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Attention and spatial cognition: Neural and anatomical substrates of visual neglect Marine Lunven a,b,*, Paolo Bartolomeo a a b

Inserm U1127, UPMC-Paris 6, CNRS UMR 7225, Brain and Spine Institute, Groupe Hospitalier Pitie´-Salpeˆtrie`re, 75013 Paris, France Inserm UMR_S 1028, CNRS UMR 5292, ImpAct, centre des neurosciences de Lyon, universite´ Lyon-1, 69500 Bron, France

A R T I C L E I N F O

A B S T R A C T

Article history: Received 30 May 2015 Accepted 6 January 2016

Unilateral spatial neglect (USN) is a neurological disorder often observed following damage to the right cerebral hemisphere. Patients with USN are no longer able to take into account stimuli presented on the left side of space. In this article, we will discuss the neuroanatomical correlates that underlie visuospatial attention and can cause USN, an area of growing research interest in the past 20 years. This syndrome has often been related to cortical damage, notably in the inferior parietal lobule. Other data have also implicated lesions in the inferior frontal gyrus or the superior temporal gyrus. In this article, we will highlight the relevance of viewing USN as a disconnection syndrome of interconnected cerebral areas, as opposed to a focal cortical syndrome. We will review data that provide evidence of intrahemispheric disconnection, in particular within the right hemisphere’s frontoparietal networks connected by the superior longitudinal fasciculus. Recent findings suggest that interhemispheric disconnection could also contribute to the manifestations of USN. Most importantly, interhemispheric disconnection might be a predictive factor for the chronicity of this disorder. This hypothesis implies that the left hemisphere by itself is not able to compensate for the patients’ deficits. Recovery requires the ability to exchange information between the two hemispheres, particularly in the posterior parietal and occipital regions. ß 2016 Elsevier Masson SAS. All rights reserved.

Keywords: Visual neglect Interhemispheric disconnection Frontoparietal network Chronic neglect Visuospatial attention

It is now widely accepted that visuospatial functions are not distributed symmetrically between the hemispheres. This was initially observed in brain-damaged patients in whom spatial deficits were most often associated with damage to the right hemisphere as opposed to the left hemisphere 1941 [1]. In 1962, He´caen [2] investigated the occurrence of spatial deficits in a large group of patients with unilateral post-Rolandic lesions. Spatial neglect, along with the inability to orient themselves on a map, loss of topographic memory, constructional apraxia and also dressing apraxia were found more often in patients with right hemisphere lesions. Since then, advances in brain imaging methods, in particular functional MRI, diffusion MRI, and transcranial and intracerebral magnetic stimulation have refined our understanding of anatomo-clinical relationships. In this article, we will review the neuroanatomical correlates of visuospatial attention and spatial neglect.

* Corresponding author. Inserm UMR_S 1028, CNRS UMR 5292, ImpAct, centre des neurosciences de Lyon, Universite´ Lyon-1, 69500 Bron, France. E-mail address: [email protected] (M. Lunven).

1. Anatomical and functional models of visuospatial attention Neuroimaging data in healthy subjects have inspired an anatomo-functional model of visuospatial attention [3]. The model is composed of a dorsal attentional network (DAN), made up of the intraparietal sulcus, superior parietal lobule, precuneus, and frontal eye field, which shows increased BOLD signal when subjects voluntarily direct their attention towards a visual target. A ventral attentional network (VAN), including the temporoparietal junction and the middle and inferior frontal gyri, has an increased BOLD signal when the subject attempts to process a target in an unexpected location. These regions underpin nonspatial attentional processes such as waking, and also the reorientation of attention towards new or important unexpected events [4]. In healthy subjects, the two networks interact continuously. Importantly, the DAN is represented bilaterally on the two hemispheres, while the VAN is lateralised to the right hemisphere. These two frontoparietal networks are anatomically supported by white matter tracts that form the superior longitudinal fasciculus (SLF). Three SLF branches have been identified in the monkey [5]. Recently, the use of tractography (reconstruction of

http://dx.doi.org/10.1016/j.rehab.2016.01.004 1877-0657/ß 2016 Elsevier Masson SAS. All rights reserved.

Please cite this article in press as: Lunven M, Bartolomeo P. Attention and spatial cognition: Neural and anatomical substrates of visual neglect. Ann Phys Rehabil Med (2016), http://dx.doi.org/10.1016/j.rehab.2016.01.004

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Fig. 1. Visualisation of the frontoparietal network supporting visuospatial attention processes: (A) The three branches of the superior longitudinal fasciculus as identified by diffusion-based tractography; (B) Its cortical projections as identified by tractography; (C) Cortical areas activated in functional imagery during orienting of visuospatial attention [3]; (D) Cortical areas related to the emergence of visuospatial neglect; (E) IPs: intraparietal sulcus; SPL: superior parietal lobule, FEF: frontal eye field, TPJ: temporoparietal junction, IPL: inferior parietal lobule, STg: superior temporal gyrus, VCF: ventral frontal cortex, IFg: inferior frontal gyrus, MFg: middle frontal gyrus. Adaptation of figure originally published in Nature Neuroscience 14(10);1245–6:2011 ‘‘A lateralised brain network for visuospatial attention’’, by M. Thiebaut de Schotten, F. Dell’Acqua, S.J. Forkel, A. Simmons, F. Vergani, D.G. Murphy, M. Catani. ß 2011, with permission from Nature Publishing Group.

white matter tracts through diffusion imaging) has identified a similar architecture in humans [6] (Fig. 1A). The most dorsal branch (SLF I) originates at the precuneus and the superior parietal lobule (Brodmann areas, BA 5 and 7) and projects towards the superior frontal and anterior cingulate gyri (BA 8, 9, 32). The intermediate branch (SLF II) originates at the anterior intraparietal sulcus and the angular gyrus (BA 39 and 40), and joins the posterior portions of the superior and middle frontal gyri (BA 8 and 9). The most ventral branch (SLF III) originates at the temporoparietal junction (BA 40) and ends at the inferior frontal gyrus (BA 44, 45 and 47). The cortical projections of these three branches overlap with nodes of the VAN and DAN [3] (Fig. 1B and C). The SLF I connects brain regions within the DAN. The SLF II connects parietal regions of the VAN with the DAN’s prefrontal regions, allowing these two networks to communicate. The SLF III connects regions within the VAN network. In most subjects, these fibres are arranged in an asymmetric anatomical gradient, consistent with the functional asymmetry demonstrated in Corbetta and Shulman’s model [3]: the SLF III is larger on the right than the left, the SLF I is symmetric, and the SLF II tends to be larger in the right hemisphere [6].

2. Unilateral spatial neglect: from a focal cortical syndrome to a disconnection syndrome Unilateral spatial neglect (USN) is defined as ‘‘a failure to report, respond, or orient to stimuli that are presented contralateral to a brain lesion when this failure is not due to elementary sensory or motor disorders’’ [7]. Signs of neglect can occasionally develop following a left hemispheric lesion, but are far more common, severe and long-lasting after a right hemispheric lesion, causing patients’ inability to consider events that occur in the left side of body or external space (contralateral to lesion). It is now generally accepted that 85% of patients with right hemispheric lesions have signs of neglect in the subacute phase, with moderate to severe signs in 36.2% of cases [8]. 2.1. Lesion sites Ischaemic or haemorrhagic strokes in the right perisylvian regions appear to be the main trigger for the development of neglect. Nevertheless, neglect can also occur following a stroke in the territories of the anterior cerebral artery [9] or of the posterior

Please cite this article in press as: Lunven M, Bartolomeo P. Attention and spatial cognition: Neural and anatomical substrates of visual neglect. Ann Phys Rehabil Med (2016), http://dx.doi.org/10.1016/j.rehab.2016.01.004

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cerebral artery [10]. Moreover, signs of neglect have also been described after traumatic brain injury [11], brain tumours [12], neurodegenerative diseases [13] and even demyelinating diseases (multiple sclerosis) [14]. As already mentioned, despite a strong association with right hemisphere lesions, neglect can also occur after left hemisphere lesions [15]. A growing number of studies have been published concerning the anatomical sites lesioned in neglect (approximately 80 studies listed in a recent meta-analysis [16]). Many studies highlight the importance of lesions in the right posterior parietal lobe, particularly the temporoparietal junction, including portions of the angular and supramarginal gyri and the posterior part of the superior temporal gyrus [17–19]. A distinction has been proposed concerning the involvement of the posterior parietal lobe: while lesions to the inferior parietal lobule–particularly the supramarginal gyrus–would be related to USN, those affecting the superior parietal lobule would instead be associated with difficulties in visuomotor integration (optic ataxia) [19]. Later on, a study performed in patients who had suffered a stroke in the territory of the middle cerebral artery reported the angular gyrus in the lateral surface of the inferior parietal lobule as the critical lesion site for USN [18]. According to the authors, damage to the angular gyrus determines USN because of the role of this region in maintaining attention on spatial locations. However, a German team challenged the association between parietal lesions and USN, by reporting that the maximum lesion superimposition in spatial neglect patients was located at the superior temporal gyrus, particularly when no visual field deficits are present [20]. They explained their findings by the fact that this region is located at the junction between two visual processing networks, the ‘‘where’’ pathway and the ‘‘what’’ pathway. This region receives multisensory inputs from the two pathways, and thus represents a site of multimodal sensory convergence. However, not every study has found this region to be involved [21]. Moreover, signs of neglect can also be found following lesions in the inferior frontal gyrus (premotor cortex) [22]. Damage in this region has been related to poor performance on target cancellation tests (as opposed to line bisection tests). This suggests that these lesions induce specific challenges in focusing attention during visual exploration tasks towards the side contralateral to the lesion when the visual environment is information-rich. In patients with lesions confined to the right frontal lobe, the degree of USN was higher when more distractors were presented during the target cancellation tests [22]. The frontal lobe may play a specific role in selecting relevant visual information and rejecting non-relevant information. Other studies have implicated subcortical lesions in areas such as the thalamus [19,23], putamen, caudate nucleus and pulvinar [24], insula or basal ganglia [19,24]. These lesions would lead to dysfunction in the parietal and frontal cortical areas due to diaschisis. The commonly reported lesions sites can be superimposed to the attentional networks described by Corbetta et al., and to the SLF II-III cortical projections (Fig. 1 B–D). According to Corbetta et al., neglect is the result of VAN lesions. These lesions induce functional changes in the DAN (anatomically intact), which are the origin of USN development. These authors performed functional MRI in 11 patients showing signs of spatial neglect in the subacute phase (4 weeks poststroke) [25]. During a spatial attention orientation task, compared to healthy controls, these patients had generalised cortical hypoactivation in the two hemispheres, which was more pronounced in the right hemisphere. An analysis of the patients’ lesions showed that most patients had lesions in the VAN, while the DAN was intact. There was also an imbalance in the functional activity between the two DANs, particularly at the level of the right and left dorsal parietal regions. The DAN’s functional alteration by the VAN would act as a short-circuit that would be at the origin of a lack of voluntary exploration of the left half-field. The same team

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also suggested that the middle frontal gyrus may be the common area where the two networks communicate [26]. Finally, a recent meta-analysis [16] has provided evidence that various signs of USN can occur after damage to a multitude of cortical sites over the entire lateral surface of the right hemisphere. This suggests that beyond pure cortical damage being associated with USN, network dysfunction induced by damage to white matter tracts could more specifically explain why this syndrome develops [27]. 2.2. Summary of lesion patterns associated with various neglect profiles Since Binder et al.’s seminal work [28], there have been attempts to associate the behavioural heterogeneity of neglect with distinct anatomical correlates. In their study, patients with a right deviation in line bisection tasks had posterior lesions, while those with cancellation deficits had more anterior or subcortical lesions. These results were confirmed in a more recent study of 80 patients with right-sided stroke [29]. These patients performed a series of paper-and-pencil tests in order to study the different performance patterns from an anatomical point of view. Lesions of the right inferior parietal lobule were associated with a perceptual/ visuospatial component of neglect (including line bisection and reading), while more anterior lesions involving the right inferior frontal gyrus and anterior dorsolateral prefrontal cortex, along with the posterior part of the middle frontal gyrus, were related to an exploratory/visuomotor component (target cancellation tasks). Finally, lesions in the temporal lobe were associated with allocentric/object-centred neglect (i.e., neglect for the left part of objects independent of their position in space). The above-mentioned meta-analysis of 20 studies [16] reported that neglect during target cancellation tasks was associated with a network distributed throughout the dorsolateral and parietal prefrontal areas, while line bisection shifts were related to more posterior damage, including the inferior and superior parietal lobules. Nevertheless, both tasks were associated with lesions of the posterior portion of the angular gyrus. Allocentric neglect was associated with more ventral lesions, including the parahippocampal gyrus, while egocentric neglect (the typical neglect for leftsided objects with respect to the patient’s midsagittal plane) was associated with more dorsal lesions in the premotor cortex [29,30]. The lesions sites associated with various behavioural patterns are shown in Fig. 2. Different lesion patterns have also been found for neglect for extrapersonal object vs. personal neglect (i.e., neglect for the patients’ own left body parts) [31]. Extrapersonal neglect (evaluated through target cancellation, line bisection, reading and visual illusion tasks) was associated with lesions of the frontal lobe (inferior precentral and middle inferior gyri), the anterior portion and middle of the superior temporal gyrus and of the sublenticular part of the corona radiata in the temporal lobe. According to these authors, this lesion pattern would be related to the VAN network [3], implicated in the mobilisation of allocations for exogenous attention and reorientation of attention in space. Personal neglect was associated with lesions of the parietal lobe (supramarginal and postcentral gyri), the posterior portion of the superior temporal gyrus, the sublenticular part of the corona radiata and the semi-oval centre of the parietal lobe. 2.3. Dysfunction of intrahemispheric networks: frontoparietal disconnections As mentioned above, researchers have also looked into the role of brain connections in USN. Two studies on stroke patients suggested that neglect was associated with white matter damage

Please cite this article in press as: Lunven M, Bartolomeo P. Attention and spatial cognition: Neural and anatomical substrates of visual neglect. Ann Phys Rehabil Med (2016), http://dx.doi.org/10.1016/j.rehab.2016.01.004

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Fig. 3. White matter tracts and spatial neglect. Visualisation of the inferior longitudinal fasciculus (ILF, in green) and of the inferior frontoparietal fasciculus (IFOF).

Fig. 2. Anatomical–clinical patterns of visuospatial neglect [16]. Cortical areas associated with different deficits in neglect tests. Purple spheres: neglect tested with line bisection tasks; red spheres: neglect tested with cancellation tasks; green spheres: neglect tested with a combination of tasks; blue spheres: allocentric neglect; black spheres: personal neglect. Reproduced from Frontiers in Human Neuroscience 6;78:2012 ‘‘Is there a critical lesion site for unilateral spatial neglect? A meta-analysis using activation likelihood estimation’’ by P. Molenberghs, M.V. Sale and J.B. Mattingley.

in frontoparietal networks [17,32]. Advances in neuroimaging methods have allowed innovative research into the injury sites to be carried out. One example is our team’s work into the clinical manifestations of neglect during intracerebral electric stimulation in patients being operated for low-grade glioma [33]. To avoid cognitive sequelae after tumour excision, the patient is awakened during the operation. This allows the neurosurgeon to temporarily inactivate regions of the brain using electric stimulation, while the patients perform neuropsychological tasks. If the patient shows decreased performance in a given task, the neurosurgeon will not remove this region, so as to maintain function. Using this method, the performance of two patients was evaluated during a line bisection task. The largest deviations occurred when the frontoparietal fibres were inactivated, namely SLF II, suggesting that their damage plays a predominant role in the manifestation of neglect (see [34] for recent confirmatory evidence). The case of a neglect patient with transient left-sided neglect after a vascular lesion affecting only the white matter has also been described [35]. By using tractography, the authors showed that the SLF was damaged. Two recent metaanalysis studies also highlight the major contribution of the white matter to the development of neglect in stroke patients [16,36]. The most extensively damaged region during the development of neglect was again the white matter in the SLF. Together, these data suggest that beyond cortical damage, neglect can be viewed as a disconnection syndrome that creates hypo-functioning of a large network of connected brain areas, particularly in the right frontoparietal network [27]. Other association tracts have been linked with USN, such as the inferior fronto-occipital fasciculus (IFOF) [37] and the inferior longitudinal fasciculus (ILF) [10] (Fig. 3). The IFOF is the only direct connection between the frontal and occipital areas [38]. Damage in

this area could contribute to the occurrence of neglect due to alteration of the top-down modulation of the frontal cortex on visual areas [37]. As for the ILF, it connects the temporal lobe with the occipital areas [38]. A study of neglect patients who had suffered a posterior cerebral artery stroke has shown that maximum overlap of their lesions were located in the white matter, in an area consistent with the ILF’s trajectory [10] (but also with that of the IFOF). 2.4. Involvement of the interhemispheric network: callosal neglect Although after a surgical section of the corpus callosum patients do not usually show neglect signs [39], evidence suggests that callosotomy can result in left neglect in some cases [40]. For example, following the rupture of an aneurysm of the anterior communicating artery with involvement of the corpus callosum, a patient was described as having severe neglect on target cancellation tasks with the right hand [41]. In recent years, a potential involvement of disconnection of the posterior portion (splenium) of the corpus callosum in the development, severity and persistence of neglect after right hemisphere damage has been proposed. For example, the severity of neglect in the subacute phase was associated with damage of the splenial white matter after middle cerebral artery stroke [42]. Neglect can also occur following a posterior cerebral artery stroke that involves ventrocaudal brain regions but spares the frontoparietal networks. In these cases, data tend to show that interhemispheric disconnection is involved in the development of USN [43]. A study of 45 patients who had suffered a posterior cerebral artery stroke [44] found a relationship between signs of neglect and occipital and splenial lesions. These findings were later confirmed by other research teams [10,45]. In fact, the presence of a visual field deficit and an occipital lesion without splenium involvement is not sufficient to trigger USN. A study in monkeys [46] led to the proposal that that neglect can occur because of splenial disconnection associated with hemianopia. This would prevent visual inputs from the left visual field from having access to the left hemisphere. As a consequence, it would be impossible to explore the left-sided field. We have recently described the case of a patient suffering with neglect following a right posterior cerebral artery stroke (which also caused lateral homonymous hemianopia) with involvement of the splenium of the corpus callosum [43]. When this patient performed target cancellation tasks with her right hand, the neglect was severe, with many left-sided omissions. Conversely, her performance was normal with the left hand. Reconstruction of the frontoparietal and

Please cite this article in press as: Lunven M, Bartolomeo P. Attention and spatial cognition: Neural and anatomical substrates of visual neglect. Ann Phys Rehabil Med (2016), http://dx.doi.org/10.1016/j.rehab.2016.01.004

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interhemispheric networks showed relative preservation of the SLF; however, the occipital regions in the two hemispheres were no longer connected between them. We concluded that direct activation of the right frontoparietal network (when using the left hand) allowed her to explore the left hemispace, thus leading to disappearance of neglect. Splenium damage has also been linked to representation neglect, i.e. impaired description from memory of the left side known places [47,48]. However, another study [45] found only selective involvement of the visual modality, with no representational neglect, in two patients with direct damage to the splenium, in one case, and to the occipital fibres in the forceps major in the other case. 2.5. Role of the left hemisphere in neglect: compensation or poor adaptation? It has been proposed that USN is related to increased activity in the left, healthy hemisphere. According to Kinsbourne’s hypothesis [49], pathological hyperactivity in the left hemisphere would direct attention towards the right side and cause neglect of the left side. Supporting evidence for this model came from functional MRI findings showing that recovery from neglect is associated with normalisation of the interhemispheric imbalance, particularly by restoring the coherence between brain activity in the homologous regions of the parietal cortex [25,26]. Moreover, in acute stroke patients neglect can subside after a second (subsequent) lesion in the healthy left hemisphere [50] or after transcranial magnetic stimulation sessions interfering with left hemisphere activity [51]. A magnetoencephalography study performed by our team in neglect patients also showed that left frontal activity selectively preceded omissions of left-sided targets [52]. Koch et al. performed various studies with transcranial magnetic stimulation to better understand the events at the origin of this interhemispheric imbalance. They found that even at rest, the connection between the posterior parietal cortex and the frontal motor cortex (M1) in the left hemisphere was specifically hyperexcitable in patients with neglect [53]. Thus, right hemispheric lesions in these patients induced changes in the corticocortical excitability of specific areas and of circuits in the non-injured hemisphere. This same team also showed that this hyperexcitability in the left hemisphere of patients with neglect could be explained by a physiological asymmetry in interhemispheric communications: the right, but not the left, posterior parietal cortex, has a strong inhibitory activity over the contralateral homologous region [54]. This effect could be supported by fibres running in the posterior portion of the corpus callosum (portions IV and V). According to these authors, this is an important mechanism underlying the asymmetry in visuospatial functions. However, other data suggest that the interhemispheric competition model is not sufficient to explain the development of USN. Heilman and Valenstein [7] described the case of a patient with signs of USN after a corpus callosum lesion. She had an older right hemisphere lesion. The authors noted that the interhemispheric competition model assumes that neglect occurs following release of the left hemisphere after removal of the inhibition exerted by the right hemisphere [25,49,55]. The model would have predicted development of neglect after the initial right-sided lesion, but the subsequent callosal lesion should have reduced neglect, by interrupting the inhibitory activity of the left hemisphere over the right hemisphere. The alternative hypothesis suggests that the bias towards the lesion side would be induced by hypoactivation of the damaged hemisphere [7]. In this case, cutting the corpus callosum would have no beneficial effect. On the contrary, it would increase rather than decrease the USN, as described by Heilman and Valenstein. The healthy hemisphere should be able to compensate for the damaged hemisphere [27].

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Moreover, in the acute phase of a vascular stroke, relative hyperactivation of the left parietal cortex does not seem to be an exclusive feature of neglect. In fact, it can also occur in patients without neglect [56]. Thus, transient left hyperactivity could be a simple by-product of the structural lesion in the right hemisphere. Conversely, the attentional regions in the left hemisphere could provide functional compensation when the right hemisphere is damaged. These data are consistent with work showing that the healthy hemisphere can have a compensatory role, as is the case for motor recovery after stroke [57]. The recovery from neglect also seems correlated with restoration of the basal metabolism, not only in structurally healthy regions of the right hemisphere, but also in the left hemisphere [58]. A recent functional MRI study of patients with neglect before and after they participated in a prism adaptation protocol showed that the BOLD signal was increased during therapy-induced recovery from neglect, not only in the right frontoparietal network, but also in the homologous structures of the left hemisphere [59]. We have recently contributed to this debate by performing a longitudinal study of 45 patients who suffered a middle cerebral artery stroke. We found that USN persistence in the chronic phase (more than 1 year after the stroke) was associated with signs of splenial disconnection [60]. This evidence suggests that the left hemisphere is not able to compensate for the patients’ deficits in the absence of efficient inter-hemispheric communication. Instead, neglect recovery might be achieved by improving the exchange capacity between the two hemispheres, particularly in their parietal and occipital regions. To conclude, attentional processes are supported by frontoparietal functional and anatomical networks, with partial lateralisation to the right hemisphere. Damage to these networks can trigger the appearance of neglect, with a dramatic deficit of awareness for events occurring on the side contralateral to the lesion. These signs can become chronic if the posterior portions of the two hemispheres cannot exchange information through the corpus callosum. This obstacle to communication between the two hemispheres can prevent the left hemisphere from compensating for the deficits brought on by damage in the right hemisphere. Neglect is thus better understood as the result of disconnection between interconnected areas, rather than of focal cortical damage. This hypothesis leaves open the possibility of improving behavioural deficits in patients using rehabilitation methods that focus on exchanging information between the two hemispheres.

Disclosure of interest The authors declare that they have no competing interest.

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Please cite this article in press as: Lunven M, Bartolomeo P. Attention and spatial cognition: Neural and anatomical substrates of visual neglect. Ann Phys Rehabil Med (2016), http://dx.doi.org/10.1016/j.rehab.2016.01.004

Attention and spatial cognition: Neural and anatomical substrates of visual neglect.

Unilateral spatial neglect (USN) is a neurological disorder often observed following damage to the right cerebral hemisphere. Patients with USN are no...
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