You are here

  • Home
  • Archive
  • Volume 99, Issue 4
  • Correlations among ocular surface temperature difference value, the tear meniscus height, Schirmer's test and fluorescein tear film break up time

Article Text

Article menu

Download PDFPDF

Clinical science
Correlations among ocular surface temperature difference value, the tear meniscus height, Schirmer's test and fluorescein tear film break up time
  1. Tai Yuan Su1,
  2. Wei Ting Ho2,
  3. Chien Yi Lu1,
  4. Shu Wen Chang2,
  5. Huihua Kenny Chiang1
  1. 1Institute of Biomedical Engineering, National Yang-Ming University, Taipei, Taiwan
  2. 2Department of Ophthalmology, Far Eastern Memorial Hospital, New Taipei City, Taiwan
  1. Correspondence to Professor Huihua Kenny Chiang, Institute of Biomedical Engineering, National Yang-Ming University, No. 155, Sec. 2, Linong Street, Beitou District, Taipei 1121, Taiwan; hkchiang{at}ym.edu.tw

Abstract

Purpose To report the use of a thermographer for measuring ocular surface temperature, and to evaluate the correlation among the obtained temperature difference values (TDVs) and dry eye parameters (tear meniscus height (TMH); Schirmer's test results; fluorescent tear breakup time (FTBUT)).

Methods Forty-three participants (age 40.2±14.7 years; range 21–67 years) from Far Eastern Memorial Hospital, Taiwan were recruited for the study. The surface temperature was measured at the centre of the ocular surface for 4 s after blinking. TDV was defined as the change in corneal surface temperature relative to that of the preceding eye opening, where TDV01, TDV02, TDV03, and TDV04 represent the values obtained 1, 2, 3, and 4 s after blinking, respectively. Anterior segment optical coherence tomography (AS-OCT) was employed to measure the lower TMH. Schirmer's test with topical anaesthetic was conducted to measure the basal tear secretion. The FTBUT was recorded using a digital camera.

Results TDV measurement exhibited high reliability (intraclass correlation coefficient=0.91). TDV03 exhibited the highest significance and strongest positive correlation with the TMH (r=0.52, p=0.0003) and Schirmer's test value (r=0.39, p=0.008), whereas the TDV03–FTBUT correlation was non-significant. Age correlated negatively and significantly with the TDV (r= −0.35, p=0.021), TMH (r= −0.33, p=0.031), and Schirmer's test value (r= −0.31, p=0.044). TDV03 remained significantly correlated with the TMH and Schirmer's test value after adjustment for age.

Conclusions The thermographer was effective in capturing temperature changes in the ocular surface. The temperature difference 3 s after blinking appears to be correlated with lower TMH and Schirmer test values.

  • Tears
  • Imaging
  • Diagnostic tests/Investigation

https://doi.org/10.1136/bjophthalmol-2014-305183

Statistics from Altmetric.com

    Request Permissions

    If you wish to reuse any or all of this article please use the link below which will take you to the Copyright Clearance Center’s RightsLink service. You will be able to get a quick price and instant permission to reuse the content in many different ways.

    Introduction

    Dry eye disease is among the most common eye diseases treated in daily clinics, and it is a disease with a multifactorial pathophysiology.1 ,2 Because dry eye disease is complex, the definition of dry eye disease has been expanded to account for the increased understanding of the disease entity.3 Traditionally, dry eye disease is categorised as either aqueous tear-deficient or evaporative dry eye. The change in the tear film, which may cause decreased production or excessive evaporation, leads to clinical symptoms and affects the quality of vision.

    When diagnosing dry eye, physicians examine the patient's medical history to identify any clinical symptoms and conduct various diagnostic tests, including fluorescein tear breakup time (FTBUT), ocular surface staining, and Schirmer's tests. However, these diagnostic tests have limited sensitivity and specificity, and some are invasive, which can influence the test result and cause discomfort to the patients. Thus, developing a non-invasive diagnostic method is necessary. Anterior segment optical coherence tomography (AS-OCT) is a non-invasive diagnostic tool used for quantitative tear evaluation.4–7 Because the tear meniscus contains 75–90% of the total volume of tears, the tear meniscus height (TMH) is directly correlated with the thickness of the tear film.8 Shen et al9 reported that AS-OCT can be used to non-invasively measure the TMH, and TMH has high sensitivity and specificity in the diagnosis of dry eye resulting from Sjögren's syndrome. However, evaluating the TMH by using AS-OCT can be subjected to interference under certain circumstances, such as when a patient has conjunctivochalasis.10

    Tear evaporation measurement has been used to evaluate Meibomian gland dysfunction.11–15 The tear evaporation rate can be measured on a sequence of thermographic images,14 which detect temperature changes in real time across the entire ocular surface.16–19 Thermography after 10 s of eye opening has also been advocated as a simple, non-invasive screening test for dry eyes.16 ,17 ,19 Temperature difference value (TDV), a parameter derived using thermography, represents the temperature difference relative to the temperature after the last eye opening.16 Previous studies have indicated that the corneal surface temperature decreases faster in patients with normal eyes than in patients with tear deficiencies.12 ,13 ,18 ,19 However, no study has examined the correlation between the change in ocular surface temperature and tear volume.

    In this study, a thermographer was employed to measure the ocular surface temperature to obtain the TDV. Furthermore, we evaluated the relationship between the TDV and other tear volume indicators, including the TMH, Schirmer's test value, and FTBUT.

    Methods

    All procedures in this study were conducted in accordance with the tenets of the World Medical Association Declaration of Helsinki, and approval was received from the Institution Review Board at Far Eastern Memorial Hospital, Taiwan. Informed consent was obtained from each participant after explaining the research purpose and procedures. Forty-three participants (30 women, 13 men) with a mean age of 40.2±14.7 years (range 21–67 years) in good health and with no history of contact lens wear, current ocular diseases, fluorescein allergy, or previously diagnosed dry eye were recruited.

    Extensive anterior segment examination was done to exclude ocular surface abnormalities, previous ocular surface surgery, and superficial punctate keratopathy. None of the participants received eye drop instillations within 6 h before conducting the measurements. All examinations were performed between 10:00 and 15:00 in a room with constant temperature (22±1.8°C) and humidity (70±5.0%). First, the TMH was measured using AS-OCT, followed by thermographic imaging. The FTBUT was recorded using a slit-lamp-adapted digital recording system, and finally, the Schirmer's test with topical anaesthetics was conducted to determine basal tear secretion. A 10-min break was allowed between each procedure to minimise the carry-over effect.

    Tear meniscus height

    The left eye of each participant was scanned by conducting AS-OCT using the cornea–anterior module in the RTVue V.4.0.7.5 (OptoVue, Fremont, California, USA). The participants looked directly ahead, and the lower tear meniscus was captured in a vertical scan that was centred on the inferior cornea and lower eyelid immediately following an entire blinking motion. The tear meniscus was defined as the triangular wedge of tear film between the lower lid margin and cornea, and the TMH was evaluated using a digital calliper (figure 1). Each eye was measured three times, with three measurements obtained each time. The means of the measurements were calculated for further analysis.

    Figure 1
    Figure 1

    Tear meniscus height (TMH) measurements. (A) A scan was performed using anterior segment optical coherence tomography immediately after a full blink. Three TMH values were measured at the centre of lower eyelid (LL) (b), and 1 mm on the right (c) and left sides (a). (B) Cornea (CO), LL, and TMH (282 µm).

    Thermography measurement procedure

    For ocular surface thermography, we used an IT-85 ocular surface thermograph (United Integrated Services Co, Taiwan) to capture the image non-invasively (figure 2). The measurements were performed as follows: (1) the participants blinked normally; (2) the eye was closed for 9 s; (3) the participants blinked normally again; (4) the participants held their eyes open for 4 s. An audio recording was used to deliver prerecorded instructions to the participants. The images were captured at a rate of 30 films/s for 13 s. The eye measurements were conducted four times.

    Figure 2
    Figure 2

    The ocular surface thermograph. Thermography captures the ocular surface thermographic image in a non-invasive manner.

    Region of interest selection

    After recording the thermogram, the temperature was measured at the region of interest (ROI). The ROI was selected by viewing a thermal image and marking four bars for the outer canthus (P1), inner canthus (P3), upper eye led (P2), and lower eye led (P4). The bars were marked without considering any visual obstruction caused by the eyelashes (figure 3). Subsequently, the ROI was defined as a 5 mm circle, the vertical position of ROI was defined by the centre between P2 and P4, and the horizontal position was defined by the centre between P1 and P3 (area=20 mm2, 1000 pixels). The ROI temperature was calculated as the mean of all pixels in the ROI.

    Figure 3
    Figure 3

    Region of interest (ROI) selection. The selection method assisted in avoiding any visual obstruction resulting from the eyelashes. Four bars were marked at outer canthus (P1), inner canthus (P3), upper eye led (P2), and lower eye led (P4). The ROI was positioned on the middle of P1 and P3 in horizontal direction and on the middle of P2 and P4 in vertical direction.

    ROI tracking

    After obtaining the thermogram, we developed the ROI tracking algorithm to adjust the position of the ROI in each image. The algorithm is a standard approach for feature detection.20 The inner canthus was selected as the template at the start of the test. The thermogram images recorded over the following 4 s were compared with the template to obtain the best-matched position. Although the eye position shifted, the algorithm ensured that the ROI was adjusted accordingly (figure 4).

    Figure 4
    Figure 4

    Region of interest (ROI) tracking method. (A) Initial thermogram with the selected template and an ROI. The relative position of the template and the ROI was fixed. (B) Shifted thermogram at the third second. The template-matching method was used to detect the inner canthus of the image, and adjust the ROI accordingly. The arrow (y) indicates the magnitude of displacement.

    Temperature difference value

    After selecting and tracking the ROI, the mean temperature was calculated for each thermogram to indicate the temperature at the ROI. Figure 5 shows the change in temperature during the measurement, which is detailed as follows: (1) the eye was closed until the participant opened their eye (ie, the period marked (a)); (2) as the participant opened their eye, the temperature increased (ie, the point marked (b)); (3) the participant blinked (ie, the period marked (c)); and (4) the participant kept their eyes open for 4 s (ie, the period marked (d)). The TDV was defined as the difference in the temperature relative to the temperature after the participant opened their eye (ie, the point marked (e)). Four TDV values were calculated to represent the temperature difference at 1 (TVD01), 2 (TDV02), 3 (TDV03), and 4 (TDV04) seconds after the participant opened their eye, and the changes were subsequently analysed.

    Figure 5
    Figure 5

    Change in mean temperature at the region of interest (ROI) versus time, where (A) represents the change in the temperature while the eye was initially closed, (B) represents where the eye was first fully opened, (C) represents the period in which the participant blinked, (D) represents the following 4 s during which the eye was opened, and (E) represents the temperature difference values (TDVs).

    Schirmer's test

    The Schirmer's test with anaesthesia (Jones test) was performed as follows. First, one drop of a 0.5% proparacaine hydrochloride ophthalmic solution (Alcaine, Alcon Laboratories, Inc, Belgium) was applied twice at 5-min intervals. After adequate ocular surface anaesthesia, filter paper strips (5 mm×35 mm Whatman no. 41 filter paper) were placed at the outer lower conjunctival fornix for 5 min with the eye closed. Subsequently, the paper strips were removed, and the wetting of the paper was measured.

    Fluorescent tear film break up time test

    A 2 μL volume preservative-free solution consisting of 2% fluorescent dye was applied onto the bulbar conjunctiva using a micropipette. Then a slit lamp was used to record the fluorescent break up image, and the time taken for the first dark spot to appear was recorded. Each eye was measured four times. The means of the measurements were calculated for further analysis.

    Statistical analysis

    Data analysis was performed using SPSS V.20 (IBM, Chicago, Illinois, USA). Data were presented as mean±SD. Pearson's correlation coefficient was calculated to test the correlations among the TDV, TMH, Schirmer's test result, and FTBUT. The correlations between the TDV and the TMH or Schirmer's test results were adjusted for age in the linear regression analysis, and the level of statistical significance was set at p<0.05. The reliability of the TDV03 measurements was determined by calculating the intraclass correlation coefficients (ICCs), and measurements were considered reliable where ICC >0.7.

    Results

    The mean TMH, basal secretion Schirmer's test value, and FTBUT were 218.6±94.8 µm (range 55–516 µm), 7.0±5.1 mm (range 2–28 mm) after 5 min, and 3.8±3.3 s (range 1–15 s), respectively. Regarding the thermography examination, the mean eye movement along the vertical plane was 0.32±0.35 mm (maximum 1.9 mm), and along the horizontal plane it was 0.25±0.38 mm (maximum 2 mm). Following the ROI selection and ROI tracking, the image deviation was adjusted accordingly. The ICC among the four TDV measurements for all participants was 0.91 (95% CI 0.84 to 0.94).

    Figure 6 shows the TDVs. The TDVs increased constantly from TDV01 to TDV04. The increase from TDV02 to TDV03 was statistically significant, which represents an abrupt decrease in ocular surface temperature in this interval.

    Figure 6
    Figure 6

    Temperature difference values (TDVs) at 1–4 s after the final eye opening (TDV01–04). A significant increase was observed between TDV02 and TDV03.

    Table 1 shows the Pearson's correlation coefficient for the correlations between the four TDVs and the TMH, Schirmer's test values, FTBUT, and age. TDV01–TDV03 exhibited a positive correlation with TMH, and the highest level of significance was observed between TDV03 and TMH. Although a positive correlation was observed between TDV04 and TMH, the relationship was non-significant (p=0.1). TDV03 exhibited the most positive and significant correlation with the Schirmer's test value. However, the correlations were non-significant between all TDVs and the FTBUT. All TDVs were negatively correlated with age, and were statistically significant at TDV02 and TDV03.

    View this table:
    Table 1

    Correlations between the TDVs and TMH, Schirmer's test value, FTBUT, and age

    Figure 7 shows the correlation map for TDV03, the TMH, Schirmer's test value, and age. All parameters correlated negatively with age. TDV03 positively and significantly correlated with the TMH and Schirmer's test value, and the correlation remained statistically significant after adjusting for age in the linear regression model. However, the correlation between the TMH and Schirmer's test value was non-significant.

    Figure 7
    Figure 7

    Correlation map for TDV03, the TMH, Schirmer's test value, and age. The solid lines represent a significant correlation, and the dashed line represents a non-significant correlation. r=Pearson's correlation coefficient; p=level of significance. TDV, temperature difference value; TMH, tear meniscus height.

    Discussion

    In this study, we demonstrated that an ocular surface thermographer can be used to monitor changes in ocular temperature. The thermography measurement procedure was fast and noncontact. No reflex tearing was reported, and the procedure did not cause any discomfort to the participants. We also developed an algorithm for ROI tracking and selection, which enabled us to monitor the temperature changes continually in a selected area to obtain the TDVs. Our results show that the TDV measurements exhibited high ICCs, and TDV03 correlated significantly with the TMH and Schirmer's test value. TDVs are the change in ocular temperature, and temperature change results from tear film evaporation; thus, TDVs may relate to the change in tear volume and the evaporation of the tear film.

    Several features of the ocular surface thermographer system were arranged to achieve reliable and consistent TDV measurement results. First, the ROI selection method was used to identify the centre of the ocular surface; the 5 mm ROI diameter identified the centre of the ocular surface area without interference from the eyelashes, and without causing reflex tearing while the eye was open. This approach can be applied to increase the repeatability of the measurement. Second, an ROI tracking method was adopted to minimise the eye movement effect. The degree of movement was up to 1.9 mm during the measurements, which was relatively large compared to the size of the ROI. To improve the measurement accuracy, we developed a tracking method to reduce the effect of eye movement during the measurements. The ROI tracking algorithm assisted in obtaining accurate measurements. Third, we employed a standardised protocol to instruct the participants on when to blink and open their eyes. Previous studies have shown that blinking can interfere with the ocular surface temperature measurement, because higher blinking rates in patients with dry eye can resulted in an increase in ocular surface temperature.21 In our study, an audio speaker was used to broadcast a sequence of instructions for the participants, and the participants followed the instructions (ie, close your eyes for 9 s, open your eyes, blink once immediately, and then keep your eyes open for 4 s). This protocol potentially reduced any confounding effects caused by patients aberrantly blinking and opening their eyes; also keeping eyes open for relatively shorter time can reduce the reflex tearing. Employing these standardised measurement procedures for thermography systems improves the consistency of results. In this study, the ICC was 0.91, indicating that the measured TDVs were highly reliable.

    In this study, we examined the relationships among TDVs, the TMH, Schirmer's values, and age. TDV03 exhibited the most significant and positive correlation with the TMH and Schirmer's test (figure 7). Both TMH and Schirmer tests are used for tear evaluation in dry eye patients.4–7 However, these examinations are subject to certain limitations. For example, conjunctivochalasis can occupy the tear pool, which can change the TMH. An excessively large conjunctival fold may interfere with the measurement of the TMH using AS-OCT. TDVs are measurements of temperature change at the ocular surface, and provide real-time information. Furthermore, we selected an ROI at the centre of the ocular surface, thereby reducing the interference from the eyelashes or conjunctival fold. Because TDV03 correlated positively with both the TMH and Schirmer's test value (table 1), TDV03 can be a reliable parameter for tear film evaluation. Moreover, because tear volume can represent the extent of dry eye disease.4–6 ,22 ,23 the significant correlation between TDV03 and the TMH and Schirmer's test result implies that TDV03 is suitable for evaluating tear volume in future studies.

    There are some limitations in the present study. The TDV and TMH were measured at different times. The two measurements were performed sequentially with a 10-min break to minimise the carry-over effect. However, the tear film condition could have changed between the two measurements. If the TDV03 and TMH were measured simultaneously, the correlation between them could be strengthened. However, because TDV03 and the TMH were both non-invasive measurement results, the adverse confounding effects may have been minimised. In the normal participants the FTBUT, Schirmer and TMH were within a small range, therefore the relation between these tests and temperature differences were not found. In the present study, a group of participants with a broad age range was tested and the results of the FTBUT, TMH, and Schirmer test were found to range widely. Further studies with large sample sizes including subgroups such as dry eye are warranted.

    In our study, all parameters correlated negatively and significantly with age. Previous studies have shown that the TMH and Schirmer's test values decrease as patients increase in age.24 ,25 Because TDV03 correlated with age (r= −0.35, p=0.021), verifying the correlation between TDV03 and other parameters after adjustment for age is crucial. The linear regression model results confirmed that TDV03 remained positively and significantly correlated with both the TMH and Schirmer's test value.

    Although both the FTBUT and Schirmer's test have been used frequently for diagnosing dry eye related diseases, their application remains limited by their invasive nature and unavoidable variability. They are also limited by low sensitivity and specificity, because the results are easily confounded by external factors. For example, the inadequate instillation of topical analgesics may not eliminate reflex tearing in Schirmer's test. Consequently, discrimination between basal and reflex tear secretion is more difficult. In this study, we also observed a poor correlation between the TMH and Schirmer's test results (figure 7). The contact required in Schirmer's test increases the invasiveness of the test and compounds the discomfort experienced by patients. By contrast, the thermography approach is advantageous because it is non-contact and the results are consistent. This is indicated by the high ICC of 0.91.

    Recently, other non-invasive methods have also been applied for detecting dry eye disease. For example, the Hartmann-Shack wavefront sensor is used to measure dynamic wavefront aberrations, and greater instability has been demonstrated in dry eye patients.26 Likewise, corneal topography projects Placido rings onto the cornea, and changes in the projected rings are correlated with tear film break-up.27 However, these methods only measure the optical change on the corneal surface. In contrast, thermography can detect the temperature change on the whole ocular surface as well as on the eyelids. Because dry eye disease often affects several components of the ocular surface system simultaneously, thermography may provide a more comprehensive evaluation.

    In conclusion, the thermographer was effective in capturing temperature changes in ocular surface. The temperature differences 3 s after blinking correlated with lower TMH and Schirmer's test values, but did not correlate with FTBUT. We expect that the tear volume estimated using thermography and the TDV indicators presented in this report will become an established method for evaluating tear film quality.

    Acknowledgments

    The authors thank the staff at Far Eastern Memorial Hospital and National Yang Ming University, as well as the research participants. The authors thank to Yu-Han, Ou for her assistance, and also thank Dr S Daraszewicz for his support and advice.

    References

    1. ↵
      1. Goto E,
      2. Yagi Y,
      3. Matsumoto Y, et al
      . Impaired functional visual acuity of dry eye patients. Am J Ophthalmol 2002;133:181–6.
      OpenUrlCrossRefPubMedWeb of Science
    2. ↵
      1. Miljanović B,
      2. Dana R,
      3. Sullivan DA, et al
      . Impact of dry eye syndrome on vision-related quality of life. Am J Ophthalmol 2007;143:409–15.e2
      OpenUrlCrossRefPubMedWeb of Science
    3. ↵
      1. Lemp MA
      . The definition and classification of dry eye disease: report of the Definition and Classification Subcommittee of the International Dry Eye WorkShop (2007). Ocul Surf 2007;5:75–92.
      OpenUrlCrossRefPubMedWeb of Science
    4. ↵
      1. Fukuda R,
      2. Usui T,
      3. Miyai T, et al
      . Tear meniscus evaluation by anterior segment swept-source optical coherence tomography. Am J Ophthalmol 2013;155:620–4, 24.e1–2.
      OpenUrlCrossRefPubMed
    5. ↵
      1. Tung CI,
      2. Perin AF,
      3. Gumus K, et al
      . Tear meniscus dimensions in tear dysfunction and their correlation with clinical parameters. Am J Ophthalmol 2014;157:301–10.e1.
      OpenUrlCrossRefPubMed
    6. ↵
      1. Qiu X,
      2. Gong L,
      3. Lu Y, et al
      . The diagnostic significance of Fourier-domain optical coherence tomography in Sjogren syndrome, aqueous tear deficiency and lipid tear deficiency patients. Acta ophthalmol 2012;90:e359–66.
      OpenUrlCrossRefPubMed
    7. ↵
      1. Ibrahim OM,
      2. Dogru M,
      3. Takano Y, et al
      . Application of Visante optical coherence tomography tear meniscus height measurement in the diagnosis of dry eye disease. Ophthalmol 2010;117:1923–9.
      OpenUrlCrossRef
    8. ↵
      1. Hosaka E,
      2. Kawamorita T,
      3. Ogasawara Y, et al
      . Interferometry in the evaluation of precorneal tear film thickness in dry eye. Am J Ophthalmol 2011;151:18–23.e1.
      OpenUrlCrossRefPubMed
    9. ↵
      1. Shen M,
      2. Li J,
      3. Wang J, et al
      . Upper and lower tear menisci in the diagnosis of dry eye. Invest Ophthalmol Vis Sci 2009;50:2722–6.
      OpenUrlAbstract/FREE Full Text
    10. ↵
      1. Gumus K,
      2. Crockett CH,
      3. Pflugfelder SC
      . Anterior segment optical coherence tomography: a diagnostic instrument for conjunctivochalasis. Am J Ophthalmol 2010;150:798–806.e2.
      OpenUrlCrossRefPubMed
    11. ↵
      1. Goto E,
      2. Endo K,
      3. Suzuki A, et al
      . Tear evaporation dynamics in normal subjects and subjects with obstructive Meibomian gland dysfunction. Invest Ophthalmol Vis Sci 2003;44:533–9.
      OpenUrlAbstract/FREE Full Text
    12. ↵
      1. Tsubota K,
      2. Yamada M
      . Tear evaporation from the ocular surface. Invest Ophthalmol Vis Sci 1992;33:2942–50.
      OpenUrlAbstract/FREE Full Text
    13. ↵
      1. Rolando M,
      2. Refojo MF
      . Tear evaporimeter for measuring water evaporation rate from the tear film under controlled conditions in humans. Exp Eye Res 1983;36:25–33.
      OpenUrlCrossRefPubMedWeb of Science
    14. ↵
      1. Tan J-H,
      2. Ng E,
      3. Acharya UR
      . Evaluation of tear evaporation from ocular surface by functional infrared thermography. Med Phys 2010;37:6022–34.
      OpenUrlCrossRefPubMedWeb of Science
    15. ↵
      1. Arciniega JC,
      2. Wojtowicz JC,
      3. Mohamed EM, et al
      . Changes in the evaporation rate of tear film after digital expression of Meibomian glands in patients with and without dry eye. Cornea 2011;30:843–7.
      OpenUrlCrossRefPubMedWeb of Science
    16. ↵
      1. Su TY,
      2. Hwa CK,
      3. Liu PH, et al
      . Noncontact detection of dry eye using a custom designed infrared thermal image system. J Biomed Opt 2011;16:046009.
      OpenUrlCrossRefPubMed
    17. ↵
      1. Kamao T,
      2. Yamaguchi M,
      3. Kawasaki S, et al
      . Screening for dry eye with newly developed ocular surface thermographer. Am J Ophthalmol 2011;151:782–91.e1.
      OpenUrlCrossRefPubMed
    18. ↵
      1. Tan JH,
      2. Ng E,
      3. Acharya UR
      . Evaluation of tear evaporation from ocular surface by functional infrared thermography. Med Phys 2010;37:6022.
      OpenUrlCrossRefPubMedWeb of Science
    19. ↵
      1. Mori A,
      2. Oguchi Y,
      3. Okusawa Y, et al
      . Use of high-speed, high-resolution thermography to evaluate the tear film layer. Am J Ophthalmol 1997;124:729–35.
      OpenUrlCrossRefPubMedWeb of Science
    20. ↵
      1. Burger W,
      2. Burge MJ
      . Digital image processing. Springer, 2008.
    21. ↵
      1. Nakamori K,
      2. Odawara M,
      3. Nakajima T, et al
      . Blinking is controlled primarily by ocular surface conditions. Am J Ophthalmol 1997;124:24–30.
      OpenUrlCrossRefPubMedWeb of Science
    22. ↵
      1. Mainstone JC,
      2. Bruce AS,
      3. Golding TR
      . Tear meniscus measurement in the diagnosis of dry eye. Curr Eye Res 1996;15:653–61.
      OpenUrlCrossRefPubMedWeb of Science
    23. ↵
      1. Li J,
      2. Shen M,
      3. Wang J, et al
      . Clinical significance of tear menisci in dry eye. Eye Contact Lens 2012;38:183–87.
      OpenUrlCrossRefPubMed
    24. ↵
      1. Mathers WD,
      2. Lane JA,
      3. Zimmerman MB
      . Tear film changes associated with normal aging. Cornea 1996;15:229–34.
      OpenUrlCrossRefPubMedWeb of Science
    25. ↵
      1. Wright J,
      2. Meger G
      . A review of the Schirmer test for tear production. Arch ophthalmol 1962;67:564.
      OpenUrlCrossRefPubMedWeb of Science
    26. ↵
      1. Wang Y,
      2. Xu J,
      3. Sun X, et al
      . Dynamic wavefront aberrations and visual acuity in normal and dry eyes. Clin Exp Optom 2009;92:267–73.
      OpenUrlCrossRefPubMedWeb of Science
    27. ↵
      1. Hong J,
      2. Sun X,
      3. Wei A, et al
      . Assessment of tear film stability in dry eye with a newly developed keratograph. Cornea 2013;32:716–21.
      OpenUrlCrossRefPubMed

    Footnotes

    • HKC and SWC contributed equally.

    • Contributors TYS and SWC designed the experiment. TYS, WTH and CYL conducted the experiment. TYS, CYL and SWC analysed/interpreted the data. TYS, WTH and SWC wrote the article. HKC and SWC proofed/revised the article.

    • Funding National Science Council, Taiwan (101-2622-E-010-001-CC2) funded this study.

    • Competing interests None.

    • Patient consent Obtained.

    • Ethics approval Institution Review Board at Far Eastern Memorial Hospital, Taiwan.

    • Provenance and peer review Not commissioned; externally peer reviewed.

    Linked Articles

    • At a glance
      Highlights from this issue
      Keith Barton James Chodosh Jost Jonas
      British Journal of Ophthalmology 2015; 99 i-i Published Online First: 23 Mar 2015. doi: 10.1136/bjophthalmol-2015-306887