Download The Effect of Lid Closure upon the Ocular Temperature

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.
Downloaded From: http://iovs.arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933629/ on 05/15/2017