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Impact of Rigid Gas-Permeable Contact Lens Extended Wear on Corneal Epithelial Barrier Function

¹ From the School of Optometry and the ² Division of Public Health Biology and Epidemiology, School of Public Health, University of California, Berkeley, California.

	Abstract

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PURPOSE. To measure the effect of hypoxia and eye closure on epithelial permeability to fluorescein (P_dc) during rigid lens extended wear (EW).

METHODS. Central corneal thickness (CT) and P_dc were measured in 42 subjects with an optical pachometer and automated scanning fluorophotometer, respectively. All subjects had been successfully wearing rigid gas-permeable (RGP) lenses on a 6-night EW regimen, and each individual was randomized to wear either medium- or high-oxygen-permeable (Dk) RGP lenses (two types of siloxane-fluorocarbon polymer lenses with Dk of 49 and 92). CT and P_dc measurements were performed at an afternoon visit (baseline) and were repeated in the morning after 8 hours of overnight wear. Subjects slept with a patch over the right eye. The patch was not removed until immediately before the morning measurement.

RESULTS. The mean overnight swelling response for subjects in the medium-Dk group was greater than that in the high-Dk group. Results of a paired t-test indicate that the eye wearing the medium-Dk lens with a patch overnight had a significant increase in epithelial permeability. Results of mixed-effect models suggest that eye closure and lens-induced hypoxia are significant factors in altering P_dc.

CONCLUSIONS. The results indicate that corneal epithelial permeability increases with hypoxic dose and that epithelial barrier function is impaired by overnight rigid lens wear.

	Introduction

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Contact lens extended wear (EW) creates a stressful environment (e.g., chronic pressure, mechanical stress, and lens-induced hypoxia) for the cornea and has been associated with many serious ocular complications. Several studies have shown an association between ocular surface disorders in contact lens wearers and microbial keratitis that could cause blindness.^{1 2 3} Therefore, understanding the mechanisms that lead to alterations in the corneal epithelium may be important in minimizing the incidence of such vision-threatening complications. Although most clinicians and researchers believe that alterations in the corneal epithelium may be related to contact lens-induced hypoxia, there has been very little clinical evidence to substantiate a direct link between corneal hypoxia and epithelial barrier function.

To explore the effects of contact lens wear on the corneal epithelium, our Berkeley research group developed a method of assessing epithelial barrier function by measuring the permeability of the epithelium to fluorescein (P_dc).⁴ We have found that when a standard disposable soft contact lens is worn with the eyes closed for as little as 1 hour, there is an increase in epithelial permeability of approximately 40%,⁵ and when the same lenses are worn overnight for 2 weeks, the P_dc increases 99%.⁶ There is, however, no association between increased P_dc and either wearing a contact lens that causes corneal hypoxia with the eyes open⁷ or exposing the cornea to hypoxia without contact lens wear.⁸ These studies suggest that decreased barrier function occurs when the corneal epithelium is exposed to a hypoxic environment, the presence of a contact lens, and eye closure.

Although changes in epithelial integrity are associated with contact-lens–induced hypoxia and eye closure for soft contact lenses, it is not known whether this relationship holds for other lens types (e.g., rigid) that perform differently on the eye. In addition, although epithelial permeability has been shown to increase under the hypoxic conditions of closed-eye lens wear, it is not known whether this relationship is hypoxia dose dependent. In this study, we investigated these questions by measuring P_dc before and after overnight wear on subjects in extended wear (EW) using rigid gas-permeable (RGP) lenses with a range of oxygen transmissibilities (Dk/t).

	Methods

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Subject Recruitment
Forty-two experienced rigid-lens wearers (53% men and 47% women) aged 21 to 42 years (mean ± SD, 24 ± 4.8 years) were recruited from the Berkeley Contact Lens Extended Wear Study (CLEWS). All subjects entering CLEWS had no prior overnight lens wear experience and minimal or no history of soft lens day wear. The CLEWS clinical trial protocol required that all subjects first adapt to day wear and then extended wear involving high oxygen-permeable (Dk) RGP contact lenses. After successful extended wear adaptation, subjects were randomized to either medium- or high-Dk lenses. With the exception of Dk, the randomized lenses were made with identical parameters to the adaptation lenses. After randomization, subjects reported for quarterly visits over a 12-month follow-up period at which both clinical and laboratory assessments were performed. Subject eligibility criteria for CLEWS have been described in detail elsewhere.⁹

Subjects recruited for the P_dc study had worn the assigned study lenses for 6-nights/wk extended wear for a minimum of 1 month, with subjects in both Dk groups having up to 12 months of EW experience. Ten subjects (five in the medium-Dk group and five in the high-Dk group) were asked to participate in the P_dc study after completing CLEWS and were therefore required to resume full-time EW for 1 month before P_dc assessment. Informed consent was obtained from all study participants after a full description of the measurement procedures. This research project adhered to the tenets of the Declaration of Helsinki, and the research protocol was approved by the institutional review board (Committee for Protection of Human Subjects, University of California, Berkeley).

Contact Lens Materials
The medium- and high-Dk contact lenses used in this study were made from a siloxane-fluorocarbon polymer (paflufocon B and D; Paragon Vision Sciences, Mesa, AZ). Before dispensing, lens parameters including base curve radius, diameter, power, and central thickness were verified using standard verification instruments. The central Dk/t of four randomly selected lenses from each lens group was determined using Fatt’s polarographic technique.¹⁰ For the study lenses of the 42 subjects, the average central lens thickness was 0.16 and 0.18 mm, which correspond to the average Dk/t of 28 x 10^-9 and 53 x 10^-9 (cm/mL · O₂)/(sec/mL · mm Hg) for the medium- and high-Dk lenses, respectively. For both lens materials, the average overall lens diameter was 9.2 mm. Lenses were fitted to achieve alignment. The details of the lens fitting criteria have been reported elsewhere.⁹

Instrumentation and Procedures
A Haag-Streit optical pachometer and an automated scanning fluorophotometer (Fluorotron Master; Ocumetrics, Mountain View, CA) were used to measure corneal thickness and epithelial permeability, respectively. The calibration and measurement techniques of both instruments have been described previously.^{4 11}

The experimental procedure required an afternoon (PM, baseline) visit and a morning (AM) visit after 8 hours of overnight wear. Subjects were asked to report to our laboratory for the PM visit a minimum of 4 hours after awakening, so that we could obtain afternoon baseline values for corneal thickness (CT) and P_dc. Before the CT measurements, the lens in the right eye was gently removed with a suction cup, and 20 replicate CT readings were taken and averaged. After repeating this procedure for the left eye, the background stromal fluorescence of both eyes was measured. Then 2 µL 0.35% NaF dye was instilled in the right eye and the eye was immediately scanned, followed by dye instillation and scanning of the left eye. Thereafter, a series of scans was made every 2 minutes, alternating between eyes, over a period of 20 minutes. At the end of this period, the eyes were thoroughly rinsed, and the stromal fluorescence of both eyes was measured again. The details of estimating P_dc from the fluorescence readings have been described elsewhere.⁴

At the PM visit, subjects were instructed to patch their right eyes immediately before sleep the night before the AM visit, and they were required to return to the laboratory within 2 hours of awakening the next morning with the patch in place. Subjects were first trained in the laboratory in patching procedures to ensure that the eye would remain completely closed during sleep, but without excessive pressure that could compress the lens on the cornea and cause adherence. After demonstrating the correct patching technique, subjects were dispensed gauze and surgical tape, along with written instructions to be reviewed that night, at the time of patching. Immediately after removal of the patch and lenses at the AM visit, CT and P_dc measurements were repeated according to the same procedures as described for the PM visit.

At the completion of both the PM and AM permeability measurements, a masked observer performed a detailed slit lamp examination using both white light and cobalt blue light with a yellow filter. The presence of corneal staining with fluorescein was graded on a 1 to 4 scale, where punctate staining of fewer than five points was grade 1; 5 to 10 points as grade 2; 11 to 25 points as grade 3; and more than 26 points as grade 4. Subjects exhibiting more than five punctate stains in the central cornea were excluded from the analysis to avoid an overestimate of the P_dc.

Statistical Methods
Epithelial permeability was transformed by natural logarithm to stabilize the variance and better approximate normality. We examined the effects of hypoxia and overnight RGP wear on the log permeability, ln(P_dc), using mixed-effects analysis of variance models, implemented on computer (Proc Mixed; SAS, Cary, NC).¹² Among the various models explored were fixed effects for hypoxic dose, morning versus afternoon measurement (Visit), patched versus unpatched eyes, and length of time the eyes were open before P_dc measurements (TOpen). Hypoxic dose was characterized by medium- versus high-Dk lens group (DKGroup) or by the lens-specific oxygen transmissibility (Dk/t). A random effect for right or left eye was specified, with a compound symmetric covariance structure that assumes a common covariance in the repeat measurements on each subject (two eyes x two visits) and independence between subjects. We also assessed the impact of other variables, including age, gender, ethnicity, contact lens history, and corneal thickness.

	Results

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Descriptive
Thirty-six myopic subjects successfully completed the study, 19 wearing the medium-Dk (mean [95% CI] lens power, -3.50 D [-2.50, -4.25]), and 17 wearing the high-Dk lenses (mean, -2.75 D [-2.00, -3.50]). Previous investigations have determined that the accuracy and precision of the P_dc measurement technique, although inadequate for individual P_dc assessment, make it appropriate for group studies.⁴ Several sources of variability may contribute to error in the estimation of P_dc, including the presence of corneal staining, reflex tearing, and differences in the alignment of the subject between individual scans within a measurement session or between sessions. Of 42 subjects initially measured, four were not included in the analysis because central corneal staining was observed after the permeability assessment. Their inclusion could have resulted in an overestimate of the P_dc. Two subjects were excluded because of negative estimates of their P_dc, which were most likely caused by slight differences in the alignment of the subject between the background and postrinse fluorescence readings. If the subjects were unable to maintain a consistent alignment, the variation in measurement angles between the background scans and the postrinse scans could have resulted in lower mean postrinse stromal fluorescence compared with mean background fluorescence. This could have caused an erroneous negative estimate of the permeability, which is impossible by definition. The remaining 36 subjects included in the analysis showed no evidence of central corneal staining or lens adhesion and reported no experience of ocular discomfort on awakening.

Table 1 presents the mean, minimum, and maximum lens Dk/t in both eyes of the medium- and high-Dk subjects. On average, the groups differed by approximately 25 Dk/t units, and there was no overlap between groups, confirming that they received distinctly different hypoxic doses. The mean ± SE overnight swelling response for subjects in the medium-Dk group was greater for both patched (5.8% ± 0.8%) and unpatched eyes (4.6% ± 0.8%), compared with the high-Dk group (4.5% ± 0.7% and 2.6% ± 0.6% for the patched and unpatched eyes, respectively). As expected, the mean percentage of corneal swelling was greater in the patched eyes in both groups because of corneal deswelling (i.e., recovery) in the unpatched eyes, which were open, on average, for up to 90 minutes before the AM pachometry measurements. The separate Dk/t distributions and overnight corneal swelling results confirm that each group received a different hypoxic dose, resulting in correspondingly different physiological reactions and thereby providing the experimental conditions necessary to explore the effects of hypoxic dose on epithelial barrier function.

View larger version (30K): [in this window] [in a new window]   Figure 1. Readings for ln(Pdc), in units of ln(nanometers per second), taken at the baseline PM and overnight AM visits, in both the medium- and high-Dk lens groups. Arrows: mean ln(Pdc).

View larger version (12K): [in this window] [in a new window]   Figure 2. Model predictions using Dk/t and TOpen. The ln(Pdc) is in units of ln(nanometers per second). The parallel lines for medium- and high-Dk lens groups indicate that the epithelium was significantly more permeable, on average, in subjects wearing lower Dk/t lenses and was more permeable after overnight wear for both levels of Dk/t. Reference points are shown for the measurement of patched eyes immediately after eye opening in the AM (0 minutes), the maximum time that unpatched eyes were open before AM measurement (90 minutes), and the median time that eyes were open before PM measurements (390 minutes).

To carefully assess the difference in epithelial permeability between Asians and non-Asians, we used a model taking into account all variables (ethnicity, age, gender, corneal curvatures, TOpen, lens power, lens Dk/t, lens base curve radius (BCR), and months of EW), to avoid any possible bias from confounding variables. After excluding the insignificant variables, we devised the models that are shown in Table 5 , which suggest that epithelial permeability is dependent mostly on ethnicity, TOpen, and Dk/t, whereas all other variables do not play a significant role in changing P_dc. The first model showed a greater P_dc in Asians than non-Asians, with marginal significance (P = 0.07). This simple additive (i.e., noninteraction) model is illustrated in Figure 3 , which shows parallel lines for the overnight change in ln(P_dc) for two levels of Dk/t, both of which were shifted upward by a constant amount for the Asian subgroups. We then fitted a series of models permitting differences in the slopes of the lines (i.e., interactions) for different levels of hypoxia or Asian versus non-Asian ethnicity. Although several different models were considered, the second model shown in Table 5 , which permits the slopes of the overnight P_dc change to differ for Asians and non-Asians, provided the best fit to the data. This model reveals significant effects for hypoxia dose (P = 0.02), the time the eyes were open before measurement (P = 0.02), Asian ethnicity (P = 0.01), and the interaction between ethnicity and TOpen (P = 0.04). Figure 4 depicts this model graphically, showing that within each ethnic category there was greater permeability with greater hypoxic dose, on average, and an overnight increase in P_dc for both levels of Dk/t, but that both the overall average P_dc and the magnitude of the overnight increase in P_dc were much greater among the Asian subgroups.

View larger version (16K): [in this window] [in a new window]   Figure 3. Additive model predictions for Asians versus non-Asians using Dk/t and TOpen. The ln(Pdc) is in units of ln(nanometers per second). The parallel lines for the overnight change in ln(Pdc) in the medium- and high-Dk lens groups were shifted upward by a constant amount in Asian subjects (top two lines), reflecting greater Pdc. Reference points are as in Figure 2 .

View larger version (15K): [in this window] [in a new window]   Figure 4. Interaction model predictions for Asians versus non-Asians using Dk/t and TOpen. The ln(Pdc) is in units of ln(nanometers per second). Both the overall average Pdc and the magnitude of the overnight increase in Pdc were greater in the Asian group (two lines with steeper slopes). Reference points are as in Figure 2 .

	Discussion

Top Abstract Introduction Methods Results Discussion References

Although P_dc was found to be greater with a higher hypoxic dose and greater after overnight wear, our results suggest that the magnitude of the overnight change in P_dc is not dependent on the level of oxygen available. Subjects wearing medium-Dk lenses had, on average, higher P_dc than those wearing high-Dk lenses at both afternoon and morning visits; however, the amount of overnight increase in P_dc was roughly the same in both lens groups. This finding may be partly a result of a higher baseline P_dc, on average, for our medium-Dk subjects, and further study is needed to determine whether the overnight increase in P_dc would be the same for medium- and high-Dk lenses among neophyte lens wearers with no baseline difference in P_dc between lens groups.

The greater P_dc observed at the afternoon baseline visit for our medium-Dk subjects is of potential clinical interest. Because all subjects had worn lenses on a full-time overnight basis for at least 30 days before P_dc measurements, the difference in baseline P_dc between the Dk groups suggests that individuals wearing lower Dk lenses may have reduced epithelial barrier function throughout the day and not just for a short period after overnight wear. This elevation in daytime P_dc could be explained by the cumulative effects of continuous exposure to a greater hypoxia dose in subjects wearing medium-Dk lenses. Several studies have shown that contact lens-induced hypoxia can have a substantial impact on the morphology and physiology of corneal epithelial cells. For example, low oxygen-permeable lenses (rigid or soft) can inhibit cell mitosis,¹³ reduce cell desquamation rate,¹⁴ enlarge superficial epithelial cells,¹⁵ and increase bacterial binding.¹⁶ Such hypoxia-driven alterations in the epithelial cell layer could explain the persistence of an elevated P_dc and impaired barrier function during the day in our medium-Dk group.

In addition to our findings that contact lens–induced hypoxia and eye closure affect P_dc, we also found that Asian eyes are more susceptible to changes in epithelial barrier function than are non-Asian eyes. This higher level of susceptibility to changes in epithelial permeability is apparently not due to the differences in age, corneal curvature, and lens power. In searching for other clues to account for the differences in P_dc between the two groups, we note that earlier studies have reported that both vertical palpebral aperture size¹⁷ and orbital fat content differ between Asian and non-Asians.^{18 19} Both parameters could affect the physical contact lens–corneal fitting relationship. For example, the narrow palpebral aperture size and lid tightness associated with Asian eyes may produce excessive lens–corneal apical pressure leading to greater epithelial trauma (increased P_dc) in the Asian compared with the non-Asian eye. The difference in P_dc is in agreement with a report that shows that lens-induced epithelial trauma, based on the presence of superficial punctate keratitis, is more common in Asian than in non-Asian eyes.²⁰ These findings may be partly explained if one could demonstrate that Asian eyes have greater epithelial fragility; however, to our knowledge there is no published work that has examined differences in epithelial fragility between Asians and non-Asians. Further studies are needed to better understand the complex set of factors that may make the Asian eye more prone to altered epithelial response during contact lens wear.

We found that changes in P_dc associated with RGPEW was substantially lower than in subjects wearing soft EW contact lenses.⁶ For example, we have previously shown that subjects wearing soft lenses had a 99% increase in P_dc after 2-week overnight wear.⁶ In the present study, subjects wearing rigid lenses showed an average increase of 20% in P_dc. We also observed that after overnight RGP wear, the unpatched eye had less change in P_dc than the patched eye. This is in contrast to our recent P_dc measurements for overnight soft lens wear in which the unpatched eye had an increased permeability compared with the patched eye.¹³ Because the RGP and soft lens P_dc studies used similar experimental protocols, the differences in P_dc may be due to lens performance. For example, during sleep, trapped debris and other metabolic byproducts build up under the lens and are removed by tear exchange. Soft lenses have a much lower tear exchange rate than rigid lenses,^{22 23} and it is possible that the relatively long retention time of trapped debris under the soft lens after sleep may lead to epithelial trauma (e.g., increased P_dc) and make the cornea more susceptible to contact lens associated complications such as microbial keratitis.

In conclusion, we have shown in the present study that for rigid contact lenses, a greater dose of hypoxia is associated with increased permeability of the corneal epithelium, and that epithelial barrier function is impaired after overnight, closed-eye contact lens wear. Further, we have shown that both the overall hypoxic effect on permeability and the overnight difference in P_dc appear to be more pronounced among Asian subjects. In summary, our findings suggest that if contact lenses are to be worn on an overnight basis, lenses with the highest oxygen transmissibility and fastest rate of tear exchange are preferred, to minimize disruption of the corneal epithelial cell layer and maintain an adequate barrier to infection at the ocular surface.

	Footnotes

 
Supported by National Eye Institute Grant R01-EY-07728.

Submitted for publication June 5, 2001; revised November 27, 2001; accepted December 11, 2001.

Commercial relationships policy: N.

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: Meng C. Lin, School of Optometry, University of California, Berkeley, CA 94720-2020; mlin{at}spectacle.berkeley.edu

	References

Top Abstract Introduction Methods Results Discussion References

 

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