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THERMAL VARIATIONS OF THE HUMAN

BY Joseph M. Dixon, MD AND (BY INVITATION) Lisa Blackwood, RMA

INTRODUCTION HUMAN CORE BODY TEMPERATURE REMAINS ALMOST CONSTANT, BUT THE temperature ofperipheral body structures fluctuates with environmental changes, behavior, and metabolism.' Previous studies2-3 of the temperature of the eye have been done in animals. Huber,5 without recording the number of cases tested, used a thermistor and found the surface of the center of the human to be several degrees Celsius below general body temperature. Duke-Elder6 states that the avascularity of the cornea must be largely responsible for this. Mishima and Maurice3 studied evaporation ofthe tear film from the eye of the rabbit and found that the anterior oily layer of the tear film is protective of evaporation and is not removed by . Benjamin and Hill7 found an increasing corneal oxygen demand with increasing tem- perature. The purpose of this study is to document the thermal variations of the and its adnexa in health and disease and in comparison with standard oral clinical measurements.

MATERLALS AND METHODS Oral, corneal and upper and lower fornix temperatures in patients making routine office visits were recorded. Oral and fornix temperatures were measured with a digital fever thermometer (Becton Dickinson model 403000) (Fig 1). Corneal temperature measurements were made using a 2100 tele-thermometer (Yellow Springs Instrument Co Inc) (Fig 2) and a 3.4-mm diameter micro thermistor probe that does not require topical anesthesia (Fig 3). Informed consent was obtained from all patients. Simultaneous testing of the two digital thermometers and the thermistor probe used in this study, performed on a sample offluid, gave readings of 99.7°F and 99.6°F for the digital thermometers and 99.6°F for the probe. Standard deviations were calculated according to Wheeler.8 TR. AM. OPHTH. Soc. vol. LXXXIX, 1991 184 Dixon

FIGURE 1 Measurement of fornix temperature.

FIGURE 2 Instrument used to measure corneal temperature. Thermal Variations of the Human Eye 185

FIGURE 3 Probe used to measure corneal temperature.

Twenty-five patients were measured in each of the first six categories listed below. Eighteen patients with unilateral were measured in the seventh category. All measurements were made indoors at room temperatures. The categories were as follows: 1. Mouth and lower fornix of one eye 2. Lower fornix and upper fornix of one eye 3. Lower fornix and central cornea of one eye (without anesthesia) 4. Lower fornix of one eye before and after instillation of mydriatic drops (phenylephrine hydrochloride 10% or tropicamide 1%) 5. Lower fornix before and after patching of one eye for 30 to 50 minutes 6. Mouth, lower fornix, surface of contact , and cornea under a of one eye. Lens was removed and probe was immediately placed on the cornea without blinking or anesthesia, and reading was obtained in a few seconds. 7. Lower fornix of both .

RESULTS Test results obtained for each ofthe seven categories measured are shown in Tables I through VII. The average increase of mouth temperature 186 Dixon

TABLE I: DIFFERENCES IN TEMPERATURE RECORDED BETWEEN MOUTH AND LOWER FORNIX IN 25 PATIENTS* Greatest difference 3.70F Smallest difference 1.30F Mean 2.20F Average mouth temperature 97.90F Average temperature lower fornix 95.30F *Average increase of mouth temperature above lower fornix temperature was 2.20F Standard deviation calculated for mouth 0.544, and for lower fornix 0.845.

TABLE II: DIFFERENCES IN TEMPERATURE RECORDED BETWEEN UPPER FORNIX AND LOWER FORNIX IN 25 PATIENTS* Greatest difference 1.4°F Smallest difference .0°F Mean 0.3°F Average temperature upper fornix 96.16°F Average temperature lower fornix 95.80F *Average increase of upper fornix tempera- ture above lower fornix temperature was 0.30F. Standard deviation calculated for upper fornix 0.811, and for lower fornix 0.950.

TABLE III: DIFFERENCES OF TEMPERATURE RECORDED BETWEEN LOWER FORNIX AND CENTRAL CORNEA IN 25 PATIENTS WITHOUT ANESTHESIA* Greatest difference 4.0°F Smallest difference 1.3°F Mean 2.70F Average corneal temperature 92.70F Average lower fornix temperature 95.70F *Average increase oflower fornix temperature above corneal temperature was 2.770F Stan- dard deviation calculated for lower fornix 0.744, and for central cornea 0.949. Thermal Variations of the Human Eye 187

TABLE IV: LOWER FORNIX TEMPERATURE IN ONE EYE OF 25 PATIENTS BEFORE AND AFTER INSTILLATION OF DROPS* BEFORE DROPS AFTER DROPS ('F)t ('F)t Highest reading 97.0 97.3 Lowest reading 93.3 94.7 Mean 95.5 95.7 *Average increase of lower fornix temperature after drops was 0.21°F; there were no decreases. Greatest temperature differences was 1.8°F Standard devia- tion calculated before drops 0.921, and after drops 0.873. tEither phenylephrine hydrochloride 10% or tropi- camide 1%.

TABLE V: LOWER FORNIX TEMPERATURE IN ONE EYE OF 25 PATIENTS AFTER PATCHING FOR 30 TO 50 MINUTES* BEFORE AFTER PATCHING ('F) PATCHING ('F) Highest reading 97.6 98.6 Lowest reading 93.5 93.8 Mean 95.2 96.18 *Patched eyes increased an average temperature of 0.92°F Standard deviation calculated before patching 0.968, and after patching 1.01.

TABLE VI: TEMPERATURES OF MOUTH, LOWER FORNIX, SURFACE OF CONTACT LENS, AND CORNEA UNDER CONTACT LENS OF ONE EYE OF 25 PATIENTS WHO HABITUALLY WEAR CONTACT * MEAN HIGHEST LOWEST CHANGE READING ('F) READING ('F) MEAN ('F) GRADIENT Mouth 98.9 97.0 98.1 Lower fornix with contact lens 96.8 93.3 95.0 -3.1 Cornea under contact lens 98.9 93.0 92.0 -3.0 Surface of contact lens 92.8 89.9 91.1 -0.9 *There was no significant difference in decrease of corneal temperature under rigid or soft lenses. Standard deviation calculated for mouth 0.521, for lower fornix with contact lens 0.778, for cornea under contact lens 0.787, for surface of contact lens 0.819. 188 Dixon

TABLE VII: COMPARATIVE MEASUREMENTS IN LOWER FORNIX OF EACH EYE WITH UNILATERAL EYE ABNORMALITIES* TEMPERATURE NO. OF CASES INCREASE ('F) Iritis 1 1.3 Conjunctivitis 6 1.1, 2.7, 2.2, 1.1, 1.8, 1.5 Superficial punctate 1 0.6 Subconjunctival hemorrhage 1 0.4 2 0.6, 0.3 Trauma with aqueous flare 2 0.7, 0.6 Granulomatous uveitis 1 0.6 Corneal foreign body with rust 1 1.7 ring Chalazion of upper lid 2 1.6, 1.1 Chronic and conjunc- 1 2.0 tivitis *Each case showed an increase in temperature for affected eye. above lower fornix temperature was 2.2°F. The average increase of upper fornix temperature above lower fornix temperature was 0.3°F. The aver- age increase of lower fornix temperature above corneal temperature was 2.7°F. The average increase of lower fornix temperature after instillation of drops was 0.21°F, with no decreases; the greatest difference was 1. 8°F The average temperature increase after patching was 0.92°F. There was no significant difference in the decrease of corneal temperature under rigid or soft contact lenses. In the 18 patients with unilateral disease, all affected eyes showed an increase in temperature.

DISCUSSION Temperature gradients between the avascular cornea, the vascular ocular adnexa, and oral temperature are normal and are expected. Multiple factors are responsible for these gradients. The cooling effect of a contact lens on the cornea, as demonstrated in this study, was not expected. The average corneal temperature with a contact lens was 92.0°F, and the average corneal temperature without a contact lens was 92.7°F To verify this finding, 12 measurements were made on the mouths and of healthy individuals in the morning before a contact lens was applied and were repeated later in the day after a contact lens had been worn. The corneal temperature was consistently decreased under a contact lens, regardless ofwhether it was a soft hydrophilic lens or a rigid lens, and this was not parallel with changes in mouth temperature. The anterior oily layer ofthe tear film over the cornea, which is protective ofevaporation as Thermal Variations of the Human Eye 189

Temp OF 100 97.9 98

96 ~~~96.16 95.8

92.7 9 91.1 90 ~~~ ~ ~ ~ ~~~~~9.

Mouth Upper Lower Surface Cornea Surface Fornix Fornix of Under of Cornea Contact Contact Lens Lens FIGURE 4 Thermal variations of human eye. studied by Mishima and Maurice,3 may be disturbed over the surface of a contact lens, and increased evaporation may be responsible for lowering the temperature. Mean mouth temperature in category 1 was 97.90F, and mean mouth temperature in category 6 was 98.1°E This 0.20 variation is not signifi- cant. The slight variation before and after instillation of mydriatic or cyclo- plegic drops was only 0.210F, which is not significant. The increase of almost one degree with patching may be clinically significant in wound healing as described by Friedenwald and Buschke,9 who found more rap- id epithelial proliferation with increasing temperature and slowing prolif- eration with decreasing temperature. The increase of upper fornix tem- perature 0. 3°F above lower fornix temperature represents a normal phys- iologic variation. This study documents these physiologic gradients (Fig 4). Further studies are indicated in the arctic, the tropics, and the desert as well as in febrile patients. We therefore expect conditions that increase ocular temperature, such as patching and various diseases, to increase the oxygen demand of the cornea. Other conditions that decrease ocular surface temperature, such 190Dxo190 Dixon as wearing of contact lenses, would therefore decrease oxygen demand of the cornea, and probably of adjacent tissues as well. When treating an injury to the , we should consider that the corneal temperature of an eye that is patched will be about 2° above the temperature under a bandage soft contact lens. This tempera- ture increase under a patch should increase the rate of epithelial repair.

REFERENCES 1. Guyton AC: Textbook ofMedical Physiology, 7th ed. Philadelphia, WB Saunders, 1986, p 849. 2. Schwartz B, Feller MR: Temperature gradients in the rabbit eye. Invest Ophthalmol 1962; 1:513-521. 3. Mishima S, Maurice DM: The oily layer of the tear film and evaporation from the corneal surface. Exp Eye Res 1961; 1:39-45. 4. Schwartz B: The effect of lid closure upon the ocular temperature gradient. Invest Ophthalmol 1964; 3:100-106. 5. Huber A: Temperaturmessung am Auge. Ophthalmologica 1960; 139:351-357. 6. Duke-Elder S: System of IV. St Louis, CV Mosby, 1968, p 339. 7. Benjamin WJ, Hill RM: Closed lid factor influencing human corneal oxygen demand. Acta Ophthalmol 1986; 64:644-648. 8. Wheeler R: Modern Mathematics, 7th ed. Pacific Grove, CA, Brooks/Cole, 1988, pp 710-612. 9. Friedenwald JS, Buschke W: The influence of some experimental variables on the epithelial movement in the healing of corneal wounds. J Cell Comp Physiol 1944; 23:95-107.

DISCUSSION DR B. DOBLI SRINIVASAN AND DR D. JACKSON COLEMAN. In their paper the authors have examined the temperature distribution in the head and region and the eye and adnexa of 25 patients in routine clinical practice using commer- cially available digital thermometers and thermistors. Results are presented in terms of temperature gradients between adjacent areas. The effects of anesthesia and patching, corneal temperature under contact lens, and the lower fornix temperature in eyes with unilateral disease compared with the fellow eye are also examined. The expected gradient is seen for average temperatures as the thermometer is moved further from the body core. Addition- al findings are a temperature increase in cases of unilateral disease and following patching, and a temperature gradient decrease under contact lenses. The study identifies several interesting issues in the body's thermal regulatory function in response to local modifications such as patching and the use of contact lens. It suggests the need for larger-scale studies to provide a more robust statistical base for examining the effect of thermal variations, both natural and induced, on a wide range ofphysiological and functional topics. As is mentioned in the discussion, oxygen demand is strongly related to local temperature, and this may be a critical tomponent of wound healing. This should be another fruitful Thermal Variations of the Human Eye 191 area for additional research. Doctor Dixon also cites a study on the oily film layer ofthe cornea and suggests that disruption ofthis surface by a contact lens may lead to additional evaporative cooling of the corneal surface. An alternate hypothesis may be that the contact lens acts as an additional surface radiator causing cooling. This could be examined using an infrared bolometric technique. The study provides confirmation of the temperature variations of the eye as compared to oral temperatures and provides a base for further studies of environ- mental conditions that could affect not only contact lens wear but other issues such as refractive surgical modelling of the cornea. DR SLOAN WILSON. We are at least scratching the surface in ophthalmology related to thermology. This is an exciting field in many other parts of medicine, particularly in the field of transplant. Last year at ARVO and also at the Society I reported a series of intravitreal temperatures, which I had taken in 17 eyes undergoing . I stumbled on this while trying to define the thermal effects in the center ofthe vitreous when cryocoagulation was performed. In the process I found that the average temperature was some 10 degrees less than body temperature. Vitreous temperature averaged 88.9°F We used a variety of thermal probes which were calibrated against known thermal variables. At the Retina Society this paper was dubbed the most original research with absolutely no clinical application. That may well be true. However, I think that when one considers it a little more, thermal adjuncts will play an increasingly important role in the treatment ofmany diseases. I can think offour: (1) organ transplantation, (2) the various solutions which are infused into the eye and their effects on the tissues, (3) control of possibly even infectious diseases, and (4) refinement of thermal instruments (diathermy, cryo, cautery, etc). So I thank the authors for their contribution and I hope that others will pick up where they leave off. DR ARTHUR H. KEENEY. Thank you Doctor Blodi. Doctor Dixon reports a handy and simple technique for measuring temperature about the eye. Some years ago one of the residents and I at Wills decided to measure and record temperature on about 200 different eyes and orbits using the AGA Thermovision infrared scanner from Sweden. This provides a scale below the orbital or facial picture and can be set at 5 or 10°C. In a normal eye the cilia are obviously much cooler than the cornea and the cornea is cooler than its surrounding . The eye is warmer in the inner as compared to the outer canthus. We also found, ofcourse, that the nose tends to be cold. An isothermic line can be superimposed indicating a given uniform level. The are, obviously, hotter. Fig 1 is a normal eye and an isotherm would show maximum heat in the inner canthal area. The eye lashes and are ofsimilar cool temperature. A complete facial temperature map can easily be obtained. A normal temporal and its frontal branch are uniformly warmer than the nearby . Localized temporal arteritis also shows hot spots and their distribution. The isotherm marker, again, delineates temperature along this artery. Temperature does have diagnostic significance. In herpes zoster ophthalmicus, the face is obviously hot in the neural distribution on that side of 192 Dixon the face. Increasing blackness represents increasing heat; or increasing whiteness represents increasing coolness. A contusion injury to one orbital area is quite cool and obviously opposite to inflammation. In uncertainty over a swollen and painful area, thermograms quickly differentiate an infected lesion from contusion edema. Fig 2 shows the increased heat (blackness) ofan adenocarcinoma involving the left and antrum. These thermograms and correlated materials were originally published in the Transactions of the American Academy of Ophthalmology. DR J. TERRY ERNEST. Yesterday afternoon I was sitting on my balcony and a number of birds flew over and landed on the railing. They told me that the American Ophthalmological Society golfers were out in force and that they were hitting their golfballs too high and that there were cross currents up in the air and it was not a safe place for birds. This reminded me that birds fly fast and they must keep their eyes open, especially around here to avoid golfballs. The birds' corneas thus have a high rate of evaporation and as a consequence their eyes should be cold. In order to prevent the temperature of the retina from falling or, indeed, changing at all, it is carefully regulated. This is done by a highly vascular organ projecting into the vitreous cavity (Pecten). This vascular structure is thought to help control the temperature of the retina so that the heat loss from the birds' corneas is compensated for by a high blood flow in their Pectens. Lest you think this is all for the birds, in man it appears that the choroidal circulation acts as a similar heat exchanger. Indeed, the blood flow is so high in the that its total oxygen extraction need be only a few percent. The low oxygen difference between choroidal arterial and venous blood means that the blood flow is much higher than necessary for the nutrition of the outer retina. Indeed, the high flow exists to act as a heat exchanger. The blood enters around the area ofthe optic and travels in the choroid forward, exiting in the vortex . Thus, unlike the birds whose circulation warms the retina, our choroidal circulation cools the retina keeping it at a constant temperature when is shining on it. The question I have for Doctor Dixon is, does he have information about the circulation in his patients since this seems to be the critical factor controlling tissue temperature? DR MITCHELL H. FRIEDLAENDER. We have very few objective ways of measuring ocular pathology. One of the most difficult findings to document is ocular inflam- mation. We usually rate this on a 1 to 4 + scale. However, ocular surface tempera- ture can be used to quantify inflammation. We have looked at antiinflammatory agents for their ability to reduce allergic inflammation of the . The temperature ofthe conjunctiva goes up about 0.5°C when inflamed. This is similar to Doctor Dixon's findings. I wanted to ask Doctor Dixon if he has encountered the same problems we have, such as instability of measurements and interference from drafts, blinking, and eye movements. The temperature increase has not correlated as well as we would like it to with subjective inflammation in the end. It may be that subjective measurements are superior, but I think the objectivity of Thermal Variations of the Human Eye 193 temperature measurements has the potential to give us better data for measuring ocular inflammation. DR JOSEPH M. DIXON. I thank the discussers. I did not think that this subject was that interesting. Doctor Keeney, thank you for your information. I'm learning too, just as the discussers here. Doctor Ernest, I don't know anything more about the circulation in the choroid than we have in the literature. We know that the cornea has no circulation and we assume that that is mainly responsible for the cornea being cooler than other parts of the body. I agree with Doctor Friedlaender that the rec'ness itself is an indication of inflammation. We learned that as medical students, that inflammation is red and swollen and is tender and if you put your on it you can feel it and you know that you have inflammation, with an increase in temperature. It is surprising to me that a subconjunctival hemorrhage makes a temperature increase. It's mainly loose blood that is not circulating, but it does increase the temperature of that eye. Doctor Wilson, we appreciate the information of the vitreous. Thank you.