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The magnitude image was combined with the Phase image to create an enhanced contrast magnitude susceptibility image.
All SWI scans were blindly analyzed by a senior neuroradiologist PL. The SWI sequence can show a fine band of low signal following the contour of the motor strip of the cerebral cortex and in the periphery of the putamen.
This appears as a thin line of low signal looking as if traced with a black pencil [ 14 ]. This pencil lining in the motor strip of the cerebral cortex was scored with a system based on previous methods described in the literature as present or absent [ 14 ].
To assess SWI signal intensity in the caudate nucleus, putamen, globus pallidus, red nucleus and dentate nucleus, we used a region-of-interest ROI method similar to Meijer et al.
The signal intensity of the CSF was measured by ROI placement in the lateral ventricle. To limit the potential non-uniformity of the CSF signal, the signal intensity of two measurements bilaterally in the lateral ventricle were averaged.
Additionally, the ROIs were placed avoiding vessels, flow voids, the choroid plexus and were not including the edges of the structures.
The ROI method was performed by a senior neuroradiologist PL blinded to the clinical symptoms and diagnosis. See Additional file 1 : Figure S1 for an example placement of an ROI bilateral in the lateral ventricle and the left caudate nucleus.
All statistical analyses were performed with SPSS version 23, IBM, USA. Prior to analyzing the effect of age on brain iron deposition, potential confounding factors were tested by assessing possible imbalances within and between decades of life.
In addition, distributions and assumptions within the group of healthy subjects were checked and because of the non-normality of the data, non-parametric testing was used to compare for group differences and gender effects Mann-Whitney U test.
Given that the healthy subjects showed an equal distribution of gender, mean age, and number of subjects between and within each decade of life, we did not include these factors in the study analyses.
Analysis of Variance ANOVA was performed to evaluate potential group differences. Figures were made in R version 3. Since no equal distributions between NBIA patients and healthy subjects was present due to the small number of patients, no statistical analysis was performed between the two groups.
The qualitative SWI scan analysis revealed that the presence of cortical pencil lining was positively correlated with age. In Additional file 1 : Figure S2 differences in the presence or absence of cortical pencil lining in healthy subjects age 35 are shown.
No cortical pencil lining was observed in healthy subjects in their first decade of life. Age-related iron deposition lining the motor cortex and putamen in 81 healthy subjects.
The graph shows the percentage of healthy subjects Y-axis per decade of life X-axis that exhibit hypointense signals on SWI in a the motor cortex and b the putamen.
The presence of putaminal pencil lining was also positively correlated with age. No putaminal pencil lining was observed in healthy subjects in their first decade of life.
Putaminal pencil lining was observed in two BPAN cases who were diagnosed in their first decade of life, but was absent in the 2-year-old PKAN and year-old BPAN patients Fig.
Presence or absence of putaminal pencil lining. To further study the natural dynamics of iron accumulation in the brain during healthy aging, we investigated the normalized signal intensity ratio NSIR of SWI scans of the caudate nucleus, putamen, globus pallidus, red nucleus and dentate nucleus in our cohort of healthy subjects over different decades.
We observed significant positive correlations between age and the NSIR of all subcortical nuclei Fig. The strongest correlations were detected for the red nucleus and putamen both R 2 of 0.
This suggests that iron accumulation occurs relatively fast early in life in the globus pallidus. Additionally, the caudate nucleus and putamen showed a more linear increase of NSIR, reflecting a quite modest iron accumulation over time Fig.
Age-related regional SWI signal intensity. Normalized signal intensity ratio NSIR ratio between the signal intensity of the lateral ventricle and a region of interest ROI ; right and left hemisphere values are averaged and the signal intensity of the ROI in five subcortical nuclei: globus pallidus a , red nucleus b , dentate nucleus c , caudate nucleus d , and putamen e over time.
Red rounds, blue triangles and green squares denote healthy females, healthy males and NBIA subjects, respectively. The thick continuous line is the smoothened conditional mean of healthy subjects.
X-axis: age in years; Y-axis: NSIR. The four NBIA patients showed an increased NSIR in the globus pallidus compared to age-matched healthy subjects that was not observed for the other subcortical nuclei.
In addition, the dynamics of the NSIR in the other subcortical nuclei of the NBIA cases showed a similar pattern as seen in healthy subjects Fig.
Although no statistical analysis could be performed due to the small number of NBIA cases, our SWI scan data points to pathological iron accumulation in the globus pallidus as a hallmark of NBIA.
This study, where iron imaging data from the very early decades of life are reported, showed that cortical pencil lining is potentially less specific as a general marker for NBIA.
On the other hand, putaminal pencil lining in the first decade of life was seen in specific NBIA cases only and not in age-matched healthy individuals suggesting its potential as a specific marker of pathological iron accumulation in specific subtypes of young NBIA patients.
Finally, this work characterized NSIR in subcortical nuclei of the brain during healthy aging, where a positive correlation between age and NSIR in all subcortical nuclei was shown.
None of our NBIA patients, including BPAN and PKAN, showed cortical pencil lining in their first or second decade of life.
Additionally, this might also be explained by a more diffuse iron accumulation throughout the brain in neuroferritinopathy cases, whereas the iron accumulation in BPAN and PKAN cases is more isolated to the basal ganglia.
Alternatively, we speculate that quantification of the different pencil linings may discriminate between NBIA subtypes and between NBIA patients and healthy subjects.
Such quantification has been demonstrated to be useful in the diagnosis of amyotrophic lateral sclerosis ALS and primary lateral sclerosis PLS [ 20 , 21 ].
It should be noted that current approaches for diagnosing NBIA subtypes are based on a combination of clinical characteristics, genetic testing and MRI findings.
Furthermore, because of the broad range of possible clinical features present in NBIA, MRI findings often provide the first strong clue for the diagnosis.
This further accentuates the importance of this kind of research providing a normal baseline for a frequently used MRI sequence. To our knowledge, this is the largest study on iron deposition in the brain using SWI focusing on healthy subjects that also includes individuals in their first decade of life.
This period of life is of particular interest given the age of onset of the classic disease types of NBIA. This is further substantiated by the identification of putaminal pencil lining exclusively in young NBIA cases but not in age-matched healthy individuals.
This suggests that the occurrence of putaminal pencil lining in the first decade of life may be a potential marker in specific subtypes of NBIA, as none of the healthy subjects in their first decade of life had any signs of putaminal pencil lining.
In the early period of life we observed dynamic iron accumulation in the globus pallidus, red nucleus, and dentate nucleus. The non-linear pattern of SWI signal intensity change reflecting iron accumulation in the globus pallidus was reported before [ 18 ].
However, the exponential increase of iron accumulation in the red nucleus and dentate nucleus has, to our knowledge, not been described before.
Speculatively, this may point to a primary versus secondary effect of pathological brain iron accumulation, i. Some limitations should be noted in this study.
First, the sample size of subjects per decade is relatively small and only a few cases of NBIA are examined as a contrast group. Future studies including higher subjects are advisable to confirm the validity and normal ranges of these results.
Second, although SWI was used, which is a well-established surrogate marker for in vivo iron quantity [ 32 ], the signal intensity may be affected by other components such as calcium and lipids.
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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