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The effect of lid closure upon the ocular temperature gradient Bernard Schwartz The effect of lid closure and opening upon the ocular temperature gradient was studied in the rabbit eye by determining the changes in temperature of the anterior surface of the central cornea, the pupillary area of the anterior chamber, and the midiris area of the posterior chamber. With lid closure the temperature of all three areas rose to a similar level of 37.7° C. so that the ocular temperature gradient was essentially abolished. The time for rise of temperature with lid closure was greater than the time for fall ivith lid opening in the posterior chamber. As an incidental observation, it tuas noted that loith the lids open the mean temperatures of all three areas were generally lower in the horizontal head position (visual axis perpendicular to the ground) than those in the vertical head position (visual axis parallel to the ground). This observation is interpreted as due to a decreased heating of the cornea by the lack of a flmoing tear film because of pooling in the conjunctival cul-de-sac with the head in the horizontal position. The physiologic position of the lids will also create in the anterior segment of the eye, superiorly and inferiorly, a peripheral to central ocular temperature gradient in addition to the existing posterior to anterior gradient. The blink reflex is too infrequent in the rabbit to influence the ocular temperature gradient, but closure of the lids such as during sleep will abolish the temperature gradient while lid retraction or globe protrusion will increase the temperature gradient. I n a previous investigation1 the ocular temperature gradient was described. Preliminary observations indicated that such physiologic variables as lid closure and environmental temperature affected the ocular temperature gradient. The effect of lid closure upon ocular temperature had been noted incidentally by other investigators.2'7 However, it appears that only Nakaos had conducted a detailed study using the implanted thermocouple technique. It is the purpose of this paper to describe the rates of change as well as the changes of temperature of the central, anterior corneal surface and the anterior and posterior chambers on lid closure and opening, especially in regard to the effect upon the ocular temperature gradient. Materials and methods The temperature measuring device, the thermistor, with associated Wheatstone Bridge and recorder, has been described fully previously.1 The central, corneal surface temperature was measured by a bead thermistor mounted at the end of a long, flexible plastic tube. For measurement of anterior and posterior chamber temperatures, the hypodermic needle thermistor probe was used. Except for the distal portion penetrating the eye, the remainder of the needle was covered by a polyethylene tube to prevent heat loss by conduction along the needle shaft. New Zealand albino male rabbits weighing 2.0 to 2.5 kilograms From the Division of Ophthalmology, Department of Surgery, State University of New York, Downstate Medical Center, Brooklyn, N. Y. This investigation was supported in part by Research Grant B-1820 from the National Institute of Neurological Diseases and Blindness, National Institute of Health, United States Public Health Service, Bethesda, Md. 100 Downloaded From: http://iovs.arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933629/ on 05/15/2017 Volume 3 Number 1 Effect of lid closure on ocular temperature gradient 101 were the experimental animal. Before each set of measurements, the air temperature one inch in front of the right and left eyes was measured as well as the humidity and rectal and inferior conjunctival sac temperatures with the use of 0.5 per cent proparacaine hydrochloride (Ophthetic) 0 as the local anesthetic. General anesthesia was then induced with an intravenous dose of 25 mg. per kilogram body weight of pentobarbital sodium (Nembutal). t For opening and closing the lids, 4-0 catgut sutures were placed in the skin of the upper and lower lids near the lid margin. Rectal and inferior conjunctival sac temperatures were again measured. Most of the ocular temperature measurements were made with the rabbit's head in the erect or vertical position (visual axis parallel to the ground) while the others were made with the rabbit's head in the horizontal position (visual axis perpendicular to the ground). For each temperature measurement, the thermistor probe was placed in the respective tissue until a constant temperature was noted on the recorder. In order to measure anterior or posterior chamber temperatures, a small superficial incision was made at the limbus with the tip of a keratome in the superior temporal quadrant with the superior rectus muscle for fixation. The incision was then completed by penetration of the needle thermistor, so that the anterior chamber was not lost when the needle thermistor entered the eye. The needle thermistor was then positioned in the pupillary area of the anterior chamber or in the inferior nasal quadrant midway between the pupillary border and the recess of the angle in the posterior chamber, and recording started immediately. The lids were then closed by grasping the sutures, and were maintained closed until a constant temperature was again noted on the recorder. The lids were then opened and kept open until the temperature again became constant. All anterior chamber measurements were determined initially except one where the posterior chamber temperature was determined first. Five of the twelve posterior chamber temperatures were determined initially while the others were taken subsequent to an anterior chamber measurement. Care was taken to insure that the nictitating membrane was retracted and not overlying the cornea when measurements were made with the lids open. The pupil size averaged 6 to 7 mm. throughout all the measurements under general anesthesia. All studies were done during the winter months in the late afternoon. For statistical analysis, the student t test of significance was used in comparing the difference of two means °Allergan Pharmaceuticals, Los Angeles, Calif. f Abbott Veterinary Nembutal, Abbott Laboratories, North Chicago, 111. while the least significant difference test ( I S . D.) was used for more than two comparisons. A probability of 5 per cent (P < 0.05) was chosen as the level of significance. Results The environmental conditions under which the data were obtained as well as the rectal and conjunctival sac temperatures of the experimental animals are shown in Table I. The conjunctival temperatures of the right and left eyes have been grouped, as it had been shown previously that there was no statistically significant difference between the right and left inferior conjunctival sac temperatures.1 Figs. 1, 2, and 3 are representative tracings of the temperature response of the central, anterior corneal surface and anterior and posterior chambers to lid closure and opening. Table II shows the data for the temperature responses of these three areas as well as the times taken to reach steady states. The data for rise and fall of temperature were taken from measurements on the individual eye. With lid closure all three areas showed a rise in temperature and with lid opening the temperature returned to a level which was not significantly different from the initial temperature with the first opening of the lids. Similarly, the amounts of rise and fall of temperature were not significantly different. The time for Table I. Environmental conditions and rectal and conjunctival temperatures of experimental animals Room temperature (° C.) Range \ Mean 24.8 to 28.2 26.9 Air temperature 1 inch in front of eye (° C.) 25.5 to 29.0 27.3 35.2 Relative humidity ( % ) 27 Rectal temperature ( ° C.) pre-Nembutal post-Nembutal 39.2 to 40.3 38.2 to 40.3 39.51 39.31 Inferior conjunctival sac temperature ( ° C.) pre-Nembutal post-Nembutal 38.0 to 39.6 37.4 to 40.0 38.71 38.74 Downloaded From: http://iovs.arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933629/ on 05/15/2017 to 43 102 Schwartz lnoenligatioc Ophthalmology February 1964 rise and fall was not significantly different for central cornea and anterior chamber. But the time for rise of the posterior chamber temperature was significantly CLOSURE - — 8.0- .— ~. 4.0" —T — • — : : ~ — : . . __ — ~ . . • OPENING : — r— — - . — r.-_- — — — • - - - 7— rrr . — — — T-: •77: 1 i i iii! LJ t< — _ z— — 6.0u D | . — iliii! : . l! r.~ . . . . . . 2.0" — n • - —•: riz-i :.-: • : " : .-- • 30 : = ~rr 60 90 • • — 120 TIME (SECONDS) CHANGE IN TEMPERATURE OF CENTRAL ANTERIOR CORNEAL SURFACE WITH LID CLOSURE AND OPENING Fig. 1. The change in temperature of the central, corneal anterior surface with lid closure and opening. OPENING CLOSURE 20 50 80 110 TIME (SECONOS) CHANGE IN TEMPERATURE OF CENTRAL ANTERIOR CHAMBER WITH LID CLOSURE AND OPENING Fig. 2. The change in temperature of the central anterior chamber (pupillary area) with lid closure and opening. CLOSURE TIME (SECONDS) CHANGE IN TEMPERATURE OF POSTERIOR CHAMBER WITH LID CLOSURE AND OPENING Fig. 3. The change in temperature of the posterior chamber (midiris area) with lid closure and opening. greater than the time for fall (0.050 > P > 0.025). Table III separates the data of Table II into those measurements taken with the head in the vertical and horizontal positions. The data show that generally the mean temperatures with lid opening in the horizontal head position were lower than those in the vertical head position (significant on first lid opening for anterior chamber and on second lid opening for cornea and anterior chambers). Also, the mean rise and fall of temperatures and the mean time taken for the rise and fall of temperature were greater for the horizontal head position than the vertical head position (significant for the temperature rise of cornea and posterior chamber, for the temperature fall of cornea, for the time of rise of cornea, anterior and posterior chamber, and for the time of fall of anterior chamber). However, the final temperature on lid closure was similar in both head positions except for the anterior chamber measurements which were significantly different (P <0.001). Because of these differences due to head position, comparison of the different areas must take head position into account. Thus, the mean corneal temperatures on first and second lid openings were significantly lower than the mean anterior and posterior chamber temperatures for both head positions. Also, on first lid opening, the mean anterior chamber temperature was significantly lower than that of the posterior chamber but only for the horizontal head position. On second lid opening, for both horizontal and vertical head positions, there was no significant difference between the mean anterior and posterior chamber temperatures. The final temperature on lid closure was not significantly different for cornea and anterior chamber or for cornea and posterior chamber in either head position. However, the mean anterior chamber temperature on lid closure was significantly different from the mean posterior chamber temperature only in the horizontal head position. The mean times for rise of tern- Downloaded From: http://iovs.arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933629/ on 05/15/2017 Volume 3 Number 1 Effect of lid closure on ocular temperature gradient 103 perature of the posterior chamber were significantly greater than those for anterior chamber and cornea in the vertical head position only. There was no significant dif- ference in the mean times for fall of the three areas. For each area and head position, the only significant difference between time of rise and fall was in the posterior Table II. Ocular temperature changes on lid closure and opening Central cornea anterior surface0 Anterior chamber (pupillary area)0 Posterior chamber (midiris area)0 35.0 ± 1.4 (17) 36.4 ± 1.1 (12) 36.9 ± 0.8 (12) 37.7 ± 1.2 (17) 37.7 ± 0.7 (12) 38.1 ± 0.6 (12) 35.2 ± 1.2 (16) 36.5 ± 1.2 (11) 36.9 ± 0.8 (8) . 2.7 ± 0.8 (17) 1.3 ± 0.7 (12) 1.2 ± 0.7 (12) 2.5 ± 0.9 (16) 1.1 ± 0.8 (11) 1.1 ± 0.6 (8) Time for rise (min.) 1.4 ± 1.3 (17) 1.6 ± 1.1 (12) 2.8 ± 1.6 (12) Time for fall (min.) 1.4 ± 0.7 (16) 1.2 ± 0.8 (11) 1.6 ± 0.7 (8) Temperature with first opening of lids (° C.) Temperature with lids closed (° C.) Temperature with second opening of lids (° C.) Rise of temperature with lid closure (° C.) Fall of temperature with opening of lids (° C.) "Mean ± standard deviation (no. of determinations). Table III. Ocular temperatures on lid closure and opening with change in head position Central corneal anterior surface0 Horizontal Vertical head head position position Temperature with first opening of lids (° C.) 35.4 ±1.4(11) Temperature with lids closed 37.811.5(11) Temperature with second opening of lids (° C.) 35.611.2(10) Rise of temperature with lid closure (° C.) 2.4 + 0.5(11) Fall of temperature with opening of lids 2.210.8(10) Time for rise (min.) Time for fall (min.) Anterior chamber (pupillary area)0 Horizontal Vertical head head position position Posterior chamber (midiris area)0 Horizontal Vertical head head position position 34.3 ±1.0(6) 37.2±0.6(6) 35.5±0.9(6) 37.3±0.7(5) 36.6 + 0.8(7) 37.610.5(6) 38.3 + 0.4(6) 37.1 + 0.4(6) 38.0 + 0.7(5) 38.110.6(7) 34.4 + 0.9(6) 37.410.6(5) 35.7 + 1.0(6) 37.210.6(3) 36.8 + 0.9(5) 3.310.9(6) 1.1 + 0.1(6) 1.6 + 0.1(6) 3.2 ±0.8(6) 0.8 + 0.7(5) 1.410.9(6) 0.7 + 0.4(3) 1.4 + 0.6(5) 0.8 ±0.5(11) 2.4± 1.7(6) 0.910.4(6) 2.311.1(6) 1.610.7(5) 3.611.4(7) 1.2+0.7(10) 1.7 + 0.5(6) 1.6 + 0.8(6) 1.2 + 0.3(3) 0.610.3(5) 'Mean ± standard deviation (no. of determinations). Downloaded From: http://iovs.arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933629/ on 05/15/2017 0.7 + 0.4(5) 1.5 + 0.6(7) 1.8±0.8(5) Investigative Ophthalmology February 1964 104 Schwartz chamber data for the horizontal head position (0.05 > P > 0.02). In order to define the effect of blink rate in the rabbit on ocular temperature, a number of observations were made of the blink frequency. Eight rabbits were observed for a total of 29 five minute periods. In 19 of these periods no blinks were noted. In 4 periods—one blink, in 3 periods—2 blinks, in 2 periods—3 blinks, and in 1 period—7 blinks were observed for a mean frequency of 1 blink every 6.3 minutes. Discussion From the data presented it is apparent that with lid closure the ocular temperature gradient is essentially abolished within a short time. Both the central, anterior corneal surface as well as the anterior and posterior chamber temperatures rise rapidly to a common level which is similar to the mean orbital temperature of 37.7° C.1 The amount of rise and fall of temperature is a function of the initial temperature. The vessels of the palpebral conjunctiva provide enough heat to warm rapidly the anterior segment of the eye. When compared to the central corneal surface, the anterior chamber showed no significant time lag in reaching the same temperature level on lid closure, indicating that the cornea is an excellent heat conductor. Although the temperature of the posterior chamber was initially higher than the temperature of the cornea or the anterior chamber, the time for rise and fall with lid closure and opening was relatively greater. This difference is probably due to the iris acting as a good insulator. Goldmann9 has demonstrated a similar finding in his studies on the effect of infra-red radiation on the production of cataracts. Previously, all temperatures described for determining the ocular temperature gradient were measured with the head in the vertical position.1 The differences of ocular temperatures with the lids open between the horizontal and vertical positions of the rabbit's head noted in this study indicate another factor influencing the ocular temperature gradient. One probable explanation for this difference is the role of warm tears in maintaining the temperature of the anterior corneal surface greater than the environmental temperature. Because of infrequent blinking in the rabbit, the spread of tears across the cornea must be primarily by flow. With the head in the horizontal position, tears pool in the superior and inferior conjunctival sacs at the base of the protruding cornea. With continuous exposure one can observe the cornea to dry. The temperature difference with the lids open could be then due to the lack of heating effect of the constant tear flow. One would expect, therefore, that with lid closure no temperature difference would be observed between the horizontal and vertical head positions. Although this was true for the cornea, the anterior chamber did show a significant difference. Some additional factors may be operating, perhaps cardiovascular in nature. It appears that the heating effect of tears (approximately 1.40° C. for cornea and anterior chamber) outweighs any cooling effect by evaporation. A similar conclusion regarding the lack of cooling produced by evaporation of the tear film in rabbits was reached by Mishima and Maurice.10 The importance of the environmental temperature in determining the ocular temperature gradient is indicated by the data for central, anterior corneal surface and anterior chamber temperatures which are higher than those obtained in previous experiments.1 The difference is approximately 3° C, while the average room temperature was higher by 4° C. in the present experiments. Similar amounts of temperature change, as observed in these experiments, were noted by Michel2 and Nelson3 for the anterior chamber, by Walther6 for the cornea, and by Goldmann4 for the anterior and posterior chamber on partial and complete lid closure and opening. Nakao's data showed an average rise of 2.14° C. on opening and closing the lids for the central corneal surface.8 He also noted that 1.54° Downloaded From: http://iovs.arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933629/ on 05/15/2017 Volume 3 Number 1 Effect of lid closure on ocular temperature gradient 105 C. was the average rise on closing the lids for the anterior part of the vitreous body and 0.62° C. for the posterior part of the vitreous body. However, Goldmann observed no change for the temperature of the posterior surface of the lens. Since the temperature of the anterior segment of the eye essentially determines the ocular temperature gradient, one would expect that opening and closing of the lids exerts an effect on the temperature gradient even in the posterior part of the eye. Both Nakao and Goldmann reported longer periods of time for obtaining steady-state levels of temperature after opening and closing of the lids that noted here. This may be attributed to a lower room temperature since both their sets of experiments were conducted at room temperatures of about 15 to 18° C. The lower the room temperature, the longer it may take for the cornea to reach a steady-state temperature. This is also indicated by the larger rise and fall of temperature as well as the longer time shown for rise and fall with lid closure and opening in the horizontal head position where temperatures were initially lower. It is evident that with sleep, the ocular temperature gradient is eliminated, and any metabolic or physiologic functions dependent upon the temperature gradient would also be diminished.1 Since the rectal temperature of rabbits probably decreases during sleep,11 the absolute ocular temperature also probably decreases so that the final ocular temperature instead of being 37.7° C. is closer to 36° C, providing that there are no other ocular circulatory changes. Thus, the previously chosen figure of 35° C. for lens culture can be considered only approximately close to physiologic levels during lid closure with sleep. However, temperature dependent physiologic processes of both the cornea and anterior chamber, which are at lower temperatures with the lids open, would undoubtedly exhibit increased rates with lid closure. The blink frequency observed in these studies, 1 blink every 6.3 minutes, is about one half the frequency noted by Mishima and Maurice.1- The blink reflex in the rabbit is too infrequent to influence the temperature gradient significantly. In man, the blink reflex has also probably no effect on the temperature gradient since its duration is 0.5 seconds.13 The warming effect of the lids probably increases the temperature at the periphery of the cornea, especially where they overlay the superior and inferior limbus. Some evidence of this effect is noted in Nakao's observations of an increased temperature at the periphery of the cornea and angle of the anterior chamber compared to the central areas.14 Thus there is also a peripheral to central as well as anterior to posterior temperature gradient in the anterior segment of the eye. The peripheral to central temperature gradient may be partially responsible for the pattern of convection currents in the anterior chamber.35 The movement of particles in the anterior chamber should be more prominent after the lids have been opened some time so that the temperature gradient is increased across the anterior chamber. Similarly, with retraction of the lids or protrusion of the globe, there is a decrease in central and peripheral temperatures of the anterior segment of the eye.s- 1G The rise in temperature with closure of the lids may have significance in clinical situations. It is well known that cornea! ulcers tend to heal more rapidly when the lids are closed. This may be due to several factors, the one most frequently cited is prevention of rubbing of the corneal surface and ulcer edge.17 Closure of the lids also supplies increased metabolic nutrients such as oxygen from the vessels on the lid palpebral conjunctiva.ls However, the rise in corneal temperature with lid closure would increase the mitotic rate of corneal epithelium and also the speed of migration of corneal cells over the ulcer area.19 I wish to thank Mr. Walter Nazimowitz and Miss Myra Nager for their expert technical assistance, and Mrs. Aurora Clahane for statistical advice. Downloaded From: http://iovs.arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933629/ on 05/15/2017 106 Schwartz Investigative Ophthalmology February 1964 REFERENCES 1. Schwartz, B., and Feller, M. R.: Temperature gradients in the rabbit eye, INVEST. OPHTH. 1:513, 1962. 2. Michel, V.: Die Temperatur—Topographie des Auges, Arch. f. Ophth. 32:227, 1886. 3. Nelson, F.: Experimenteller Beitrag zur Frage der Temperatur in der Vorderen Augenkammer, insbesondere bei Anwendung des Dampfkauters nach Wessely, Klin. Monatsbl. Augenh. 78:48, 1927. 4. Goldmann, H.: Experimentelle Untersuchungen iiber die Genese des Feuerstars. III. Mitteilung, die Physik des Feuerstars, Arch. f. Ophth. 130:93, 1933. 5. Kokott, W.: Zur Frage der Kurzwellenbehandlung des Auges: Untersuchungen iiber die Erwarmung des Glaskorpers im Kaninchenauge bei Kurzwellenbestrahlung mit einemm Rohrensender, Klin. Monatsbl. Augenh. 97:448, 1936. 6. Walther, J., Bishop, F. W., and Warren, S. L.: The temperature pattern of laboratory animals in normal and febrile states in American Institute of Physics: Temperature, its measurement and control in science and industry, New York, 1941, Reinhold Publishing Corporation, p. 474. 7. Stephenson, W. V.: Thermal variations in diseases of the eye, 4 Congresso Panamer. Oftalm. 2: 1224, 1952. 8. Nakao, S.: Thermometrical studies on the variation of temperature of the ocular tissues in rabbits. Part 3. On the anatomical factors influencing the variation of temperature of the ocular tissues in rabbits, Folia Ophth. Jap. 8:311, 1957. 9. Goldmann, H.: Experimentelle Untersuchungen iiber die Genese des Feuerstars. IV. Mitteilung, die Physik des Feuerstars, Arch, f. Ophth. 130:131, 1933. 10. Mishima, S., and Maurice, D. M.: The effect of normal evaporation on the eye, Exper. Eye Res. 1:46, 1961. 11. Halberg, F.: Temporal coordination of physiologic function, Cold Spring Harbor Symposia on Quantitative Biology, Long Island Biological Association, Cold Spring Harbor, L. I., N. Y., 1960, vol. 25, p. 289. 12. Mishima, S., and Maurice, D. M.: The oily layer of the tear film and evaporation from the corneal surface, Exper. Eye Res. 1:39, 1961. 13. Adler, F. H.: Physiology of the eye. Clinical application, ed. 3, St. Louis, 1959, The C. V. Mosby Company, p. 27. 14. Nakao, S.: Thermometrical studies on the variation of temperature of the ocular tissues in rabbits. Part 2. On temperatures topographically measured in the ocular tissues of normal rabbits, Folia Ophth. Jap. 8:305, 1957. 15. Amsler, M., Verrey, F., and Huber, A.: L'humeur aqueuse et ses fonctions, Paris, 1955, Masson & Cie, p. 295. 16. Schmidt, R.: Uber Warmeverhaltnisse im gesunden und kranken Kaninchenauge nach verschiedenen therapeutischen Massnahmen, Klin. Monatsbl. Augenh. 102:788, 1939. 17. Duke-Elder, W. S.: Textbook of ophthalmology, Injuries, St. Louis, 1954, The C. V. Mosby Company, vol. 6, p. 5996. 18. Langham, M.: Utilization of oxygen by the component layers of the living cornea, J. Physiol. 117:461, 1952. 19. Friedenwald, J. S., and Buschke, W.: The influence of some experimental variables on the epithelial movement in the healing of corneal wounds, J. Cell. & Comp. Physiol. 23:95. 1944. 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