Anti-inflammatory effectiveness in the cornea of topically administered prednisolone
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1 Anti-inflammatory effectiveness in the cornea of topically administered prednisolone Howard M. Leibowitz and Allan Kupferman The relative ability of two of the most widely used ophthalmic prednisolone formulations to suppress inflammation in the cornea with an intact epithelium was determined. Use was made of an experimental model which permits objective quantitdtion of corneal inflammation. The inflammatory response was induced by the injection of clove oil directly into the corneal stroma, resulting in the chemotactic attraction of large numbers of polymorphonuclear leukocytes to the site. These cells were previously systemically labeled with intravenously administered tritiated thymidine, and the degree of radioactivity in the cornea was measured by scintillation counting techniques. That the radioactivity is primarily associated with the invading polymorphonuclear leukocytes has been verified by radioautography. The magnitude of the decrease in corneal radioactivity following topical administration of prednisolone provides an objective measure of the degree of involution of labeled polymorphonuclear leukocytes effected by each drug, and thus a measure of its anti-inflammatory effectiveness. The results document that prednisolone acetate 1.0 per cent ophthalmic suspension is more effective than prednisolone phosphate 1.0 per cent ophthalmic solution in suppressing comeal inflammation. Comparison of the present data with comparable studies of dexamethasone provide the following relative values for mean decrease in corneal inflammatory activity: (1) prednisolone acetate 1.0 per cent ophthalmic suspension, 51 per cent; (2) dexamethasone alcohol 0.1 per cent ophthalmic suspension, 40 per cent; (3) prednisolone phosphate 1.0 per cent ophthalmic solution, 28 per cent; (4) dexamethasone phosphate 0.1 per cent ophthalmic solution, 19 per cent; and (5) dexamethasone phosphate 0.05 per cent ophthalmic ointment, 12 per cent. It is emphasized that the relative order of corneal anti-inflammatory potency reported here applies only to the situation in which the epithelium of the inflamed cornea is intact. -L. opically administered corticosteroids differ in their ability to penetrate into the corneal stroma. 1 " These differences in corneal bioavailability suggest a corre- From the Department of Ophthalmology, Boston University School of Medicine, Boston, Mass. This investigation was supported in part by Public Health Service Grants EY (National Eye Institute) and PHS , by a grant from the Massachusetts Lions Eye Research Fund, and by a grant from Research to Prevent Blindness, Inc. Submitted for publication April 24, Reprint requests: Dr. H. M. Leibowitz, Department of Ophthalmology, Boston University School of Medicine, 80 E. Concord St., Boston, Mass sponding difference in the ability of ophthalmic corticosteroid preparations to suppress inflammation in the cornea. Investigation of this possibility has documented that dexamethasone formulations do indeed vary in their ability to suppress inflammation in the cornea. 7 The present studies demonstrate that different derivatives of prednisolone also are not equivalent in corneal anti-inflammatory effectiveness following their topical administration to the eye. Methods Experimental animals were New Zealand albino rabbits of either sex weighing between 1.5 and 2.0 kilograms. The animals were anesthetized with
2 758 Leiboioitz and Kupferman Investigative Ophthalmology October 1974 Table I. Mean decrease in corneal inflammatory activity following topical prednisolone therapy* Treatment protocol acetate (0.125% suspension) phosphate (0.125% solution) acetate (1.0% suspension) phosphate (1.0% solution) Group I (0.05 ml. each hour for 6 hours (± 8.2) (± 3.8 )t (± 6.0) (± 4.9 )t immediately after induction of inflammation) Group II (0.05 ml., every hour for 6 hours immediately after induction of inflammation, then lapse of 18 hours, then repeat 0.05 ml. every hour for 7 hours) (± 3.6 )f (±5.1) (± 4.8)f (±3.1) Group III (0.05 ml. every hour for 6 hours beginning 24 hours after induction of inflammation, then lapse of 18 hours, then 0.05 ml. every hour for 7 hours) (± 5.2)f (± 2.8) (± 3.6)t, (± 2.0)\ "Table entries are the arithmetic mean ± standard error of data derived from the study of 12 eyes (six rabbits). Values are expressed as per cent difference from the mean of 12 unt ltreated control eyes (six rabbits). f Indicates significant difference between per cent and 1.0 per cent of the same corticosteroid derivative in the same treatment protocol (p < 0.05). (Indicates significant difference between acetate and phosphate derivative of the same concentration in the same treatment protocol (p < 0.05). intravenous sodium thiamylal, 15 ing. per kilogram. Duration of anesthesia was approximately five minutes. A corneal inflammatory response was produced in both eyes of each anesthetized animal by the interlamellar inoculation of laboratory grade clove oil. A single lot of clove oil was employed throughout to ensure standardization of the material. The clove oil (0.03 ml.) was injected centrally with a 30-gauge needle attached to a tuberculin syringe producing a 3 to 4 mm. central stromal bleb. All animals were given intravenous injections of an aqueous solution of tritiated thymidine, systemically labeling white blood cells, particularly the polymorphonuclear leukocytes. 8 The adequacy of the dose used for this purpose in the present experiments was confirmed by radioautography of smears of peripheral blood and bone marrow aspirates. Three treatment protocols were evaluated. Each animal in Group I received two intravenous inoculations of 0.05 mci. per kilogram of tritiated thymidine (6.7 Ci. per millimole) 24 hours apart. The second thymidine injection was given 24 hours prior to the induction of the corneal inflammatory response. Therapy was initiated immediately after the intracorneal injection of clove oil and consisted of a single standard drop (0.05 ml.) of drug every hour for a total of six doses. Each animal in Group II received intravenous tritiated thymidine in the identical amount and according to the identical protocol described for Group I animals. Therapy was begun immediately after the intracorneal inoculation of clove oil. A standard drop (0.05 ml.) of drug was instilled every hour for a total of six doses and then, after a lapse of 18 hours, seven additional hourly doses were administered so that each rabbit received a total of 13 drops over a 30-hour period. Each animal in Group III received three intravenous inoculations of 0.05 mci. per kilogram of tritiated thymidine (6.7 Ci. per millimole) at 24-hour intervals. The intracorneal injection of clove oil was given coincident with the third thymidine injection. Twenty-four hours later therapy was initiated. The regimen consisted of a standard drop (0.05 ml.) of drug every hour for a total of six doses and then, after a lapse of IS hours, one drop was administered hourly for an additional total of seven doses. Four commercial ophthalmic corticosteroid preparations were studied; each was handled and administered in the same manner. The four drugs were: (1) prednisolone acetate per cent ophthalmic suspension, (2) prednisolone acetate 1.0 per cent ophthalmic suspension, (3) prednisolone phosphate per cent ophthalmic solution, and (4) prednisolone phosphate 1.0 per cent ophthalmic solution. Both eyes of each animal were treated identically. Each individual experimental trial contained animals that were being treated with different drugs according to a single
3 Volume 13 Number 10 Topically administered prednisolone 759 treatment protocol. Thus, the six animals (twelve eyes) that made up a given experimental treatment group (Table I) were studied at varying times. A control group was run with each experimental trial; control animals were handled in the same manner as simultaneously run experimental animals except that the control animals received no treatment in either eye. Following completion of each protocol, a 10 mm. penetrating corneal button was removed by trephination and the tissue samples solubilized with a commercially available solubilizing agent (Soluene - Packard Instrument Corporation). The soluble samples were counted in a Packard Tricarb scintillation counter for a minimum of 10 minutes, quantitatively documenting the amount of radioactivity in the cornea as described previously. 1-2 Analysis of the data from individual experimental trials indicated a variability in the corneal tritiated thymidine levels of similarly treated animals studied at different times. Therefore, to ensure the validity of the data, each experimental trial contained its own control group. The data from scintillation counting were converted to decompositions per minute per cornea, and the mean value for the untreated controls of each experimental trial was calculated and considered as unity. Differences in radioactivity following treatment were, in each instance, determined by comparison with the simultaneously run control group. The data from individually treated eyes were expressed as per cent change in radioactivity relative to their own untreated controls, and these differences were averaged to determine a mean value for each treatment group. Handling of the data in this manner permitted elimination of baseline variability among experimental trials. Statistical comparisons were performed by standard methods including random block analysis. 0 ' 10 The calculations used to determine the data presented in Table I were as follows: 1. The decompositions per minute of each sample (D 8 ) were determined by the formula: D s = A/E where A = the counts per minute in the corneal sample. E = the counting efficiency as determined with a known internal standard (tritiated toluene). 2. The mean of D s for all control eyes in a given experimental trial was calculated (Dm). 3. The per cent decrease in corneal radioactivity resulting from treatment for each experimental eye (R) was calculated from the formula R = Dm - D s D m 4. The mean and standard error of R for all eyes in a given drug treatment group were cal- culated. This is the value reported in Table I. Glucocorticoids may have depressant effects on leukocyte production and maturation. This, in turn, could influence the number of polymorphonuclear leukocytes invading the cornea in response to an inflammatory stimulus. Therefore, a total and a differential white blood cell count were performed on all animals immediately prior to clove oil injection and at the time the corneal sample was obtained. The total number of polymorphonuclear leukocytes per microliter of blood was calculated by multiplying the percentage of these cells in the peripheral smear by the white blood cell count. The figure for decompositions per minute found in the cornea after scintillation analysis was then corrected to reflect any statistically significant change in total circulating polymorphonuclear leukocyte count between treated animals and untreated control animals. Results were expressed as a per cent change in corrected corneal decompositions per minute between simultaneously run treated and untreated animals. In those drug treatment groups where a significant alteration in the total number of polymorphonuclear leukocytes per unit of peripheral blood was noted, the value R as calculated above was corrected as follows: 1. The per cent difference between treated and control eyes in total peripheral polymorphonuclear leukocytes was calculated by the formula: P = Y-X X Where X = the mean of total peripheral blood polymorphonuclear leukocytes per microliter in the control eyes of a given experimental trial. Y = the mean of total peripheral blood polymorphonuclear leukocytes per microliter in the experimental eyes of the same experimental trial. 2. Value D s as described above was corrected by the following formula: D'. = D. - (P x D.) 3. D' B is substituted for D 8 in step 3 of the above calculations. Results The intracomeal injection of clove oil rapidly produced an inflammatory response. The details of this inflammatory response have been reported. 14 Essentially, it is characterized by conjunctival injection and chemosis and by edema and infiltration of the corneal stroma. Histologic examination reveals that the stromal infiltrate is composed largely of polymorphonuclear leuko-
4 760 Leiboioitz and Kupferman Investigative Ophthalmology October 1974 Table II. The effect on systemic leukocytes of bilateral topical administration of prednisolone phosphate ophthalmic solution in rabbits Group I Group II Group III No treatment 0.125% 1.0% No treatment 0.125% 1.0% No treatment 0.125% 1.0% Total WBC's 13,320 12,881 9,900 11,871 10,198 8,723 9,198 8,267 7,738 per microliter 0 (±321) (±408) (±481) (±511) (±428) (±502) (±480) (±308) (±699) Polymorphonu clear leukocytes (%) Total poly- (±3) 6,600 (±2) 7,854 (±5) 7,326 (±4) 6,173 (±5) 6,731 (±5) 6,193 (±3) 4,250 (±4) 4,894 (±7) 5,657 morphonu- clear leukocytes Per cent change in polymorphonuclear leukocytes Table entries for total white blood cells per microliter and for per cent polymorphonuclear leukocytes are the arithmetic mean ± standard error of the mean of data derived from the study of at least six animals. cytes concentrated in the peripheral cornea adjacent to the limbus and centrally surrounding the injection site. Radioautographic sections demonstrate that the great majority of silver granules (i.e., radioactivity) are located in association with the polymorphonuclear leukocytes. All four steroid preparations studied diminished inflammatory activity in the cornea as measured by a decrease in radiolabeled polymorphonuclear leukocytes. The relative anti-inflammatory effectiveness of each formulation is presented in Table I. At the lower, per cent, steroid concentration no significant difference was found between the acetate and phosphate derivatives in any of the experimental situations studied. There also was no significant difference in anti-inflammatory effectiveness at the 1.0 per cent concentration of the two derivatives after topical administration of only six drops at hourly intervals (Group I). However, continued treatment demonstrated that the acetate derivative of prednisolone was substantially more effective than the phosphate derivative. This difference was greatest in the Group III animals, where the corneal inflammatory response was most prolonged and most severe. In this instance, 1.0 per cent prednisolone acetate ophthalmic suspension produced a 50.5 per cent decrease in corneal radioactivity, while the comparable 1.0 per cent prednisolone phosphate ophthalmic solution lowered corneal radioactivity by only 27.6 per cent. Topical application of prednisolone phosphate caused a statistically significant (p < 0.05) reduction in the total white cell count per unit volume of peripheral blood but also caused a simultaneous increase in the percentage of polymorphonuclear leukocytes (Table II). These changes did not occur after administration of the acetate derivative. The hematologic alterations induced by prednisolone phosphate resulted in a greater total number of polymorphonuclear leukocytes per unit volume of blood, presumably making a greater number of these cells available to participate in a corneal inflammatory response. The data reported for the prednisolone phosphate-treated animals in Table I have been corrected to reflect significant changes in the blood. These corrections assumed a linear relationship between the total number of polymorphonuclear leukocytes per unit volume of blood and the total number of these cells available to invade the cornea. The corrected values impart a greater anti-
5 Volume 13 Number 10 Topically administered prednisolone 761 inflammatory effectiveness to prednisolone phosphate than do the uncorrected values from which the data were derived. Should our assumption in correcting the data be incorrect, it would not alter the conclusion drawn (i.e., that prednisolone acetate is a more effective corneal anti-inflammatory agent than is prednisolone phosphate). Rather, the lesser degree of efficacy indicated by the uncorrected values lends even greater support to that conclusion. Discussion The present studies make use of an experimental model which permits objective quantitation of corneal inflammation. The inflammatory response is induced by the injection of clove oil, a necrotizing toxic agent, directly into the corneal stroma. Large numbers of inflammatory cells, almost exclusively polymorphonuclear leukocytes (pseudoeosinophils), are chemotactically attracted to the site and, therefore, are the logical component of the inflammatory reaction to quantitate. This is accomplished by administering tritiated thymidine intravenously to systemically radiolabel these cells and then, using scintillation counting techniques, measuring the degree of radioactivity in the cornea. That the radioactivity is primarily associated with the invading polymorphonuclear leukocytes has been verified by radioautography. 11 With respect to attempts to modify the inflammatory response, two inherently different situations are simulated. In Groups I and II, therapy was begun at the same time the inflammatory stimulus was introduced. One is, therefore, measuring the ability of the corticosteroid to inhibit the initiation of inflammation, a situation encountered clinically in the patient about to undergo corneal surgery. In contrast, an intense corneal inflammatory reaction was present in Group III animals before corticosteroid treatment was started. Here, then, one is measuring the ability of the drug to suppress active inflammation, a more common clinical situation. The data from this group are, therefore, the most meaningful for direct comparison of the formulations under study. In both situations, the two prednisolone derivatives studied, the acetate and the phosphate, significantly reduce the number of polymorphonuclear leukocytes invading the cornea. Both derivatives are therefore effective as anti-inflammatory agents in the cornea following their topical administration to the eye. When used to inhibit the initiation of inflammation, a significant antiinflammatory effect can be documented after the instillation of only seven drops over a six-hour period (Group I). No difference in therapeutic effectiveness could be demonstrated between the two prednisolone derivatives at this early period. At the lower of the two concentrations available to the ophthalmologist (0.125 per cent), continued treatment also did not elicit any demonstrable difference between the two prednisolone derivatives, either in inhibiting the initial phases of a corneal inflammatory response (Group II) or in suppressing active inflammation (Group III). At the higher, 1.0 per cent, concentration, however, prednisolone acetate proved to be superior to prednisolone phosphate. This tendency became apparent in Group II animals but could not be conclusively proved statistically. In Group III animals, however, where the corneal inflammatory reaction was most severe, prednisolone acetate was clearly more effective than prednisolone phosphate in suppressing corneal inflammation (p < 0.05). Increasing the concentration of prednisolone acetate from per cent to 1.0 per cent results in a significant enhancement of its anti-inflammatory effectiveness in the cornea. In a tissue where the inflammatory process can rapidly produce irreversible structural alterations sufficient to impair vision, use of the higher concentration therefore seems justifiable. Indeed, these studies do not establish the optimal concentration of prednisolone acetate. It is
6 762 Leibowitz and Kupferman Investigative Ophthalmology October 1974 possible that concentrations of the acetate higher than 1.0 per cent might be even more effective and warranted for the treatment of selected clinical problems. Surprisingly, the same increase in prednisolone phosphate concentration failed to produce any consistent, significant increase in anti-inflammatory effect in the cornea. However, this increase in concentration (from per cent to 1.0 per cent) is followed by an almost sevenfold increase in the level of prednisolone phosphate present in the cornea.' ; Thus, administration of additional quantities of the drug (in the form of the higher concentration), though seemingly of negligible therapeutic benefit, does have a greater potential for inducing unwanted side effects. This observation also suggests that prednisolone acetate is, per se, a more potent antiinflammatory agent in the cornea than is prednisolone phosphate and that its therapeutic superiority is not simply a reflection of greater corneal bioavailability under the present experimental conditions. It has been well established in systems outside the eye that dexamethasone is a more potent corticosteroid than is prednisolone. Estimates vary slightly, but it is generally held that the relative anti-inflammatory potency of dexamethasone is six times that of prednisolone. 1 - However, since dexamethasone is made available to the ophthalmologist in a 0.1 per cent formulation, while prednisolone is available as a 1.0 per cent formulation, the tenfold difference in concentration seems to give prednisolone a slight edge. Comparison of the present data with previously run but comparable studies of dexamethasone 0 supports this conclusion. Comparing Group III animals, we have the following relative values of mean decrease in corneal inflammatory activity: (1) prednisolone acetate 1.0 per cent ophthalmic suspension, 51 per cent; (2) dexamethasone alcohol 0.1 per cent ophthalmic suspension, 40 per cent; (3) prednisolone phosphate 1.0 per cent ophthalmic solution, 28 per cent; (4) dexamethasone phosphate 0.1 per cent ophthalmic solution, 19 per cent; and (5) dexamethasone phosphate 0.05 per cent ophthalmic ointment, 12 per cent. The results of these experiments indicate that among the corticosteroid formulations studied to date, prednisolone acetate 1.0 per cent ophthalmic suspension is the most effective topical anti-inflammatory agent when the epithelium of the inflamed cornea is intact. It must be re-emphasized that because of differences in the aqueous solubility of these compounds and because of the nature of the lipophilic barrier of the corneal epithelium, the relative order of corneal anti-inflammatory potency among these drugs may differ when the epithelium is not intact. This possibility is under investigation. REFERENCES 1. Cox, W. V., Kupferman, A., and Leibowitz, H. M.: Topically applied steroids in corneal disease. I. The role of inflammation in stromal absorption of dexamethasone, Arch. Ophthalmol. 88: 308, Cox, W. V., Kupferman, A., and Leibowitz, H. M.: Topically applied steroids in corneal disease. II. The role of drug vehicle in stromal absorption of dexamethasone, Arch. Ophthalmol. 88: 549, Kupferman, A., Pratt, M. V., Suckewer, K., et al.: Topically applied steroids in corneal disease. III. The role of drug derivative in stromal absorption of dexamethasone, Arch. Ophthalmol. 91: 373, Kupferman, A., and Leibowitz, H. M.: Topically applied steroids in corneal disease. IV. The role of drug concentration in stromal absorption of prednisolone acetate, Arch. Ophthalmol. 91: 377, Kupferman, A., and Leibowitz, H. M.: Topically applied steroids in corneal disease. V. Dexamethasone alcohol, Arch. Ophthalmol. In press, Kupferman, A., and Leibowitz, H. M.: Topically applied steroids in corneal disease. VI. Kinetics of prednisolone phosphate, Arch. Ophthalmol. In press, Leibowitz, H. M., and Kupferman, A.: Pharmacology of topically applied dexamethasone, Trans. Am. Acad. Ophthalmol. Otol. In press, Robb, R. M., and Kuwabara, T.: Corneal wound healing. II. An autoradiographic study of the cellular components, Arch. Ophthalmol. 72: 401, 1964.
7 Volume 13 Number 10 Topically administered prednisolone Snedecor, G. W.: Statistical Methods Applied to Experiments in Agriculture and Biology. Ed. 5. Ames, Iowa, 1956, Iowa State College. 10. Cochran, W. C, and Cox, C. M.: Experimental Designs. New York, 1957, J. Wiley and Son, Inc., pp Leibowitz, H. M., Lass, J. H., and Kupferman, A.: Quantitation of inflammation in the cornea, Arch. Ophthalmol. In press. 12. Sayers, G., and Travis, R. H.: Adrenocortical steroids and their synthetic analogs. In The Pharmacological Basis of Therapeutics, Goodman, L. S., and Gilman, A., editors. Ed. 4. New York, 1970, The Macmillan Co., p
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