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Influence of eye position on the Schirmer tear test Etty Bitton a,∗ , Walter Wittich b a b

Ecole d’optométrie, Université de Montréal, Montreal, Quebec, Canada MAB-Mackay Rehabilitation Centre, Montreal, Quebec, Canada

a r t i c l e

i n f o

Article history: Received 30 August 2013 Received in revised form 18 October 2013 Accepted 26 November 2013 Keywords: Open and closed eye Schirmer test Gaze position

a b s t r a c t Introduction: The Schirmer test (ST) evaluates the volume of tears in potential dry eye candidates via a strip placed in the lower tear lake. Previously reported inconsistencies in the results may be in part due to the lack of standardization as to the methodology, e.g. the eye position during the test. The purpose of this study was to evaluate the effect of eye position on the ST score. Methods: . A ST was performed in a randomized fashion with and without anesthesia in three open eye positions (primary, superior and inferior) at 20◦ from each other. Palpebral aperture, age and a dry eye questionnaire (OSDI) were evaluated for correlation with the ST. Results: In the 20 non-dry eye volunteers (n = 20, ages 18–40, mean OSDI score 10.5), the ST results were, as expected, lower overall (p < .001) with anesthesia (11.33 ± 7.78 mm) than without (19.74 ± 2.83 mm). The inferior gaze position resulted in higher values (p < .03) than the other two positions, regardless of the use of anesthesia. No correlation was noted between the palpebral aperture, age, questionnaire and the ST. Conclusion: The ST seems to be influenced by the position of gaze. However, the mechanism for this, effect remains unclear. Further studies could focus on whether an inferior gaze of 20◦ compresses the tear film falsely, thereby elevating the tear volume. It is recommended that the clinician should adopt a standard eye position for the ST and that future reports provide specifics as to the methodology used. © 2013 Published by Elsevier Ltd on behalf of British Contact Lens Association.

1. Introduction The Schirmer tear test, first described by Otto Schirmer [1], has been used to indirectly measure the volume of tears. Tearing has a basal and an induced component due to stimulation of the trigeminal nerve [2–4] each of which is evaluated by a different Schirmer test. Schirmer test #1 uses no anesthesia and evaluates basal tear secretion coupled with the trigeminal reflex tearing, whereas Schirmer test #2 evaluates the basal component only when anesthesia is used prior to the test [5]. In the original description of the test [1], the tip of the 35 mm × 5 mm paper strip was placed in the lower cul-de-sac of each eye with the patient seated and with the eyes open [6]. Since then, the Schirmer test has become a staple in the evaluation of the tear film in dry eye (DE) patients [7–10] as well as contact lens candidates [11–13]. A Schirmer score of greater than 10 mm/5 min is widely accepted as the norm, whereas less than 5 is indicative of tear deficiency [10,13,14]. However the methodology of the test, when reported, has changed over the years, contributing, in part, to its variability [14]. Some

∗ Corresponding author. Tel.: +1 514 343 7302; fax: +1 514 343 2382. E-mail address: [email protected] (E. Bitton).

reports specify that the test be performed with eyes open [1,15–19], others with eyes closed [10,20–28], while others remain unspecified [29–39]. Table 1 summarizes Schirmer tear test evaluations in the past two decades in which eyelid condition (open or closed) has been noted. More recently, some reports have evaluated the effect of open versus closed eye positions on the value of the Schirmer test [40,41]. In both of these reports, the closed eye position revealed lower values. Despite these differences, neither report specified what constitutes an open or closed eye condition. One can assume that a closed eye is when the upper and lower lids gently come together. The open eye condition, however can be affected by gaze, such that looking slightly above primary gaze provides a larger palpebral aperture, which can enhance tear film evaporation. Conversely an inferior gaze can be somewhat protective by reducing the palpebral aperture and consequently tear film evaporation. In order to standardize the Schirmer test further and be able to compare results across studies, a uniform protocol needs to be adopted. Consequently, the purpose of this study was to investigate the influence of eye position on the Schirmer test score in non-dry eye (NDE) subjects. Based on previous work [14,27], it was expected that the Schirmer scores would be lower in participants with the anesthesia condition; however, an interaction effect was predicted, whereby this difference would depend on gaze.

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Age (years)

Population type

Anesthesia

Avg Schirmer score (mm)

Placement of test strip along lower lid

Open/closed eye condition

Gaze

Patient position

Pre-manipulation

Schirmer

1903

100

N/A

N



>15

Open

Unspecified

Unspecified

Unspecified

D. Roetth

1941

162

5 to >70

N



N/A

Unspecified

Unspecified

Unspecified

Unspecified

Henderson and Prough

1950

231

16–67

N



N/A

Unspecified

Unspecified

Unspecified

Unspecified

Wright and Meger van Bijsterfeld

1962 1969

10–80 20–74

12–17 N/A

Closed Unspecified

Unspecified Unspecified

Unspecified Unspecified

Unspecified Unspecified

1970 1972 1972 1975

19–41 14–79 Unspecified Unspecified

N N DE N N N N

− −

Pinschmidt Tabak Zappia and Milder Hanson et al.

266 550 43 7 85 232 140

Margin of the lower lid Junction of outer and middle third Adjacent to punctum Nasal 1/3 Unspecified

− − − −

43% < 15 N/A 69% < 15 N/A

Unspecified Unspecified Unspecified Unspecified

Unspecified Unspecified Unspecified Unspecified

Unspecified Unspecified Unspecified Unspecified

Unspecified Unspecified Unspecified Unspecified

Shapiro and Merin

1979

440

18–25

N



33.1

Unspecified Unspecified Unspecified Slightly lateral from center Lateral 1/3

Open

Seated

Unspecified

Feldman and Wood Lamberts et al.

1979 1979

11 233

19–28 12–84

N N

+ ±

Range 11–25 STna > STa

Lateral Lateral 1/3

Closed Open

Fixation slightly above the direct line of gaze Unspecified Unspecified

Unspecified Unspecified

Prause et al.

1982

Lateral 1/3

Closed

Unspecified

Lying down



Open or closed

Unspecified

Seated

Unspecified

1984 1988 1993

Unspecified 8–15 25–32

Unspecified Unspecified Lateral 1/3

Open Unspecified Closed

Unspecified Unspecified Unspecified

50

22–71

Lateral

Unspecified

Unspecified Unspecified Up and left (OD only) Unspecified

Unspecified Unspecified Seated

1997

22.3 7.6 15.1 N/A Range 0–26 min–1 77% < 5

Lateral 1/3

Kurihashi Zygulska-Mach Cho and Yap (Schirmer test II) Danjo

N DE N DE N N N Chinese DE (Sjogren). Japanese

20

1982

N/A 27–76 Unspecified



Nelson

5 32 13 7 310 577 10

Unspecified cul-de-sac was blotted with tissue following anesthesia Unspecified

Unspecified

Unspecified

Toda et al.

2001

64

Avg 32.3 ± 8.3

Bawazeer and Hodge

2003

30

Avg 53.9

Nichols, Nichols and Mitchell

2003

75

Nichols, Mitchell and Zadnik

2004

Serin et al.

− + − Unspecified +

Lower post LASIK

Unspecified

Unspecified

Unspecified

Unspecified

DE

+

Range 0–21

Lateral 1/3

Open

Unspecified

Unspecified

21–81 Avg 46

DE



Lateral

Closed

Unspecified

Unspecified

75

21–81

DE



2 mm from lateral canthus

Closed

Unspecified

Unspecified

Unspecified

2007

14

21–44

N



Significant relation with fluorescein staining Better repeatability with scores STc

.5% fluorescein and anesthesia instilled prior to test Inf fornix dried with a cotton tip applicator Unspecified

2–3 mm from lateral canthus

Open vs closed

Unspecified

Unspecified

Serruya et al.

2009

30

Avg 28

N

±

Sullivan et al. Kashkouli et al.

2010 2010

Sullivan et al. Li et al.

2012 2012

299 34 34 52 110

18–82 18–23 35–70 22–82 Avg 39.5

N N DE (Sjogren) DE DE

Unspecified

Open vs closed

Unspecified

Unspecified

− Unspecified

STo > STc ST1 > ST2 20.2 mm ± 11.3 STo > STc

Inf fornix dried with a cotton tip applicator Unspecified

Unspecified Unspecified

Unspecified Open vs closed

Unspecified Unspecified

Unspecified Unspecified

Unspecified Unspecified

− ±

13.1 mm ± 11.5 STna > STa

Unspecified Lateral 1/3

Unspecified Closed

Unspecified Unspecified

Unspecified Seated

Unspecified Inf fornix dried with a cotton tip applicator

ST, Schirmer test; STo, ST with eyes open; STc, ST with eyes closed; STna, ST with no anesthesia; STa, ST with anesthesia; N, normal; DE, dry eye.

G Model

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Table 1

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Fig. 1. Positioning of the participant in front of a target board (70 cm away) insuring a visual marker at 20◦ above and below primary gaze.

2. Methods The study received approval from the University of Montreal’s internal ethics committee, and all procedures were conducted in accordance with the tenets of the Declaration of Helsinki [42]. Informed written consent was obtained from all participants before the first of two testing sessions. The first session was to describe the study, and verify if they met the inclusion and exclusion criteria. The second session, at least 48 h later, evaluated the Schirmer test #1 (without anesthesia) and #2 (with anesthesia) in three different eye positions, notably at primary gaze and 20◦ above and below it. Eligibility criteria included NDE participants between the ages of 18–40 years. The ocular surface disease index (OSDI) questionnaire [43] was used to determine if the participant had DE. An OSDI score of less than 30 was required. The OSDI is a 12-question self-administered symptom test, with individual symptoms having a value of 0 (none of the time) to 4 (all the time). If a symptom does not apply, the participant can circle the “not applicable” option. The total OSDI score is then calculated as the sum of all the questions answered × 25, divided by the total number of questions answered. The total OSDI score can vary from 0 to 100, with increasing scores indicative of an increased severity of dryness [43]. Participants had to be free of systemic conditions and take no systemic medications, with the exception of birth-control pills. Over the counter medication had to be discontinued 24 h prior to the evaluation, and eye lubricants or contact lens wear had to be discontinued 48 h prior. Exclusion criteria were DE (OSDI value of >30), any type of ocular surgery within the past 12 months, systemic diseases that could potentially affect the tear film (e.g. arthritis, thyroid eye disease, diabetes), glaucoma, and smokers. A biomicroscopic evaluation of each participant verified that there were no anomalies affecting the anterior segment of the eye, such as blepharitis, meibomian gland dysfunction, entropion, ectropion or poor lid apposition. Participants were randomized as to the order of the Schirmer test series (e.g. with or without anesthesia), and each series was randomized for gaze position (primary, up or down of 20◦ ). A 30min pause interval was chosen between the Schirmer test series. The temperature and relative humidity of the room was measured using a digital gauge (SportTimer, PTFitnessTM ). Participants were seated comfortably in an ophthalmic chair in a typical examination room at the University of Montreal Optometry Clinic, with fixed windows limiting drafts or air currents. A board was placed 70 cm in front of the participant and a central fixation point was chosen as the primary gaze target (Fig. 1). A laser pointer

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Fig. 2. Schirmer test scores for three different gaze positions, with and without the use of anesthesia. The down-position had significantly higher values than both other positions, p < .02, respectively. Values were generally higher for measurements without anesthesia, p < .001. Error bars indicate one standard error from the mean.

assured that the patient’s outer canthus, the corneal gaze and the fixation point were aligned, to insure primary gaze for each participant. The ophthalmic chair was raised or lowered as a consequence if this was not the case. A pre-set fixation target positioned at 20◦ above and below the primary gaze was calculated on the board and served as visual markers for the participant during the Schirmer test evaluations. The palpebral aperture of each participant was measured using a metric ruler while in primary gaze. One drop of topical proparacaine (ALCAINE .5%, ALCON) was used to anesthetize each eye when the Schirmer test #2 was performed. Although both eyes were anesthetized, only the right eye was used for evaluation. Schirmer diagnostic strips (40 mm × 5 mm, tear graduated ophthalmic sterile strips by AlphaMedTM ) were placed within 2–3 mm from the lateral canthus for each gaze position for 5 min. All the test strips used during the study came from the same box (Lot # TE/SCH/1001). The cul-de-sac was not pre-treated or manipulated in any way prior to testing. Each participant was instructed to blink normally while fixating on the appropriate test target. Following the 5-min test time, the strip was removed and the wetted area was read directly from the graduated scale on the strip. Power analysis indicated that a sample size of n = 20 would be sufficient to detect small to medium effect sizes at an alpha level of .05 with a power of .80 [44]. Statistical analysis was performed using SPSS Version 17.0 for Windows. 3. Results Twenty NDE volunteer participants completed the study (18 F; 2 M, ages 22–37, M = 26.7, SD = 5.1 years, mean OSDI scores ranging from 0 to 29/100, with a mean of 10.5 ± SD 8.9). The average palpebral fissure of the participants varied between 7 and 11.5 mm, with an average of 9.9 mm. The room’s temperature remained stable with an average of 71.1 ± 1.1 ◦ F and a relative humidity of 36.0 ± 6.6%. Repeated-measures analysis of variance (ANOVA) did not reveal an interaction effect of anesthesia state (present/absent) and gaze position (up/primary/down); as anticipated, there was a statistically significant main effect of anesthesia state, whereby Schirmer scores with anesthesia were lower overall than without (11.33 mm ± 7.78 with versus 19.74 mm ± 2.83 without, p < .001), regardless of gaze position, F(1, 19) = 25.2, p < .001, 2 = .57 (Fig. 2). The main effect of gaze position was statistically significant, F(2, 38) = 4.95, p < .02, 2 = .21. Post hoc analysis indicated that inferior gaze resulted in higher values (p < .02) than the other two positions

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Table 2 Results of eyelid position on Schirmer tests #1 and #2. Gaze

Anesthesia

p

Without (Schirmer #1) Superior (S) Primary (1◦ ) Inferior (I) Total

16.73 mm 19.45 mm 23.05 mm 19.74 mm

± ± ± ±

10.8 9.65 10.43 2.83

With (Schirmer #2) 10.25 mm 9.98 mm 13.75 mm 11.33 mm

± ± ± ±

8.33 8.47 9.23 7.78

p < .02 (I > S/1◦ ) p < .001

of gaze that did not differ from each other, regardless of the use of anesthesia (Table 2). No statistically significant correlations were noted between the palpebral aperture, age, OSDI score and the Schirmer test (see Table 3). 4. Discussion This study investigated whether Schirmer scores are influenced by eye position in the presence or absence of anesthesia, in order to bring uniformity to the measurement of tear volume. The results indicated that Schirmer scores with anesthesia were lower than those without, replicating previous reports in the literature [14,16,27,28]. In our study, Schirmer scores were influenced by gaze position, resulting in higher scores in the inferior gaze (of 20◦ ) when compared to either of the two other positions (primary and 20◦ superior). This finding leads us to recommend that gaze position should both be consistent in the clinic and be reported in a systematic fashion in order to allow for direct comparison. The participants were representative of a NDE population, having an average OSDI score (10.5/100) well below the mild range (determined as 13–22) [45] as well as having Schirmer scores greater than 10 mm/5 min [14]. Two participants had entering OSDI scores of 27 and 29, placing them in the mild to moderate DE range. Excluding them from the analysis did not alter the overall outcome, still revealing that the inferior gaze provides higher Schirmer scores than either of the other positions (p = .02, respectively). This study did not test for anxiety or stress related to the insertion of the Schirmer strip, which may contribute to nervousness and excessive tearing. However, randomization of both the eye position and the use of anesthesia were performed to counterbalance such possible effects. Furthermore, all measurements were performed in the same examination room taking precautions to avoid drafts and air currents. All of the measurements were completed within several weeks of each other (in the late fall), avoiding any seasonal differences that may cause large changes based on temperature fluctuations. These results contradict somewhat those reported both by Serin et al. [40] and Serruya et al. [41] which report higher Schirmer scores in the open eye condition that those in the closed eye condition for NDE participants. Serin [40] and Serruya [41], along with their co-authors, propose that extrinsic factors such as tear evaporation, ocular irritation due to eye movements over the paper strip, and other environment irritants can be contributory factors to increase reflex tearing, resulting in higher values in the open eye condition. Consequently they advocate that the closed

eye condition provides a more uniform condition for the test with less variability. Kashkouli et al. [46] found similar results in normal and DE subjects using the standard 5 min test and a modified 1 min version. The closed eye condition revealed shorter Schirmer scores in both the 5 min and 1 min version of the test for both groups. However, none of these three studies provided specifics as to the definition of what constitutes an open eye condition. Although the present study did not have a true “closed” eye condition, the inferior gaze did reveal higher values than those in the more “open” positions. A possible hypothesis for this is that a compression of the tear meniscus occurs upon inferior gaze, resulting in an accumulation of tears in the inferior cul-de-sac, which is clinically translated to an increased Schirmer score. It is possible that under a true closed eye condition, the tear film spreads under the lids to lubricate the ocular surface, and leave less in the inferior cul-de-sac, resulting in reduced wetting of the Schirmer strip. Further studies in our lab are ongoing to corroborate this hypothesis by evaluating the effect of differing angles in the inferior gaze (10–40◦ ) versus a closed eye condition. Other authors have explored open versus closed eye protocols for tear volume evaluation with other tests, such as the phenol red thread test (PRT) [47]. The closed eye condition provided marginally lower scores than the open eye, but was not statistically significantly different. The open eye was described as eye level fixation of a distance eye chart, while closed eye was a gentle closing of the lids. Despite the lack of a clear difference between open and closed eye in the one-time use of the PRT in this study, the authors advocate that clear protocols need to be stated so that comparisons across studies can be made. The average palpebral aperture (9.9 mm) in this study was also representative of an average adult population, with apertures between 7 and 11 mm [48,49]. Ethnic differences in palpebral aperture have been found to affect the tear film parameters, such as tear film stability and tear volume [31,50,51] and may need to be considered in future studies. All subjects in this study were Caucasian. An increase in palpebral fissure, as in patients suffering from Graves disease, increases the evaporation of the tear film due to a greater exposure to external elements such as air currents [52,53]. Consequently, there are less tears on the eye to be absorbed by the Schirmer strip. Systemic diseases, including thyroid disease, were part of the exclusion criteria of this study and as such not a consideration in the interpretation of the results. It is noteworthy that the absence of systemic diseases was self-reported. Despite the unpopularity of the Schirmer test, it remains a valuable diagnostic tool, especially when assessing tear-deficient DE [10]. That being said, the present knowledge base on the methodology of the Schirmer test is confusing and, as a result, studies are difficult to compare. The open versus closed eye dilemma remains unsubstantiated. Consequently, it is advisable that future studies on the Schirmer test include specifics, such as the type of test that was performed (with or without anesthesia), the eye condition that was used (closed or open), the gaze position that was evaluated (head/eye position), the environmental factors (air currents, humidity and temperature), the palpebral aperture (due to ethnic considerations), the brand of Schirmer strip, the population (DE or NDE) and how each of these variables were

Table 3 Correlation coefficients (and p-values) for all dependent measures. Position

Without anesthesia Primary

Up

Down

Primary

Up

Down

Age

OSDI

Palp. Ap.

Age OSDI score Palpebral aperture

−.07 (.77) .38 (.12) .12 (.64)

.33 (.19) .42 (.08) −.06 (.81)

.18 (.48) .21 (.41) .13 (.56)

−.30 (.22) .21 (.41) .29 (.25)

.07 (.79) .20 (.42) −.06 (.80)

−.09 (.73) .15 (.56) .33 (.17)



−.46 (.06) –

−.17 (.51) −.01 (.99) –

With anesthesia

Note: OSDI = ocular surface disease index.

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determined. A standardized protocol would go a long way in increasing the reliability of the Schirmer test. 5. Conclusion The Schirmer tear test remains a valuable diagnostic tool in the assessment of DE subjects. Regardless, reported methodology varies in the literature causing confusion and poor test repeatability. This study investigated the influence of eye position on the Schirmer test score 20◦ above, below, and at primary gaze, whereby the inferior gaze resulted in higher scores than the other two. In order for studies to be comparable in the future, authors should state specifics as to the eye condition (open versus closed), gaze, the use of anesthesia or not, the brand of Schirmer strip used, and details as to inclusion and exclusion criteria for the population studied. Consensus on test methodology and parameters are required in order to improve the interpretability of the Schirmer test. Acknowledgements We thank Marie-Claude Forget and Marie-Pier Landreville, optometry students at the time, for the data collection and the Canadian Optometric Education Trust Fund (COETF) for partial funding of this project. References [1] Schirmer O. Studies on the physiology and pathology of the secretion and drainage of tears. Albrecht von Graefes Arch Klin Ophthalmol 1903;56:197–291. [2] Jones LT. The lacrimal secretory system and its treatment. Am J Ophthalmol 1966;62(July (1)):47–60. [3] Jones LT, Wobig JL. The Wendell L. Hughes Lecture. Newer concepts of tear duct and eyelid anatomy and treatment. Trans Sect Ophthalmol Am Acad Ophthalmol Otolaryngol 1977;83(July–August (4 Pt 1)):603–16. [4] Stein R, Hurwitz J. Anatomy and physiology of tear secretion. In: Hurwitz J, editor. The lacrimal system. Philadelphia: Lippincott-Raven; 1996. p. 1–8. [5] Farris R, Stuchell R, Mandell I. Basal and reflex human tear analysis. I. Physical measurements: osmolarity, basal volumes and reflex flow rate. Ophthalmology 1981;88:852–7. [6] de Roetth A. On the hypofunction of the lacrimal gland. Am J Ophthalmol 1941;24:20–5. [7] Balik J. The lacrimal fluid in keratoconjunctivitis sicca: a quantitative and qualitative investigation. Am J Ophthalmol 1952;35:773–82. [8] De Roetth Sr A. Lacrimation in normal eyes. AMA Arch Ophthalmol 1953;49(February (2)):185–9. [9] Farris R, Gilbard J, Stuchell R, Mandel I. Diagnostic tests in keratoconjunctivitis sicca. CLAO J 1983;9:23–8. [10] Nichols KK, Mitchell GL, Zadnik K. The repeatability of clinical measurements of dry eye. Cornea 2004;23(April (3)):272–85. [11] Sorbara L, Talsky C. Contact lens wear in the dry eye patient: predicting success and achieving it. Can J Optom 1988/1989;89:234–41. [12] Veys J, Meyler J, Davies I. Essential contact lens practice. Part 4. Assessment of the tear film. Optician 2007;233(6104):27–40. [13] Bennett E, Watanabe R, Begley C. Preliminary evaluation. Clinical manual of contact lenses. 3rd ed. Philadelphia: Lippincott Williams & Wilkins; 2009. p. 13–4. [14] Cho P, Yap M. Schirmer test. I. A review. Optom Vis Sci 1993;70(February (2)):152–6. [15] Shapiro A, Merin S. Schirmer test and break-up time of tear film in normal subjects. Am J Ophthalmol 1979;88(October (4)):752–7. [16] Lamberts D, Foster S, Perry H. Schirmer test after topical anesthesia and the tear meniscus height in normal eyes. Arch Ophthalmol 1979;97: 1082–5. [17] Nelson P. A short Schirmer tear test. Optom Mon 1982;October:568–9. [18] Kurihashi K. Diagnostic tests of lacrimal function using cotton thread. In: Holly F, editor. The preocular tear film: in health, disease and contact lens wear. Lubbock: Dry Eye Institute, Inc.; 1986. p. 89–116. [19] Bawazeer A, Hodge W. One minute schirmer test with anesthesia. Cornea 2003;22(4):285–7.

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Please cite this article in press as: Bitton E, Wittich W. Influence of eye position on the Schirmer tear test. Contact Lens Anterior Eye (2013), http://dx.doi.org/10.1016/j.clae.2013.11.011

Influence of eye position on the Schirmer tear test.

The Schirmer test (ST) evaluates the volume of tears in potential dry eye candidates via a strip placed in the lower tear lake. Previously reported in...
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