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Autonomic Denervation Hypersensitivity in the Primary Glaucomas

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Autonomic Denervation Hypersensitivity in the Primary Glaucomas Eye ( 1989) 3, 349-354 Autonomic Denervation Hypersensitivity in the Primary Glaucomas CHARLES V. CLARK Edinburgh Summary Autonomic denervation hypersensitivity of the iris was assessed in 44 patients with primary closed-angle glaucoma, 20 patients with primary open-angle glaucoma, and 40 age- and sex-matched control subjects. Significantly increased pupillary con­ striction in response to 2.5% methacholine chloride, indicating parasympathetic denervation hypersensitivity, was present in both closed-angle (p<0.02) and open­ angle glaucoma patients (p<O.OOl), compared with the control group. Significantly increased pupillary dilatation in response to 0.5 per cent phenylephrine hydro­ chloride, indicating sympathetic denervation hypersensitivity of the iris, was also present in both closed-angle glaucoma (p<O.Ol) and open-angle glaucoma patients (p<0.05). The association between autonomic neuropathy and the primary glaucomas is discussed, with particular reference to the potential effects of autono­ mic dysfunction on aqueous dynamics. Elevation of intraocular pressure in the ulation of the autonomic nervous system in primary glaucomas occurs as a consequence of the anterior segment of the eye. The efficacy impaired outflow of aqueous humour from the of ocular autonomic nerve function can be anterior chamber of the eye. The mechanism inferred from the assessment of denervation of obstruction to outflow forms the basis of hypersensitivity. In the presence of autono­ categorisation in glaucoma: in closed-angle mic neuropathy, receptor density is signifi­ glaucoma rhe exit of aqueous from the cantly increased at the postsynaptic receptor anterior chamber is physically prevented by site,! and may be detected by the measure­ apposition of peripheral iris to cornea; in ment of exaggerated end-organ responses to open-angle glaucoma the site of obstruction specific autonomic agonists. The pupil pro­ lies within the angle, probably the trabecular vides an excellent model for the assessment of meshwork, and the entrance to the angle is autonomic integrity in the eye; pupillary not a primary contributing factor to the diameter represents a balance between para­ glaucomatous process. The pathological sympathetic and sympathetic activity in the effects of raised intraocular pressure on the anterior segment, and assessment of denerva­ retinal nerve fibre layer are well established, tion hypersensitivity permits these com­ however the aetiological factors precipitating ponents of the autonomic nervous system to the primary glaucomas have not been fully be individually measured by a simple, non­ defined. Autonomic nerve function is a major invasive and accurate technique. Several determinant of intraocular pressure; pharmacological agents have been employed glaucoma therapeutics are based upon manip- in the assessment of autonomic denervation Correspondence to: Mr C. V. Clark, FRCS, FCOphth, Princess Alexandra Eye Pavilion, Chalmers Street, Edinburgh EH3 9HA. 350 C. V.CLARK hypersensitivity;2,3,4 the only prerequisite to Subjects known to have medical disorders the utilisation of any drug for this purpose is predisposing to autonomic nerve dysfunction, the preliminary determination of the normal or taking medication with effects on the response. Parasympathetic de nervation autonomic nervous system, were similarly hypersensitivity may be effectively assessed excluded from the study. by topical application of 2.5% methacholine chloride,5,6 and sympathetic denervation sen­ Autonomic Denervation Hypersensitivity sitivity is demonstrated by the pupillary (i) Parasympathetic nervous system effects of 0.5% phenylephrine hydro­ Pupil diameters were recorded photo­ chloride;? normal age-adjusted tolerance graphically between 9 and 11 am under stan­ intervals to both agents have recently been dardised lighting conditions; the subject faced documented.6,? a surface with measured luminance of 20 apos­ The aim of this study was to assess autono­ tilbs, whilst low, constant background mic nerve function in the anterior segment of illumination was maintained. The subjects the eye in patients with primary closed-angle were positioned on an ophthalmic head-rest, glaucoma and primary open-angle glaucoma, thereby effecting reproducible positions for by measurement of pupillary responses to photography. A scale was placed against the pharmacological agents recognised to be lower eyelid in the perpendicular plane of the indicative of autonomic denervation iris, the subjects fixated at 6 metres, then a hypersensitivity. photograph at x 3 magnification was taken of both eyes together using a Nikon F camera Patients and Methods with Medical Nikkor 120 mm f4 lens and After informed consent had been obtained, Kodak Ektachrome Professional Film (ASA ocular autonomic nerve function was assessed 200). One drop of 2.5% methacholine chlo­ in 44 patients with closed-angle glaucoma ride solution was placed in the conjunctival (mean age 66.5 ± 10.2 years), 20 patients with sac of one eye, and one drop of sterile normal open-angle glaucoma (mean age 66.7 ± 7,9 saline solution concurrently placed in the con­ years), and 40 age- and sex-matched control junctival sac of the contralateral eye. In open­ subjects (mean age 65.3 ± 12.7 years). The angle glaucoma patients and control subjects diagnosis of open-angle glaucoma and closed­ the choice of the eye to be tested was selected angle glaucoma was made according to estab­ randomly, In closed-angle glaucoma patients lished criteria.8,9,IO The open-angle glaucoma only fellow eyes were tested. Forty-five min­ group consisted of 20 consecutive new refer­ utes later, a second pupil photograph was rals to a glaucoma clinic, prior to the com­ taken. Responses to 2.5% methacholine, if mencement of treatment. A comprehensive present, were of short duration; pupil diam­ medical history was obtained from each sub­ eters returned to normal within one and a half ject, followed by systematic general medical hours of instilling methacholine. and ocular examination; applanation tonome­ try was specifically not performed until after (ii) Sympathetic nervous system the assessment of denervation hypersen­ Three days later, the assessment of sympa­ sitivity. Eyes were excluded from assessment thetic denervation hypersensitivity was if there was a history of: performed using essentially the same tech­ (i) ocular operations: only unoperated eyes nique, substituting 2.5% methacholine by were included in the study. In patients 0.5% phenylephrine hydrochloride. Assess­ with closed-angle glaucoma, assessments ments were performed on the same eye in were performed only in unoperated fel­ each subject. low eyes. Eyes which had closed-angle glaucoma were specifically excluded. (iii) Pupil measurement (ii) ocular trauma The photographic slides were projected on to (iii) current ophthalmic drug treatment a white screen at fivemetres, and were magni­ (iv) corneal disease fied by a factor of 17. Horizontal pupil diam­ (v) dry eyes eters were measured directly from the screen AUTONOMIC DENERV A TlON HYPERSENSITIVITY IN THE PRIMARY GLAUCOMAS 351 to an accuracy of ± 0.5 mm, and were then the iris, was also present in both major cate­ corrected to actual values by comparison with gories of primary glaucoma. 0.5% phe­ relative magnification of the scale. Effec­ nylephrine ratios were significantly higher in tively, measurement of pupil diameter was patients with closed-angle glaucoma (1.30 ± accurate to within ± 0.03 mm. 0.03) (p<O.01) and open-angle glaucoma Parsympathetic denervation hypersen­ (1.30 ± 0.08) (p<0.05) than the control group sitivity was expressed as the 2.5% meth­ (1. 19 ± 0.03). acholine ratio: horizontal pupil diameter 45 minutes post-test Discussion The concept of denervation hypersensitivity horizontal pupil diameter pre-test originated in the early years of the 20th cen­ Sympathetic denervation hypersensitivity tury; in 1904, Meltzer described paradoxical 12 was also determined by the ratio of the post­ pupil dilatation in response to adrenaline, to pre-test horizontal pupil diameter, and and in 1905 Markusl3 and Andersonl4 sep­ expressed as the 0. 5% phenylephrine ratio. arately noted sensitivity of the denervated The concurrent assessment of an age- and pupil to cholinergic drugs. Sensitisation of the sex-matched control group provided effective denervated pupillary sphincter to acetyl­ standards for comparison. All assessments choline was confirmedby Shen and Cannon in were performed on a double-masked basis. 1936;15 the principles of denervation hyper­ sensitivity were initially proposed by Cannon in 193916 and subsequently confirmedin a defi­ Statistical analysis nitive treatise by Cannon and Rosenbluth in Comparisons were made between the results 1949.17 of the control group and both categories of Assessment of denervation hypersensitivity primary glaucoma separately; significance permits accurate and objective measurement was assessed by Student's unpaired t test. of autonomic efficacyin the anterior segment Dunnett's multiple comparison procedure of the eye. The results of the present study was applied to the levels of significance thus have demonstrated increased pupillary obtained, to prevent incorrect conclusions responses to minute quantities of parasym­ from multiple comparisons with a control. II pathetic and sympathetic agonists in both Results are expressed as mean ± SEM. closed-angle and open-angle glaucoma patients, compared with an age- and sex­ Results matched control group. Although the degree (i) Parasympathetic denervation
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