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(Investigative Ophthalmology and Visual Science. 2005;46:1593-1598.)
© 2005 by The Association for Research in Vision and Ophthalmology, Inc.
DOI:  10.1167/iovs.04-0864
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Association between Symptoms and Signs of Dry Eye among an Elderly Chinese Population in Taiwan: The Shihpai Eye Study

Pei-Yu Lin,1 Ching-Yu Cheng,1,2,3 Wen-Ming Hsu,1 Su-Ying Tsai,4 Ming-Wei Lin,5,6 Jorn-Hon Liu,1,7 and Pesus Chou4

1From the Department of Ophthalmology, National Yang Ming University School of Medicine and Taipei Veterans General Hospital, Taipei, Taiwan; 2Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland; the 3Institute of Clinical Medicine, the 4Community Medicine Research Center and Institute of Public Health, and the 5Faculty of Medicine, National Yang Ming University, Taipei, Taiwan; the 6Department of Medical Research and Education, Taipei Veterans General Hospital, Taipei, Taiwan; and the 7Cheng Hsin Rehabilitation Medical Center, Taipei, Taiwan.


   Abstract
Top
 Abstract
Materials and Methods
 Results
 Discussion
 Appendix 1
 References
 
PURPOSE. To analyze the association between dry-eye symptoms and signs in an elderly Chinese population in Taipei, Taiwan.

METHODS. The participants were those of the Shihpai Eye Study, a population-based survey of eye diseases in the elderly (≥65 years) in Shihpai, Taipei, Taiwan. Of 2045 randomly selected noninstitutionalized residents, 1361 (66.6%) participated in the study. Dry-eye symptoms were evaluated with an interviewer-administered questionnaire. Dry-eye signs, including tear-film breakup time, Schirmer test result, score for fluorescein staining of the cornea, and meibomian gland dysfunction, were assessed. Correlations between symptoms and signs were analyzed.

RESULTS. Of the participants, 33.7% (459/1361) were symptomatic, defined as reporting one or more symptoms often or all the time. A Schirmer result of ≤5 mm was the only sign associated with frequent symptoms (P = 0.028). Its sensitivity and specificity in detecting symptomatic subjects were 62.5% and 43.7%, respectively. The agreement between each sign was statistically significant, although weak, except that no correlation was found between the Schirmer result and meibomian gland anomalies. Of the symptomatic subjects, 85.4% (392/459) had either a low Schirmer result or a meibomian gland anomaly; 38.8% (178/459) of them were abnormal on both tests.

CONCLUSIONS. The Schirmer test was shown to be incapable of detecting meibomian gland disease. However, a low Schirmer result was significantly associated with dry-eye symptoms in this elderly Chinese population. This result differs from that of previous reports of elderly white populations. Further studies are needed to determine whether this difference indicates racial diversity in the distribution and behavior of dry-eye diseases.

Studies of the epidemiology of dry eye are often hindered by the fact that there is no gold standard for the diagnosis of dry eye. Some recent population-based studies defined dry eye as having frequent dry-eye symptoms,1 2 3 4 5 which is reasonable because the treatment goal for dry eye is primarily to relieve the patient’s symptoms. In clinical practice, dry-eye tests are often performed in symptomatic patients to confirm the diagnosis. However, a poor correlation between dry-eye symptoms and dry-eye tests has been demonstrated in population-based studies by Schein et al.1 in the United States and McCarty et al.6 in Australia. The heterogeneity of dry eye and the reporting bias of the participants are potential explanations suggested by the authors.1 7 Each dry-eye test that is frequently performed in clinical practice seeks only to measure a specific disorder of dry eye. Consequently, a patient with normal Schirmer test results, which reflects normal aqueous tear secretion, may report dry-eye symptoms resulting from meibomian gland disease. If the dry-eye symptoms could also be categorized into subtypes (i.e., symptoms of aqueous tear deficiency, symptoms of meibomian gland diseases, and symptoms of mucin anomalies), then more logical analyses of the correlations between symptoms and signs could be made.

Another explanation of the poor association between dry-eye symptoms and signs is that the frequently used dry-eye tests do not reliably reflect the tear-film conditions in the non–clinic-based general population and consequently have limited value as screening tests.

To clarify the correlation between dry-eye symptoms and signs, analyses were performed on data gathered from the Shihpai Eye Study, a population-based survey of subjects ≥65 years of age in Shihpai, Taipei, Taiwan.


   Materials and Methods
Top
 Abstract
 Materials and Methods
Results
 Discussion
 Appendix 1
 References
 
Subjects
The methods used in the Shihpai Eye Study have been described previously.4 8 To summarize briefly, this study was conducted between July 1, 1999, and December 31, 2000. The goal was to recruit a random sample of residents of Shihpai, Taipei, Taiwan, aged at least 65 years, for participation in several distinct studies related to ocular disease and aging. In 1999, the Shihpai community, located in the Peitou district of Taipei, had 4750 residents aged at least 65 years, according to the official household registration database. Our goal was to recruit a random sample of approximately 2000 residents 65 years of age or older with complete baseline information. The sample size was chosen based on the estimates of the prevalence of visual impairment. Excluding vacant households (n = 658), residents who died before they were interviewed (n = 48), and inpatient, paralyzed, and disabled residents (n = 298), 3764 residents were eligible. Of these 3764 subjects, 2045 were randomly selected to be enrolled in the Shihpai Eye Study.

Questionnaire and Examinations
The study protocol was approved by the institutional review board, and the study was conducted according to the tenets of the Declaration of Helsinki of the World Medical Association regarding scientific research on human subjects.

Trained interviewers contacted the potential participants and administered a structured questionnaire that included questions addressing demographic data, health and drug history, psychological condition, personal habits, lifestyle, and dry-eye symptoms. The questions regarding dry-eye symptoms consisted of eight items4 (see Appendix). Six of the items were the same as those used by Schein et al.1 Two more symptoms (sticky and tearing) were added because they are included in the questionnaires of other dry-eye studies.6 9 When a respondent indicated the presence of a symptom, he or she was asked to indicate whether the symptom was experienced rarely, sometimes, often, or all the time. The subjects were then invited to the Taipei Veterans General Hospital for detailed eye examinations.

The dry-eye tests included the tear-film breakup time test, fluorescein staining of the cornea, slit-lamp assessment of the meibomian gland, and the Schirmer test. The tear-film breakup time test was performed before the other dry-eye tests to avoid any untoward interference. The test was repeated three times for each eye, and the average time was recorded. Fluorescein staining of the cornea was observed through a slit lamp with a cobalt-blue filter and was graded 0 (no staining), 1 (mild staining with a few disseminated stains, and limited to less than one third of the cornea), 2 (moderate staining with a severity between grades 1 and 3), or 3 (severe staining with confluent stains, and occupying half or more of the cornea).6 The condition of the meibomian gland was determined by observing the lid margin with a slit lamp. Because there is no universal grading system of meibomian gland dysfunction (meibomian gland disease), we defined meibomian gland disease as the presence of meibomian gland orifice plugging or lid margin telangiectasia. The presence of lid margin telangiectasia was recorded, and any meibomian gland obstruction was graded (we defined grade 0 as no obstruction; grade 1, plugged with translucent serous secretion when the lid margin was compressed; grade 2, plugged with viscous or waxy white secretion when the lid margin was compressed; and grade 3, plugged with no secretion when the lid margin was compressed). The Schirmer test was performed last, so that ocular irritation by the test strip would not interfere with other examination results. One minute after instillation of a drop of 0.5% proparacaine, any visible fluid in the inferior fornix or lid margin was gently dried with a cotton swab. A precalibrated filter strip (Color Bar; Eagle Vision, Inc., Memphis, TN) was then placed temporally in each lower fornix and left in place for 5 minutes. The patient was allowed to either blink normally or to close his or her eyes. After 5 minutes, the strip was removed, and the amount of wetting (in millimeters) was recorded from the precalibrated strip. We did not perform rose bengal staining, because rose bengal is toxic to epithelial cells and irritating to the eye. We were reluctant to add more discomfort and waiting time to these elderly study participants.

Diagnosis and Statistical Analysis
Dry eye was defined as having one or more symptoms often or all the time. Positive signs were if one or both eyes revealed tear-film breakup time of ≤10 seconds,10 a Schirmer test score of ≤5 mm,11 a fluorescein score ≥1,11 or the existence of meibomian gland disease which was diagnosed when telangiectasia at the lid margin or plugging of the gland orifices was present (≥ grade 1).

Statistical analysis was performed to describe the distribution of symptoms and signs, to assess the correlations between variable clinical signs of dry eye, and to explore the association between dry eye symptoms and variable clinical signs. The normality of the data was checked with the Shapiro-Wilk test. A K-means cluster analysis was used to explore symptom reporting patterns and to understand better symptomatic heterogeneity in the study population. The technique is a classification technique that is particularly useful in identifying characteristics of homogeneous subgroups. In other words, subjects with similar dry eye symptoms were put in the same group. All data analyses were performed with a commercial statistical software package (Stata; Stata Corp., College Station, TX).


   Results
Top
 Abstract
 Materials and Methods
 Results
Discussion
 Appendix 1
 References
 
Of the 2045 subjects randomly recruited, 2038 (99.7%) cooperated with the household interview and completed the questionnaire. Seven (0.3%) subjects could not be contacted after three attempts and were not interviewed. After finishing the questionnaire, 1361 (66.6%) subjects came to the hospital and completed the eye examinations. The analyses of this study are based on data gathered from these 1361 participants. The comparison between the participants and nonparticipants has been described previously.8 In general, participants (mean age, 72.2 ± 5.1 years; range, 65–91) were younger than nonparticipants (74.3 ± 6.0 years), more likely to be male (60.4%), and had a higher level of education and a higher frequency of current smoking and alcohol drinking (all P < 0.05).

Table 1 summarizes the results of the questionnaire on dry-eye symptoms by sex and age. The questionnaire data show that 33.7% of the population reported one or more symptoms to be present often or all the time. Table 2 summarizes the result of the dry-eye tests in the worse eye only, by sex and age. The overall mean tear breakup time was 8.2 seconds. The overall mean Schirmer test result was 5.7 mm. The corneas of 33.4% of the participants were positively stained with fluorescein, 53.6% of participants had signs of meibomian gland obstruction, and 70% had lid margin telangiectasia.


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  		TABLE 1. Subjects Reporting Dry Eye Symptoms

 

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  		TABLE 2. Clinical Signs of Dry Eye

 
The associations between dry-eye symptoms and various dry-eye tests are shown in Table 3 . The Schirmer test was the only test to show a significant association with dry-eye symptoms, regardless of whether they were analyzed with all eight questions in the questionnaire or with only the six questions used by Schein et al.1 Figure 1 illustrates the frequencies of the Schirmer test results for the lower-scoring eye of each participant. Of all study subjects, 58.4% had a Schirmer result of ≤5 mm. With a cutoff value of 5 mm, the Schirmer test demonstrated 62.5% sensitivity and 43.7% specificity in detecting symptomatic subjects. The association between the Schirmer result and dry-eye symptoms became nonsignificant when the eight items in the questionnaire were analyzed individually. The same lack of association was identified between other dry-eye tests and individual items in the questionnaire, except that a significantly positive association was found between the question, "Are your eyes ever red?" and the presence of meibomian gland anomalies (plugging, P = 0.024; lid margin telangiectasia, P = 0.015).


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  		TABLE 3. Associations between Symptoms with Various Clinical Signs of Dry Eye

 


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  		FIGURE 1. Frequency of Schirmer test results for the lower-scoring eyes of the participants.

 
Categorizing various dry-eye symptoms to specific dry-eye disorders was attempted initially by grouping the subjects according to similar responses to the questionnaire, using K-means cluster analysis (Table 4) . The subjects could be grouped into 4 groups: group 1, more likely to report dry (192/1361 = 14.1%); group 2, more likely to report sticky and watery (234/1361 = 17.2%); group 3, more likely to notice crusting (33/1361 = 2.4%); and group 4, no dry eye symptoms. We then analyzed whether the subjects in any one group presented with specific dry-eye signs. However, no statistically significant result was obtained.


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  		TABLE 4. Cluster Analysis of Dry Eye Symptoms

 
The agreement between the various dry-eye test results is shown in Tables 5 and 6 . The correlations between tear breakup time, Schirmer result, and fluorescein staining score are statistically significant, although weak. The associations between meibomian gland disease and other signs are also significant, except with the Schirmer result. The results for the right eye were consistent with those for the left eye.


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  		TABLE 5. Correlation between Various Dry Eye Signs*

 

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  		TABLE 6. Correlation between Meibomian Gland Disease and Other Dry Eye Signs

 
Figure 2 illustrates the distribution of subjects with low Schirmer results, meibomian gland disease (MGD), and frequent symptoms. Most subjects (85.4%, 392/459) with frequent dry-eye symptoms had either a low Schirmer result or a meibomian gland anomaly (MGD), whereas 38.8% (178/459) of them had abnormal findings on both tests. When the other two signs (tear breakup time of ≤10 seconds and corneal fluorescein staining score ≥1) were included, 96.1% (441/459) of symptomatic individuals had at least one positive sign.



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  		FIGURE 2. Agreement between dry-eye symptoms, a low Schirmer result, and meibomian gland disease (n = 1361). MGD, meibomian gland disease.

 

   Discussion
Top
 Abstract
 Materials and Methods
 Results
 Discussion
Appendix 1
 References
 
This study shows that the Schirmer test result, with a cutoff value of 5 mm, correlates significantly with dry-eye symptoms (P = 0.028 for eight questions; P = 0.012 for six questions). This finding differs from that reported by Schein et al.,1 who observed no association between the presence of more frequent symptoms and a lower Schirmer result, regardless of whether the analysis was based on mean scores with a cutoff value of 5 or a cutoff value of 7. Although the Schirmer test was the only single test to be associated with frequent dry-eye symptoms in this population, we do not suggest that it could be used as the best screening tool for dry eye. Its sensitivity and specificity in detecting symptomatic subjects were low. One of the major reasons for the low sensitivity and specificity is the heterogeneity of dry-eye syndrome. The Schirmer result has been shown to be higher in patients with ocular irritation due to meibomian gland disease than in those due to aqueous tear deficiency.12 Subjects with a normal Schirmer result might report dry-eye symptoms due to meibomian gland disease. Statistically significant correlations were demonstrated in this population between different dry-eye signs, except between the Schirmer result and meibomian gland anomaly. This finding provides more objective evidence to support the increasingly recognized classification of dry eye that includes deficient aqueous production and excessive evaporation.13

In our previous report,4 we have emphasized that 96% of the individuals who had dry-eye symptoms also had at least one positive sign, which indicated the importance of symptoms in the diagnosis of dry eye. Of the symptomatic subjects, 62.5% had a low Schirmer result, 61.7% had positive signs of meibomian gland dysfunction, 85.4% had abnormal results on either test, and 38.8% on both tests. Schein et al.7 reported that of the symptomatic individuals, 15.1% had a low Schirmer result (≤5 mm), and 5.8% had anatomic features of meibomitis, as reflected by a slit lamp grade of 2 or 3 for collarettes or meibomian gland plugging. There was no mention of the fractions of symptomatic individuals with abnormalities on either test or on both tests. The lower incidence of meibomitis in Schein et al. compared with our data is partly due to different definitions of meibomitis. McCarty et al.6 did not report any information about meibomian gland function.

Why did the Schirmer test reach a significant association with dry-eye symptoms in this study, despite the fact that dry eye is heterogeneous in etiology? One explanation is that meibomian gland dysfunction may play a less significant role in causing dry-eye symptoms in this Chinese population in Taiwan. Ong14 observed that Asians produced more meibomian secretion than whites. Bowman et al.15 noted that meibomian gland dysfunction occurred less frequently among patients with blepharitis in warmer climates compared with cooler climates. Taiwan has a subtropical climate. Further studies are necessary to resolve this question.

We had hoped that the responses describing symptoms could be sorted into groups that were in accord with specific presentations of signs. An initial cluster analysis grouped the symptomatic subjects into those who were more likely to report "dry," those more likely to report "sticky and watery," and those more likely to report "crusting." However, further analyses failed to associate the three groups significantly with any specific presentation of signs. Perhaps a more sophisticated questionnaire could resolve the complexity of the correlations between dry-eye symptoms and signs.

The other problem in identifying dry-eye disease with dry-eye tests is in deciding the cutoff values. McCarty et al.6 concluded that, among the clinical tests they performed, the Schirmer test was the least useful in discriminating symptoms. However, they defined dry eye using a less strict cutoff value for the Schirmer result (8 mm), but a stricter cutoff for tear breakup time (8 seconds) and fluorescein staining (grade 2) than we used in this analysis. This is probably one of the reasons why the Schirmer test yielded the highest number of false positives in McCarty et al. We set the cutoff value at 5 mm for the Schirmer test to comply with the criteria often used for the diagnosis of keratoconjunctivitis sicca. The false-positive rate was still rather high; 37.3% (508/1361) of subjects who had a low Schirmer result did not report frequent symptoms. The use of anesthetics has been suggested to explain this high false-positive rate.6 A previous study showed that topical anesthesia reduces the Schirmer result by 40%.16 Topical anesthesia might dampen the initial reflex secretion due to irritation, although the Schirmer result increased in variability, probably because of differences in susceptibility to the anesthetic.17 We used anesthetics in this study because other similar population-based studies1 6 performed the test under anesthesia and because we wanted to minimize the discomfort and false-negative responses induced by the irritation caused by the test strips.

In the study by Schein et al.,7 individuals reporting their general health to be poor had a higher tendency to report dry-eye symptoms than did other respondents (16.9% vs. 10.6%, respectively; P < 0.001), but did not display a lower Schirmer result. A similar phenomenon was observed in the Shihpai population. Individuals reporting poor general health were more likely to report dry-eye symptoms than were other respondents (9.4% vs. 4.9%, respectively; P = 0.001). None of the dry-eye tests was associated with self-reported general health. The possibility of reporting bias proposed by Schein et al., (i.e., that some subjects are simply more likely to report symptoms in general) is also relevant in this study. However, most subjects (96.1%) reporting frequent dry-eye symptoms had at least one positive dry-eye sign, indicating that they did have certain ocular-surface problems.

In conclusion, a low Schirmer result of ≤5 mm is associated in this population with frequent dry-eye symptoms. However, the high false-positive rate reduces the usefulness of this test in identifying asymptomatic subjects. The Schirmer test also has limitations in detecting patients with dry eye secondary to meibomian gland disease, because the association between the Schirmer result and meibomian gland anomaly is low. A low Schirmer result is significantly associated with symptoms in this elderly Chinese population but not in elderly white populations, as reported previously.1 6 This finding suggests a different distribution of dry-eye etiologies between white and Asian populations.


   Appendix 1
Top
 Abstract
 Materials and Methods
 Results
 Discussion
 Appendix 1
References
 
Dry Eye Questionnaire
(Allowable responses: never, rarely, sometimes, often, or all the time.)

  1. Do your eyes ever feel dry?
  2. Do you ever feel a gritty or sandy sensation in your eyes?
  3. Do your eyes ever have a burning sensation?
  4. Do your eyes ever feel sticky?
  5. Do your eyes ever feel watery or tearing?
  6. Are your eyes ever red?
  7. Do you notice much crusting or discharge on your lashes?
  8. Do your eyes ever get stuck shut in the morning?


   Acknowledgements
 
The authors thank Yung-Chieh Yen for excellent statistical assistance and helpful discussions of the manuscript.


   Footnotes
 
Presented in part at the 18th Congress of the Asia-Pacific Academy of Ophthalmology, Taipei, Taiwan, March 2001.

Supported by Grants from Taipei Veterans General Hospital (VGH 89-404-1, VGH 90-445-1, and VGH 91-382-1) and by Yen Tjing Ling Medical Foundation (C-YC), Taipei.

Submitted for publication July 23, 2004; revised December 13, 2004; accepted January 10, 2005.

Disclosure: P.-Y. Lin, None; C.-Y. Cheng, None; W.-M. Hsu, None; S.-Y. Tsai, None; M.-W. Lin, None; J.-H. Liu, None; P. Chou, None

The publication costs of this article were defrayed in part by page charge payment. This article must therefore be marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact.

Corresponding author: Ching-Yu Cheng, Department of Ophthalmology, Taipei Veterans General Hospital, 201 Sec. 2, Shih-Pai Road, Taipei, Taiwan; cychengs{at}ms16.hinet.net.


   References
Top
 Abstract
 Materials and Methods
 Results
 Discussion
 Appendix 1
 References
 

  1. Schein OD, Tielsch JM, Munõz B, Bandeen-Roche K, West S. Relation between signs and symptoms of dry eye in the elderly: a population-based perspective. Ophthalmology. 1997;104:1395–1401.[ISI][Medline][Order article via Infotrieve]
  2. Shimmura S, Shimazaki J, Tsubota K. Results of a population-based questionnaire on the symptoms and lifestyles associated with dry eye. Cornea. 1999;18:408–411.[CrossRef][ISI][Medline][Order article via Infotrieve]
  3. Moss SE, Klein R, Klein BE. Prevalence of and risk factors for dry eye syndrome. Arch Ophthalmol. 2000;118:1264–1268.[Abstract/Free Full Text]
  4. Lin PY, Tsai SY, Cheng CY, Liu JH, Chou P, Hsu WM. Prevalence of dry eye among an elderly Chinese population in Taiwan: the Shihpai Eye Study. Ophthalmology. 2003;110:1096–1101.[CrossRef][ISI][Medline][Order article via Infotrieve]
  5. Lee AJ, Lee J, Saw SM, et al. Prevalence and risk factors associated with dry eye symptoms: a population based study in Indonesia. Br J Ophthalmol. 2002;86:1347–1351.[Abstract/Free Full Text]
  6. McCarty CA, Bansal AK, Livingston PM, Stanislavsky YL, Taylor HR. The epidemiology of dry eye in Melbourne, Australia. Ophthalmology. 1998;105:1114–1119.[CrossRef][ISI][Medline][Order article via Infotrieve]
  7. Schein OD, Munõz B, Tielsch JM, Bandeen-Roche K, West S. Prevalence of dry eye among the elderly. Am J Ophthalmol. 1997;124:723–728.[ISI][Medline][Order article via Infotrieve]
  8. Cheng CY, Hsu WM, Liu JH, Tsai SY, Chou P. Refractive errors in an elderly Chinese population in Taiwan: the Shihpai Eye Study. Invest Ophthalmol Vis Sci. 2003;44:4630–4638.[Abstract/Free Full Text]
  9. Bjerrum KB. Keratoconjunctivitis sicca and primary Sjögren’s syndrome in a Danish population aged 30–60 years. Acta Ophthalmol Scand. 1997;75:281–286.[Medline][Order article via Infotrieve]
  10. Manthorpe R, Oxholm P, Prause JU, Schiødt M. The Copenhagen criteria for Sjögren’s syndrome. Scand J Rheumatol. 1986;61(suppl)19–21.
  11. Danjo Y. Diagnostic usefulness and cutoff value of Schirmer’s I test in the Japanese diagnostic criteria of dry eye. Graefes Arch Clin Exp Ophthalmol. 1997;235:761–766.[CrossRef][Medline][Order article via Infotrieve]
  12. Pflugfelder SC, Tseng SC, Sanabria O, et al. Evaluation of subjective assessments and objective diagnostic tests for diagnosing tear-film disorders known to cause ocular irritation. Cornea. 1998;17:38–56.[CrossRef][ISI][Medline][Order article via Infotrieve]
  13. Lemp MA. Report of the National Eye Institute/Industry workshop on Clinical Trials in Dry Eyes. CLAO J. 1995;21:221–232.[Medline][Order article via Infotrieve]
  14. Ong BL. Relation between contact lens wear and meibomian gland dysfunction. Optom Vis Sci. 1996;73:208–210.[Medline][Order article via Infotrieve]
  15. Bowman RW, Dougherty JM, McCulley JP. Chronic blepharitis and dry eyes. Int Ophthalmol Clin. 1987;27:27–35.[CrossRef][ISI][Medline][Order article via Infotrieve]
  16. Lamberts DW, Foster CS, Perry HD. Schirmer test after topical anesthesia and the tear meniscus height in normal eyes. Arch Ophthalmol. 1979;97:1082–1085.[Abstract]
  17. Clinch TE, Benedetto DA, Felberg NT, Laibson PR. Schirmer’s test: a closer look. Arch Ophthalmol. 1983;101:1383–1386.[Abstract]



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