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Köksal V, Osama M, Alvi M A. Non-traumatic Causes of Brown-sequard Syndrome: A Case Series and Clinical Update With Systematic Review. Iran J Neurosurg 2021; 7 (2) :92-106
URL: http://irjns.org/article-1-263-en.html
1- Department of Neurosurgery, Samsun Health Practices and Research Center, University of Samsun, Samsun, Turkey , vanerkoksal@hotmail.com
2- Faculty of Medicine, Zagazig University, Zagazig, Egypt
3- Mayo Clinic Neuro-Informatics Laboratory, Mayo Clinic, Rochester, Minnesota, USA
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1. Background and Importance
Brown-Sequard Syndrome (BSS), first described in 1846 by Charles-Edouard Brown-Séquard, is a rare neurological syndrome that evolves due to a hemisection injury to or unilateral compression on the spinal cord. As a result of interruption of both ascending spinothalamic and descending corticospinal tracts, a constellation of symptoms and signs appears, including ipsilateralloss of motor function (presenting as hemiplegia or hemiparesis), proprioception, vibration, and fine touch sensation, and contralateral loss of temperature and pain sensation. In addition, there is an ipsilateral loss of all sensations and motor functions at the level of the lesion [1]. Etiologies of BSS include surgically treatable (traumatic and non-traumatic injuries) and medically treatable causes. Traumatic injuries were often reported as the main surgical causes of BSS. However, non-traumatic etiologies have been more frequent in recent years, as reported in the literature. Surgically treatable non-traumatic etiologies of BSS include Cervical intervertebral Disc Herniation (CiDH), Spinal Cord Herniation (SCH), spinal canal stenosis with cervical spondylosis, primary and secondary tumors, spinal stenosis, Ossified Posterior Longitudinal Ligament (OPLL), intramedullary cystic diseases, some infectious diseases, such as spinal cysticercosis [2, 3] and syphilitic gumma [4], as well as rare conditions, such as cervical synovial cyst [5], and Kirschner wire after clavicular osteosynthesis [6]. Early surgical interventions performed for these pathologies have a great impact on the prognosis of patients. Herein, we present a case series of surgically treatable non-traumatic causes of BSS along with a systematic review of the literature. We aimed to raise awareness that there are more non-traumatic causes of BSS. This work has been reported with preferred items for systematic review and meta-analysis PRISMA guidelines which is an evidence-based minimum set of items for reporting in systematic reviews and meta-analyses [7]. 

2. Case Presentation 
Seventeen patients were admitted to our clinic in the Department of Neurosurgery, University of Health Sciences-Samsun Health Practices and Research Center, Samsun, Turkey, between 2008 and 2020. They presented the aforementioned clinical picture of BSS. The patients consisted of 12 men (70.6%) and 5 women (29.4%). The age of the patients ranged from 48 to 85 years (mean= 65 years). The etiologies of BSS in these patients as revealed by cervical Magnetic Resonance Image (MRI) were as follows: 6 cases were produced by CDH alone (35.3%), 5 patients by OPLL (29.4%), 1 patient by spinal canal stenosis with cervical spondylosis (5.9%), 3 patients by epidural hematoma (17.6%), and 2 patients by cervical spinal stenosis (11.8%) (Table 1; Figure 1).

All patients with disc herniation and spinal canal stenosis with cervical spondylosis denied any history of major traumas. In most patients, the symptoms were observed during their daily activities. Few of them had a history of minor traumas in the form of falling at the same level [8]. Written consent was taken from the patients for performing the appropriate surgical intervention. According to the diagnosis, the patients underwent the following surgical interventions: anterior cervical discectomy for CDH, anterior oblique corpectomy for OPLL, posterior hemilaminectomy for epidural hematoma, and total posterior laminectomy for spinal stenosis and some cases of CDH (Table 1).

In addition to our cases, we systematically performed a comprehensive literature search in PubMed, Scopus, and CINAHL for retrieval of all relevant case series and case reports that reported surgically-treatable causes of BSS with the way of management and postoperative outcome for the past 20 years according to PRISMA guidelines [9], using the following keywords: “Brown-Sequard”, “Brown-Séquard”, “surgery”, “surgical intervention”, “operation”, “surgical approach”, “neurosurgery”, “case report”, “report”, and “case series”. The search results were checked for duplication, then underwent screening.

3. Results
Our patients were followed up for 2 to 3 years; their long-term outcomes post-operatively ranged from partial to complete recovery, as shown in Table 1. Four cases completely recovered, whereas 13 showed incomplete recovery in the form of sensory and motor deficits. In our cases, complete recovery was mainly associated with patients with acute CDH and epidural hematoma, whereas incomplete recovery was mainly associated with OPLL, lateral stenosis, calcified CDH, and spinal stenosis. Moreover, our patients’ outcomes showed that late surgical treatment after the occurrence of BSS did not have enough benefit, and poor neurological conditions persisted. The comprehensive search in the aforementioned databases yielded 482 case series and reports. Of these, 75 articles were excluded for deduplication, 97 articles because of title and abstract screening, and 157 articles because of full-text screening for reporting cases treated medically and conservatively. Finally, 153 articles were included for qualitative synthesis as demonstrated by the PRISMA flow chart (Figure 2) for estimating the frequency of each surgically treatable cause of BSS for the past 20 years.

Of these 153 articles, 52 reported major traumatic injuries, and 101 reported micro- or non-traumatic injuries (Table 2).

CDH was the most common surgically treatable non-traumatic cause for the past 20 years (frequency=28), followed by SCH (frequency=27), micro- or non-traumatic epidural hematoma (frequency=14), and Intramedullary Spinal Cord Metastasis (ISCM) (frequency=6) (Figure 3, Table 2).

Males were affected more often than females (males=59 cases; females=42 cases). The ages of the patients reported in these studies ranged from 7 to 86 years (mean=50 years; 95%CI: 47 to 53) (Figure 4, Table 2).

4. Discussion
Surgically treatable etiologies of BSS

BSS may occur due to spontaneous non-traumatic causes, major traumatic injuries, or some infectious diseases. Many of these causes require conservative treatment, such as medical or rehabilitation therapy, and the others require surgical intervention. In recent years, BSS frequently occurs due to micro- or non-traumatic injuries, such as CDH, SCH, epidural hematoma, OPLL, cervical canal stenosis, and benign and metastatic tumors, as noticed in our cases. We classified surgically treatable causes of BSS into two categories based on our case series and a comprehensive search in the literature: major traumatic injuries and micro- or non-traumatic injuries (Figure 5).

Major traumatic injuries result from direct injuries to the spinal cord, including stab injuries (accounting for 26% of spinal cord injuries) [10], blunt traumas [11], gunshot [12], penetrating glass injuries [13], cervical vertebral dislocation, acute traumatic cervical disc herniation, and traumatic vertebral fracture. Major traumatic injuries are usually accompanied by Horner’s syndrome when traumas involve the cervical region [14] and usually require urgent surgical intervention for spinal cord decompression, removal of foreign objects, repair of the affected area, and preservation of the spinal cord in its correct position. On the other hand, micro- or non-traumatic injuries result from trivial traumas, physical activities, or hyperextension [8]. The definitive diagnostic tool for such cases is MRI, which demonstrates the etiology and extension of the lesion. Micro- or non-traumatic injuries have been reported more frequently than before for the past 20 years. Based on the results from 153 case reports, there are 19 different surgically treatable non-traumatic etiologies that can result in BSS. CDH constitutes most of these causes as found in our cases [15, 16], followed by SCH, spinal epidural hematoma, ISCM, and benign tumors (Figure 5). CDH occurs mainly due to minor traumatic events (the main cause of herniation) or develop progressively over a long period of time [17]. In addition to disc herniation, SCH has been also reported as a surgically treatable non-traumatic cause of BSS occurring as a result of pre-existing dural defects, unrecognized traumatic events, surgical intervention (iatrogenically), or rarely, congenital defects. However, this clinical entity was not present in our patients. Spinal epidural hematoma comes in the third place among non-traumatic causes of BSS. It may occur spontaneously or evolve secondarily due to minor traumas, vascular malformation, hemorrhagic diseases [18], anticoagulant therapy, hypertension, or pregnancy. The fourth most common non-traumatic cause of BSS is tumors, which can be classified into primary and metastatic. Primary tumors include cavernous hemangioma, schwannoma, meningioma and osteochondroma [19, 20]. Secondary metastasis from remote sites includes malignant mesothelioma [21], colonic carcinoma [22], squamous cell carcinoma of the maxillary sinus [23], and gastric adenocarcinoma [24], leading to intramedullary spinal cord metastasis. Spinal canal stenosis with cervical spondylosis and OPLL are forms of degenerative conditions that develop over the years and affect the vertebral column and surrounding ligaments [14]. Cervical spinal stenosis is the commonest form of spinal canal stenosis developing mainly from spinal canal stenosis with cervical spondylosis and OPLL and therefore requires surgical intervention for dilatation of the spinal canal and release of any compression on the spinal cord. BSS is produced by these conditions mainly due to compression on the spinal cord by bone spurs and degenerated intervertebral disc herniation [25]. Overlap between some spinal canal pathologies is common in real life such as CDH, spinal canal stenosis with cervical spondylosis, and OPLL. Time of surgical intervention plays a vital role and has a great impact on the postoperative outcome; the earlier the intervention, the better the prognoses and postoperative outcomes. Therefore, most non-traumatic injuries have good prognosis after early surgical interventions and patients achieve complete recovery, except for ISCM and calcified CDH that carry moderate to bad prognosis [21, 26]. Other surgically treatable non-traumatic causes of BSS that have been reported rarely include neurenteric cyst, cervical synovial cyst, ganglion cyst, spinal arteriovenous fistula, intramedullary abscess, intramedullary tuberculosis, and regional kyphosis (Figure 3).

Overview of medically treatable etiologies of BSS
Non-surgical causes of BSS are treated conservatively without a need for surgical intervention. They include spinal cord ischemia and infarction, many infectious diseases, such as varicella virus infection, treated with acyclovir and steroid [27, 28], and neurodegenerative diseases, such as multiple sclerosis. Spinal cord ischemia, usually followed by infarction, occurs due to diminished blood supply to the spinal cord. The causes of blood supply cessation include compression on the blood vessels supplying the spinal cord by tumors or hernias, circulating thrombi, or iatrogenically following endovascular embolization of vertebral hemangioma [29, 30, 31, 32]. The treatment is usually conservative with anticoagulation and antiplatelets [31].

5. Conclusion
Surgically treatable non-traumatic causes of BSS are more frequent than major traumatic injuries in recent years, as reported in the literature. CDH has been reported as the commonest surgically treatable non-traumatic surgical cause of BSS, followed by SCH, spinal epidural hematoma, ISCM, benign tumors, OPLL, and spinal canal stenosis with cervical spondylosis. Regarding the postoperative outcomes of our patients, the cases with acute epidural hemorrhage achieved complete recovery after surgery, whereas neurological deficits in the other cases, especially those with severe cervical spinal canal stenosis, persisted despite adequate surgical decompression. 

Ethical Considerations
Compliance with ethical guidelines

Ethics approval Consent to participate written informed consent was obtained from the patients for publishing this article accompanied by the MRI images. Consent for publication Written informed consent was obtained from the patients for publishing this article accompanied by the MRI images.

Funding
This research did not receive any grant from funding agencies in the public, commercial, or non-profit sectors. 

Authors' contributions
Data Collection: Mahmoud Osama, Vaner Köksal, Mohammed Ali Alvi; Data Analysis and Interpretation: Mahmoud Osama, Vaner Köksal, Mohammed Ali Alvi; Drafting the article: Mahmoud Osama, Vaner Köksal, Mohammed Ali Alvi; Critically revising the article: Mahmoud Osama, Vaner Köksal, Mohammed Ali Alvi; Reviewing submitted version of manuscript: Mahmoud Osama, Vaner Köksal, Mohammed Ali Alvi; Approving the final version of the manuscript: Mahmoud Osama, Vaner Köksal, Mohammed Ali Alvi.

Conflict of interest
The authors have no conflict of interest to declare.

Acknowledgements
The authors would like to thank Mahmoud Osama for his drawings.


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Type of Study: Case Series | Subject: Neurotrauma

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