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Journal Français d'Ophtalmologie
Volume 41, n° 1
pages 45-49 (janvier 2018)
Doi : 10.1016/j.jfo.2017.06.010
Received : 24 Mars 2017 ;  accepted : 20 June 2017
Articles originaux

Oculomotor palsy in diabetics
Paralysie oculomotrice chez les diabétiques
 

H. Lajmi , W. Hmaied, W. Ben Jalel, Z. Chelly, A. Ben Yakhlef, F. Ben Zineb, L. El Fekih
 Internal security forces hospital, Mohamed Fadhel Ben Achour street, Marsa Safsaf, Tunis, Tunisia 

Corresponding author. Ophthalmology department, internal security forces hospital, Mohamed Fadhel Ben Achour street, Marsa Safsaf, Tunis, Tunisia.
Summary
Introduction

Oculomotor palsy is one of the most frequent neuro-ophthalmologic complications of diabetic patients. It generates less interest in the literature than the other ocular manifestations. Our goal was to study the clinical, epidemiological, therapeutic and prognostic characteristics of oculomotor palsy in the diabetic.

Methods

This is a retrospective study of 24 diabetic patients with oculomotor palsy. The ophthalmological examination emphasized ocular motility. We performed an orthoptic assessment and a Hess–Lancaster test. Neuro-imaging was ordered in case of IIIrd and IVth nerve involvement, bilateral involvement, multiple ocular cranial nerve palsy or associated optic neuropathy. Treatment consisted of glucose management and alternating monocular occlusion or prisms for the diplopia. Data were entered and analyzed on SPSS 11.5 software.

Results

The mean age of the patients was 58.5±11.9 years. Binocular diplopia was the main symptom. The oculomotor palsy involved the VIth nerve in 50% of cases and was bilateral in two cases. Three patients also had an optic neuropathy. The mean duration of diabetes was 11.7±11 years; poorly controlled diabetes was found in 75% of cases and an association with diabetic retinopathy was noted in 56% of cases.

Conclusions

Long-standing uncontrolled type 2 diabetes, hypertension, coronary artery disease, left ventricular hypertrophy, and elevated hematocrit are the most common risk factors. The VIth nerve is commonly involved. Certain characteristics of the pupillary light reflex can help to differentiate an ischemic insult from an aneurysmal injury to the IIIrd nerve.

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Résumé
Introduction

La paralysie oculomotrice est l’une des complications neuro-ophtalmologiques les plus fréquentes du diabétique. Elle soulève moins d’intérêt dans la littérature que les autres manifestations oculaires. Notre objectif était d’étudier les caractéristiques cliniques, épidémiologiques, thérapeutiques et évolutives de la paralysie oculomotrice du diabétique.

Méthodes

Étude rétrospective sur 24 diabétiques atteints de paralysie oculomotrice. Nous avons insisté sur l’examen de l’oculomotricité complété par un bilan orthoptique et un test de Hess–Lancaster. L’imagerie cérébrale était demandée en cas d’atteinte des nerfs III et IV, d’affection bilatérale, de paralysies multiples ou de neuropathie optique associée. Le traitement consistait à équilibrer le diabète et à l’occlusion monoculaire alternée ou les prismes pour la diplopie. Les données ont été saisies et analysées sur le logiciel SPSS 11.5.

Résultats

L’âge moyen des patients était de 58,5±11,9 ans. La diplopie binoculaire était le principal symptôme. La paralysie oculomotrice concernait le VIe nerf dans 50 % des cas et elle était bilatérale dans deux cas. Trois patients avaient une neuropathie optique associée. La durée moyenne d’évolution du diabète était de 11,7±11 ans, un diabète déséquilibré était trouvé dans 75 % des cas et une association avec la rétinopathie diabétique était notée dans 56 % des cas.

Conclusions

Un diabète de type 2 déséquilibré et ancien, l’hypertension artérielle, la coronaropathie, l’hypertrophie ventriculaire gauche, l’hématocrite élevé sont les facteurs de risque les plus fréquents. Le VIe nerf est communément concerné. Le réflexe photomoteur peut aider à différencier une lésion ischémique d’une lésion anévrysmale du IIIe nerf.

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Keywords : Diabetes, Ocular cranial nerve palsy, Optic neuropathy

Mots clés : Diabète, Paralysie oculomotrice, Neuropathie optique


Introduction

Neuro-ophthalmological manifestations are among the most common ocular pathologies in diabetics after diabetic retinopathy, cataract and glaucoma. The severity of these affections is variable, but they could lead to important visual function impairment. Oculomotor nerve palsy (ONP) raises less interest in literature than diabetic retinopathy which is a public health problem in our country. The onset of this disease can be explained by metabolic alterations, inflammation or vascular occlusion producing the ischemic degeneration of the nerve, infarction or hemorrhage in the nucleus or in the path of the cranial nerve from its emergence to the orbit. Our aim was to study clinical, epidemiological therapeutic and evolutionary features of ONP in diabetics.

Methods

This is a retrospective study including 24 patients with diabetes-associated ONP who were referred to our department between December 2011 and 2015. A detailed medical history and past history of the subjects were taken:

age and gender;
informations related to diabetes (type, duration, glycemic control, treatment and the presence of other microangiopathy);
associated pathologies (high blood pressure, dyslipidemia, heart disease, stroke, anemia);
functional signs such as diplopia, painful eyes, headache, visual acuity alteration and other neurological localizing signs, as well as their mode of onset and evolution.

Our patients underwent a bilateral and complete ophthalmological examination including:

the best corrected visual acuity (Log Mar scale);
pupils examination, checking for size, shape, and light reflexes;
an anterior segment evaluation and a measurement of intra-ocular pressure;
fundus examination;
Goldmann visual field was asked if optic neuropathy was associated.

Particular attention was paid to lid examination, pupillary reflexes and extra-ocular movements. We noted the presence of a vicious attitude of the head, ptosis or deviation of the eyeballs. The study of extra-ocular movements included: duction and version with an orthoptic assessment measuring the importance of the deviation and searching for a sensory disorder. All of our patients had a Hess–Lancaster test.

A specialized neurological examination with a brain magnetic resonance imaging (MRI) were asked in case of IIIrd and IVth nerves involvement, bilateral affection, multiple ocular cranial nerve palsy or associated optic neuropathy.

The treatment consisted on diabetes equilibration and altered monocular occlusion or prisms for the diplopia.

All these patients were monitored regularly with a complete ophthalmological examination and a Hess–Lancaster test.

Data were entered and analyzed on SPSS 11.5 software. The univariate analysis by the simple linear regression method was used to search for ONP risk factors. Only factors with a threshold of significance P <0.05 have been introduced in the multivariate analysis.

Results

The mean age of patients was 58.5±11.9 years (from 36 to 80) with a sex ratio of two (male/female).

Patients with IVth nerve palsy were significantly younger than the IIIrd nerve palsy (P =0.008).

Concerning the diabetes history, 90.9% of cases (22 patients) had type 2 diabetes and two patients had type 1 diabetes, these subjects had exclusively a IVth nerve palsy. No statistic link was found between the type of the diabetes and the ONP.

The mean evolution of the disease was of 11.7±11 years. Twenty-five percent of these patients were under insulin, 62% had oral anti-diabetic medications and the three remaining patients were not known diabetics when they presented the ONP.

The glycated hemoglobin ranged from six to 12.3%. Seventy-five percent of our patients had poorly controlled diabetes. Only the VIth nerve palsy was significantly linked to a poor glycemic control (P =0.046), compared to the IIIrd nerve and the IVth nerve palsy.

Most of our patients had other micro angiopathy risk factors, which were summarized in Table 1.

Degenerative complications of diabetes were noted in 16 patients (66.7%) (Table 2). Among them, 14 patients (58.3%) had a diabetic retinopathy that was not significantly correlated to the ONP (P =0.26). However, the retinopathy was more severe in the VIth nerve palsy (46% of patients versus 11% in the IIIrd nerve palsy), but was not significant (P =0.06).

Regarding functional signs, binocular diplopia was the main symptom (87.5% of patients’ complaints). Ptosis was noted in three others, explaining the absence of diplopia in these cases.

The ONP involved the VIth, the IIIrd and the IVth nerves in respectively 50%, 37.5% and 12.5% of cases.

The IIIrd nerve palsy was total in two cases and partial in 6 cases. One patient initially diagnosed with a partial IIIrd nerve palsy, has secondarily developed a IVth nerve palsy. The disease was bilateral in two cases: a bilateral VIth cranial nerve palsy and a case of bilateral paresis of the IIIrd nerve occurring in a patient with a previous VIth nerve palsy.

Spontaneous resolution was noticed in all patients after a mean delay of 4.5 months (one to seven months), it was complete in 23 patients and incomplete in a patient with a VIth cranial nerve palsy who kept a moderate diplopia in the lateral gaze, compensated by prisms. He was a man of 62 years old with an imbalanced type 2 diabetes evolving for 26 ans. He had degenerative complications (retinopathy, neuropathy and nephropathy) and the deviation angle was important (45°).

Three patients presented recurrences with a mean delay of 14 months (five to 30 months). Two of them had one recurrence and one patient had two recurrences (eight months and two years after the first episode).

The same eye was concerned in two patients and both eyes in another. The recurrence concerned the same nerve in one patient and other nerves in two patients. These episodes were brief and resolute in two weeks on average (one to three weeks) (Table 3).

We noticed an association with a bilateral optical neuropathy in three patients. Two of them had a IIIrd nerve palsy and the third had a VIth nerve palsy. An unbalanced diabetes is significantly linked to acute anterior ischemic optic neuropathy (P =0.02) (Table 4).

Discussion

ONP affects 0.4% to 14% of diabetics; it is seven to eight times commoner in these subjects than in non-diabetic ones [1].

The average age of this complication onset in our series was 58.5±11.9 years and the lesion is predominant in male as found in literature [2]. We noted a significantly younger age in patients with IVth cranial nerve paralysis.

Many risk factors were involved: an unbalanced and ancient type 2 diabetes represents often a significant one [3, 4, 5]. In our series, only the VIth nerve impairment is significantly linked to high blood sugar rates.

Other conditions such as blood hypertension, coronary artery disease, left ventricular hypertrophy, high hematocrit, are thought to promote ONP. Greco et al. proved that complications of diabetes and arteriosclerosis were significantly more frequent in the paralysis of the VIth cranial nerve [6].

The VIth cranial nerve is commonly concerned [7, 8]. The IVth cranial nerve palsy is not common with an incidence of about six to 15% [9], despite its limited number of nervous fibers compared to the other oculomotor nerves (making it more susceptible to micro-vascular lesions).

ONP in diabetes is due to micro-angiopathy that results in nerves lesions by the mean of vasa nervosum occlusion and leads to mesenchymal and interstitial tissues necrosis particularly in the intra-cavernous portion [10].

Anatomy and pathophysiology explain the rarity of multiple and bilateral forms. In fact, the three oculomotor nerves had a common blood supply at the cavernous sinus by internal carotid artery branches. Some authors explained the simultaneous nervous lesions by one of these branches occlusion; ischemia of the posterior fossa is another physiopathological hypothesis [11, 12]. Ushi et al. found a thickening and a proliferation in the intima layers of intra-neural vessels of these nerves in post-mortem in a patient who presented a simultaneous palsy of the IIIrd and the IVth nerves [13].

The bilateral involvement especially of the same nerve is even rarer [14]. The possibility of two vasa nervosum infarction at the same time remains relatively low. It is even rarer for ischemia to involve the identical vasa nervosum on both sides at the same time [15]. An ischemic injury of the oculomotor nerves nuclei might be another explanation, in the absence of histological evidence. The diabetic origins of bilateral palsies remain an exclusion diagnosis, neurological exploration and MRI are compulsory and other differential diagnosis must be eliminated in theses cases, such as: tuberculous or fungal meningitis, syphilis, botulism, thyroid ophthalmopathy, multiple sclerosis, arteritis, insufficiency of the basilar artery, Wernicke encephalopathy or rarely a tumor.

Clinically, binocular diplopia is the main symptom; however, it can be unrecognized when the palsy is minimal. In our case, it was noted in 41.6% of patients. That is why, any headache in diabetics must evoke a sub-clinical oculomotor palsy, especially in the presence of unexplained visual disturbances.

Evaluation of light reflex may be contributory to diagnosis. In fact, pupillary involvement in diabetes-associated oculomotor nerve palsy occurs in about 1/4th of all cases. Certain characteristics help to differentiate an ischemic insult from an aneurysmal injury to the IIIrd nerve such as an incomplete involvement and anisocoria<2mm. Patients with pupillary involvement had mostly no diabetic retinopathy changes or less severe grades of diabetic retinopathy. Besides, ophthalmoplegia resolves much earlier than anisocoria in diabetic oculomotor nerve palsies [16].

In three of our patients, ONP was associated with an optic neuropathy. All of them had: a mean age more than 50 years; a frequent hypertension; an unbalanced type 2 diabetes evolving for more than 10 years and the absence of a diabetic retinopathy.

This association is rarely reported in the literature [17, 18]. In these cases, the lesions are in the same side. Brain imaging is essential to eliminate a tumoral, a vascular or an inflammatory cause. We noted a particular association with the lesion of the third nerve, but the main feature of our series is the initial or the secondary bilateralism of the optic neuropathy.

ONP regresses spontaneously after three months in average. Seventy-three percent of patients cure within 6 months following the acute episode [19]. A complete resolution might be obtained in 86% to 100% of cases [20]. In our series, only one patient had an incomplete resolution.

ONP in diabetics are alternating and recurrent (up to 13 recurrences in the literature) [18]. The relapse does not obscure the prognosis and the average time of evolution is shorter than the first episode [21]. The average duration of recurrences in our series does not exceed 3 weeks.

Because of a spontaneous resolution, the clinical monitoring and an equilibration of diabetes is the rule. It may be associated with an alternating occlusion or prism wearing, to control diplopia. Botulinum toxin has also been used successfully in some diabetics [22]. The surgery is indicated from nine to 12 months of evolution in the absence of diplopia regression.

Conclusion

Neuro-ophthalmological complications of diabetes, especially ONP, are uncommonly treated in literature. It would be interesting to complete this work by comparative studies between the diabetic patients and non-diabetic and multiply studies to deepen our knowledge about the physiopathology, the epidemiological profile and the different clinical forms.

Disclosure of interest

The authors declare that they have no competing interest.

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