Optometry & Vision Science

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Optometry & Vision Science:
doi: 10.1097/OPX.0000000000000029
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The Relation Between Blinking and Conjunctival Folds and Dry Eye Symptoms

Pult, Heiko*; Riede-Pult, Britta H.; Murphy, Paul J.

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Dipl Ing(FH)


Dr. Heiko Pult - Optometry and Vision Research (HP, BHR-P), Weinheim, Germany; Contact Lens and Anterior Eye Research Unit (HO, PJM), School of Optometry and Vision Sciences (HP, BHR-P), Cardiff University, Cardiff, Wales, United Kingdom; and School of Optometry and Vision Science (PJM), University of Waterloo, Ontario, Canada.

Heiko Pult Dr. Heiko Pult - Optometry and Vision Research Steingasse 15, 69469 Weinheim Germany e-mail: ovr@heiko-pult.de

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Purpose: To investigate the relationship between blink action, dry eye symptoms, and lid-parallel conjunctival folds (LIPCOF).

Methods: In 30 subjects (14 were women; mean [standard deviation {SD}] age, 42.4 [±12.3] years), spontaneous blinks were recorded from a temporal-inferior view (high-speed video), and the blink extent (incomplete [IC], almost complete [AC], and complete [CC]) was evaluated. Dry eye symptoms were evaluated using the Ocular Surface Disease Index (OSDI), and nasal and temporal LIPCOF grades were noted. Correlations between groups were calculated with Pearson correlation (or Spearman rank in nonparametric data), and differences between groups were calculated with an unpaired t-test (or U-test Mann-Whitney in nonparametric data).

Results: Blink rate was significantly higher in females (22.0% [±16.8]) than in males (8.6% [±7.2]; unpaired t-test: p = 0.007). The percentage of AC of all blinks (AC%) was significantly correlated to LIPCOF sum (nasal + temporal) and OSDI scores (r > 0.570, p < 0.001). The percentage of IC was significantly correlated to LIPCOF sum (r = −0.541, p < 0.001) but not to OSDI.

Conclusions: The frequency and type of blinking may have an effect on dry eye symptoms and LIPCOF severity since almost all complete blinks were significantly related to both factors.

Blinking is vital in maintaining optical performance, ocular surface health, and tear film drainage and is considered essential for spreading the lipid layer and may promote the release of oil mechanically from the meibomian glands.1–5 However, in the presence of an insufficient tear film, the mechanical forces involved in blinking can damage the ocular surface.6–8 For example, conjunctival folds are assumed to be related to increased friction in blinks,6 which might follow from an insufficient composition of the resident mucins at the ocular surface or in the tear film.6,9

Bulbar conjunctival folds were first described by Hughes10 and named conjunctivochalasis (CCH) implicating a relation between age and CCH. However, within the spectrum of conjunctival folds, at the small, subclinical level, age does not seem to be correlated with their formation,11 leading Höh et al.11 to describe this form as lid-parallel conjunctival folds (LIPCOF; Fig. 1). It is thought that LIPCOF might represent the first mild stages of CCH and thus share the same aetiology. To avoid confusion, in this study, LIPCOF refers only to subclinical conjunctival folds at a defined location, observed without fluorescein instillation, and classified by an optimized grading scale.6,9,12 Subclinical means being restricted to those cases where the number of folds does not increase in forced blinks.13 Several causes of bulbar conjunctival folds are hypothesized: conjunctival “looseness” as a result of inflammatory processes,14–16 a decrease in elastic fibers,15,16 or lymphatic dilation by mechanical forces between the lower lid and the conjunctiva that gradually interferes with lymphatic flow.17 Increased friction in blinking might follow from insufficient mucins or an altered composition of resident mucins at the ocular surface.6,9,18

Figure 1
Figure 1
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Berry et al.6 reported increased LIPCOF scores in mucin insufficiency. Mucins are vital for the lubrication and protection of the cornea, for anchoring the aqueous tear film to the corneal epithelium during blinking, thus protecting the epithelium from shear forces, as well as protecting against epithelial desiccation and bacterial contamination.19 Furthermore, LIPCOF seems to be related to lid wiper epitheliopathy (LWE).6,20 Both LWE and LIPCOF scores are increased in contact lens wearers,21 compared to non–lens wearers, supporting the mechanical hypothesis, since the coefficient of friction of a lens material is commonly higher than that of the cornea.22,23 However, it remains to be seen whether similar findings would be found in patients wearing the most recent comfort-enhancing contact lens materials that have a lower coefficient of friction. While LWE seems to be an immediate indicator of increased friction in blinks, LIPCOF seems to signal longitudinal effects of mechanical forces in blinks.21

As reviewed by Korb et al.,24 there is a common assumption in our understanding of complete blinks, that there will be contact between the entire upper and lower lid surfaces across the full eyelid length.25 Indeed, Doane26 defined a blink as being complete only when the upper and lower lids meet each other. In line with this, the anterior portions of the upper and lower lid margins have been referred to as the occlusal surfaces or the cutaneous occlusal zones.25,27,28 However, it was recently demonstrated that the central portions of the lids do not touch in spontaneous blinks.24,29,30 Interestingly, when videoing blinks from a temporal-inferior view in Caucasians, rather than a frontal view, the upper lid was found to overlap the lower lid, a feature named as an “overblink” (Fig. 2), while still appearing to be fully closed in complete apposition of the lid margins from a frontal view.29 This earlier experiment revealed that the temporal-inferior view in the observation of lid touch during blinking can provide an improved observation method, particularly since, in a frontal or side view, the eyelashes obscure the central lid margins and make it difficult to classify any overblink.

Figure 2
Figure 2
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With this new observation method, and the proposed model for the development of LIPCOF, the aim of this study was to evaluate the correlations between blink frequency and completeness and between dry eye symptoms and LIPCOF.

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The normal spontaneous blinks of 30 randomly selected subjects (drawn by lots; 14 were women; mean [standard deviation {SD}] age, 42.4 [±12.3] years; mean [SD] age of women, 39.9 [±11.1] years; mean [SD] age of men, 44.6 [±13.2] years) were videoed in both a temporal-inferior view and a frontal view. Dry eye symptoms were evaluated using the Ocular Surface Disease Index (OSDI),31 and nasal and temporal LIPCOF grades were noted.

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Exclusion Criteria

Subjects were excluded if they did not show normal eyelid kinematics, such as irregular lid margins, supra-nuclear motor impairment of lid movements, Grave upper eyelid retraction, cicatricial lagophthalmos, ptosis, or apraxia, and if they had any ocular surface abnormalities, such as can be associated with rheumatoid arthritis, diabetes, recent ocular infections, hay fever, any history of ocular surgery, use of any medication or eye drops known to affect the ocular surface, worn contact lenses, or were pregnant. All procedures were conducted in accordance with the Declaration of Helsinki (1983), and approval for the study was given by the Cardiff School of Optometry and Vision Sciences Human Ethics Committee. All subjects gave written informed consent before participating in the study.

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Lid-Parallel Conjunctival Folds

Lid-parallel conjunctival folds were evaluated without fluorescein in the area perpendicular to the temporal and nasal limbus on the bulbar conjunctiva above the lower lid (temporal and nasal LIPCOF, respectively) with a slit-lamp microscope using 16× to 25× magnification, as necessary,6,9,32 and was classified using the optimized grading scale (Table 1).6,9,32 A further combined LIPCOF score (LIPCOF sum) was calculated by adding together the nasal LIPCOF grade and the temporal LIPCOF grade.9 Care was taken to differentiate between parallel, permanent, conjunctival folds (LIPCOF) and disrupted microfolds.6,9,13,32–35 The differentiation between microfolds and LIPCOF was done by comparing fold thickness; a single LIPCOF is about 0.08 mm thick, while that of a microfold is 0.01 mm.36

Table 1
Table 1
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Ocular Surface Disease Index

Each subject’s symptoms were evaluated after assessment using the OSDI questionnaire.31 Total OSDI scores were calculated as recommended by Schiffman et al.31

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Spontaneous blinks were recorded over a period of 30 seconds in a temporal-inferior view using a high-speed video camera (250 frames per second; GZ-GX1BE, JVC, Japan). Thirty seconds was felt sufficient to provide enough blink episodes for an analysis.29 Simultaneously, blinks were videoed in a frontal view using a video slit-lamp microscope (DigiPro2; bon Optic, Lübeck, Germany). Subjects were asked to look straight ahead, in a relaxed manner, and were not required to do any task. Blinks were defined to be spontaneous in this study when subjects are looking straight ahead and are making unforced and nonreflex blinks. Blinks were subdivided into complete (CC), incomplete (IC), and almost complete (AC). Blinks were noted as CC if there seemed to be alignment between the posterior upper lid margin and the anterior lower lid margin across the full length. An AC blink was defined as being a partial touch of the nasal and temporal portions of the lids but with a small portion of the upper and lower lid margins still showing a vertical gap of up to half of the upper lid margin’s thickness (from the temporal-inferior view; Fig. 3). An IC blink was defined as being all other forms of blinks. Blink rate was calculated from CC and noted in blinks per minute. Percentages of each blink type were calculated relative to the total number of blinks (IC + AC + CC).

Figure 3
Figure 3
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Analyses of CC, IC, and AC were masked against OSDI and LIPCOF evaluation. Subjects were masked against LIPCOF.

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Statistical Analyses

Data were examined for normality using the Shapiro-Wilk test. Correlations were calculated with Pearson correlation (or Spearman rank in nonparametric data), and differences between groups were calculated with an unpaired t-test (or U-test Mann-Whitney in nonparametric data). Data were analyzed using SPSS version 20.0 (SPSS, Inc., Chicago, IL) and WinSTAT 2005.1-Software (R. Fitch Software, Bad Krozingen, Germany).

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Mean (SD) blink rate was 14.9 (±14.1) blinks per minute. Blink rate was significantly higher in females than in males (unpaired t-test: p = 0.007; female, 22.0% [±16.8]; male, 8.6% [±7.2]), whereas there was no significant difference between gender in IC and AC (p > 0.278). 34.0% (±19.0) of all blinks were AC (Fig. 3), 24.8% (±23.5) were IC, and 41.2% (±22.6) were CC (Fig. 4).

Figure 4
Figure 4
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Mean (SD) OSDI score was 11.5 (±9.2), and mean (SD) LIPCOF scores were 1.4 (±0.8) for temporal, 0.7 (±0.7) for nasal, and 2.1 (±1.4) for sum. The percentage of AC (AC%) of all blinks was significantly correlated to LIPCOF scores (Table 1 and Figs. 5 and 6) and OSDI scores. The percentage of IC (IC%) was significantly, negatively correlated to LIPCOF scores but was not related to the OSDI scores. No correlations were found between the percentage of CC (CC%) and LIPCOF or OSDI. However, when adding AC% and CC% and grouping subjects by LIPCOF sum (cutoff value, 2),6,9,12 the LIPCOF sum score of 2 or higher group showed a significantly higher number of blinks (83.1% [±15.5]) compared to the group of subjects with LIPCOF sum scores less than 2 (63.1% [±28.6]; paired t-test; p = 0.019). Overlapping of lids was not related to OSDI or LIPCOF (Table 1).

Figure 5
Figure 5
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Figure 6
Figure 6
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As reviewed by Korb et al.,24 blinks are commonly described as normal (unconscious, unforced, or spontaneous), reflex (provoked), and voluntary (conscious or forced).26 In the normal, unforced blink—named a spontaneous blink in this article—no appreciable upward rotation of the globe was observed. A forced blink of the upper eyelid usually results in a significant demonstration of Bell’s movement.37 In addition, the globe moves posteriorly as the upper eyelid descends, probably caused by eyelid pressure during the closing phase of the blink.26 This may be independent of the Bell’s phenomenon.38 Spontaneous blinking occurs in the absence of an individual consciously eliciting or directing a blink.24 Spontaneous blinks are further subdivided into complete and incomplete blinks. Doane39 showed that the upper lid frequently did not contact the lower lid during normal spontaneous blinking, although more than 80% of the exposed ocular surface was covered during the blink.

Compliant with the literature,26,40–42 this study has shown that many of the blinks observed in the subjects were not complete and that the blink rate was significantly higher in females than in males. However, such a matching of results is not an exacting standard because there is a broad spectrum of reported results for the IC% in a population of healthy individuals, ranging from 10% to 80%.26,40–42 This may be due to the different measurement protocols and procedures, the visual task, or the method used for the detection of eyelid motion. For example, according to Abelson and Holly,40 an incomplete blink was defined as being when the upper lid covered less than two thirds of the cornea during the downward movement. As reviewed by Cruz et al.,5 the mean blink rate observed in this study seems to be normal based on the mean age of this population. Blink rate increases with age and seems to be around 20 blinks per minute5 at the age of 42 years. Although the age of the observed males in this study was slightly higher than that of the females, this aging effect might not solely explain the difference in blink rates between gender since the gender difference is also reported in literature.43,44 Interestingly, Yolton et al.43 also reported a significantly increased blink rate in females taking oral contraceptives compared to females who were not.

Significantly, our investigation showed that some of the blinks, which appeared to be complete from a frontal view, were not complete when observed from the temporal-inferior view. These blinks were described as AC and may represent an additional sub-group of spontaneous blinks, showing nearly similar blink amplitude as CC. The frontal observation was recorded by normal video slit-lamp microscope, not high-speed video recording. Therefore, it cannot be excluded that the AC could be detected using high-speed video recording from a frontal view, too. However, we assume AC blinks—being so close to CC blinks—are indistinguishable from CC blinks in the frontal view.

It is known that blink rate is associated with tear film quality.45,46 Even in longer interblink intervals, the tear film will be stable in normal subjects, in contrast to dry eye patients for whom any tear film thinning may force them to take more frequent blinks. Similarly, incomplete blinking can result in dry eye and exposure keratopathy.4 Such a patient will have a significantly longer interblink interval, producing a shorter tear breakup time that might be revealed by a higher incidence of dry eye symptoms, as represented in this patient cohort. In this study, the AC percentage was significantly correlated to OSDI scores and LIPCOF scores. This relationship has a good supporting hypothesis because LIPCOF are reported to be caused by mechanical forces during blinking,6 with a higher IC% resulting in less mechanical stress to the inferior bulbar conjunctiva. Indeed, this was what was found: as the IC% increased, lower LIPCOF scores were observed, and in subjects with a high AC%, LIPCOF scores were significantly increased. A higher IC% was also associated with less OSDI scores and LIPCOF scores. However, once the lid made a larger movement over the eye, then the blink frequency was found to be related, once again, to LIPCOF scores. These results suggest that evaluation of AC rate with this technique may be a useful additional test in the evaluation of dry eye symptoms.

One hypothesis for an underlying mechanism for these effects may be that the LIPCOF physically interfere with some of the spontaneous blinks, inhibiting the complete blink by creating a barrier between the lid margins. On the basis of a median fold thickness of 0.08 mm,36 the largest distance created in this way between the lid margins may be up to 0.24 mm, for a LIPCOF degree of 3. Another possibility could be related to the observation that the lid margins seem to be slightly tilted, with a larger distance between the posterior lid margins than the anterior lid margins.47 In this study, the median nasal LIPCOF scores were smaller than the temporal LIPCOF scores, suggesting that the lid margin separation due to LIPCOF is less visible or that the LIPCOF are small enough to fit within the posterior lid margin space. However, further investigation is needed to evaluate this hypothesis, especially in contact lens wearers, who have higher degrees of LIPCOF than subjects who do not wear lenses.12,48,49

Finally, since it is reported that LIPCOF are related to mucin deficiency,6 it can also be hypothesized that the lids may be hindered in their movement as they approach the point of closing because of increased friction between the upper lid and the bulbar conjunctiva. In support of this hypothesis, subjects with increased LIPCOF scores showed a higher blink frequency when adding together AC% and CC%, suggesting that a poorer tear film might have made the subjects blink more often.45,46 Since an insufficient tear film—regardless of whether it is due to an aqueous-deficient dry eye or an evaporative dry eye—is associated with loss of mucin,50 friction is increased in such subjects and might result in LIPCOF over a longer period.6,21 On the basis of this hypothesis, we can speculate that a chronic insufficient tear film may cause LIPCOF due to an increased blink rate accompanied by increased friction between the lid and the bulbar conjunctiva, resulting in an increased AC%. Both AC and CC blinks possess the possibility of causing the highest impact on ocular surface, in terms of friction, compared to IC. However, CC was not related to LIPCOF or OSDI. It can be hypothesized that, in those subjects showing higher degrees of LIPCOF, the lids were not able to close completely during blinking in a higher percentage of blinks, resulting in more AC of all apparent full blinks (AC plus CC) than observed in subjects with lower degrees of LIPCOF, who showed almost all of the apparent full blinks as being completed (CC). Furthermore, the portion of the bulbar conjunctiva between lid margins in AC might not be properly lubricated, promoting the development of LIPCOF. However, these hypotheses must be investigated in further research, this being a first pilot study.

In conclusion, AC blinks were significantly related to dry eye symptoms and LIPCOF, indicating clinically that AC blinks may give additional information in dry eye evaluation. The relationship between blinking and LIPCOF seems to strengthen the mechanical cause of LIPCOF.

Heiko Pult

Dr. Heiko Pult - Optometry and Vision Research

Steingasse 15

69469 Weinheim


e-mail: ovr@heiko-pult.de

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This study was not funded, and the authors have no proprietary or commercial interest in any materials discussed in this article. The authors have no potential conflict of interests in this article.

Received March 6, 2013; accepted June 17, 2013.

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spontaneous blinks; overblink; lid-parallel conjunctival folds; LIPCOF; dry eye; OSDI

© 2013 American Academy of Optometry


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