.
Most alterations correlate with age and prevalent cardiovascular disease. Electrophysiological changes, many detected on the surface ECG, may be more specific for advanced atrial impairment.
These include increased P wave terminal force, P or PR prolongation, or excessive supraventricular ectopic activity, 75 , — or short atrial runs. Echocardiographic measures of left atrial LA size and function are broadly available.
Rheumatic mitral stenosis indicates a highly prothrombotic milieu. Blood biomarkers and genetics applied as polygenic risk scores may be indicative of AF-related stroke.
Markers of hypercoagulability have been related to post-stroke AF, , or, more generally, thyroid-stimulating hormone. Recently, atrial cardiomyopathy has been characterized as any complex of structural, architectural, contractile, or electrophysiological changes affecting the atria with the potential to produce clinically relevant manifestations.
Echocardiography is currently the imaging technique of choice. Two-dimensional speckle-tracking echocardiography and atrial strain have been used as more sensitive markers to detect early functional remodelling before anatomical changes occur.
Cardiac CT computed tomography or MRI magnetic resonance imaging can be used for a more accurate assessment of atrial volumes, while late gadolinium enhancement on MRI may quantify atrial fibrosis.
Cardiac disease is clearly associated with VBI. The relationship between AF, cardiac disease, and VBI remains enigmatic and will require much future research to determine whether AF is more bystander than a villain.
This paper was published as part of a supplement financially supported by the European Society of Cardiology ESC , Council on Stroke.
Conflict of interest: B. La Fibrillazione Atriale in Italia. Prevalence of atrial fibrillation in the Italian elderly population and projections from to for Italy and the European Union: the FAI Project.
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