Spinal cord infarction in children: Can gymnastics be a cause?

Abstract

INTRODUCTION:

Spinal cord infarction (SCI) in children is rare and difficult to diagnose. Fibrocartilaginous embolism (FCE) is probably the underlying cause for some unexplained cases of spinal cord infarcts. Abrupt back pain followed by a progressive syndrome of myelopathy appears to be the typical presentation, with a close temporal relationship between the onset of symptoms and preceding minor trauma. Supportive care and rehabilitation are essential in the treatment of children with SCI.

CASE REPORT:

A previously healthy 12-year-old girl who practiced acrobatic gymnastics was admitted to a rehabilitation centre 14 days after being diagnosed with an acute anterior SCI with no identified cause. Sensory modality of pin prick and light touch were impaired, with the former more significantly affected. She was not able to run and had difficulty on monopodal standing and performing motor sequencing. Additionally, she mentioned ineffective cough along with flatus incontinence and normal bladder function. After a 4-week multidisciplinary rehabilitation program her neurologic deficits improved.

DISCUSSION:

Given the patient’s age and clinical presentation, a literature review led to the consideration of FCE as the most likely definitive diagnosis. It should be recognized as a cause of SCI especially in those involved in sport activities, even if previous trauma is denied.

1. Introduction

Spinal cord infarction (SCI) in children is rare and difficult to diagnose [1, 2, 3, 4]. The most frequent causes are parainfectious vasculopathies, aortic, cardiac or spinal surgery and minor trauma complicated by fibrocartilaginous embolus [2]. The definitive diagnosis of fibrocartilaginous embolism (FCE) is made by histological examination [2]. Therefore, FCE is likely the underlying etiology of some unexplained cases of SCI [5] and of some syndromes previously described by the literature, namely Spinal Cord Injury without Radiographic Abnormality (SCIWORA) and Surfer’s Myelopathy (SM).

Accurate diagnosis of SCI in children requires assessment of the entire spine through T2 weighted magnetic resonance imaging (MRI) with axial and sagittal views as well as diffusion-weighted imaging to document ischemia [1, 6, 7].

Supportive care and rehabilitation programs are key in the treatment of children with SCI [1, 7]. Management depends on the etiology but primarily targets the prevention of complications and improvement of quality of life with pharmacological and physical therapy [4, 8]. Patients must remain hemodynamically stable with appropriate mean arterial blood pressure [7]. Pain control, high-dose steroids, and anticoagulation have been discussed but their efficacy remains unclear [7, 10]. Anticoagulation with low molecular weight heparin and aspirin improved outcomes in patients with thrombotic disorders and high-dose corticosteroids have been shown to improve long-term outcomes for patients with traumatic spinal cord infarcts [4]. However, their role in spinal cord ischemia due to FCE is unclear [4].

Prognosis depends on the extent and type of injury, level of spinal cord damage, American Spinal Injury Association (ASIA) score on patient admission, age, early identification and reversal of ischemia and follow-up with intensive physical therapy and medical support [1, 4, 9, 11, 12].

According to a recent paper [13], there have been 68 cases to-date in the literature. We describe one more clinically diagnosed case.

2. Case report

A previously healthy 12-year-old girl presented to the emergency department with sudden onset of intense midthoracic back pain that awakened her. During observation, she reported the onset of numbness and weakness of the left lower limb. Bladder and bowel changes were denied. History of previous infectious event, head injury, chest or abdominal trauma was not reported. She had started practicing acrobatic gymnastics 3 months earlier, 3 days/week, with multiple trivial falls on her knees. On examination, she was apyretic and hemodynamically stable. Neurological examination revealed an unsteady gait, flaccid paraparesis [grading 4/5 on Medical Research Council (MRC) scale], normal deep tendon reflexes and impaired sensitivity to light touch of her lower limbs. Meningeal irritation signs were absent. Laboratory investigation showed no evidence of infection, autoimmune, inflammatory or coagulation abnormality. Electrocardiogram and chest, cervical, thoracic and lumbar spine radiographs were unremarkable. Thoracic and lumbar spine computed tomography (CT) and echocardiography revealed no alterations. Diffusion weighted MRI (DWI) 24 hours after symptom onset showed an increased sign in the thoracic cord extending from T2 to T3 and from T6 to T7 affecting the anterior portion and the right side of the cord predominantly with no gadolinium enhancement and with restricted diffusion, consistent with an acute ischaemic lesion. The patient was medicated with acetylsalicylic acid and after 14 days she was transferred to a rehabilitation centre.

On physical examination, key muscle function corresponding to C5-T1 and L2-S1 myotomes and deep tendon reflexes were normal. Left Babinsky sign was present. The patient presented with bilateral plantar flexor spasticity [grade 1 in Modified Ashworth Scale (MAS)] with absent ankle clonus. Sensory modality of pin prick and light touch of her lower limbs were impaired, with the former more significantly affected. Proprioception was intact. A digital rectal examination revealed normal perianal sensation with diminished anal tone, intact deep anal pressure and diminished voluntary anal contraction. Anal reflex was present. Patient was classified as having a paraplegia AIS D neurologic level of lesion (NLI) T5, according to ASIA scoring. She was able to independently perform all activities of daily living. However, balance was impaired. She was not able to run, and she had difficulty with monopodal standing and performing motor sequencing (such as assuming the standing position from kneeling position). Additionally, she mentioned ineffective cough along with flatus incontinence, but had normal bladder function.

The patient continued on acetylsalicylic acid and started an intensive and multimodal rehabilitation program in order to gain muscle strength (including pelvic floor musculature), improve balance and gait pattern, promote aerobic reconditioning and assess bowel and respiratory function. The program included physiotherapy, hydrotherapy, rehabilitation nursing and nutrition.

The patient was discharged after 4 weeks. She recovered from her motor impairments and bowel incontinence. However, she maintained the sensory impairment previously described. At discharge, recommendations included avoiding gymnastics and other impact activities until she had reassessment by Neurology and a new MRI.

3. Discussion

Known causes of SCI include both systemic (hypotension, cardiovascular emboli, hematological conditions associated with thrombosis and iatrogenic causes including heart surgery angiography) and local pathologies (demyelinating, infectious, hematological, autoimmune, vascular and neoplastic processes) [7]. Although not performed for our patient, spinal angiography may demonstrate the underlying etiology of the SCI such as vasospasm, vessel avulsion or vascular malformations [14, 15]. However, its use as a diagnostic tool is not well established in children [16]. Most of these causes were excluded. However, in the author’s opinion, a cerebral spinal fluid (CSF) examination should have been performed in order to exclude other causes of acute myelopathy, namely acute transverse myelitis.

Nontraumatic spinal cord injury diagnosis is challenging and for some children the etiology of SCI is unclear even after extensive workup [17]. The only risk factor identified was the beginning of gymnastics training with multiple trivial falls, shortly before symptom onset. No acute traumatic event was reported. Nevertheless, minor trauma has been associated with SCI [1].

A possible SCI etiology the authors considered was FCE. It is a rare but increasingly recognized cause of anterior spinal artery infarction in children, which occurs after minor trauma [4, 7, 10, 13, 16, 18, 19]. Inciting events include weightlifting, stooped posture, forced head movement, Valsalva maneuver and activities resulting in axial loading of the vertebral column [4, 8, 10, 20]. In a recent review [21], vigorous exercise was the most common trigger event.

The intervertebral disc and nucleus pulposus remain vascularized until late adolescence and share the same blood supply as the spinal cord [4, 6]. Axial loading of the spinal column results in retrograde flow and embolization of nucleus pulposus into the anterior radicular artery causing an anterior spinal artery stroke [4, 8, 10, 18, 21]. This seems to be the most plausible theory given the absence of disc herniation and vertebral anomalies (e.g., Schmorl nodes) on MRI in the majority of children with SCI [4, 21]. According to Quinn et al., transient increased intravertebral disc pressure is often triggered by minimal stresses [13]. Other mechanisms are traumatic injury of the annulus fibrosus (followed by extrusion of fragments of nucleus pulposus into the spinal arterial system), embolization of nucleus pulposus material through vertebral body venous sinusoids via Schmorl’s nodules, and injury to vertebral bodies and discs, given the anatomic contact between nucleus pulposus and vertebral body’s venous system [6]. Disc rupture may account for FCE in adults who have an avascular nucleus pulposus [4].

FCE shows a bimodal distribution with peaks in adolescence and late middle age [17, 21] with an average age of 14.6 years [10]. Female gender predominance is reported [10, 17, 21]. Cervical or thoracic regions are commonly affected, although it has been reported at all levels of the spinal cord [4, 8]. FCE typically presents with sudden severe neck and back pain, followed by progressive sensory and motor deficits in a pattern corresponding to an anterior spinal syndrome (which may be asymmetric), after a suggestive history of a minor traumatic event, including minor sport related falls [4, 8, 10, 11, 21]. Symptom onset is quite variable occurring either immediately after the inciting factor or with a delayed (from a few hours to a few weeks) presentation [4, 8, 10, 21].

Definitive diagnosis of FCE can only be made histologically [8, 19, 21]. However, clinical diagnosis is considered possible [21]. MRI is the mainstay of the diagnosis [10]. Typical findings on MRI include: spinal cord expansion with increased linear signal extending multiple spinal levels on T2 weighted imaging, without early contrast enhancement; restricted diffusion; and an owl’s eye pattern on axial images [4, 10, 21]. According to Reisner et al. [7] and Grilhoesl [6], DWI must be included in standard MRI of the spinal cord when SCI by FCE is considered. Emergent MRI scans may be normal [10] and should be repeated [6]. CSF analysis reveals no specific alterations and is often unremarkable [4, 20, 22].

FCE is one of the pathophysiological mechanisms proposed for SM, which is a rare, nontraumatic spinal cord injury associated with hyperextension of the back [9, 12]. The clinical syndrome begins with nontraumatic back pain which evolves to paraparesis/paraplegia, sensory loss and bladder dysfunction [9, 12]. Although initially described in young surfers, activities such as gymnastics, cheerleading, acrobatics, yoga, Pilates, ballet and weight lifting may cause SM [9, 12, 15]. Some of these have also been associated with pediatric cases of FCE [4, 7, 22]. Gandhi et al. [12] report an average age of 25 years with the youngest reported case being a 7-year-old girl. Other SM pediatric cases have been described [9, 15, 23].

SM is hypothesized to be caused by hyperextension of the spine leading to dynamic compression, vasospasm and thrombotic infarction [12]. Other suggested mechanisms include avulsion of perforating vessels and FCE [12, 15]. Spinal hyperextension preceding SM may be sufficient to cause FCE and therefore this etiology cannot be excluded [15]. DWI sequencing in MRI reveals T2 hyperintensity and focal-restricted diffusion, consistent with SCI [9, 12, 15].

Before the advent of MRI, SCIWORA was diagnosed in children who developed paralysis immediately or following a latent period of 30 minutes to 4 days after trauma, with no evidence of skeletal injury on plain radiographs and CT [3, 16, 24]. This is not a definitive diagnosis nowadays given the improvement in imaging modalities [6]. Nevertheless, those with no lesions on neuroimaging should be classified as SCI without neuroimaging abnormality (SCIWNA) [25]. A proposed mechanism for SCIWORA was that the inherent elasticity of the juvenile spine which permits self-reducing but significant intersegmental displacements when subjected to flexion, extension and distraction forces, would result in reactive vasospasm or compression of vertebral and/or spinal arteries, leading to SCI [1, 3, 24, 25]. Hyperextension as a proposed mechanism for SCI is similar to that associated with SM.

Therefore, FCE seems to be a plausible mechanism underlying some of the SCI syndromes previously described in the literature, especially among children and young adults engaging in sport activities, likely due to their inherent spine elasticity and disc vascularization. This has also been proposed by Albuja et al. [15]. Consequently, FCE may be more common than presumed [6].

Authors assumed that the patient’s gymnastic practice may have led to spinal cord vascular compromise. Attending to her age, clinical presentation (with back pain as the initial presenting symptom followed by rapid and progressive neurologic deficit corresponding to an anterior spinal syndrome), absence of prodromal illness and MRI findings, a literature review led to the consideration of FCE of the spinal cord as the most likely final clinical diagnosis.

Integration into a comprehensive multimodal rehabilitation program is of utmost importance in the evaluation and treatment of neuromotor and functional deficits and to improve the chance of a more favorable long-term outcome [4, 10, 11], as shown in the present case report. Although FCE was initially associated with poor recovery, many patients improve [4, 7, 10], particularly those with lower spinal cord lesions and subjected to intensive physical therapy [4, 10]. Complete recovery has also been described [10], including one report of a pediatric patient [4]. Indeed, rehabilitation and the presence of an incomplete deficit were associated with favorable outcomes in children [4, 7]. In our case, we believe that admission ASIA score evaluation, initial neurologic assessment, prompt medical treatment and early integration into an intensive rehabilitation program contributed to the patient’s good recovery with only moderate sensory deficits remaining. Persistence of altered sensation has been described in similar cases [3, 4].

Regarding future gymnastics training, it seems reasonable that FCE risk diminishes over time, since spinal flexibility and disc vascularization decline with age [15]. Also, preventive measures described for SM [12] may be suitable and should be promoted among children engaging in sport activities. Those include a proper warm-up, core strength exercises and back stretching, in order to counteract the inherent flexibility of the juvenile spine. We also advise children to avoid Valsalva maneuver during exercise effort phase.

In conclusion, SCI is a rare cause of spinal cord injury in children and once demonstrated, FCE must be considered, especially in those involved in sport activities, even if previous trauma is denied. This case places greater importance in recognizing FCE by emergency medicine physicians as more children become involved in competitive sports. Furthermore, a definitive diagnosis reassures the patient and caregivers and allows for a more targeted rehabilitation program and proper recommendations.