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Original Article

A 3‑Year Review of Cranial Palsies from the University of Port Harcourt Teaching Hospital Eye Clinic, Nigeria

Chinyere Nnenne Pedro‑Egbe, Bassey Fiebai, Elizabeth Akon Awoyesuku

ABSTRACT Access this article online Website: Purpose: To provide the types, frequency and clinical information on common cranial nerve www.meajo.org palsies seen at the Eye Clinic at the University of Port Harcourt Teaching Hospital. DOI: Materials and Methods: A chart review was performed of patients who presented with cranial 10.4103/0974-9233.129770 nerve palsy at the Eye Clinic over a 3‑year period (January 2009‑December 2011). Data were Quick Response Code: collected on age, sex, type of cranial nerve palsy, a history of systemic disease such as mellitus (DM), and cerebrovascular disease. Exclusion criteria included medical charts with incomplete data. Data was analyzed using Epi‑info Version 6.04D. Statistical significance was indicated byP < 0.05. Results: Twenty‑four patients had cranial nerve palsies. There were 11 males and 13 females with a mean age of 34.50 ± 18.41 years. Four patients (26.6%) had while three patients (20%) had . Complete ophthalmoplegia was noted in two patients (13.3%). The 3rd and 6th cranial were affected in seven patients each (29.2%) and five patients (20.8%) had 7th cranial nerve palsy. Approximately 38% of patients with cranial nerve palsies had systemic disorders (16.7% systemic hypertension; 12.5% DM). The relationship between cranial nerve palsy and systemic disorder was statistically significant (P < 0.01). Conclusion: This is the first study in the literature on ocular cranial nerve palsies in Southern Nigeria. Third and sixth cranial nerve palsies were the most common cases to present to the University of Port Harcourt Teaching Hospital Eye Clinic. There was a statistically significant association to systemic disorders such as hypertension and DM and majority of cases with 6th cranial nerve palsy.

Key words: Cranial Nerve Palsies, Eye Clinic, Port Harcourt

INTRODUCTION to determine the probable etiology. The 3rd, 4th and 6th cranial nerve palsies can limit eye movements and produce . ranial nerve palsy is a form of palsy involving one or The orientation of the diplopia is usually based on the affected Cmore of the . It may cause a complete cranial nerve. In addition to the limitation of eye movements, or partial weakness or paralysis of the areas innervated a 3rd nerve palsy can also cause or . Some by the affected nerve. Cranial nerve palsies can be cranial nerve palsies are easy to identify because they affect congenital or the result of traumatic or vascular disorders eye movements or facial expression with resultant difficulty in (hypertension, diabetes mellitus (DM), , ). controlling eye movements or engaging in facial expressions such They can also be due to infections, headaches, tumors as smiling. Some cranial nerve palsies resolve spontaneously, or elevated . The age of the patient as well especially if they are due to microvascular causes such as DM as clinical findings suggests the type of diagnostic tests required and hypertension.

Department of ( Unit), College of Health Sciences, University of Port Harcourt, Port Harcourt, Nigeria Corresponding Author: Dr. Pedro‑Egbe Chinyere Nnenne, Department of Surgery (Ophthalmology Unit), College of Health Sciences, University of Port Harcourt, Port Harcourt, Nigeria. E‑mail: [email protected]

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Pedro‑Egbe. et al.: Ocular Cranial Nerve Palsies in Port Harcourt

Of all ocular cranial nerve palsies, several authors have reported RESULTS that 6th cranial nerve palsy was the most common, followed by the 3rd and then 4th cranial nerves.1‑3 From these studies, A total of 24 patients presented with cranial nerve palsies. the common causes of ocular cranial nerve palsies include There were 11 males and the male to female ratio was 1:1.2. head trauma, space‑occupying lesions, and vascular lesions The mean age of the patients was 34.50 ± 18.41 years (DM, hypertension and ).2 In a cohort of 915 (range, 4 years to 75 years). The age and gender distribution of stroke patients, Rowe et al., reported ocular motor cranial the study subjects is as presented in Table 1. Most of the patients nerve palsies in 10% of the patients.4 Most (58%) of the with cranial nerve palsies (N = 14/24; 58.3%) were between palsies involved the 6th nerve, followed by the 3rd (26%) and 20 years and 39 years old [Table 1]. then the 4th cranial nerves (16%).4 They4 reported unilateral third nerve palsy in 23 patients (26%), unilateral fourth nerve The most common presenting symptoms were headache and palsy in 14 patients (16%) and unilateral in diplopia, affecting 7 (21.2%) patients each; this was followed 52 patients (58%). They4 found that the most common location by fever in 5 patients (15.2%) [Table 2]. of a stroke lesion causing cranial nerve palsy was the brainstem or cerebellum. They also reported that the presence of manifest was normal (VA = 6/6) in 41 eyes (85.4%), was significantly higher in third and fourth nerve impaired (VA <6/18) in 6.3% (N = 3) eyes and 4 eyes (8.3%) palsies than sixth nerve palsy. were blind (VA = <3/60). Table 3 presents the ocular findings. Two patients each (13.3%) had 15° exotropia and 15° esotropia, This study provides clinical information and the frequency of respectively, while two patients each (13.3%) had severe ptosis the most common types of cranial nerve palsies evaluated at the and complete ophthalmoplegia. Three patients (20.0%) had University of Port Harcourt Teaching Hospital Eye Clinic and and 8 of the 24 patients (33.3%) had sluggishly their association to systemic disorders. reactive .

MATERIALS AND METHODS Table 4 presents the type of cranial palsy. The 3rd and 6th cranial nerves were affected in seven patients each (29.2%; N = 7/24) A retrospective chart review was performed of all patients with cranial nerve palsies who presented to the University Table 1: Age and gender distribution of patients with cranial of Port Harcourt Teaching Hospital Eye Clinic from January nerve palsies 2009 to December 2011. Data were collected and analyzed on Age group (Years) Sex Total age, sex, history of systemic disease such as diabetes mellitus, Male Female hypertension and cerebrovascular disease. The details of the <10-19 0 (0.0) 2 (8.3) 2 (8.3) 20‑29 6 (25.0) 5 (20.8) 11 (45.8) systemic diseases were recorded from the patient charts. 30‑39 2 (8.3) 1 (4.2) 3 (12.5) Ocular examination data were collected on the presenting 40‑49 0 (0.0) 1 (4.2) 1 (4.2) symptoms and signs, visual acuity, range of extraocular motility 50‑59 2 (8.3) 2 (8.3) 4 (16.7) and pupillary light reaction. Visual acuity was assessed with 60‑69 1 (4.2) 1 (4.2) 2 (8.3) 70‑79 0 (0.0) 1 (4.2) 1 (4.2) a Snellen chart. Total 11 (45.8) 13 (54.2) 24 (100.0) Chi square=4.29, P=0.64* not statistically significant Our diagnosis of cranial nerve palsy was mainly clinical and was based on the presenting symptoms and signs, Table 2: Presenting symptoms of patients with cranial nerve which included severe headaches and fever, ptosis, diplopia, palsies lagophthalmos, deviation of the mouth to one side, esotropia, Symptoms Frequency (%) exotropia, or complete ophthalmoplegia. Headache 7 (21.2) Computed tomography of the was performed in Diplopia (horizontal and vertical) 7 (21.2) 9 patients; 8 were within normal limits and one showed an Fever 5 (15.2) intracranial mass. Exclusion criteria included case files with Negative 2 (6.1) Eye ache 1 (3.0) incomplete records (five) and the only case resulting from Blurred vision 2 (6.0) orbital trauma. Cannot close right upper 1 (3.0) Drooping of right upper eyelid 2 (6.1) Drooping of the left upper eyelid 2 (6.1) Data were analyzed using Epi‑info Version 6.04D (Centers for Otalgia 2 (6.1) Disease Control and Prevention, Atlanta, GA, USA). P values Deviation of the mouth to the left 1 (3.0) less than 0.05 were considered statistically significant. This study Neck stiffness 1 (3.0) adhered to the Tenets of the Declaration of Helsinki. Total 33 (100.0)

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Pedro‑Egbe. et al.: Ocular Cranial Nerve Palsies in Port Harcourt

while five patients (20.8%) had 7th cranial nerve palsy [Table 4]. Table 7 presents the relationship between cranial nerve palsy Only four patients (16.6%) had multiple cranial nerve and systemic disorders. About 38% of those with cranial nerve palsies [Table 4]. palsies had systemic disorders. Of these, two (12.5%) were diabetic, four had systemic hypertension (16.7%) and one each The relationship between cranial nerve palsy and pupillary had asthma, cerebral malarial and loss [Table 7]. The reaction is presented in Table 5. Most cranial nerve relationship between cranial nerve palsy and systemic disorder palsies (70.8%; N = 17/24) were associated with normal was statistically significant (P < 0.01) [Table 7]. There was pupillary reaction [Table 5]. Only 29.2% of cranial nerve palsies however no statistically significant difference between cranial were associated with sluggishly reactive pupils. Those with 3rd and nerve palsy and those with fever (not shown on table). multiple cranial nerve palsies had sluggishly reactive pupils. The relationship between cranial nerve palsies and pupillary reaction DISCUSSION was statistically significant (P = 0.02) [Table 5]. Over a three‑year period, only 24 cases of cranial nerve palsies Table 6 presents the relationship between cranial nerve palsy presented, compared to other studies where larger numbers and age. Most patients (48.3%; N = 11/24) with cranial nerve were seen. This is not surprising as stroke patients are rarely palsies were aged between 20 and 29 years old [Table 6]. This referred to our clinic from the medical outpatient department of is followed by those in the 50‑59 year age range, making up the Hospital. The few patients who presented were “walk‑ins” 16.7% (N = 4) of all cases of cranial nerve palsies [Table 6]. This without referral. Similarly, some cases, especially facial nerves relationship was statistically significant (P < 0.01) [Table 6]. palsies are managed by the ENT department explaining the very small number reported here. Table 3: Physical findings (ocular) of patients with cranial nerve palsies Our results show that most of the patients with cranial nerve Frequency (%) palsies were between 20 and 39 years of age with a mean of 15° Exotropia 2 (13.3) 34.50 ± 18.41 years (range, 4‑75 years). This differs from a 15° Esotropia 2 (13.3) 4 15° Hypertropia 1 (6.7) study by Rowe et al., where the mean age was 69.18 ± 14.19 30° Esotropia 1 (6.7) years (range, 1‑94 years). This difference is not surprising since 45° Exotropia 2 (13.3) Rowe et al.,4 study involved only stroke patients which may have Complete ophthalmolplegia 2 (13.3) accounted for the older age group as the risk factors to developing Lagophthalmos 3 (20.0) Severe ptosis 2 (13.3) a stroke are greater in older individuals. The most common Total 15 (100) presenting symptoms were headaches, fever, diplopia and ptosis. Diplopia and ptosis are in keeping with the functions of some of the affected cranial nerves. The only patient with fever and neck Table 4: Type of cranial nerve palsy in patients presenting to the University of Port Harcourt Teaching Hospital Eye Clinic stiffness had meningitis. Other fevers were ruled out as malaria Type of Palsy Frequency (%) as it is endemic in our region and commonly presents as fever. 3rd cranial nerve (LE) 4 (16.7) 3rd cranial nerve (RE) 3 (12.5) In our study, most patients (87.5%) had horizontal diplopia. 4th cranial nerve 1 (4.2) This was expected as the 3rd and 6th cranial nerves were the most 6th cranial nerve (LE) 2 (8.3) 4 th affected. In a study of stroke patients, Rowe et al., reported that 6 cranial nerve (RE) 5 (20.8) rd th 7th cranial nerve palsy (RE) 5 (20.8) the 3 and 6 cranial nerves were most affected, similar to our Multiple cranial nerves (LE) 2 (8.3) study. Of the seven patients with 6th cranial nerve palsy, four were Multiple cranial nerves (RE) 2 (8.3) hypertensive, two were diabetic and one patient had cerebral Total 24 (100.0) malaria. This concurs with other studies where abducens palsy is considered the most commonly encountered extraocular muscle Table 5: Relationship between cranial nerve palsy and pupillary palsy with an incidence of 11.3 per 100,000 people.5 Berlit reaction et al.,6 in their study of 165 patients suffering from abducens Cranial nerve palsy Pupillary reaction Total (%) nerve palsy found that a vascular origin (29.7%) was the most Sluggish (%) Active (%) common, followed by inflammatory diseases (19.4%) and 3rd cranial nerve 3 (12.5) 4 (16.7) 7 (29.2) tumors (10.9%), while traumatic abducens paresis (3.1%) was th 4 cranial nerve 0 (0.0) 1 (4.2) 1 (4.2) 7 6th cranial nerve 0 (0.0) 7 (29.1) 7 (29.2) rare. This confirms an earlier report by Moster who identified 7th cranial nerve 0 (0.0) 5 (20.8) 5 (20.8) vascular such as diabetes mellitus, hypertension Multiple cranial nerves 4 (16.7) 0 (0.0) 4 (16.6) and atherosclerosis. Moster found the vascular group was older Total 7 (29.2) 17 (70.8) 24 (100.0) compared to the younger group with and Chi square=18.54, P=0.02* statistically significant tumors as the more common causes.7

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Pedro‑Egbe. et al.: Ocular Cranial Nerve Palsies in Port Harcourt

Table 6: Relationship between cranial nerve palsy and age Age‑groups Cranial nerve palsy Total (%) 3rd Cranial N 4th Cranial N 6th Cranial N 7th Cranial N Multiple CN <10‑19 ‑ ‑ 1 (4.2) 1 (4.2) 2 (8.3) 20‑29 5 (20.8) ‑ 2 (8.3) 3 (12.5) 1 (4.2) 11 (48.3) 30‑39 1 (4.2) ‑ ‑ 1 (4.2) 1 (4.2) 3 (12.5) 40‑49 ‑ 1 (4.2) ‑ 1 (4.2) 50‑59 1 (4.2) 2 (8.3) 1 (4.2) 4 (16.7) 60‑69 1 (4.2) 1 (4.2) 2 (8.3) 70‑79 1 (4.2) 1 (4.2) Total 7 (29.2) 1 (4.2) 7 (29.2) 5 (20.8) 4 (16.7) 24 (100) Chi square=52.42, P<0.01* statistically significant

Table 7: Relationship between cranial nerve palsy and systemic disorder Cranial nerve palsy Systemic disorder DM HTN Asthma Cerebral malaria Hearing loss Total 3rd cranial nerve ‑ ‑ ‑ ‑ ‑ ‑ 4th cranial nerve ‑ ‑ ‑ ‑ ‑ ‑ 6th cranial nerve 2 (8.3) 4 (16.7) ‑ 1 (4.2) ‑ 7 (29.1) 7th cranial nerve ‑ ‑ 1 (4.2) ‑ ‑ 1 (4.2) Multiple cranial ‑ ‑ ‑ ‑ 1 (4.2) 1 (4.2) nerves RE Total 2 (8.3) 4 (16.7) 1 (4.2) 1 (4.2) 1 (4.2) 9 (37.5) Chi square=52.42, P<0.01* statistically significant

The mechanism of traumatic palsy may be direct fixed to the pons and more or less held in the cavernous sinus, mechanical or an indirect injury. The indirect injury it will therefore be pressed up against the sharp border of the results from nerve ischemic change due to vessel compression or petrous temporal bone causing an interruption in conduction vasospasm.8,9 The three cranial nerves (3rd, 4th and 6th) are fed by and palsy of the lateral rectus. A similar condition may follow a comprehensive network of arterial blood vessels, and thus are compression of the skull in difficult labor with or without forceps susceptible to vascular compromise particularly localized lesions and may explain 6th nerve palsy at birth. A review of the medical and disturbances at the level of the brainstem cranial nerve literature11,12 has shown that abducens nerve vulnerability results nuclei as well as in the cavernous sinus just before innervating from factors other than its intracranial length. the .10 Of the 24 patients we reviewed, only 9 underwent neuro‑imaging. Paralysis of the 6th cranial nerve has no localizing value because Eight results were normal and one showed an intracranial it may be affected by, almost any type of cerebral lesion. Many space‑occupying lesion. The observation that the neuro‑imaging theories have been proposed for this observation.11 Collier results were normal should not give a false of hope. This thought that this happens because of the shifting backwards was shown in a case reported by Hoenig14 of a 62‑year‑old male of the brainstem since the direction of the nerve is mostly with facial nerve palsy who was managed over an 18‑month fronto‑caudal. Affection of the 6th nerve is followed by the period with initial normal magnetic resonance imaging results. 3rd, 7th and 8th cranial nerves. The more fragile 4th nerve Hoenig14 therefore cautioned that normal neuro‑imaging results with its longer intracranial course (75 mm) is less affected might be falsely misleading in identifying the cause of cranial because it is thought to be protected by, the free margin of the nerve palsy. tentorium cerebelli. Alternately, the 6th nerve, has the longest extradural course (even though its entire length is 1/3 that of the In the current study, approximately one third (33.3%) of the 4th nerve), thereby making it vulnerable to intracranial insults as patients had sluggishly reactive pupils; and the relationship seen in meningitis and subarachnoid hemorrhage.12 Cushing13 between cranial nerve palsy and pupillary reaction was postulated that when the anterior inferior cerebellar artery ran statistically significant (P = 0.02). Complete 3rd nerve palsy ventral to the 6th nerve it may press on and groove the nerve and would almost definitely affect pupillary reaction, hence this the underlying pons due to increased intracranial pressure and result is not unexpected. All cases of 7th cranial nerve palsy thus cause lateral rectus palsy. Another author suggested that the were idiopathic except one patient who had associated hearing bend over the sharp apex of the petrous temporal bone exposes loss. Recent research has shown that Bell’s palsy occurs when the 6th nerve to insult when there is an increase in intracranial the herpes simplex virus gets reactivated in the temporal bone. pressure with resultant coning of the brain. If the 6th nerve is 15 This may explain the associated otalgia in one of the patients.

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Bell’s palsy is the most common facial nerve palsy encountered, palsy using a population‑based method. Ophthalmology accounting for approximately 75% of cases.16 2004;111:369‑75. 6. Berlit P, Reinhardt‑Eckstein J, Krause KH. Isolated abducens paralysis–a retrospective study of 165 patients. Fortschr Neurol The limitations of this study included the very small sample size, Psychiatr 1989;57:32‑40. and most patients were lost to follow‑up. Hence it is difficult 7. Moster ML, Savino PJ, Sergott RC, Bosley TM, Schatz NJ. to assess the final outcome of management. A future study Isolated sixth‑nerve palsies in younger adults. Arch Ophthalmol involving other departments that manage patients with cranial 1984;102:1328‑30. 8. Kim MS, Cho MS, Kim SH. Delayed bilateral abducens nerve palsies is required. nerve palsy after head trauma. J Korean Neurosurg Soc 2008;44:396‑8. CONCLUSION 9. Ayberk G, Ozveren MF, YildirimT, Ercan K, Cay EK, Koçak A. Review of a series with abducens nerve palsy. Turk Neurosurg 2008;18:366‑73. The most common cranial nerve palsies in patients present at 10. Ciuffreda KJ, Kapoor N, Rutner D, Suchoff IB, Han ME, Craig S. the University of Port Harcourt Teaching Hospital Eye Clinic Occurrence of oculomotor dysfunctions in acquired brain were the 3rd and 6th cranial nerves, followed by the 7th nerve. injury: A retrospective analysis. Optometry 2007;78:155‑61. Most cases of 6th cranial nerve palsy were related to systemic 11. Last RJ. Eugene Wolff’s Anatomy of the Eye and . 6th ed. disorders such as hypertension, DM and cerebral malaria. Nerves, Chapter 6. London: HK Lewis and Co. Ltd; 1968. p. 293‑4. This association was statistically significant. A further study 12. Milanes‑Rodríguez G, Ibañez‑Valdés L, Foyaca‑Sibat H, involving other relevant departments would provide a more Perez‑Fernandez M. The abducens nerve in . Internet comprehensive summary of the frequency of the occurrence J Neurol 2008;10:2. of cranial nerve palsies. 13. Cushing H. Strangulation of the nervi abducens by lateral branches of the basilar artery in cases of brain tumor: With an explanation of obscure palsies on the basis of arterial REFERENCES constriction. Brain: A journal of Neurology 1910; 33:204‑35. 14. Hoenig PA. Multiple cranial‑nerve palsies. N Engl J Med 1990; 1. Rush JA, Younge BR. Paralysis of cranial nerves 3, 4 and 322:1889. 6. Cause and prognosis in 1000 cases. Arch Ophthalmol 15. Bell’s palsy diagnosis and treatment. Available from: 1981;99:76‑9. http://www.facialparalysisinstitute. com/5/bellpalsy. 2. Rucker CW. The causes of paralysis of the third, fourth and html. [Last accessed on 2013 Oct 13]. sixth cranial nerves. Am J Ophthalmol 1966;61:1293‑8. 16. Peitersen E. Bell’s palsy: The spontaneous course of 2,500 3. Richards BW, Jones FR Jr, Younge BR. Causes and prognosis peripheral facial nerve palsies of different etiologies. Acta in 4,278 cases of paralysis of the oculomotor, trochlear, and Otolaryngol Suppl 2002;(549):4‑30. abducens cranial nerves. Am J Ophthalmol 1992;113:489‑96. 4. Rowe F; VIS group UK. Prevalence of ocular motor cranial nerve palsy and associations following stroke. Eye (Lond) Cite this article as: Pedro-Egbe CN, Fiebai B, Awoyesuku EA. A 3-year review 2011;25:881‑7 of cranial nerve palsies from the University of Port Harcourt Teaching Hospital Eye Clinic, Nigeria. Middle East Afr J Ophthalmol 2014;21:170-4. 5. Patel SV, Mutyala S, Leske DA, Hodge DO, Holmes JM. Incidence, associations, and evaluation of sixth nerve Source of Support: Nil, Conflict of Interest: None declared.

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