Histopathological Alterations in Ciliary Ganglions in Meningitis: An Experimental Study

Abstract

Background: Although it is well known that meningitis frequently results in optic nerve (ON) and oculomotor nerve (OMN) dysfunctions, the effects of meningitis on the ciliary ganglion (CG) have not been studied. It is expected that the CG may be affected due to the involvement of these cranial nerves in meningitis. In this study, we aimed to investigate the effect of meningitis on the CG. Methods: This study was conducted on thirteen rabbits. Experimental meningitis has been achieved with Streptococcus pneumonias inoculation into the cisterna magna of the animals. After follow-up of two months, all animals were sacrificed. CGs of all animals were examined histopathologically. Neuron numbers and morphological changes of the CGs were examined. Results: Arachnoiditis and axonal degeneration at the cisternal segments of both oculomotor and optic nerves were observed. Neuronal irregularity, cellular angulation, shrinkage, nuclear irregularity and cytoplasmic condensation were observed in neurons of the CG. The mean number of live neurons in a CG was 3200 in healthy rabbits, whereas it was 2800 in animals with meningitis. Conclusion: Cisternal segments of the ON and OMN have a meningeal sleeve and a rich vascular supply. Meningitis may cause vasculitis or vasospasm at these arteries and may result in infectious neuropathy of the OMN and ON, and also afferent and efferent loops of the light reflex were structurally interrupted. Consequently, parasympathetic preganglionic denervation of the CG may occur and may result in degeneration in the neurons of the CG.

Key words

Meningitis - ciliary ganglion - neurodegeneration - rabbit

References

• 1 Warwick V. The ocular parasympathetic nerve supply and its mesencephalic sources.  J Anat. 1954;  88 71-93
• 2 Sinnreich Z, Nathan H. The ciliary ganglion in man.  Anat Anz. 1981;  150 287-290
• 3 Rhoton A L. The orbit.  Neurosurgery. 2002;  51 303-334
• 4 Chiu C H, Lin T Y, Huang Y C. Cranial nerve palsies and cerebral infarction in a young infant with meningococcal meningitis.  Scand J Infect Dis. 1995;  27 75-76
• 5 Miwa H, Koshimura I, Mizuno Y. Recurrent cranial neuropathy as a clinical presentation of idiopathic inflammation of the dura mater: a possible relationship to Tolosa-Hunt syndrome and cranial pachymeningitis.  J Neurol Sci. 1998;  154 101-105
• 6 Torras S J. Optic neuropathies and peripheral oculomotor disorders in patients with AIDS.  Rev Neurol. 1996;  24 1605-1613
• 7 Giombini S, Ferraresi S, Pluchino P. Reversal of oculomotor disorders after intracranial anerysm surgery.  Acta Neurochir. 1991;  112 19-24
• 8 Ferreira R C, Phan G, Bateman J B. Favorable visual outcome in cryptococcal meningitis.  Am J Ophthalmol. 1997;  124 558-560
• 9 Sakaki T, Kinugawa K, Tanigake T, Miyamoto S, Kyoi K, Utsumi S. Embolism from intracranial aneurysm.  J Neurosurg. 1980;  53 300-304
• 10 Kerr F WL, Hollowel O W. Location of pupillomotor and accommodation fibers in the oculomotor nerve. Experimental observations on paralytic mydriasis.  J Neurol Neurosurg Psychiatr. 1964;  27 473-481
• 11 Ramirez-Moreno J M, Aguirre-Sanchez J J, Duran-Herrera C, Parrilla-Ramirez J L, Vialas-Simon J, Gonzalez-Dorrego F. Paralysis of the nucleus of the third cranial nerve secondary to a mesencephalic hematoma.  Rev Neurol. 1999;  29 808-810
• 12 Ing E B, Sullivan T J, Clarke M P, Buncic J R. Oculomotor nerve palsies in children.  J Pediatr Ophthalmol Strabismus. 1992;  29 331-336
• 13 Murakami K. A case of late onset group B Streptococcus meningitis with transient oculomotor nerve palsy.  No To Hattatsu. 1999;  31 549-552
• 14 Keane J R. Intermittent third nerve palsy with cryptococcal meningitis.  J Clin Neuroophthalmol. 1993;  13 124-126
• 15 Menon V, Arya A V, Prakash P. Pupillary automatism.  Indian J Ophthalmol. 1989;  37 30-31
• 16 McGravey A R. A dilated unreactive pupil in acute bacterial meningitis: oculomotor nerve inflammation versus herniation.  Pediatr Emerg Care. 1989;  5 187-188
• 17 Zhang Y L, Tan C K, Wong W C. An ultrastructural study of the ciliary ganglia of the cat and monkey (Macaca fascicularis) following preganglionic axotomy.  Neurodegeneration. 1996;  5 367-377
• 18 Zhang Y L, Tan C K, Wong W C. The ciliary ganglion of the monkey: a light and electron microscope study.  J Anat. 1994;  184 251-260
• 19 Chang Z, Shen Z, Sun Y, Wang N, Cao D. Early repair treatment of electrical burns and recovery of tendons and nerves. Report of 194 operations.  Ann NY Acad Sci. 1999;  888 327-333
• 20 Gundersen H JG. Notes on the estimation of the numerical density of arbitrary particles: the edge effect.  J Microsc. 1977;  111 219-223
• 21 Sterio D C. The unbiased estimation of number and sizes of arbitrary particles using the dissector.  J Microsc. 1984;  134 127-136
• 22 Cruz-Orive L M, Weibel E R. Recent stereological methods for cell biology: a brief survey.  Am J Physiol. 1990;  258 148-156
• 23 Gundersen H J. Stereology of arbitrary particles. A review of unbiased number and size estimators and the presentation of some new ones, in memory of William R. Thompson.  J Microsc. 1986;  143 43-45
• 24 Gundersen H J, Bendtsen T F, Korbo L, Marcussen N, Moller A, Nielsen K, Nyengaard J R, Pakkenberg B, Sorensen F B, Vesterby A. Some new, simple and efficient stereological methods and their use in pathological research and diagnosis.  APMIS. 1988;  96 379-394
• 25 Purvin V A. Adie's tonic pupil secondary to migraine.  J Neuroophthalmol. 1995;  15 43-44
• 26 Hersh J H, Douglas C, Houston J, Weisskopf B. Familial iridology.  J Pediatr Ophthalmol Strabismus. 1987;  24 49-50
• 27 Bertinotti L, Pietrini U, Rosso A Del, Casale R, Colangelo N, Zoppi M, Matucci-Cerinic M. The use of pupillometry in joint and connective tissue diseases.  Ann NY Acad Sci. 2002;  966 446-455
• 28 Currie J, Lessell S. Tonic pupil with giant cell arteritis.  Br J Ophthalmol. 1984;  68 135-138
• 29 Schmid G F, Papastergiou G I, Lin T, Riva C E, Laties A M, Stone R A. Autonomic denervations influence ocular dimensions and intraocular pressure in chicks.  Exp Eye Res. 1999;  68 573-581
• 30 Sharma S, Hoskin-Mott A, Benstead T, Maxner C. Correlation of the pilo-pupil ratio average, a new test for autonomic denervation, to the severity of diabetic retinopathy.  Can J Ophthalmol. 1997;  32 170-171
• 31 Clark C V, Mapstone R. Anterior segment autonomic dysfunction in ocular hypertension.  Doc Ophthalmol. 1986;  64 201-207
• 32 Ozkan U, Aydin M D, Gundogdu C, Onder A. Histopathologic changes in oculomotor nerve ciliary ganglion in aneurysmatic compression injuries of oculomotor nerve.  Minim Invas Neurosurg. 2004;  47 107-110
• 33 Clark C V, Mapstone R. Parasympathetic denervation hypersensitivity of the iris in ocular autonomic nerve function in proliferative diabetic retinopathy.  Eye. 1988;  2 96-101
• 34 Faschinger C, Kleinert K. Histologic and ultrastructural findings in the ciliary ganglion in normal eyes and in patients with glaucoma.  Klin Monatsbl Augenheilkd. 1986;  189 400-401
• 35 Tschernjawsky G J, Pletschkowa E K. Morphological changes in ciliary ganglions of healthy subjects and glaucoma patients.  Albrecht Von Graefes Arch Klin Exp Ophthalmol. 1979;  211 235-241