ORIGINAL ARTICLE
Acute Abducens Nerve Paralysis in the Pediatric Emergency Department Analysis of 14 Patients Ozlem Teksam, MD,* Ayse Gultekingil Keser, MD,* Bahadir Konuskan, MD,† Goknur Haliloglu, MD,† Kader Karli Oguz, MD,§ and Dilek Yalnizoglu, MD† Objectives: Sixth cranial nerve (SCN) palsy is an uncommon but important neurological problem in patients admitted to pediatric emergency department. The underlying etiology of SCN palsy has a wide range from viral infections to intracranial tumors; therefore, a careful and systematic approach is necessary while examining these patients. Methods: Fourteen patients who presented with acute SCN paralysis to pediatric emergency department during the last 10 years were examined. Results: The age at the time of admission ranged between 14 months and 16 years (median, 9.5 years). Of the 14 patients, 5 were girls and 9 were boys. A total of 3 of the 14 patients had bilateral cranial nerve VI paralysis, and 9 patients had additional abnormal findings on neurological examination. Neuroimaging studies included cranial tomography (n = 3) and brain magnetic resonance imaging in all patients. The underlying etiology was malignancy (n = 3); glioma, medulloblastoma, acute lymphoblastic leukemia, and dural sinus thrombosis (n = 2); as well as Guillain-Barre syndrome (n = 2), multiple sclerosis (n = 1), pseudotumor cerebri (n = 1), and meningitis (n = 1). The remaining 4 patients had miscellaneous benign etiologies. Conclusions: Other lesions of primary brain tumors causing increased intracranial pressure constitute 50% of the underlying etiology, followed by Guillain-Barre syndrome (14.2%). However, these patients had neurological symptoms signs, in addition to diplopia or SCN paralysis. Patients admitted to pediatric emergency department with acute SCN paralysis should be examined in detail to disclose the underlying etiology especially if they present with additional clinical signs or symptoms. Key Words: abducens nerve paralysis, neuroimaging, acute (Pediatr Emer Care 2016;32: 307–311)
S
ixth cranial nerve (SCN) palsy is considered to be the most common cranial nerve palsy in children.1,2 Etiologies underlying SCN palsy vary from minor causes such as viral infections to neoplasms causing increased intracranial pressure.1 Neoplasms and trauma are found to be the most common etiologies causing SCN palsy in children, followed by other causes of increased intracranial pressure, inflammation, congenital causes, and miscellaneous other etiologies.2,3 Considering the high frequency of serious causes of SCN palsy, immediate and careful evaluation and treatment of patients are crucial. We evaluated the underlying etiologies of patients with acute SCN palsy who were admitted to our pediatric emergency department.
From the *Department of Pediatrics, Division of Pediatric Emergency Medicine, †Department of Pediatrics, Division of Pediatric Neurology, and §Department of Radiology, Hacettepe University Medical Faculty, Ankara, Turkey. Disclosure: The authors declare no conflict of interest. Reprints: Ozlem Teksam, MD, Department of Pediatrics, Division of Pediatric Emergency Medicine, Hacettepe University Medical School, İhsan Doğramacı Children's Hospital, Sihhiye, Ankara 06100 Turkey (e‐mail: [email protected]; [email protected]). Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved. ISSN: 0749-5161
METHODS We retrospectively reviewed medical records of patients who were admitted to Hacettepe University Children's Hospital Pediatric Emergency Department between January 1, 2002 and December 31, 2012. Hacettepe University Children's Hospital is an urban tertiary care center in the capital of Turkey with more than 60,000 pediatric emergency patient visits annually. Patients were identified by searching the hospital's electronic data base using word root search for abducens, sixth nerve, and outward gaze paralysis. In addition, all cranial computed tomography (CT) and magnetic resonance imaging (MRI) reports performed within the last 10 years in the pediatric emergency department were reviewed. Age, sex, symptoms, complaints, neurological examination findings, as well as laboratory studies and neuroimaging results were recorded. Cranial and spinal neuroimaging studies were reevaluated by a neuroradiologist (K.K.O.) with an experience of 14 years. Final diagnosis and clinical follow-up were assessed. Approval for review was obtained from the ethics committee of Hacettepe University medical faculty.
RESULTS Within the defined period of 10 years, 21 patients with acute SCN palsy who were admitted to our pediatric emergency department were identified, and 7 patients were excluded owing to inadequate data. The age at the time of admission ranged between 14 months and 16 years (median, 9.5 years). Nine of them (64.3%) were boys. Thirteen patients (92.8%) had complaints related to SCN palsy including diplopia, inward deviation of eye, or difficulty in looking to 1 side. One patient (patient 11) (7%) did not have any complaints related to SCN palsy but had headache, vomiting, and confusion; sixth nerve palsy was found on physical examination. Three patients had isolated complaints of diplopia and/or difficulty in looking to 1 side (21.4%). Headache and vomiting were the most common accompanying symptoms (50%), followed by fever (28.5%). Clinical and diagnostic findings of all patients are summarized in Table 1. Neurological examination results revealed that 6 patients (42.8%) had sixth nerve palsy in the left eye, 5 in the right eye (35.7%), and 3 in both eyes (21.4%). Three patients had paralysis in other directions as well (21.4%), and 1 patient had nystagmus in addition to SCN paralysis. Two patients had weakness in the lower extremities and absent deep tendon reflexes (14.2%). Three patients were lethargic (21.4%). One patient had ataxia and dysmetria (7%). Two patients (14.2%) had bilateral papilledema, and one of them had central facial paralysis on the same side with gaze paralysis (7%). One patient had tongue deviation on the same side (7%). One patient (7%) had nuchal rigidity. Five patients (35.7%) had merely gaze paralysis and no other neurological abnormalities; 3 of them (21.4%) had no other complaints but gaze paralysis. Contrast-enhanced brain MRI was obtained in all patients, 3 patients had cranial CT, and 1 had spinal MRI. Ten patients
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TABLE 1. Demographic Characteristics, Clinical, Laboratory, and Neuroimaging Findings of All Patients Patient No. Age, Sex 1
5 y, F
2
9 y, F
3
6 y, F
4
10 y, M
5
16 y, M
6 7 8 9
10
11
12 13
14
Complaint on admission
Neurological Examination
Diplopia (right eye), Bilateral SCN paralysis, weakness in legs nystagmus, absent DTR, motor weakness in the lower extremities Fever, vomiting, Lethargic, SCN (left headache eye) paralysis, ataxia, dysmetria Pain in legs, Bilateral left SCN palsy, difficulty in decreased DTR, motor walking weakness in lower extremities Headache, nausea, SCN paralysis in the vomiting, right eye, Babinski strabismus, positive on the diplopia left side
Imaging Studies
Laboratory Results
Diagnosis
Cranial MRI: normal; Normal CSF, stool culture: GBS spinal MRI: Linear C. jejuni; EMG: early contrast enhancement phase of demyelinating in the cauda equina disorder Cranial MRI: pons glioma NS Pons glioma
Cranial MRI: normal
CSF: albuminocytologic dissociation; EMG : myopathic changes MTHFR homozygous mutation
Cranial CT: acute sinus thrombosis; Cranial MRI-MR venography: venous thrombosis in bilateral, transverse sinuses, superior sagittal sinus Cranial MRI: IgG index: 0.58 contrast-enhancing lesions in the right pontomedullary junction
Paresthesia in the left Lateral, upward, and arm and left leg, downward gaze diplopia, difficulty paralysis in the in looking to the right eye right side 2.5 y, M Strabismus in the SCN (left eye) paralysis Cranial MRI: normal left eye, URTI history (+) 10 y, M Diplopia SCN (right eye) paralysis Cranial MRI: right mastoiditis and petrositis 14 y, M Diplopia URTI SCN (left eye) paralysis Cranial MRI: normal history (+) 4 y, M Strabismus, Lethargic, bilateral Cranial MRI: vomiting, papilledema; left facial medulloblastoma headache, paralysis; left SCN originating from vermis, confusion paralysis hydrocephalus 14 y, M Fever, headache, SCN (left eye) paralysis, Cranial MRI: dural paresthesia in the left-sided deviation thickening and tongue, difficulty of tongue enhancement along the to look on the cerebral hemispheres left side and cranial nerves 9 y, F Headache, vomiting, Lateral and downward Cranial CT: normal; confusion gaze paralysis (right cranial MRI: diffuse eye), mild SCN (left leptomeningeal contrast eye) paralysis, nuchal enhancement around rigidity, lethargy the sixth, seventh, and eighth nerves. 14 mo, M Vomiting, strabismus, SCN (right eye) paralysis Cranial MRI: cerebral fever, fatigue volume loss 13 y, M Fever, headache, SCN (right eye) paralysis Cranial CT: right dural sinus thrombosis; vomiting, diplopia cranial MRI: thrombosis in the superior sagittal and right transverse sinus 11 y, F Diplopia, headache, Inward and outward gaze Cranial MRI: increased vomiting paralysis (left eye), perioptic CSF, left exophthalmos, arachnoid cyst bilateral papilledema
GBS
Venous thrombosis, Behcet disease
MS
NS
Unexplained
NS
Unexplained
NS
Unexplained
NS
Medulloblastoma
Bone marrow aspiration: blasts (+)
ALL
CSF: abnormal
Meningitis
NS
Unexplained
Deficiency of protein C and protein S
Sinus venous thrombosis
CSF pressure: 220 mm Hg
Pseudotumor cerebri
ALL indicates acute lymphoblastic leukemia; DTR, deep tendon reflexes; F, female; IgG, immunoglobulin; M, male; NS, not significant; SCN, sixth cranial nerve; URTI, upper respiratory tract infection.
(71.4%) had abnormal findings on MRI; 2 patients (14.2%), on CT. Neuroimaging findings are also summarized in Table 1. Brain MRI of patient 2 who had fever, headache, vomiting, ataxia,
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and dysmetria showed a diffuse pontine glioma. Brain MRI of patient 9 who had vomiting, headache, confusion, lethargy, bilateral papilledema, and left-sided facial paralysis showed a © 2015 Wolters Kluwer Health, Inc. All rights reserved.
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Pediatric Emergency Care • Volume 32, Number 5, May 2016
medulloblastoma originating from the vermis, widespread intracranial metastasis, and hydrocephalus (Fig. 1). Brain MRI of patient 10 who had headache, fever, paresthesia in the tongue, and left-sided deviation of the tongue demonstrated an abnormal bone marrow with dural thickening and contrast enhancement along the cerebral hemispheres and cranial nerves (Fig. 2). Therefore, a bone marrow aspiration was done, confirming the diagnosis of acute lymphoblastic leukemia. Brain MRI of patient 4 who experienced headache and vomiting showed venous thrombosis (Fig. 3). On follow-up, this patient was diagnosed with Behçet disease. Brain MRI of patient 13 who had headache, fever, and vomiting showed thrombosis in the superior sagittal and right transverse sinus. The MRI of patient 5 who had paresthesia in the left arm and left leg as well as outward, upward, and downward paralysis of the right eye showed contrast-enhancing lesions and consistent with multiple sclerosis (MS). The MRI of patient 11 who had headache, vomiting, confusion, lethargy, and nuchal rigidity showed diffuse leptomeningeal and bilateral contrast enhancement around the sixth, seventh, and eighth nerves; however, her lumbar puncture did not show any blood cells or microorganisms. Patients 1 and 3 had normal brain MRI; however, they had difficulty in walking and weakness in the lower extremities, along with absent or decreased deep tendon reflexes, which led to the clinical diagnosis of Guillain-Barré syndrome (GBS), confirmed with electromyelography (EMG). Findings of EMG of patient 1 showed an early phase of a demyelinating disorder, and her spinal MRI showed linear contrast enhancement in the cauda equina compatible with the diagnosis of GBS. Patient 3 had a normal EMG, and lumbar puncture was done, showing albuminocytologic dissociation. Follow-up EMG study showed myopathic changes, and her symptoms resolved without treatment. On the basis of clinical picture and cerebrospinal fluid (CSF) findings, she was diagnosed with GBS. Patient 14 had headache, vomiting, and bilateral papiledema. Her MRI showed increased perioptic CSF, bilateral papilledema, and left middle cranial fossa arachnoid cyst. She had normal CSF pressure on lumbar puncture, and her symptoms resolved with dexamethasone treatment. Patient 12 had vomiting and a suspected convulsion; neurological examination results were normal, except SCN paralysis in the right eye. Her MRI showed cerebral volume loss. Her symptoms improved during a follow-up, leading to the conclusion that the sixth nerve palsy could be caused by an infection not clearly identified. In summary, the final diagnosis was malignancy (glioma, medulloblastoma, acute lymphoblastic leukemia) in 3 patients (21.4%), dural sinus thrombosis in 2 (14.2%), GBS in 2 (14.2%),
FIGURE 1. Patient 4. Sagittal T1-weighted (T1W) MR venography (A) and axial fluid attenuated inversion recovery (B) (repetition time [TR]/echo time [TE]/inversion time; 8500/100/2000 milliseconds) images show thrombosis in the superior sagittal and straight sinuses by filling defect (arrows, A) and absence of flow void (dashed arrow, B).
Acute Abducens Nerve Paralysis in Children
FIGURE 2. Patient 9. Sagittal (A) and axial (B) postcontrast T1W (TR/TE, 550/15 milliseconds) images show midline enhancing posterior fossa mass and disseminated leptomeningeal involvement, also along with cranial nerves and nodular intraventricular seeding metastases (arrows in A and B).
MS (7%), meningitis (7%), and pseudotumor cerebri (7%) each in 1 patient. Four patients were diagnosed with idiopathic SCN palsy (28.5%).
DISCUSSION Sixth cranial nerve nucleus is located within the genu of facial nerve, and SCN has a long course from pons to lateral rectus muscle.3 Nerve fascicles arise from the anterior surface of the pontine tegmentum; exit from the pontomedullary junction, cross subarachnoid space, and ascend clivus; as well as enter petrous bone and cavernous sinus.3,4 Inside the sinus, SCN is the only nerve that travels free in the sinus wall. It then enters the orbit through the superior orbital fissure to innervate the lateral rectus muscle.4 Because of its long intracranial course, it is susceptible to injury either directly or indirectly owing to increased intracranial pressure.1 Different pathological causes affect SCN at different locations: inflammation and infection affect the nerve at the subarachnoid space; pressure and trauma at the skull base; and neoplasms, anywhere along the tract.3 Neoplasms are one of the most common etiologies found in patients with acquired SCN palsy.3,5 A total of 3 of the 14 patients had neoplasms: 2 had primary brain tumors and 1 had hematologic malignancy. Malignancies can result in SCN palsy in different ways. The location of neoplasm can directly make pressure on the nerve such as gliomas.6 However, the primary site of neoplasm can be elsewhere, such as medulloblastomas; in that case, tumor may result in increased intracranial pressure or hydrocephalus causing displacement of brain stem or stretching or compression of the nerve as well.6 Moreover, widespread intracranial leptomeningeal metastases can cause abducens palsy far from the primary location of the tumor; therefore, abducens nerve palsy should not be considered as a localizing sign in these conditions. Nevertheless, neoplasms constitute an important etiology in differential diagnosis of abducens palsy, especially if it is accompanied by headache, nausea, lethargy, focal neurological signs, or posterior fossa signs; emergent neuroimaging should be done in these patients. Presentation with isolated SCN palsy is rare in malignancy; however, it still should be ruled out, considering the high occurrence of neoplasms in these patients.3 One of our patients was found to have acute lymphoblastic leukemia, which is a rare cause for patients who present with SCN palsy. Chen et al7 described a patient who presented with SCN palsy and fever with a normal MRI, later found out to have acute lymphoblastic leukemia. Although our patient was suspected to have a bone marrow disease with pachymeningeal involvement by contribution of MRI, it should be noted that
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FIGURE 3. Patient 10. Axial precontrast (A) and postcontrast (B) T1W (TR/TE, 550/15 milliseconds) images show diffuse low signal intensity of bone marrow (arrow, A) as well as diffuse dural thickening and enhancement (double thin arrows, B). Please also note the thickening of the dura of the cavernous sinuses (dashed arrow, C).
patients with SCN palsy should be examined for hematologic malignancy even in the absence of pathological findings on MRI, especially if they have fever or symptoms related to increased intracranial pressure. Three of our patients (21.4%) had SCN palsy due to nonmalignant intracranial lesions, causing increased intracranial pressure in agreement with the study of Lee at al.3 Two of these patients had dural sinus thrombosis, and 1 had pseudotumor cerebri. Dural sinus thrombosis may cause SCN paralysis by increasing intracranial pressure. Ghosh et al8 reported that, of 13 patients with lateral sinus thrombosis, 4 (30%) were found to have SCN palsy. Dural sinus thrombosis should be included in the etiological diagnosis of patients with SCN palsy, especially if they have symptoms related to increased intracranial pressure such as headache, nausea, and papilledema. History of recent upper respiratory tract infection or otitis media should be considered in patients with SCN palsy because they may be risk factors for dural sinus thrombosis.8 One of our patients with dural sinus thrombosis had Behçet disease, and the other had protein C and protein S deficiency as the underlying etiology for thrombosis. An underlying prothrombotic disease should raise the suspicion for dural venous thrombosis in patients with acute SCN palsy. If patients with SCN palsy have symptoms related to increased intracranial pressure but there are no pathological findings on brain imaging except findings related to increased intracranial pressure, one should suspect pseudotumor cerebri because SCN palsy is one of the most common findings in patients with pseudotumor cerebri.9,10 Papilledema is the hallmark physical finding of pseudotumor cerebri, and combination of SCN palsy and papiledema and magnetic resonance (MR) findings supporting pseudotumor cerebri is enough for diagnosis even if opening pressure of lumbar puncture is not very high as that in our patient.11 Inflammatory and infectious causes can also cause SCN palsy. Four of our patients (28.5%) had an inflammatory or infectious condition (MS, GBS, meningitis), which is relatively higher than the rates reported in the literature.2,3 It is not uncommon for adult patients with MS to have SCN palsy as a presenting sign reported as 10% in adult series, but it is rarely reported in children.12 The presence of SCN palsy in these patients is usually caused by brain stem demyelination affecting the sixth nerve nucleus or fascicular portion of the nerve.12 Brain stem involvement in adult patients with MS is frequent and includes the seventh nerve involvement, ataxia, and contralateral hemiparesis along with conjugate gaze palsy as seen in our patient.12 Rarely, SCN palsy can be an isolated finding in MS, but if it is accompanied by the seventh nerve palsy, conjugate gaze palsy, ataxia, and contralateral
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hemiparesis, MS should be considered. Two of 14 patients with sixth cranial nerve palsy were diagnosed with Miller Fisher variant of GBS. According to the original description of Ropper,13 abducens nerve palsy associated with antecedent infection, acral paresthesias, hyporeflexia or areflexia, and albuminocytological dissociation should be classified as a regional variant of GBS. Our patients had weakness in the lower extremities, hyporeflexia, and albuminocytological dissociation or antecedent infection with Campylobacter jejuni, leading to the diagnosis of Miller Fisher syndrome. None of our patients with paresthesia had ataxia. All of the remaining 4 patients had isolated abducens paralysis with otherwise normal neurological examination results. The results of neuroimaging studies did not show any intracranial pathology. Previous studies showed 5% to 20% miscellaneous benign etiologies or idiopathic cases of abducens palsy.1,3 There are some case reports showing benign conditions such as sinusitis or benign masses causing isolated abducens nerve palsy; therefore, if abducens paralysis is isolated and neuroimaging studies did not show any pathological finding, miscellaneous or benign etiologies could be responsible for SCN palsy.14–16 There is a higher-than-expected risk for neoplasm in patients with isolated abducens paralysis; therefore, neuroimaging should not be delayed in patients with acute SCN palsy especially if they have accompanying signs and symptoms.17 Other cranial nerve involvements or long tract signs are usually seen in patients with trauma or tumor. The only exception in our series was patient 13 with dural sinus thrombosis who presented with isolated acute SCN palsy and had otherwise normal neurological examination findings.5 All patients with idiopathic abducens palsy or palsy due to benign conditions had normal neurological examination findings other than SCN palsy and had no additional complaints. Our hospital is a tertiary and reference university hospital in the center of Turkey with a high number of yearly pediatric emergency visits. Therefore, we can generalize the results for a fairly large population. Our results were also concordant with those of other studies because tumors are the leading cause of sixth nerve palsy in childhood.3 Trauma is another common cause of SCN palsy; however, unlike other series in the literature, none of our patients had traumatic SCN paralysis. There are other trauma centers sharing trauma cases with our hospital, which may have caused the low number of cases in our study. Although the study has limitations owing to its retrospective design and small group of patients, we were able to document multiple etiologies underlying acute SCN palsy in childhood. A thorough history and neurological examination in the pediatric emergency department are crucial for etiological diagnosis of © 2015 Wolters Kluwer Health, Inc. All rights reserved.
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Pediatric Emergency Care • Volume 32, Number 5, May 2016
SCN palsy in childhood. A small portion of patients may have signs and symptoms owing to SCN palsy as well as otherwise normal findings, and they may still have significant structural abnormalities as the underlying cause. Therefore, neuroimaging studies, particularly brain MRI, should be performed to enable prompt diagnosis and treatment at the emergency settings where available. In conclusion, we showed that etiology and differential diagnosis spectrum of patients presenting with acute SCN paralysis to pediatric emergency department are sparse. However, they may have significant causes such as tumors, increased intracranial pressure, and inflammatory disorders of the central nervous system. Therefore, patients with acute SCN palsy should be examined in detail, including neuroimaging studies, especially if they have additional clinical signs or symptoms. REFERENCES 1. Patel SV, Mutyala S, Leske DA, et al. Incidence, associations, and evaluation of sixth nerve palsy using a population based method. Ophthalmology. 2004;111:369–375. 2. Kodsi SR, Younge BR. Acquired oculomotor, trochlear, and abducent cranial nerve palsies in pediatric patients. Am J Ophthalmol. 1992;114: 568–574. 3. Lee MS, Galetta SL, Volpe NJ, et al. Sixth nerve palsies in children. Pediatr Neurol. 1999;20:49–52. 4. Chi SL, Bhatti MT. The diagnostic dilemma of neuro-imaging in acute isolated sixth nerve palsy. Curr Opin Ophthalmol. 2009;20:423–429.
Acute Abducens Nerve Paralysis in Children
7. Chen KS, Hung IJ, Lin KL. Isolated abducens nerve palsy: an unusual presentation of leukemia. J Child Neurol. 2002;17:850–851. 8. Ghosh PS, Ghosh D, Goldfarb J, et al. Lateral sinus thrombosis associated with mastoiditis and otitis media in children: a retrospective chart review and review of the literature. J Child Neurol. 2011;26: 1000–1004. 9. Babikian P, Corbett J, Bell W. Idiopathic intracranial hypertension in children: the Iowa experience. J Child Neurol. 1994;9:144–149. 10. Incecik F, Hergüner MO, Altunbaşak S. Evaluation of sixteen children with pseudotumor cerebri. Turk J Pediatr. 2011;53:55–58. 11. Friedman DI. The pseudotumor cerebri syndrome. Neurol Clin. 2014;32: 363–396. 12. Barr D, Kupersmith MJ, Turbin R, et al. Isolated sixth nerve palsy: an uncommon presenting sign of multiple sclerosis. J Neurol. 2000;247: 701–704. 13. Ropper AH. Further regional variants of acute immune polyneuropathy. Bifacial weakness or sixth nerve paresis with paresthesias, lumbar polyradiculopathy, and ataxia with pharyngeal-cervical-brachial weakness. Arch Neurol. 1994;51:671–675. 14. Mahoney NR, Liu GT. Benign recurrent sixth (abducens) nerve palsies in children. Arch Dis Child. 2009;94:394–396. 15. Taskapilioglu O, Yurtogullari S, Yilmaz E, et al. Isolated sixth nerve palsy due to plasma cell granuloma in the sphenoid sinus: case report and review of the literature. Clin Neuroradiol. 2011;21:235–238.
5. Afifi AK, Bell WE, Menezes AH. Etiology of lateral rectus palsy in infancy and childhood. J Child Neurol. 1992;7:295–299.
16. Ada M, Kaytaz A, Tuskan K, et al. Isolated sphenoid sinusitis presenting with unilateral VIth nerve palsy. Int J Pediatr Otorhinolaryngol. 2004;68: 507–510.
6. Baldawa S, Gopalakrishnan CV. Bilateral abducent nerve palsy as the initial clinical manifestation of medulloblastoma. Acta Neurochir (Wien). 2010; 152:1947–1948.
17. Dotan G, Rosenfeld E, Stolovitch C, et al. The role of neuroimaging in the evaluation process of children with isolated sixth nerve palsy. Childs Nerv Syst. 2013;29:89–92.
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Acute Abducens Nerve Paralysis in the Pediatric Emergency Department Analysis of 14 Patients Ozlem Teksam, MD,* Ayse Gultekingil Keser, MD,* Bahadir Konuskan, MD,† Goknur Haliloglu, MD,† Kader Karli Oguz, MD,§ and Dilek Yalnizoglu, MD† Objectives: Sixth cranial nerve (SCN) palsy is an uncommon but important neurological problem in patients admitted to pediatric emergency department. The underlying etiology of SCN palsy has a wide range from viral infections to intracranial tumors; therefore, a careful and systematic approach is necessary while examining these patients. Methods: Fourteen patients who presented with acute SCN paralysis to pediatric emergency department during the last 10 years were examined. Results: The age at the time of admission ranged between 14 months and 16 years (median, 9.5 years). Of the 14 patients, 5 were girls and 9 were boys. A total of 3 of the 14 patients had bilateral cranial nerve VI paralysis, and 9 patients had additional abnormal findings on neurological examination. Neuroimaging studies included cranial tomography (n = 3) and brain magnetic resonance imaging in all patients. The underlying etiology was malignancy (n = 3); glioma, medulloblastoma, acute lymphoblastic leukemia, and dural sinus thrombosis (n = 2); as well as Guillain-Barre syndrome (n = 2), multiple sclerosis (n = 1), pseudotumor cerebri (n = 1), and meningitis (n = 1). The remaining 4 patients had miscellaneous benign etiologies. Conclusions: Other lesions of primary brain tumors causing increased intracranial pressure constitute 50% of the underlying etiology, followed by Guillain-Barre syndrome (14.2%). However, these patients had neurological symptoms signs, in addition to diplopia or SCN paralysis. Patients admitted to pediatric emergency department with acute SCN paralysis should be examined in detail to disclose the underlying etiology especially if they present with additional clinical signs or symptoms. Key Words: abducens nerve paralysis, neuroimaging, acute (Pediatr Emer Care 2016;32: 307–311)
S
ixth cranial nerve (SCN) palsy is considered to be the most common cranial nerve palsy in children.1,2 Etiologies underlying SCN palsy vary from minor causes such as viral infections to neoplasms causing increased intracranial pressure.1 Neoplasms and trauma are found to be the most common etiologies causing SCN palsy in children, followed by other causes of increased intracranial pressure, inflammation, congenital causes, and miscellaneous other etiologies.2,3 Considering the high frequency of serious causes of SCN palsy, immediate and careful evaluation and treatment of patients are crucial. We evaluated the underlying etiologies of patients with acute SCN palsy who were admitted to our pediatric emergency department.
From the *Department of Pediatrics, Division of Pediatric Emergency Medicine, †Department of Pediatrics, Division of Pediatric Neurology, and §Department of Radiology, Hacettepe University Medical Faculty, Ankara, Turkey. Disclosure: The authors declare no conflict of interest. Reprints: Ozlem Teksam, MD, Department of Pediatrics, Division of Pediatric Emergency Medicine, Hacettepe University Medical School, İhsan Doğramacı Children's Hospital, Sihhiye, Ankara 06100 Turkey (e‐mail: [email protected]; [email protected]). Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved. ISSN: 0749-5161
METHODS We retrospectively reviewed medical records of patients who were admitted to Hacettepe University Children's Hospital Pediatric Emergency Department between January 1, 2002 and December 31, 2012. Hacettepe University Children's Hospital is an urban tertiary care center in the capital of Turkey with more than 60,000 pediatric emergency patient visits annually. Patients were identified by searching the hospital's electronic data base using word root search for abducens, sixth nerve, and outward gaze paralysis. In addition, all cranial computed tomography (CT) and magnetic resonance imaging (MRI) reports performed within the last 10 years in the pediatric emergency department were reviewed. Age, sex, symptoms, complaints, neurological examination findings, as well as laboratory studies and neuroimaging results were recorded. Cranial and spinal neuroimaging studies were reevaluated by a neuroradiologist (K.K.O.) with an experience of 14 years. Final diagnosis and clinical follow-up were assessed. Approval for review was obtained from the ethics committee of Hacettepe University medical faculty.
RESULTS Within the defined period of 10 years, 21 patients with acute SCN palsy who were admitted to our pediatric emergency department were identified, and 7 patients were excluded owing to inadequate data. The age at the time of admission ranged between 14 months and 16 years (median, 9.5 years). Nine of them (64.3%) were boys. Thirteen patients (92.8%) had complaints related to SCN palsy including diplopia, inward deviation of eye, or difficulty in looking to 1 side. One patient (patient 11) (7%) did not have any complaints related to SCN palsy but had headache, vomiting, and confusion; sixth nerve palsy was found on physical examination. Three patients had isolated complaints of diplopia and/or difficulty in looking to 1 side (21.4%). Headache and vomiting were the most common accompanying symptoms (50%), followed by fever (28.5%). Clinical and diagnostic findings of all patients are summarized in Table 1. Neurological examination results revealed that 6 patients (42.8%) had sixth nerve palsy in the left eye, 5 in the right eye (35.7%), and 3 in both eyes (21.4%). Three patients had paralysis in other directions as well (21.4%), and 1 patient had nystagmus in addition to SCN paralysis. Two patients had weakness in the lower extremities and absent deep tendon reflexes (14.2%). Three patients were lethargic (21.4%). One patient had ataxia and dysmetria (7%). Two patients (14.2%) had bilateral papilledema, and one of them had central facial paralysis on the same side with gaze paralysis (7%). One patient had tongue deviation on the same side (7%). One patient (7%) had nuchal rigidity. Five patients (35.7%) had merely gaze paralysis and no other neurological abnormalities; 3 of them (21.4%) had no other complaints but gaze paralysis. Contrast-enhanced brain MRI was obtained in all patients, 3 patients had cranial CT, and 1 had spinal MRI. Ten patients
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TABLE 1. Demographic Characteristics, Clinical, Laboratory, and Neuroimaging Findings of All Patients Patient No. Age, Sex 1
5 y, F
2
9 y, F
3
6 y, F
4
10 y, M
5
16 y, M
6 7 8 9
10
11
12 13
14
Complaint on admission
Neurological Examination
Diplopia (right eye), Bilateral SCN paralysis, weakness in legs nystagmus, absent DTR, motor weakness in the lower extremities Fever, vomiting, Lethargic, SCN (left headache eye) paralysis, ataxia, dysmetria Pain in legs, Bilateral left SCN palsy, difficulty in decreased DTR, motor walking weakness in lower extremities Headache, nausea, SCN paralysis in the vomiting, right eye, Babinski strabismus, positive on the diplopia left side
Imaging Studies
Laboratory Results
Diagnosis
Cranial MRI: normal; Normal CSF, stool culture: GBS spinal MRI: Linear C. jejuni; EMG: early contrast enhancement phase of demyelinating in the cauda equina disorder Cranial MRI: pons glioma NS Pons glioma
Cranial MRI: normal
CSF: albuminocytologic dissociation; EMG : myopathic changes MTHFR homozygous mutation
Cranial CT: acute sinus thrombosis; Cranial MRI-MR venography: venous thrombosis in bilateral, transverse sinuses, superior sagittal sinus Cranial MRI: IgG index: 0.58 contrast-enhancing lesions in the right pontomedullary junction
Paresthesia in the left Lateral, upward, and arm and left leg, downward gaze diplopia, difficulty paralysis in the in looking to the right eye right side 2.5 y, M Strabismus in the SCN (left eye) paralysis Cranial MRI: normal left eye, URTI history (+) 10 y, M Diplopia SCN (right eye) paralysis Cranial MRI: right mastoiditis and petrositis 14 y, M Diplopia URTI SCN (left eye) paralysis Cranial MRI: normal history (+) 4 y, M Strabismus, Lethargic, bilateral Cranial MRI: vomiting, papilledema; left facial medulloblastoma headache, paralysis; left SCN originating from vermis, confusion paralysis hydrocephalus 14 y, M Fever, headache, SCN (left eye) paralysis, Cranial MRI: dural paresthesia in the left-sided deviation thickening and tongue, difficulty of tongue enhancement along the to look on the cerebral hemispheres left side and cranial nerves 9 y, F Headache, vomiting, Lateral and downward Cranial CT: normal; confusion gaze paralysis (right cranial MRI: diffuse eye), mild SCN (left leptomeningeal contrast eye) paralysis, nuchal enhancement around rigidity, lethargy the sixth, seventh, and eighth nerves. 14 mo, M Vomiting, strabismus, SCN (right eye) paralysis Cranial MRI: cerebral fever, fatigue volume loss 13 y, M Fever, headache, SCN (right eye) paralysis Cranial CT: right dural sinus thrombosis; vomiting, diplopia cranial MRI: thrombosis in the superior sagittal and right transverse sinus 11 y, F Diplopia, headache, Inward and outward gaze Cranial MRI: increased vomiting paralysis (left eye), perioptic CSF, left exophthalmos, arachnoid cyst bilateral papilledema
GBS
Venous thrombosis, Behcet disease
MS
NS
Unexplained
NS
Unexplained
NS
Unexplained
NS
Medulloblastoma
Bone marrow aspiration: blasts (+)
ALL
CSF: abnormal
Meningitis
NS
Unexplained
Deficiency of protein C and protein S
Sinus venous thrombosis
CSF pressure: 220 mm Hg
Pseudotumor cerebri
ALL indicates acute lymphoblastic leukemia; DTR, deep tendon reflexes; F, female; IgG, immunoglobulin; M, male; NS, not significant; SCN, sixth cranial nerve; URTI, upper respiratory tract infection.
(71.4%) had abnormal findings on MRI; 2 patients (14.2%), on CT. Neuroimaging findings are also summarized in Table 1. Brain MRI of patient 2 who had fever, headache, vomiting, ataxia,
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and dysmetria showed a diffuse pontine glioma. Brain MRI of patient 9 who had vomiting, headache, confusion, lethargy, bilateral papilledema, and left-sided facial paralysis showed a © 2015 Wolters Kluwer Health, Inc. All rights reserved.
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Pediatric Emergency Care • Volume 32, Number 5, May 2016
medulloblastoma originating from the vermis, widespread intracranial metastasis, and hydrocephalus (Fig. 1). Brain MRI of patient 10 who had headache, fever, paresthesia in the tongue, and left-sided deviation of the tongue demonstrated an abnormal bone marrow with dural thickening and contrast enhancement along the cerebral hemispheres and cranial nerves (Fig. 2). Therefore, a bone marrow aspiration was done, confirming the diagnosis of acute lymphoblastic leukemia. Brain MRI of patient 4 who experienced headache and vomiting showed venous thrombosis (Fig. 3). On follow-up, this patient was diagnosed with Behçet disease. Brain MRI of patient 13 who had headache, fever, and vomiting showed thrombosis in the superior sagittal and right transverse sinus. The MRI of patient 5 who had paresthesia in the left arm and left leg as well as outward, upward, and downward paralysis of the right eye showed contrast-enhancing lesions and consistent with multiple sclerosis (MS). The MRI of patient 11 who had headache, vomiting, confusion, lethargy, and nuchal rigidity showed diffuse leptomeningeal and bilateral contrast enhancement around the sixth, seventh, and eighth nerves; however, her lumbar puncture did not show any blood cells or microorganisms. Patients 1 and 3 had normal brain MRI; however, they had difficulty in walking and weakness in the lower extremities, along with absent or decreased deep tendon reflexes, which led to the clinical diagnosis of Guillain-Barré syndrome (GBS), confirmed with electromyelography (EMG). Findings of EMG of patient 1 showed an early phase of a demyelinating disorder, and her spinal MRI showed linear contrast enhancement in the cauda equina compatible with the diagnosis of GBS. Patient 3 had a normal EMG, and lumbar puncture was done, showing albuminocytologic dissociation. Follow-up EMG study showed myopathic changes, and her symptoms resolved without treatment. On the basis of clinical picture and cerebrospinal fluid (CSF) findings, she was diagnosed with GBS. Patient 14 had headache, vomiting, and bilateral papiledema. Her MRI showed increased perioptic CSF, bilateral papilledema, and left middle cranial fossa arachnoid cyst. She had normal CSF pressure on lumbar puncture, and her symptoms resolved with dexamethasone treatment. Patient 12 had vomiting and a suspected convulsion; neurological examination results were normal, except SCN paralysis in the right eye. Her MRI showed cerebral volume loss. Her symptoms improved during a follow-up, leading to the conclusion that the sixth nerve palsy could be caused by an infection not clearly identified. In summary, the final diagnosis was malignancy (glioma, medulloblastoma, acute lymphoblastic leukemia) in 3 patients (21.4%), dural sinus thrombosis in 2 (14.2%), GBS in 2 (14.2%),
FIGURE 1. Patient 4. Sagittal T1-weighted (T1W) MR venography (A) and axial fluid attenuated inversion recovery (B) (repetition time [TR]/echo time [TE]/inversion time; 8500/100/2000 milliseconds) images show thrombosis in the superior sagittal and straight sinuses by filling defect (arrows, A) and absence of flow void (dashed arrow, B).
Acute Abducens Nerve Paralysis in Children
FIGURE 2. Patient 9. Sagittal (A) and axial (B) postcontrast T1W (TR/TE, 550/15 milliseconds) images show midline enhancing posterior fossa mass and disseminated leptomeningeal involvement, also along with cranial nerves and nodular intraventricular seeding metastases (arrows in A and B).
MS (7%), meningitis (7%), and pseudotumor cerebri (7%) each in 1 patient. Four patients were diagnosed with idiopathic SCN palsy (28.5%).
DISCUSSION Sixth cranial nerve nucleus is located within the genu of facial nerve, and SCN has a long course from pons to lateral rectus muscle.3 Nerve fascicles arise from the anterior surface of the pontine tegmentum; exit from the pontomedullary junction, cross subarachnoid space, and ascend clivus; as well as enter petrous bone and cavernous sinus.3,4 Inside the sinus, SCN is the only nerve that travels free in the sinus wall. It then enters the orbit through the superior orbital fissure to innervate the lateral rectus muscle.4 Because of its long intracranial course, it is susceptible to injury either directly or indirectly owing to increased intracranial pressure.1 Different pathological causes affect SCN at different locations: inflammation and infection affect the nerve at the subarachnoid space; pressure and trauma at the skull base; and neoplasms, anywhere along the tract.3 Neoplasms are one of the most common etiologies found in patients with acquired SCN palsy.3,5 A total of 3 of the 14 patients had neoplasms: 2 had primary brain tumors and 1 had hematologic malignancy. Malignancies can result in SCN palsy in different ways. The location of neoplasm can directly make pressure on the nerve such as gliomas.6 However, the primary site of neoplasm can be elsewhere, such as medulloblastomas; in that case, tumor may result in increased intracranial pressure or hydrocephalus causing displacement of brain stem or stretching or compression of the nerve as well.6 Moreover, widespread intracranial leptomeningeal metastases can cause abducens palsy far from the primary location of the tumor; therefore, abducens nerve palsy should not be considered as a localizing sign in these conditions. Nevertheless, neoplasms constitute an important etiology in differential diagnosis of abducens palsy, especially if it is accompanied by headache, nausea, lethargy, focal neurological signs, or posterior fossa signs; emergent neuroimaging should be done in these patients. Presentation with isolated SCN palsy is rare in malignancy; however, it still should be ruled out, considering the high occurrence of neoplasms in these patients.3 One of our patients was found to have acute lymphoblastic leukemia, which is a rare cause for patients who present with SCN palsy. Chen et al7 described a patient who presented with SCN palsy and fever with a normal MRI, later found out to have acute lymphoblastic leukemia. Although our patient was suspected to have a bone marrow disease with pachymeningeal involvement by contribution of MRI, it should be noted that
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Teksam et al
FIGURE 3. Patient 10. Axial precontrast (A) and postcontrast (B) T1W (TR/TE, 550/15 milliseconds) images show diffuse low signal intensity of bone marrow (arrow, A) as well as diffuse dural thickening and enhancement (double thin arrows, B). Please also note the thickening of the dura of the cavernous sinuses (dashed arrow, C).
patients with SCN palsy should be examined for hematologic malignancy even in the absence of pathological findings on MRI, especially if they have fever or symptoms related to increased intracranial pressure. Three of our patients (21.4%) had SCN palsy due to nonmalignant intracranial lesions, causing increased intracranial pressure in agreement with the study of Lee at al.3 Two of these patients had dural sinus thrombosis, and 1 had pseudotumor cerebri. Dural sinus thrombosis may cause SCN paralysis by increasing intracranial pressure. Ghosh et al8 reported that, of 13 patients with lateral sinus thrombosis, 4 (30%) were found to have SCN palsy. Dural sinus thrombosis should be included in the etiological diagnosis of patients with SCN palsy, especially if they have symptoms related to increased intracranial pressure such as headache, nausea, and papilledema. History of recent upper respiratory tract infection or otitis media should be considered in patients with SCN palsy because they may be risk factors for dural sinus thrombosis.8 One of our patients with dural sinus thrombosis had Behçet disease, and the other had protein C and protein S deficiency as the underlying etiology for thrombosis. An underlying prothrombotic disease should raise the suspicion for dural venous thrombosis in patients with acute SCN palsy. If patients with SCN palsy have symptoms related to increased intracranial pressure but there are no pathological findings on brain imaging except findings related to increased intracranial pressure, one should suspect pseudotumor cerebri because SCN palsy is one of the most common findings in patients with pseudotumor cerebri.9,10 Papilledema is the hallmark physical finding of pseudotumor cerebri, and combination of SCN palsy and papiledema and magnetic resonance (MR) findings supporting pseudotumor cerebri is enough for diagnosis even if opening pressure of lumbar puncture is not very high as that in our patient.11 Inflammatory and infectious causes can also cause SCN palsy. Four of our patients (28.5%) had an inflammatory or infectious condition (MS, GBS, meningitis), which is relatively higher than the rates reported in the literature.2,3 It is not uncommon for adult patients with MS to have SCN palsy as a presenting sign reported as 10% in adult series, but it is rarely reported in children.12 The presence of SCN palsy in these patients is usually caused by brain stem demyelination affecting the sixth nerve nucleus or fascicular portion of the nerve.12 Brain stem involvement in adult patients with MS is frequent and includes the seventh nerve involvement, ataxia, and contralateral hemiparesis along with conjugate gaze palsy as seen in our patient.12 Rarely, SCN palsy can be an isolated finding in MS, but if it is accompanied by the seventh nerve palsy, conjugate gaze palsy, ataxia, and contralateral
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hemiparesis, MS should be considered. Two of 14 patients with sixth cranial nerve palsy were diagnosed with Miller Fisher variant of GBS. According to the original description of Ropper,13 abducens nerve palsy associated with antecedent infection, acral paresthesias, hyporeflexia or areflexia, and albuminocytological dissociation should be classified as a regional variant of GBS. Our patients had weakness in the lower extremities, hyporeflexia, and albuminocytological dissociation or antecedent infection with Campylobacter jejuni, leading to the diagnosis of Miller Fisher syndrome. None of our patients with paresthesia had ataxia. All of the remaining 4 patients had isolated abducens paralysis with otherwise normal neurological examination results. The results of neuroimaging studies did not show any intracranial pathology. Previous studies showed 5% to 20% miscellaneous benign etiologies or idiopathic cases of abducens palsy.1,3 There are some case reports showing benign conditions such as sinusitis or benign masses causing isolated abducens nerve palsy; therefore, if abducens paralysis is isolated and neuroimaging studies did not show any pathological finding, miscellaneous or benign etiologies could be responsible for SCN palsy.14–16 There is a higher-than-expected risk for neoplasm in patients with isolated abducens paralysis; therefore, neuroimaging should not be delayed in patients with acute SCN palsy especially if they have accompanying signs and symptoms.17 Other cranial nerve involvements or long tract signs are usually seen in patients with trauma or tumor. The only exception in our series was patient 13 with dural sinus thrombosis who presented with isolated acute SCN palsy and had otherwise normal neurological examination findings.5 All patients with idiopathic abducens palsy or palsy due to benign conditions had normal neurological examination findings other than SCN palsy and had no additional complaints. Our hospital is a tertiary and reference university hospital in the center of Turkey with a high number of yearly pediatric emergency visits. Therefore, we can generalize the results for a fairly large population. Our results were also concordant with those of other studies because tumors are the leading cause of sixth nerve palsy in childhood.3 Trauma is another common cause of SCN palsy; however, unlike other series in the literature, none of our patients had traumatic SCN paralysis. There are other trauma centers sharing trauma cases with our hospital, which may have caused the low number of cases in our study. Although the study has limitations owing to its retrospective design and small group of patients, we were able to document multiple etiologies underlying acute SCN palsy in childhood. A thorough history and neurological examination in the pediatric emergency department are crucial for etiological diagnosis of © 2015 Wolters Kluwer Health, Inc. All rights reserved.
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Pediatric Emergency Care • Volume 32, Number 5, May 2016
SCN palsy in childhood. A small portion of patients may have signs and symptoms owing to SCN palsy as well as otherwise normal findings, and they may still have significant structural abnormalities as the underlying cause. Therefore, neuroimaging studies, particularly brain MRI, should be performed to enable prompt diagnosis and treatment at the emergency settings where available. In conclusion, we showed that etiology and differential diagnosis spectrum of patients presenting with acute SCN paralysis to pediatric emergency department are sparse. However, they may have significant causes such as tumors, increased intracranial pressure, and inflammatory disorders of the central nervous system. Therefore, patients with acute SCN palsy should be examined in detail, including neuroimaging studies, especially if they have additional clinical signs or symptoms. REFERENCES 1. Patel SV, Mutyala S, Leske DA, et al. Incidence, associations, and evaluation of sixth nerve palsy using a population based method. Ophthalmology. 2004;111:369–375. 2. Kodsi SR, Younge BR. Acquired oculomotor, trochlear, and abducent cranial nerve palsies in pediatric patients. Am J Ophthalmol. 1992;114: 568–574. 3. Lee MS, Galetta SL, Volpe NJ, et al. Sixth nerve palsies in children. Pediatr Neurol. 1999;20:49–52. 4. Chi SL, Bhatti MT. The diagnostic dilemma of neuro-imaging in acute isolated sixth nerve palsy. Curr Opin Ophthalmol. 2009;20:423–429.
Acute Abducens Nerve Paralysis in Children
7. Chen KS, Hung IJ, Lin KL. Isolated abducens nerve palsy: an unusual presentation of leukemia. J Child Neurol. 2002;17:850–851. 8. Ghosh PS, Ghosh D, Goldfarb J, et al. Lateral sinus thrombosis associated with mastoiditis and otitis media in children: a retrospective chart review and review of the literature. J Child Neurol. 2011;26: 1000–1004. 9. Babikian P, Corbett J, Bell W. Idiopathic intracranial hypertension in children: the Iowa experience. J Child Neurol. 1994;9:144–149. 10. Incecik F, Hergüner MO, Altunbaşak S. Evaluation of sixteen children with pseudotumor cerebri. Turk J Pediatr. 2011;53:55–58. 11. Friedman DI. The pseudotumor cerebri syndrome. Neurol Clin. 2014;32: 363–396. 12. Barr D, Kupersmith MJ, Turbin R, et al. Isolated sixth nerve palsy: an uncommon presenting sign of multiple sclerosis. J Neurol. 2000;247: 701–704. 13. Ropper AH. Further regional variants of acute immune polyneuropathy. Bifacial weakness or sixth nerve paresis with paresthesias, lumbar polyradiculopathy, and ataxia with pharyngeal-cervical-brachial weakness. Arch Neurol. 1994;51:671–675. 14. Mahoney NR, Liu GT. Benign recurrent sixth (abducens) nerve palsies in children. Arch Dis Child. 2009;94:394–396. 15. Taskapilioglu O, Yurtogullari S, Yilmaz E, et al. Isolated sixth nerve palsy due to plasma cell granuloma in the sphenoid sinus: case report and review of the literature. Clin Neuroradiol. 2011;21:235–238.
5. Afifi AK, Bell WE, Menezes AH. Etiology of lateral rectus palsy in infancy and childhood. J Child Neurol. 1992;7:295–299.
16. Ada M, Kaytaz A, Tuskan K, et al. Isolated sphenoid sinusitis presenting with unilateral VIth nerve palsy. Int J Pediatr Otorhinolaryngol. 2004;68: 507–510.
6. Baldawa S, Gopalakrishnan CV. Bilateral abducent nerve palsy as the initial clinical manifestation of medulloblastoma. Acta Neurochir (Wien). 2010; 152:1947–1948.
17. Dotan G, Rosenfeld E, Stolovitch C, et al. The role of neuroimaging in the evaluation process of children with isolated sixth nerve palsy. Childs Nerv Syst. 2013;29:89–92.
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