Surgical Management and Functional Outcomes of Cavernous Malformations Involving the Medulla Oblongata

doi:10.1016/j.wneu.2018.07.229

World Neurosurgery

Volume 119, November 2018, Pages e643-e652

https://doi.org/10.1016/j.wneu.2018.07.229 Get rights and content

Highlights

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This is the first study with largest surgical series to report CMs involving the medulla.
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The bad long-term outcome is related to increased age, multiple hemorrhages, lesion with DVAs but without perilesional edema.
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The study provides several surgical management protocols of the CMs involving the medulla oblongata.

Objective

The aim of this study was to evaluate the clinical features, surgical complications, and functional outcomes of the surgical treatment of patients with cavernous malformations (CMs) involving the medulla oblongata.

Methods

The charts of 69 patients undergoing surgical treatment of CMs in the medulla oblongata, pontomedullary, and cervicomedullary junctions between 2011 and 2017 were retrospectively reviewed. Patient demographics, lesion characteristics, operative documents, and patient outcomes were examined.

Results

Of the 69 patients, the male-to-female ratio was 1.3. The mean patient age was 32.6 years, and the mean mRS score was 2.7 on admission. Postoperatively, 21 patients (30.4%) had deficits of cough reflexes, and 6 patients (8.7%) experienced respiratory rhythm disorder and dyspnea. The mean follow-up duration was 35.3 months. At the last follow-up evaluation, the mean mRS score was 1.8, and 53 patients (80.3%) had favorable outcomes, with mRS scores ≤2. The conditions of the patients improved in 45 cases (68.2%), remained unchanged in 11 cases (16.7%), and worsened in 10 cases (15.1%) relative to their preoperative baseline. The independent adverse factors for long-term functional outcome were increased age, multiple hemorrhages, presence of developmental venous anomalies, and lack of perilesional edema.

Conclusions

Respiratory dysfunction and deficits of cough reflexes can commonly occur during the early postoperative period for surgical resection of CMs involving the medulla oblongata. Favorable functional outcomes can be achieved by surgery, especially for younger patients who experience fewer hemorrhages and have lesions with perilesional edema and the absence of developmental venous anomalies.

Introduction

Brainstem cavernous malformations (CMs) are low-flow vascular lesions characterized by accidental repeated bleeding, which can result in significant neurologic morbidity or even mortality.1, 2, 3, 4 CMs involving the medulla oblongata may be more harmful to patients than those in other locations in the brainstem because of the complicated and vital neural structures, such as the corticospinal tracts (or pyramid), brainstem respiratory network, and vagus nerve nuclei, which are densely located in the small medulla oblongata.5, 6, 7 Slight changes or injury of the medulla oblongata caused by surgical manipulation may be accompanied by life-threatening complications, such as cardiovascular and respiratory instabilities.6, 8 However, surgical treatment of CMs involving the medulla oblongata is rarely distinguished by authors from those involving the brainstem, nor are the associated morbidities of respiration, circulation, and lower cranial nerves because of their rare occurrence.1, 7, 9 Moreover, debate still exists regarding which patients will benefit most from surgical intervention, even though numerous studies have attempted to identify predictors of good outcome in patients with brainstem CMs.9, 10 Therefore, we retrospectively reviewed a single-center series of 69 cases of CMs involving the medulla oblongata, including lesions in the pontomedullary and cervicomedullary junctions, to evaluate surgical treatment with associated complications and to identify the prognostic risk factors of long-term functional outcomes.

Section snippets

Study Population

The clinical data from 69 patients who underwent surgical treatment of CMs involving the medulla oblongata between January 2011 and January 2017 in our institute were retrospectively reviewed. The Beijing Tiantan Hospital Research Ethics Committee approved this study.

All neuroimaging data were reviewed by independent neuroradiologists. The definition of a hemorrhagic event was as follows: a clear clinical history of an acute, new-onset, or worsening focal neurologic deficit, accompanied by

Patient Demographics

A total of 69 patients received diagnoses of CMs involving the medulla oblongata and were microsurgically treated Their mean age was 32.6 ± 13.3 years (range, 8–64 years), and the male/female ratio was 1.3 (Table 1). All patients presented with a clear history of symptomatic hemorrhage before undergoing microsurgical resection. Among those patients, 34 (49.3%) had 2 hemorrhages, 7 (10.1%) had 3 hemorrhages, and 1 (1.4%) had 4 hemorrhages. A total of 120 hemorrhagic events across 2249

Discussion

The medulla oblongata is a vital neurologic zone in the brainstem with densely clustered neural structures. Slight changes in or injury to the medulla oblongata caused by compression of CMs or by surgical manipulation may result in obvious or severe neurologic deficits.6, 7, 8 The clinical symptoms of CMs involving the medulla vary among lesion locations and characteristics, which were mainly associated with deficits in the lower cranial nerves (or related nuclei), motor tracts, sensory tracts,

Conclusions

Respiratory dysfunction and deficits of cough reflexes are common and dangerous complications during the early postoperative period for surgical resection of CMs involving the medulla oblongata. However, favorable functional long-term outcome can be achieved in surgery, especially for younger patients who experienced fewer hemorrhages and have lesions presenting with perilesional edema and absence of DVAs.

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In the present study, rapid relief of the respiratory deficit was observed in all our patients, and they continued to improve at long-term follow-up. The literature review also showed that most reported cases (Table 3) could achieve respiratory and social function improvement postoperatively and at follow-up, supporting an aggressive treatment attitude for BSCM with respiratory problems [32,33,38,39,42]. However, the higher rebleeding rate after acute surgery should not be neglected [26].
Impending respiratory failure is catastrophic neurological deterioration caused by repeated c of a brainstem cavernous malformation (BSCM). The benefit and outcome prediction of acute surgery for this fatal condition is rarely reported. In this study, the authors reported a case series of acute surgical treatment (≤3 weeks after the last hemorrhagic episode) for the BSCM with impending respiratory failure and reviewed literature over the past 20 years.
Clinical and outcome data from 6 consecutive acute surgically-treated BSCM patients were analyzed. Intracerebral hemorrhage (ICH) scores, primary pontine hemorrhage (PPH) scores, and Lawton's BSCM grading were applied for surgical outcome prediction. Ten related articles were included for the literature review.
There were three men and three women, with a mean age of 32.2 ± 9.3 years (range 15–45 years). The BSCMs were located at the pons in 5 cases and the medulla in 1 case. The ICH score was 1–2 in all cases, while the PPH score was 0 in all pontine BSCMs. For Lawton's BSCM grading, 3 cases were grade 2, 2 cases were grade 3, and 1 case was grade 1. All patients achieved spontaneous respiratory dysfunction relief postoperatively and significantly improved at follow-up (mean 4.47 ± 0.24 years;range4.0–5.6 years).
Repeated hemorrhagic BSCM with impending respiratory failure can benefit from acute surgical treatment. The ICH score, PPH score, and Lawton's BSCM grading are promisingly useful tools for fast and efficient surgical outcome prediction.
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We monitored 53 patients during cerebellar-pontine angle and brainstem surgeries. Vocal-CoMEPs and LAR were recorded from an endotracheal tube with imbedded electrodes or hook-wires electrodes. A LAR significant change (LAR-SC) defined as ≥ 50% amplitude decrement or loss, was classified as either transient or permanent injury to the vagus or medullary pathways by the end of the surgery.
All patients with permanent LAR loss (n = 5) or LAR-SC (n = 3), developed postoperative laryngeal dysfunction such as aspiration/pneumonia and permanent swallowing deficits (5.6%). Vocal-CoMEP findings refined postoperative vocal motor dysfunction. All seven patients with transient LAR-SC or loss, reverted by changing the surgical approach, did not present permanent deficits.
Permanent LAR-SCs or loss correlated with postoperative laryngeal dysfunction and predicted motor and sensory dysfunction of the vagus nerve and reflexive medullary pathways. In contrast, a LAR-SC or loss, averted by a timely surgical adjustment, prevented irreversible damage.
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Multiplicity, pregnancy and antiplatelet/antithrombotic use do not appear to increase the risk of haemorrhage. It is estimated that approximately 20% of CCMs are located in the brainstem (BSCMs), although some authors have reported in the literature that this figure may be as high as 35% [2,6,13,20–24]. However, the exact proportion occurring in the brainstem is difficult to accurately determine, as brainstem lesions are more likely to be symptomatic than similar lesions in the cerebrum.
Due to its eloquent location and potentially devastating neurological consequences, the management of brainstem cavernous malformations (CCMs) attracts considerable debate. There is currently a paucity of Level 1 evidence for their management. The aim of this literature review is to explore the current evidence on the risk-benefit profile of different management options.
A systemic literature search, following the PRISMA algorithm was performed on publications between 2010 and 2018 using the Pubmed database, with the relevant keywords. Only English articles were included. Articles focusing on spinal CCMs and studies with less than 30 participants were excluded.
A total of 222 search results were reviewed and after removal of duplicates and screening of abstracts, 28 clinical papers comprising 30 or more brainstem CCM cases were included in the study. The heterogeneity of the publications precluded a formal meta-analysis of results. The general consensus is that for CCMs presenting with severe symptoms and/or multiple haemorrhages that reach an accessible pial surface, surgery is considered to be the gold-standard treatment, with some authors suggesting the optimal timing to be within two to six weeks of ictus. For those patients with multiple, deep-seated CCM related haemorrhages that do not reach the pial surface, stereotactic radiosurgery (SRS) can be considered. Conservative treatment is generally considered in incidental cases. Management of brainstem cavernomas of other categories still remains controversial.
Due to their highly eloquent location, brainstem CCMs are challenging lesions to manage. Management must be balanced by the risk-benefit profile and tailored to the individual patients and their treating clinicians. This review provides a comprehensive reference considering all treatment options and provides a basis for evidence-based patient counselling.
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: Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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Original ArticleSurgical Management and Functional Outcomes of Cavernous Malformations Involving the Medulla Oblongata

Highlights

Objective

Methods

Results

Conclusions

Introduction

Section snippets

Study Population

Patient Demographics

Discussion

Conclusions

J Clin Neurosci

J Clin Epidemiol

Pulm Pharmacol Ther

Clin Neurol Neurosurg

World Neurosurg

Advances in the treatment and outcome of brainstem cavernous malformation surgery: a single-center case series of 300 surgically treated patients

Neurosurgery

Cerebral cavernous malformations: natural history and clinical management

Expert Rev Neurother

Brainstem cavernous malformations

J Neurosurg Sci

Natural history of brainstem cavernous malformations

Neurosurgery

Microsurgical anatomy of safe entry zones to the brainstem

J Neurosurg

Apnea as an uncommon preoperative manifestation of medulla cavernous malformation: surgical treatment and literature review

Br J Neurosurg

Ventilatory disorders

Front Neurol Neurosci

Impact of timing of intervention among 397 consecutively treated brainstem cavernous malformations

Neurosurgery

Brainstem cavernous malformations: surgical results in 104 patients and a proposed grading system to predict neurological outcomes

Neurosurgery

The two point method: evaluating brain stem lesions

BNI Q

Original Article
Surgical Management and Functional Outcomes of Cavernous Malformations Involving the Medulla Oblongata