Journal of the American Association for Laboratory Animal Science Vol 54, No 6

Copyright 2015 November 2015

by the American Association for Laboratory Animal Science Pages 783–787

Evaluation of Lacrimation Characteristics in

Clinically Normal New Zealand White Rabbits by
Using the Schirmer Tear Test I
Alexandra L Whittaker1,* and David L Williams2

Rabbits are a common animal model in eye research and in safety testing of novel chemical agents. In addition, ocular
disease is a routine presentation in clinical practice. However, few studies have quantitatively examined lacrimation kinetics
in this species. This study used a noninvasive method of tear measurement (the Schirmer tear test, STT) to quantify values
for basal and reflex tearing and to determine the kinetic nature of tear production in 76 New Zealand white rabbits. We ob-
tained a value of 7.58 ± 2.3 mm/min for the standard 1-min STT. Calculated values for mean residual tear volume and reflex
tear flow were 1.95 µL and 0.035 µL/s, respectively. In addition, this study provides preliminary evidence for an interaction
effect between eyes given that higher STT values were obtained from the second eye tested.

Abbreviation: STT, Schirmer Tear Test.

Rabbits are widely used in ophthalmic research and are in-
creasing in popularity as pets. However few reports evaluate
lacrimal parameters in this species,1,5,12,10 despite the relatively
high incidence of ocular disease in rabbits. Typically, ocular
disease in rabbits presents as an overproduction of tears due
to ocular foreign-body irritation or nasolacrimal duct blockage
with resultant epiphora. Accurate diagnosis of the cause of tear
overproduction is imperative for quickly and efficiently treating
the underlying pathologic mechanism.
The precorneal tear film is essential to the maintenance of
corneal health and consists of 3 components: lipid, aqueous,
and mucin. Aqueous tears account for the majority of the tear
are produced after stimulation, usually as a result of an irritant
to the ocular surface, such as a foreign body or inflammatory
response.25 The tear-test strip itself likely acts as a source of
irritation to increase tear production in the STT1.31 It has been
demonstrated that the turnover rate for reflex tearing is greater
than that during basal tear-flow kinetics, and thus the protein
profile of the 2 samples may differ.8
Because of the small volume of tears produced, the STT1 might
be more useful in the evaluation of the increased tear production
associated with ocular irritation than it is for the diagnosis of un-
derproduction, as in the case of clinical keratoconjunctivitis sicca.
1 This criticism has led some clinicians to make greater use of the

volume.23 In lagomorphs, 5 glands contribute to the precorneal
tear film: the Harderian and nictitating glands associated with
the medial canthus and the lacrimal, infraorbital, and exorbital
glands of the outer canthus.27 The orbital lacrimal gland is cred-
ited with being the primary source of the aqueous components
of tears and with the production of proteins that protect the
ocular surface against bacteria.20
The Schirmer tear test (STT) is a technique widely used in
ophthalmic examination to evaluate tear production as an aid to
diagnosing either keratoconjunctivitis sicca or overproduction
of tears. General clinical use of the test involves the placement
of a standard notched filter paper into the lower conjunctival
fornix of the eye and reading the amount of wetness produced
after 1 min.23 Specific diagnoses are made by comparing the
recorded value with the mean normal value for the species.
The STT1, which is performed without the use of topical
anesthesia, provides a measure of both basal and reflex tearing,
whereas the STT2, which is performed after topical anesthesia
with a drop of tetracaine, demonstrates basal tearing alone. Basal
tears are those produced in the absence of stimulation and are
lacrimal secretions that maintain the ocular surface. Reflex tears
Received: 16 Dec 2014. Revision requested: 09 Feb 2015. Accepted: 02 Mar 2015.
1School of Animal and Veterinary Science, University of Adelaide, Roseworthy Campus,
Australia, and 2Department of Veterinary Medicine, University of Cambridge, Cambridge,
United Kingdom
*Corresponding author. Email: alexandra.whittaker@adelaide.edu.au
phenol red test (especially in small patients). Compared with the
STT, the phenol red test requires a smaller tear volume to achieve
test-thread wetting, thus minimizing variability in reading.5
Despite these advantages, the STT remains the most commonly
used quantitative tear-assessment test in veterinary species.16,33
Previous studies in rabbits have evaluated standard 1-min
STT1 readings1,5 and 5-min readings with topical anesthesia,12
yielding 1-min values (mean ± 1 SD) of 5.3 ±2.96 mm/min,1 4.85
±2.9 mm/min,5 and a range of 0 to15 mm/min.1,5 In one study,5
the sample population consisted of 26 New Zealand White rab-
bits; another investigation1 involved a variety of breeds (which
differed in size), with the New Zealand White subpopulation
comprising 28 rabbits. That study1 found that, in general,
neither sex nor breed significantly affected STT values, except
that values of those Netherland dwarf and New Zealand Black
rabbits were higher and lower, respectively, than the results for
the remainder of the study population. Nevertheless, sample
sizes of these breeds were small (n = 2 animals), so data should
be interpreted with care. In comparison, interbreed differences
in STT1 have been demonstrated in dogs.14 In rabbits, no sig-
nificant difference on comparison of STT values between eyes
nor any evidence of an interaction between eyes was found.1
Studies involving tear-flow rates in humans have used sev-
eral different methods.7,23 For example, strips of specialized
absorbent paper (Periopaper, Oraflow, Smithtown, NY) have
been used to collect basal tears; the volume of tears collected is

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 Vol 54, No 6
Journal of the American Association for Laboratory Animal Science
November 2015

evaluated by using an electronic device (Periotron, Oraflow),

which measures the charge across 2 electrodes as an indication
of volume.7 In the same study, reflex tear production was evalu-
ated by using a STT strip, reading the wetted length after 5 min,
and then comparing that value with the wetted lengths obtained
for known volumes of egg-white lysozyme solution.7 Fluoro-
photometric means for measuring the human tear-turnover rate
have been based on the disappearance of fluorescent dye over
time.23 Tear-flow rates in rabbits have been calculated by can-
nulating the excretory duct of the lacrimal gland under general
anesthesia, to collect lacrimal gland fluid. 11 The tear-flow rate
was determined by dividing the volume by the collection time.
However, the primary aim of that study11 was to determine the
effect of the stimulation of flow on the osmolarity of lacrimal
fluid, rather than to investigate flow rates specifically.
The object of the current exploratory study was to extend
previously published work and demonstrate the kinetics of
tear flow in a single, widely used strain of rabbit (New Zealand
white) and to quantify values for reflex tear production by us- Figure 1. A standard Schirmer tear-test strip, showing dye movement
and gradation scale.
ing a simple and clinically relevant method, the STT1. A second
aim was to use the data to assess whether tear flow volumes or
kinetics differed between the left and right eyes and whether an 10 s for a total of 3 min. Test strips were held in place throughout
interaction effect existed between eyes. We hypothesized that the period of recording. The eyes were tested sequentially, with
tear production would be increased in the second eye in which recording for the second eye commencing immediately after
the test was performed compared with the first. completion of testing in the first. All test strips were from the
same lot and manufacturer (Schering–Plough Animal Health,
Kenilworth, NJ). The test is noninvasive and causes minimal
Materials and Methods distress to the rabbits. Tests were performed indoors in an en-
In vitro wetting of the STT strip. The wetting of the STT strip was
vironment of constant thermostatically controlled temperature
investigated in vitro to determine the kinetics of fluid movement
and humidity. The same researcher tested all rabbits between
along the strip. This data was used to convert wetting measured
0900 and 1200. Previous studies have suggested that diurnal
in the in vivo studies (in mm), to volume of tears (in μL). By so
fluctuations in STT readings are not biologically significant.4
doing, an estimate of reflex tear-flow volumes in New Zealand
To assess interaction between eyes, the 76 rabbits were as-
white rabbits was made. Saline volumes of 5, 7.5, 10, and 12.5 µL
signed randomly to groups according to the order in which both
plus an unlimited supply were added to the strip, and the wetted
eyes were tested. The STT was performed as described previ-
length of the strip was determined at 10-s intervals for 3 min.
ously. Results from rabbits in which the left eye was tested first
Animals. The study population comprised 76 (n = 152 eyes)
were compared with those in which the right eye was tested first.
New Zealand White laboratory-stock rabbits (Harlan, Leices-
Statistical analysis. Data were analyzed by one-way ANOVA
tershire, United Kingdom). Rabbits were health-screened at the
(Predictive Analytics Software PASW, SPSS (2009), version 17.0,
source and were deemed specific pathogen-free according to
Chicago) to compare the mean basal tear volumes and reflex
the FELASA recommendations for health monitoring of labora-
flow rates over the 3-min period and differences in rate between
tory rabbits. Because the study used a relatively noninvasive
eyes, to correlate tear production and weight or age of the rab-
procedure (the STT) that is used as a standard in clinical vet-
bit, and to identify any interaction between eyes. Statistical
erinary practice, ethics approval under the Animals (Scientific
significance was defined as a P value of less than 0.05.
Procedures) Act 1986 (United Kingdom) was not required.
However, approval for the study was obtained through the
institutional ethics and welfare committee. The rabbits were Results
housed in floor pens on dust free bedding and were clinically In vitro tear strip wetting. When volumes of saline were added
healthy, with no known ocular disease. Food (Harlan Teklad to the test strips, the results showed an approximately linear
Rabbit Diet, Harlan) and water were provided free choice, by relationship between the length of wetting and time in both lim-
using wall-mounted hoppers and drinking nipples. All rabbits ited and unlimited supply situations Figure 2. The total wetted
except 2 were female; however, previous studies have indicated length was proportional to the volume of solvent applied. Each
no difference in 1-min STT readings between does and bucks.1 point on the graph represents a mean value for 5 separate tests,
Rabbits ranged in age from 3 to 10 mo (average group weight and a plot of the maximal wetted length against the volume of
range, 4.06 to 4.55 kg) and were housed in the same room on saline yielded a linear relationship with the equation (1)
the basis of this age grouping.
In vivo tests. Each rabbit was manually restrained in a stand- y = 1.9844x ,
ard commercial polycarbonate rabbit restrainer and tested by
using the STT1, which does not involve topical anesthesia. where y is the wetted length (in mm), and x is volume of saline
Performance of the test involved insertion of the notched end (in µL).
of a commercial tear-test paper over the lower lid margin at the This relationship enables the conversion of in vivo values of
juncture of the temporal and middle third of the lid. The eyelids length of tear strip wetting into volumes of tear production,
were held shut for the period of the test. The length of tear strip assuming that fluid characteristics have a negligible influence
wetted was recorded (in mm), as shown by the advancement of on the wetting rate and that the secretion rate remains below
the blue dye on the marked standardized scale (Figure 1), every the maximal uptake rate of the paper strip.

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 Evaluation of tear production in rabbits

Figure 2. In vitro wetting of Schirmer test strips for 5 different vol-

umes of saline, showing mean ± SEM values for 5 tests.
Figure 3. Schirmer tear test results (mean ± SEM) over period of test
for both eyes analyzed separately (n = 76)
In vivo tear strip wetting. STT was studied in 76 rabbits
free from ocular disease. Data from each eye were analyzed
separately, and STT values (mean ± 1 SD) were similar for both
eyes, with no statistically significant difference between right
compared with left eyes over the whole population (P = 0.29).
Lacrimation kinetics are shown in Figure 3. Because the data
from both eyes were similar, they were combined for further
analysis Figure 4.22 After combining the data for both eyes, we
obtained a 60-s STT value of 7.6 ± 2.3 mm (range, 3 to 14 mm);
the 120-s. STT value was 8.7 mm ± 3.1 mm (range, 3 to 16 mm).
(Figure 4) reveals 3 linear trends representing different phases
of strip wetting. Values derived from these trend data provide that
Figure 4. Mean ± SEM. Schirmer tear test results over period of test for
when x = 10 s, y = 3.9 mm, which corresponds to a value of 1.9
both eyes combined (n = 142). Trend lines are shown in red. The arrow
µL, according to equation 1. Reflex tear production is calculated illustrates the gradient used for calculation of reflex tear flow rates.
from the gradient of the initial slope in (Figure 4) (indicated by
the arrow); y values for the gradient correspond to 2.8 mm, and
the x value is 40 s. Therefore the gradient is 0.07 mm/s, which
equates to 0.035 µL/s (according to equation 1).
Interaction between eyes. This evaluation of the initial results
assessed the mean difference in 60-s tear-test results between the
second eye tested and the first (that is, STTsecond – STTfirst). The
data were evaluated by plotting a frequency distribution of the
mean differences (Figure 5). The mean of the mean difference
between both eyes (that is, STTsecond – STTfirst) was 0.18 ± 0.04
(95% confidence limits) for the sample of 76 eyes.

Discussion
Various authors have studied the kinetics of capillary flow in
STT strips. From these studies, we have made the assumption
that, in the case of limited supply (as in vivo) at low secretion
rates, the rate of wetting length increase is linearly proportional
to the secretion rate when evaporation is negligible.3,6,17,18,31
Because evaporation increases with increased wetting length,
a steady state is reached at which the length of wetting is con-
stant over time. This means comparisons that are based on the
rate of wetting being equal to secretion rate can be assumed
to be true. In addition, paper and fluid characteristics have a
negligible effect on rate of wetting, so using saline as a control
is justified.3,6,17,18.
Using our results, we have shown that by plotting STT values
over time, an estimate of reflex tearing can be obtained.31 The in
vivo kinetic data (Figure 2) resemble saline control data, with
an initial rapid uptake of tears (from the tear lake), followed by
section that is associated with a decreased gradient indicative
of the reflex tear production rate, and an eventual flattening of
the graph. This flattening is caused by the increase in evapora-
tion as wetting length increases, which eventually leads to a
Figure 5. Frequency distribution of the mean differences between eyes
that is STT second eye- STT first eye.
steady-state situation.17 Values obtained for residual tear volume
and reflex tear flow in New Zealand white rabbits were 1.9 µL
and 0.035 µL/s, respectively. Plotting of STT results over time
is easily achieved and provides a simple method for determin-
ing tear turnover based on the contribution of tears from the
tear lake and for measuring tear production. This procedure
therefore yields some useful information in addition to that
obtained from a standard STT reading, which is taken at a single
time point.31 To accurately quantify basal tear production, STT2
testing after the application of topical anesthesia is needed and
might represent an avenue for further study to better quantify
lacrimation kinetics in rabbits.
The large SD likely reflects the large range in values (simi-
larly mentioned in a previous study1) rather than error in the
experimental method. Large ranges in the mean STT value are

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Journal of the American Association for Laboratory Animal Science
November 2015
not unique to rabbits: SD values typically represent a quarter
of the mean in dogs9 and cats2 and were even greater in guinea
pigs (although mean STT values were extremely low).30 In our
rabbits, the mean value for the standard 60-s STT was 7.58 ± 2.3
mm/min, with maximum of 14 mm/min and minimum of 3
mm/min. These results are in contrast to the values of 5.3 ± 3.0
mm/min1 and 4.8 ± 2.9 mm/min5 determined in previous stud-
ies. In light of the breed distribution in one of these studies,1 the
other5 is a better comparator given that it involved New Zealand
White rabbits. The difference between the values obtained in our
current study and the previous one5 might reflect our increased
sample number and a possible weight- or age-associated effect
on tear production. This effect was not investigated specifically
in the earlier study,5 but those animals weighed less than did
those in the current study (less than 4 kg). In addition, we found
no significant difference between the values for the right and left
eyes when we compared the entire sample population as a whole,
in concurrence with previous studies undertaken.1,5 This finding
led us to combine the data from both eyes, for further statistical
comparison. This approach is widely used in ophthalmologic
research in both humans and veterinary species but may be
statistically flawed and lead to false-positive results. Combining
the data from both eyes might render the t test invalid, because
the measurements from the 2 eyes of a single subject are usu-
ally related, not independent.22 This factor likely has a greater
consequence in research investigating the effects of drugs on
intraocular pressure or when assessing systemic parameters to
make treatment recommendations but should be considered
whenever studies of any ophthalmologic nature are designed.
We hypothesized that if an interaction between eyes existed,
tear production would be greater in the second eye in which
the test was performed. The mean difference between these
measurements was positive (0.18), albeit only slightly. Because
the 95% confidence limits for this value do not span 0, there is
some evidence to support the hypothesis proposed. This area
has not received much attention in previous studies in any spe-
cies, although other colleagues assessed this factor in rabbits to
find no interaction between eyes.1 The neurology of lacrimation
is complex and still under discussion. There is no reported neu-
ral system of communication between eyes that would allow a
stimulus in one eye to influence reflex stimulation in the other
and thus explain such a finding.28,26,32 It seems feasible that
a stimulus in one eye might travel within afferent trigeminal
fibers and be mediated centrally in the brainstem, possibly in
the receiving nucleus (sensory nucleus of the trigeminal nerve),
to distribute bilaterally to the lacrimal glands of both eyes.
However, this explanation is mere conjecture. Another possible
explanation for an interaction might be a psychogenic cause,
but again the paucity of evidence for a communication system
between eyes blights this hypothesis. Given the lack of studies
investigating reflex lacrimation and eye interaction effect and
in view of our findings, this area of research requires further
characterization by using larger sample sizes to elucidate both
the presence (or absence) of an interaction and the neurologic
pathway that might mediate such an effect.
A limitation of our study is that age and weight of individual
rabbits were not recorded to evaluate whether a relationship
exists between these variables and tear production. Research
has shown differences in tear production with age and weight
in dogs. One study reported an increase in tear production in
heavier animals, showing that basal tear production increased.4
Other authors conversely found a decrease in STT as dogs aged
but no significant correlation of weight with STT.15 Another
group demonstrated that older dogs were more likely to be
786
jaalas14000184.indd 786
tear-deficient among a population of 460 dogs that presented
for ophthalmic examination.19 However, other studies have
looked at STT values in normal domestic canines and felines
but found no significant difference with age or sex.14,21,29 It
seems plausible that there might be a relationship between
age and tear production by the developing lacrimal gland in
younger animals, and that a reduction in functional capacity
of the lacrimal and nictitans glands might occur in senescent
animals, leading to a decrease in tear production. The effect of
age on tear production does not appear to have been studied
previously in rabbits and merits future evaluation by using
animals that vary widely in age. The inclusion of weight as a
covariate should be considered, to elucidate the contributing
effect of each variable.
Our current study has demonstrated that the STT, widely
used in clinical practice, can provide much more information
than might appear at first. Cases of naturally occurring kera-
toconjunctivitis sicca in rabbits have not been reported, but
these animals are often used in research as a model for this
disease.12,13 In such applications, a simple method of measuring
progression of the model postoperatively is of value. In addition,
rabbit ocular disease is a common presenting problem in clinical
practice (particularly that of tear overproduction and epiphora),
and it is useful to have techniques available to evaluate factors
that might contribute to disease. Despite the large variability
in the STT results that we obtained in the current study, the test
generally is still valid because a clinical diagnosis of over- or
underproduction of tears usually is made only after several
abnormal tests have been obtained.
In conclusion, this study has extended earlier work in this
area by using a larger sample and consequently has provided
a reliable reference value for the standard, 1-60 STTs in New
Zealand white laboratory rabbits. We determined values for
tear production rates, and we present evidence that supports
the existence for an interaction between eyes in the results of
the STT1. Finally, we have highlighted potential avenues for
further study in rabbits and other species.
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