Recurrent supratentorial stroke with ipsilateral hemiplegia

INTRODUCTION

A supratentorial lesion generally leads to motor impairments on the contralateral side, as most corticospinal (CS) fibers decussate at the medulla. Ipsilateral hemiplegia is a rare clinical presentation, reported in approximately 0.17% of patients with ischemic stroke.^[1] This atypical manifestation may result from congenital uncrossed CS tracts, bilateral motor cortical networks, or cortical reorganization following prior contralateral stroke.^[2] Most frequently occurring in patients with prior contralateral stroke, advancements in functional neuroimaging and tractography over the past two decades have provided a better understanding of the significant role of uncrossed CS pathways and the remodeling of motor pathways following injury, which may contribute to the subsequent development of ipsilateral hemiplegia.^[1,3]

We present a case of ipsilateral hemiplegia associated with recurrent supratentorial infarcts and discuss the underlying mechanisms, supported by current clinical and basic neuroscience literature.

CASE REPORT

A 68-year-old right-handed woman had a medical history of hypertension and a prior ischemic stroke 3 years earlier, which had resulted in right hemiplegia with residual motor deficits. Despite these sequelae, she retained functional independence, with a modified Rankin Scale (mRS) score of 1. On November 28, 2024, she presented with a sudden alteration in consciousness and marked motor deficits on the right side, following a 72-h episode of severe diffuse headaches. She was swiftly transported to an urban medical facility, where her condition improved within 3 h, leading to a restoration of consciousness and complete recovery of motor function within 48 h. Brain computed tomography (CT) scan [Figure 1] conducted 3 days post-onset of altered consciousness identified multiple infarcts of varying ages, with the most recent located on the same side as the motor impairment, and no lesions detected in the contralateral hemisphere, necessitating her transfer to a neurology department for advanced care. During the transfer, the patient experienced deterioration in her right-sided motor function. Upon admission, the initial neurological evaluation revealed confusion, right-sided flaccid hemiplegia (3/5), right central facial paralysis with an extensor plantar reflex, and spastic dysarthria. The National Institutes of Health Stroke Scale (NIHSS) was 8, and the mRS was assessed at 4. In addition, marked orbital asymmetry was observed, accompanied by microblepharitis and an elevated right lower eyelid, which obscured the visibility of the right ocular globe.

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Figure 1:

Brain computed tomography (CT) scan. Axial non-contrast CT images obtained three days after the onset of altered consciousness. (a) Shows both the recent right superficial sylvian infarct (white thin arrow) and a chronic left pontine infarct (white short thick arrow). (b) Shows the extension of the recent right superficial sylvian infarct (white thin arrow)

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Magnetic resonance imaging (MRI) conducted approximately 20 days after the onset of vigilance impairment and 72 h after the exacerbation of motor deficits in the right hemibody revealed multiple infarcts of varying ages [Table 1]. This included two supratentorial infarcts: a sub-acute infarct located in the superficial territory of the right middle cerebral artery (MCA), an acute infarct in the deep territory of the anterior cerebral artery, and a chronic infarct in the left pons [Figure 2]. Cerebral CT angiogram indicated diffuse atherosclerosis accompanied by vascular insufficiency in the territory of the right MCA [Figure 2]. Orbital MRI demonstrated severe microphthalmia and hypoplasia of the optic nerve in the intraorbital segment [Figure 3]. The patient’s recovery was favorable under rehabilitation, leading to discharge after 16 days of hospitalization with an mRS score of 1 and mini-mental state examination score of 18.

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Figure 2:

Brain magnetic resonance imaging (MRI) and angiography. Brain MRI was performed approximately three weeks after the onset of impaired consciousness and 48 hours after the re-worsening of the right hemibody motor deficit, revealing multiple ischemic lesions of different ages. A late subacute hemorrhagic infarction in the superficial right MCA territory (white arrows) appears as (a) hypointensity on axial T1-weighted imaging(white arrow), (b) post-gadolinium T1 hyperintensity suggestive of blood–brain barrier disruption(white arrow), (c) hyperintensity on axial T2-FLAIR(white arrow), and (d) hypointensity on gradient echo sequences indicating hemorrhagic changes(white arrow). An acute infarction in the deep ACA territory (medial lenticulostriate branches, blue arrows) is identified by (e) hyperintensity on DWI (blue arrow) and (f) hypointensity on ADC, consistent with restricted diffusion(blue arrow). (g, h) MR and CT angiography demonstrate vascular paucity in the corresponding territory (red triangles). A chronic infarction involving the anteromedial and anterolateral pontine territories (yellow arrows) is demonstrated as (i) hypointensity on sagittal T1-weighted imaging(yellow arrow), (j) hyperintensity on axial T2-weighted imaging(yellow arrow), and (k) hyperintensity on ADC mapping, with no corresponding abnormalities on DWI, consistent with a porencephalic sequela(yellow arrow).

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Figure 3:

Orbital MRI (a and b) Axial spin-echo T1-weighted and T2-FLAIR sequences demonstrate microphtalmia of the left eye (red arrow), associated with hypoplasia of the intraorbital segment of the ipsilateral optic nerve (white arrow).

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DISCUSSION

Ipsilateral hemiplegia is rare and raises significant neuroanatomical and clinical concerns, particularly in the acute phase. To the best of our knowledge, 43 cases have been documented since its initial description in 1992.^[4-8] In a prospective study spanning 11 years involving 8,360 patients who experienced ischemic stroke, only 14 individuals exhibited ipsilateral hemiplegia (0.17%).^[1] Furthermore, 13 of these 14 patients (92.9%) had a history of contralateral stroke, similar to our patient.^[1] Three main pathophysiological mechanisms have been proposed [Figure 4], supported by functional MRI, tractography, and evoked potentials: (1) Functional reorganization with recruitment of ipsilateral CS fibers, (2) anomalies of pyramidal decussation, and (3) injury to the supplementary motor areas (SMAs).

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Figure 4:

Putative pathophysiological mechanisms of ipsilateral hemiplegia in supratentorial stroke this diagram outlines the three main hypothesized mechanisms explaining ipsilateral hemiplegia after supratentorial stroke: (1) Functional reorganization with progressive recruitment of ipsilateral corticospinal tract fibers following prior contralateral lesions, (2) Anomalies of pyramidal decussation, including (2a) absence of decussation, (2b) partial decussation and/or predominance of uncrossed corticospinal fibers, and (2c) double decussation. These anomalies are frequently associated with other structural neurodevelopmental anomalies, particularly those affecting the posterior cranial fossa; (3) Injuries and functional alterations of the supplementary motor areas. These mechanisms may coexist and vary depending on lesion topography, patient age, stroke subtype, and genetic factors.

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Anomalies of pyramidal decussation may involve the absence of decussation,^[9-11] a predominance of uncrossed fibers,^[4,12,13] or ipsilateral fibers with a double decussation.^[14] Although this explanation appears to be the most plausible, it has only been observed in a limited number of patients^[5,9-11] and is often associated with other developmental anomalies of the nervous system,^[15] particularly those affecting the posterior cranial fossa, such as occipital encephaloceles, Dandy–Walker malformations, and Joubert syndrome, extensive brainstem malformations such as Moebius syndrome, cellular proliferation anomalies, and axonal guidance mechanism issues.^[4,15] However, only five cases of stroke associated with contralateral hemiplegia, linked to evident anomalies in decussation, and associated with malformations of the central nervous system, have been reported^[9-12,16] [Table 2], including agenesis of the corpus callosum, hypoplasia of the brainstem, anomalies of the medulla oblongata, and progressive scoliosis observed in three reported cases,^[9,10,12] one of which was associated with a mutation in the axonal guidance receptor gene ROBO39.^[9] Our patient exhibited severe unilateral microphthalmia accompanied by optic nerve hypoplasia [Figure 3]. Ku et al. fortuitously discovered a complete absence of decussation of the CS tracts during intraoperative monitoring while performing a microsurgical resection of a vestibular schwannoma.^[14] This case illustrates that the absence of pyramidal decussation can also occur in certain adults without malformations, and that a hemispheric stroke in these patients may only affect the ipsilateral limb.^[5]

Functional reorganization with the recruitment of ipsilateral fibers has been identified as the primary mechanism, highlighting the importance of contralateral anterior lesions and the behavior of cortical fibers in their functional lateralization.^[5] Of the 43 recorded cases from 1992 to 2023, 26 had a history of contralateral stroke, similar to our patient.^[4-8] Following an anterior lesion of the contralateral crossing fibers, the uncrossed ipsilateral fibers are progressively mobilized to restore activity in the paretic limbs.^[5] Over time, a substantial portion of paretic limb function is regained owing to the predominant activity of uncrossed ipsilateral fibers.^[5,17] The occurrence of a second lesion affecting these uncrossed ipsilateral fibers results in exacerbated ipsilateral paresis.^[4,17] Reported lesions most frequently involve the corona radiata, internal capsule, putamen, pons, and globus pallidus.^[4-8] In light of prior contralateral brain lesions, the right hemiplegia observed in our patient following a right hemispheric stroke may be attributed to compensatory motor reorganization involving the uncrossed ipsilateral CS pathways. However, given the presence of congenital microphthalmia, the possibility of an associated abnormal decussation cannot be excluded. Therefore, additional mechanisms may be involved, and only advanced functional imaging and tractography can provide further insights.

The functional contributions of SMAs remain only partially elucidated. It has been suggested that damage to the precentral insular cortex, cingulate sulcus, prefrontal cortex, and corpus callosum may lead to impairment of SMAs, which could cause ipsilateral hemiparesis.^[18,19] In addition, lesions in the ipsilateral extrapyramidal tract, particularly in the corticorubral tract, have been proposed as potential underlying mechanisms. In our patient, no supplementary motor regions were affected during the third stroke episode.^[20]

Assessing the lateralization of pyramidal tract fibers in patients requiring urgent intervention remains a challenging task.^[5] The risk lies in overlooking the clinico-anatomical variations and assuming that the patient may have an acute contralateral lacunar infarct that is not yet visible on imaging, whereas the extensive ipsilateral infarct may have gone unnoticed because of early reperfusion through collateral circulation.^[5] However, the management of acute strokes resulting from proximal occlusion differs from that associated with distal occlusions or lacunar strokes, which could lead to inappropriate decisions, particularly when these patients are excluded from mechanical thrombectomy.^[5] We did not face this challenge because the patient was in the late phase and was not eligible for any reperfusion treatment.

Ipsilateral hemiplegia resulting from a stroke requires tailored rehabilitative avenues that distinguish the dominant role of the contralateral sensorimotor cortex during the subacute phase and acknowledge the subsequent chronic role of the ipsilaterally affected hemisphere.^[21] The compensatory potential of the ipsilateral secondary motor areas, typically derived from mirrored movements,^[22,23] also indicates that impairing these areas through modulation may facilitate functional recovery.^[24] Targeted modulation of these areas through neuromodulation or specific motor training may optimize rehabilitation outcomes.

CONCLUSION

Ipsilateral hemiparesis is uncommon in patients with a hemispheric stroke. The underlying mechanism, primarily observed, involves cortical organization and recruitment of ipsilateral pyramidal fibers, although it remains partially understood. Neurological malformations may be present in patients with ipsilateral hemiplegia due to a hemispheric stroke. The recovery mechanism in these patients is intricate and entails hemispheric reorganization. It is crucial to consider the possibility of ipsilateral hemiplegia during the acute phase of stroke to make appropriate emergency decisions and tailor rehabilitation for these patients in the later stages.