ARTICLE
Effect of Religious Fasting on Tear Osmolarity and Ocular Surface Bengu Ekinci Koktekir,
M.D.,
Banu Bozkurt, M.D., Saban Gonul, and Suleyman Okudan, M.D.
Objective: To evaluate the effects of religious fasting on tear secretion, tear osmolarity, corneal topography, and ocular aberrations. Methods: This prospective controlled study comprised 29 eyes of 29 healthy men. Before ophthalmologic examination, all subjects underwent corneal topography by a placido disc corneal topography and aberrometry device (OPD Scan II). Tear osmolarity was measured using OcuSense TearLab osmometer. Ocular surface disease index (OSDI) scores, tear break-up time (BUT), Schirmer I test, and lissamine green staining were evaluated. The measurements taken before and during Ramadan at the same hours between 4.00 and 5.00 PM were compared using paired sample t test, and a P value less than 0.05 was accepted as statistically significant. Results: The mean age of the study group was 27.865.9 years (range, 20–47 years). The mean tear osmolarity values were measured as 285.668.2 mOsm/L and 293.3616.0 mOsm/L, whereas the mean Schirmer I values were 14.866.0 mm and 10.665.3 mm in nonfasting and fasting periods, respectively. Tear osmolarity, OSDI, and Oxford grading scores significantly increased (P=0.02, P=0.002, P=0.003, respectively), whereas Schirmer I values and intraocular pressure decreased (both, P,0.001) during the fasting period compared with the nonfasting period. There were no significant differences in tear BUT, keratometry values, and corneal aberration measurements between nonfasting and fasting periods (P.0.05, for all). Conclusion: Fasting significantly decreases tear production and increases tear osmolarity; however, it does not deteriorate corneal topographic parameters and ocular aberrations in healthy subjects. Key Words: Ramadan aberrations—Dry eye.
month—Fasting—Tear
osmolarity—Ocular
(Eye & Contact Lens 2014;40: 239–242)
R
amadan, the ninth month in the Islamic lunar calendar, is a month of obligatory daily fasting for the Muslims. Fasting begins at dawn and ends with the sunset, during which the Muslims refrain from consuming food, drinking liquids, and smoking. The fasting people usually eat some food and drink a considerable amount of fluid to endure the effects of hunger and dehydration several minutes just before sunrise. There are only a few reports evaluating the effects of religious fasting on tear parameters and intraocular pressure (IOP) in the literature.1–4 Hypothetically, fluid restriction during day time From the Department of Ophthalmology, Selcuk University Faculty of Medicine, Konya, Turkey. The authors have no funding or conflicts of interest to disclose. Address correspondence to Bengu Ekinci Koktekir, M.D., Selcuk Universitesi, Tip Fakultesi Goz Hastaliklari AD, 42050, Selcuklu, Konya, Turkey; e-mail: [email protected] Accepted April 25, 2014. DOI: 10.1097/ICL.0000000000000044
Eye & Contact Lens Volume 40, Number 4, July 2014
M.D.,
Sansal Gedik,
M.D.,
should reduce salivary and tear secretion, resulting in dry mouth and eye symptoms during the fasting period. Fortes et al.5 reported that the measurement of tear osmolarity might be useful for the assessment of whole-body hydration status. However, previous studies could not show such a decrease in tear secretion during the fasting period, which was explained with excessive fluid loading at the predawn meal.1,4 In the study by Kerimoglu et al.1 and Dadeya et al.,2 fasting was shown to decrease IOP in healthy subjects, whereas the study by Kayikcioglu et al.3 could not find such a correlation. Regarding the corneal and anterior chamber parameters, no alterations were found related to fasting during Ramadan.1–6 Tear osmolarity was suggested as the key driver for normal homeostasis in tear film dynamics, and increased level of osmolarity was found as a reliable indicator of dry eye syndrome.7 As dehydration is expected to happen during the fasting period, tear osmolarity may be an alternative method for the assessment of tear film functions and dynamics during Ramadan, which had not been studied previously. In this study, our aim was to evaluate the changes in the tear film parameters, corneal topography, and ocular aberrations during the fasting period in healthy subjects.
MATERIALS AND METHODS Twenty-nine eyes of 29 healthy men were enrolled into this prospective study. The mean age of the study group was 27.865.9 years (range, 20–47 years). The study adhered to the tenets of Declaration of Helsinki, and the study protocol was approved by the local ethical committee. All patients gave their informed consent to participate in the study. Only healthy men who had their last meals just before the sunrise were included to standardize the time of hunger and dehydration because the food and fluid consumption may vary remarkably among fasting people. The last meal taken before fasting might be in the evening before sleeping, in the night, or just before the sunrise. As tear parameters alter during lactation or menstruation periods, women were excluded. The patients having systemic diseases including diabetes mellitus, collagen tissue disease, migraine, thyroid disease, rosacea, diabetes insipidus, diarrhea, deficiency of vitamin A, or taking systemic medications including anticholinergics, beta-blockers, antidepressants, antihistamines, antiparkinsonians, or artificial hormones like androgens or estrogens were excluded from the study. Patients with ocular diseases including dry eye, blepharitis, and allergy were excluded. Previous ocular surgeries and contact lens use were other exclusion criteria. Cornea topographic parameters and Zernike polynomials with sixth order were measured with OPD Scan II (Nidek, Osaka, Japan), which is 239
Copyright @ Contact Lens Association of Opthalmologists, Inc. Unauthorized reproduction of this article is prohibited.
Eye & Contact Lens Volume 40, Number 4, July 2014
B. E. Koktekir et al. a combined placido disc corneal topography and aberrometry device. During this measurement, the subjects were told to fixate on the internal fixation light and to blink often until an image was acquired. The images with no distortions of the rings were processed and used for comparison. Five measurements were taken and averaged automatically. After measuring best-corrected visual acuity and slitlamp examination, tear osmolarity was measured using OcuSense TearLab osmometer (OcuSense Inc., San Diego, CA). The device was checked by the check cards to reconfirm calibration at the start of each test session. Disposable kits were placed on hand pieces of the device that were used to take the osmolarity readings from the tear meniscus on the lower lid. During the measurement, the lower eyelid was not pulled down but kept in its natural position. Tear film function tests included reflex tear secretion by Schirmer I test, fluorescein tear film break-up time (TBUT), and a Lissamine green staining (LGS) test. Schirmer I test was performed by inserting a Schirmer tear test sterile strip into the inferior fornix, at the junction of middle and lateral third of the lower eyelid margin, for 5 min while the eyes were closed without topical anesthesia. Tear film BUT was measured by instilling 1 drop of 2% sodium fluorescein into the inferior fornix and determining the duration of time required for the first area of tear film break-up using cobalt blue filter with slitlamp biomicroscopy. For the assessment of lissamine staining test (Oxford grading scores), the cornea and temporal and nasal regions of the conjunctiva were scored individually from 0 to 3 using the van Bijsterveld score.8 The higher scores indicated worse ocular surface damage. Ocular surface disease index (OSDI) scoring was also determined for each patient with a modified form that was adjusted for the Turkish population.9 The OSDI questionnaire was used to quantify the impact of dry eye on quality of life.10 This questionnaire includes three subscales: ocular discomfort including symptoms of gritty or painful eyes, functioning to measure limitation of daily activities including reading or working on computer, and environmental triggers to evaluate the impact of environmental triggers such as wind or drafts on dry eye. The questions were asked with reference to 1-week recall period. Intraocular pressure (by Goldmann applanation tonometer) was measured in all patients. The first measurements were taken 2 weeks before Ramadan in the nonfasting period at 4.00 to 5.00 PM in the afternoon. The time interval from the last meal and last water intake and the amount of water intake (as liters) was also recorded for each patient. All of the measurements were repeated in the first week of Ramadan between 4.00 and 5.00 PM, approximately at the 12 hr of fasting. All the examinations were performed in the same room by the same examiner. Only one measurement was taken for each test during nonfasting and fasting periods. The statistical analysis was performed using SPSS (version 17.0; SPSS Inc., Chicago, IL). As the parameters showed normal distribution according to Kolmogorov and Smirnov method, paired sample t test was used to compare the measurements taken in nonfasting and fasting periods. The variance reported on the data was shown as mean6SD. A P value of 0.05 or lower was accepted as statistically significant.
RESULTS The duration of hunger and dehydration were approximately 3 and 12 hr in nonfasting and fasting periods, respectively. The mean 240
consumption of water during nonfasting and fasting periods were recorded as 1.6360.96 L (0.6–4.0 L) and 2.4360.93 L (1.064.0 L), respectively. There was a significantly increased water intake during the Ramadan fasting period (P,0.001). The mean tear osmolarity values were measured as 285.668.2 mOsm/L and 293.3616.0 mOsm/L, whereas the mean Schirmer I values were 14.866.0 mm and 10.665.3 mm in nonfasting and fasting periods, respectively. Tear osmolarity, OSDI, and Oxford grading scores significantly increased during the fasting period compared with the nonfasting period (P=0.02, P=0.002, and P=0.003, respectively), whereas Schirmer I values decreased (P,0.001) (Table 1). Although the total amount of fluid consumed by each individual increased during fasting in our study, we expected a hyperosmolar state, which was confirmed with the finding of increased tear osmolarity levels after a fluid restriction of 12 hr. None of the patients had osmolarity values above 308 mOsm/L in the nonfasting period, whereas osmolarity increased remarkably above 308 mOsm/L in 4 patients during fasting. When these 4 patients were evaluated individually, Schirmer test scores were significantly lower and OSDI scores were found significantly higher during the fasting period. Intraocular pressure measurements during nonfasting and fasting periods were found as 13.663.0 mm Hg (9–21 mm Hg) and 12.062.3 mm Hg (6–16 mm Hg), respectively, which was statistically significant (P=0.001). There were no significant differences in TBUT (mean TBUT was 8.061.9 and 7.262.1 for nonfasting and fasting periods, respectively; P=0.08) and corneal topography values including Sim K1 and Sim K2, amount of astigmatism, and ocular aberrations obtained by Zernike polynomials. The correlation of the water intake with tear osmolarity during nonfasting and fasting periods was also assessed. Pearson correlation coefficient was found as 20.371 (P=0.05) during nonfasting and interpreted as moderately negatively correlated, whereas this correlation was low during fasting (Pearson correlation coefficient=0.076, P=0.678) (Fig. 1). The correlation of water intake during fasting and the amount of osmolarity difference between 2 time periods was also low (Pearson correlation coefficient=0.086) (Fig. 2). The correlations of tear osmolarity values with TBUT, conjunctival staining with lissamine green, and OSDI scores was low both TABLE 1.
Measurements of Tear Osmolarity and Tear Film Function Tests During Nonfasting and Fasting Periods
Osmolarity (mOsm/L) Mean6SD Range Tear break-up time (sn) Mean6SD Range Lissamine staining (Oxford score) Mean6SD Range Schirmer I test (mm) Mean6SD Range Ocular Surface Disease Index score Mean6SD Range
Nonfasting Period
Fasting Period
285.668.2 276–306
293.3616.0 275–346
0.02
8.061.9 5–12
7.262.1 3–10
0.08
0.0 0–0
0.2860.45 0–1
0.003
14.866.0 4–25
10.665.3 3–20
,0.001
30.0618.8 0–70.8
35.6616.4 0–68.7
0.007
P
Bold values are significant.
Eye & Contact Lens Volume 40, Number 4, July 2014
Copyright @ Contact Lens Association of Opthalmologists, Inc. Unauthorized reproduction of this article is prohibited.
Eye & Contact Lens Volume 40, Number 4, July 2014
FIG. 1. Scatter diagram demonstrating correlation of water intake and tear osmolarity during the nonfasting period.
in nonfasting (r=20.27, r=20.29, and r=20.03, respectively) and fasting periods (r=20.26, r=20.01, and r=20.01, respectively) (P.0.05, for all). However, the correlations of tear osmolarity values with Schirmer I tests were found to be moderate in both nonfasting and fasting periods (r=20.41 and r=20.39, respectively; P=0.02, for both). There was poor negative correlation between nonfasting and fasting tear osmolarity values (r=20.218, P=0.52).
DISCUSSION Ramadan is a time of spiritual reflection, improvement, and increased devotion and worship in Islamic belief. The fasting begins at dawn and ends at sunset. Muslims abstain from eating, drinking, sexual relations, and generally sinful speech and behavior for several hours. Fluid abstinence during religious fasting might reduce salivary and tear secretion resulting in dry mouth and eye symptoms. However, previous studies could not confirm such an
FIG. 2. Scatter diagram demonstrating correlation of water intake and tear osmolarity during the fasting period.
© 2014 Contact Lens Association of Ophthalmologists
Tear Film During Religious Fasting association between religious fasting and dry eye.1,4 Kerimoglu et al.1 found no changes in reflex and basal tear measurements values in the 13 hr of hunger during the fasting period. Kayikcioglu et al.4 also showed that religious fasting in the winter season did not seem to affect basal tear secretion and BUT values in healthy individuals. They concluded that fasting people drink considerable amount of water compared with nonfasting people in a limited period between sunset and dawn, and a significant amount of this water intake occurs at the predawn meal just before the sunrise, which seems analogous to water loading and prevents a significant decrease in tear secretion. In this study, tear film parameters were evaluated by several different methods, including tear osmolarity, fluorescein TBUT, LGS (Oxford score), and reflex tear production with Schirmer I test. The OSDI was calculated for each patient to assess the subjective complaints. Tear secretion was reduced and OSDI scores increased after 13 hr of fasting. Mean tear osmolarity was 285.668.2 mOsm/L within a range of 276 to 306 mOsm/L before Ramadan, which increased to 293.3616.0 mOsm/L (275–346 mOsm/L) after 13 hr of fasting. In the study of Lemp et al.,11 the tear osmolarity has been proposed as a best diagnostic method with a ROC curve of 0.89. Tear osmolarity was found to have superior diagnostic performance (with 73% sensitivity and 93% specificity at a cutoff of 312 mOsm/L) compared with tear BUT, corneal staining, conjunctival staining, Schirmer test, and meibomian gland grading. In the study of Versura et al., 12 the cutoff point was given as 308 mOsm/L in people with severe dry eye. In the study of Moore et al.,13 tear osmolarity level above 308 mOsm was accepted as hyperosmolarity. Fortes et al.5 investigated the effect of fluid restriction on tear osmolarity and found significant increase of tear osmolarity from 293 to 305 mOsm/L. The authors reported that tear osmolarity might be used for rapid assessment of hydration status. We have also found an increase from 285.668.2 mOsm/L during the nonfasting period to 293.3616.0 mOsm/L during the fasting period. Although the total amount of fluid consumed by each individual increased during fasting in our study, we expected a hyperosmolar state, which was confirmed with the finding of increased tear osmolarity levels after a fluid restriction of 12 hr. Moreover, when we accepted 308 as the cutoff point in tear osmolarity levels, we observed that 4 of 29 patients had undergone hyperosmolar state. In this study, Ramadan was in August, which is the most tropical summer month in Turkey and hot weather might be the reason for the observed drying effect, although the amount of fluid intake was remarkably higher during Ramadan month. The thin tear film layer accumulates in the upper and lower menisci and spread over the corneal epithelium by every blinking and plays an important role in optical quality. Ocular aberrations were reported to be negatively correlated with ocular tear film stability in previous studies.14–17 Patients with dry eyes have larger optical aberrations than normal eyes do, which was based on the surface irregularity of the cornea in dry eye patients.17 In this study, there was a slight increase in ocular aberrations after 13 hr of fasting; however, the differences were statistically not significant. Koh et al.14 investigated the dynamic changes in tear film in subjects with normal eyes and evaporative dry eyes using a wavefront sensor and optical coherence tomography and observed a significant difference between root mean square of dry eyes and normal eyes 241
Copyright @ Contact Lens Association of Opthalmologists, Inc. Unauthorized reproduction of this article is prohibited.
B. E. Koktekir et al. measured after each blink. In the study by Wang et al.,15 wavefront aberrations and visual acuity was proposed to be affected by tear film fluctuation. Montés-Micó et al.16 found that instillation of artificial tears has produced a significant decrease in total, spherical-like and coma-like aberrations. In this study, keratometry values did not differ before and after fasting, which was consistent with the study of Nowroozzadeh et al.,6 which showed no changes in the corneal topography readings between fasting and nonfasting periods. There are few reports in the literature regarding IOP changes during the fasting period. Kerimoglu et al.1 reported that there is a double response in IOP, including a rise in the morning because of predawn meal and more fluid intake and a decrease in the afternoon because of dehydration. Dadeya et al.2 measured IOP four times during the fasting day and found significant differences in all four measurements. Unlikely, Kayikcioglu et al.3 reported no change in IOP during the fasting period. We took only one measurement of IOP, which is in the afternoon, at the 12 hr of fasting and found a significant decrease during the fasting period compared with the nonfasting period. There are some limitations in this study. First, only 1 examination in the afternoon at the end of 12 hr fasting was performed; therefore, the diurnal changes in tear and IOP parameters could not be evaluated. Second, only male subjects were included because the measurements of women might be affected in case of lactation or menstruation; however, dry eye is a disorder that is more frequently observed in female subjects. Third, as the subjects are relatively young, tear film function tests and tear osmolarity might be less affected during fasting compared with elder population, which means that age-related alterations could not be evaluated. The last limitation is the measurement of one eye of each patient because of limited number of osmolarity test kits. In conclusion, fasting significantly decreases tear production and increases tear osmolarity; however, it does not deteriorate corneal topographic parameters and ocular aberrations in healthy subjects.
242
Eye & Contact Lens Volume 40, Number 4, July 2014 REFERENCES 1. Kerimoglu H, Ozturk B, Gunduz K, et al. Effect of altered eating habits and periods during Ramadan fasting on intraocular pressure, tear secretion, corneal and anterior segment parameters. Eye (Lond) 2010;24:97–100. 2. Dadeya S, Kamlesh, Shibal F, et al. Effect of religious fasting on intraocular pressure. Eye (Lond) 2002;16:463–465. 3. Kayikcioglu O, Guler C. Religious fasting and intraocular pressure. J Glaucoma 2000;9:413–414. 4. Kayikcioglu O, Erkin EF, Erakgun T. The influence of religious fasting on basal tear secretion and tear break up time. Int Ophthalmol 1999;22:67–69. 5. Fortes MB, Diment BC, Di Felice U, et al. Tear fluid osmolarity as a severe marker of hydration status. Med Sci Sports Exerc 2011;43:1590–1597. 6. Nowroozzadeh MH, Mirhosseini A, Meshkibaf MH, et al. Effect of Ramadan fasting in tropical summer months on ocular refractive and biometric characteristics. Clin Exp Optom 2012;95:173–176. 7. Srinivasan S, Nichols K. Collecting tear osmolarity measurements in the diagnosis of dry eye. Expert Rev Ophthalmol 2009;4:451–453. 8. van Bijsterveld OP. Diagnostic tests in Sicca syndrome. Arch Ophthalmol 1969;82:10–14. 9. Irkec MT; Turkish OSDI Study Group. Reliability and validity of Turkish translation of the Ocular Surface Disease Index (OSDI) in dry eye syndrome. Invest Ophthalmol Vis Sci 2007;48:E-Abstact 408. 10. Schiffman RM, Christianson MD, Jacobsen G, et al. Reliability and validity of the ocular surface disease Index. Arch Ophthalmol 2000;118:615–621. 11. Lemp MA, Bron AJ, Baudouin C, et al. Tear osmolarity in the diagnosis and management of dry eye disease. Am J Ophthalmol 2011;151:792–798. 12. Versura P, Profazio V, Campos EC. Performance of tear osmolarity compared to previous diagnostic tests for dry eye diseases. Curr Eye Res 2010; 35:553–564. 13. Moore JE, Vasey GT, Dartt DA, et al. Effect of tear hyperosmolarity and signs of clinical ocular surface pathology upon conjunctival goblet cell function in the human ocular surface. Invest Ophthalmol Vis Sci 2011;52: 6174–6180. 14. Koh S, Tung C, Aquavella J, et al. Simultaneous measurement of tear film dynamics using wavefront sensor and optical coherence tomography. Invest Ophthalmol Vis Sci 2010;51:3441–3448. 15. Wang Y, Xu J, Sun X, et al. Dynamic wavefront aberrations and visual acuity in normal and dry eyes. Clin Exp Optom 2009;92:267–273. 16. Montés-Micó R, Cáliz A, Alió JL. Changes in ocular aberrations after instillation of artificial tears in dry-eye patients. J Cataract Refract Surg 2004;30:1649–1652. 17. Montés-Micó R. Role of the tear film in the optical quality of the eye. J Cataract Refract Surg 2007;33:1631–1635.
Eye & Contact Lens Volume 40, Number 4, July 2014
Copyright @ Contact Lens Association of Opthalmologists, Inc. Unauthorized reproduction of this article is prohibited.
Effect of Religious Fasting on Tear Osmolarity and Ocular Surface Bengu Ekinci Koktekir,
M.D.,
Banu Bozkurt, M.D., Saban Gonul, and Suleyman Okudan, M.D.
Objective: To evaluate the effects of religious fasting on tear secretion, tear osmolarity, corneal topography, and ocular aberrations. Methods: This prospective controlled study comprised 29 eyes of 29 healthy men. Before ophthalmologic examination, all subjects underwent corneal topography by a placido disc corneal topography and aberrometry device (OPD Scan II). Tear osmolarity was measured using OcuSense TearLab osmometer. Ocular surface disease index (OSDI) scores, tear break-up time (BUT), Schirmer I test, and lissamine green staining were evaluated. The measurements taken before and during Ramadan at the same hours between 4.00 and 5.00 PM were compared using paired sample t test, and a P value less than 0.05 was accepted as statistically significant. Results: The mean age of the study group was 27.865.9 years (range, 20–47 years). The mean tear osmolarity values were measured as 285.668.2 mOsm/L and 293.3616.0 mOsm/L, whereas the mean Schirmer I values were 14.866.0 mm and 10.665.3 mm in nonfasting and fasting periods, respectively. Tear osmolarity, OSDI, and Oxford grading scores significantly increased (P=0.02, P=0.002, P=0.003, respectively), whereas Schirmer I values and intraocular pressure decreased (both, P,0.001) during the fasting period compared with the nonfasting period. There were no significant differences in tear BUT, keratometry values, and corneal aberration measurements between nonfasting and fasting periods (P.0.05, for all). Conclusion: Fasting significantly decreases tear production and increases tear osmolarity; however, it does not deteriorate corneal topographic parameters and ocular aberrations in healthy subjects. Key Words: Ramadan aberrations—Dry eye.
month—Fasting—Tear
osmolarity—Ocular
(Eye & Contact Lens 2014;40: 239–242)
R
amadan, the ninth month in the Islamic lunar calendar, is a month of obligatory daily fasting for the Muslims. Fasting begins at dawn and ends with the sunset, during which the Muslims refrain from consuming food, drinking liquids, and smoking. The fasting people usually eat some food and drink a considerable amount of fluid to endure the effects of hunger and dehydration several minutes just before sunrise. There are only a few reports evaluating the effects of religious fasting on tear parameters and intraocular pressure (IOP) in the literature.1–4 Hypothetically, fluid restriction during day time From the Department of Ophthalmology, Selcuk University Faculty of Medicine, Konya, Turkey. The authors have no funding or conflicts of interest to disclose. Address correspondence to Bengu Ekinci Koktekir, M.D., Selcuk Universitesi, Tip Fakultesi Goz Hastaliklari AD, 42050, Selcuklu, Konya, Turkey; e-mail: [email protected] Accepted April 25, 2014. DOI: 10.1097/ICL.0000000000000044
Eye & Contact Lens Volume 40, Number 4, July 2014
M.D.,
Sansal Gedik,
M.D.,
should reduce salivary and tear secretion, resulting in dry mouth and eye symptoms during the fasting period. Fortes et al.5 reported that the measurement of tear osmolarity might be useful for the assessment of whole-body hydration status. However, previous studies could not show such a decrease in tear secretion during the fasting period, which was explained with excessive fluid loading at the predawn meal.1,4 In the study by Kerimoglu et al.1 and Dadeya et al.,2 fasting was shown to decrease IOP in healthy subjects, whereas the study by Kayikcioglu et al.3 could not find such a correlation. Regarding the corneal and anterior chamber parameters, no alterations were found related to fasting during Ramadan.1–6 Tear osmolarity was suggested as the key driver for normal homeostasis in tear film dynamics, and increased level of osmolarity was found as a reliable indicator of dry eye syndrome.7 As dehydration is expected to happen during the fasting period, tear osmolarity may be an alternative method for the assessment of tear film functions and dynamics during Ramadan, which had not been studied previously. In this study, our aim was to evaluate the changes in the tear film parameters, corneal topography, and ocular aberrations during the fasting period in healthy subjects.
MATERIALS AND METHODS Twenty-nine eyes of 29 healthy men were enrolled into this prospective study. The mean age of the study group was 27.865.9 years (range, 20–47 years). The study adhered to the tenets of Declaration of Helsinki, and the study protocol was approved by the local ethical committee. All patients gave their informed consent to participate in the study. Only healthy men who had their last meals just before the sunrise were included to standardize the time of hunger and dehydration because the food and fluid consumption may vary remarkably among fasting people. The last meal taken before fasting might be in the evening before sleeping, in the night, or just before the sunrise. As tear parameters alter during lactation or menstruation periods, women were excluded. The patients having systemic diseases including diabetes mellitus, collagen tissue disease, migraine, thyroid disease, rosacea, diabetes insipidus, diarrhea, deficiency of vitamin A, or taking systemic medications including anticholinergics, beta-blockers, antidepressants, antihistamines, antiparkinsonians, or artificial hormones like androgens or estrogens were excluded from the study. Patients with ocular diseases including dry eye, blepharitis, and allergy were excluded. Previous ocular surgeries and contact lens use were other exclusion criteria. Cornea topographic parameters and Zernike polynomials with sixth order were measured with OPD Scan II (Nidek, Osaka, Japan), which is 239
Copyright @ Contact Lens Association of Opthalmologists, Inc. Unauthorized reproduction of this article is prohibited.
Eye & Contact Lens Volume 40, Number 4, July 2014
B. E. Koktekir et al. a combined placido disc corneal topography and aberrometry device. During this measurement, the subjects were told to fixate on the internal fixation light and to blink often until an image was acquired. The images with no distortions of the rings were processed and used for comparison. Five measurements were taken and averaged automatically. After measuring best-corrected visual acuity and slitlamp examination, tear osmolarity was measured using OcuSense TearLab osmometer (OcuSense Inc., San Diego, CA). The device was checked by the check cards to reconfirm calibration at the start of each test session. Disposable kits were placed on hand pieces of the device that were used to take the osmolarity readings from the tear meniscus on the lower lid. During the measurement, the lower eyelid was not pulled down but kept in its natural position. Tear film function tests included reflex tear secretion by Schirmer I test, fluorescein tear film break-up time (TBUT), and a Lissamine green staining (LGS) test. Schirmer I test was performed by inserting a Schirmer tear test sterile strip into the inferior fornix, at the junction of middle and lateral third of the lower eyelid margin, for 5 min while the eyes were closed without topical anesthesia. Tear film BUT was measured by instilling 1 drop of 2% sodium fluorescein into the inferior fornix and determining the duration of time required for the first area of tear film break-up using cobalt blue filter with slitlamp biomicroscopy. For the assessment of lissamine staining test (Oxford grading scores), the cornea and temporal and nasal regions of the conjunctiva were scored individually from 0 to 3 using the van Bijsterveld score.8 The higher scores indicated worse ocular surface damage. Ocular surface disease index (OSDI) scoring was also determined for each patient with a modified form that was adjusted for the Turkish population.9 The OSDI questionnaire was used to quantify the impact of dry eye on quality of life.10 This questionnaire includes three subscales: ocular discomfort including symptoms of gritty or painful eyes, functioning to measure limitation of daily activities including reading or working on computer, and environmental triggers to evaluate the impact of environmental triggers such as wind or drafts on dry eye. The questions were asked with reference to 1-week recall period. Intraocular pressure (by Goldmann applanation tonometer) was measured in all patients. The first measurements were taken 2 weeks before Ramadan in the nonfasting period at 4.00 to 5.00 PM in the afternoon. The time interval from the last meal and last water intake and the amount of water intake (as liters) was also recorded for each patient. All of the measurements were repeated in the first week of Ramadan between 4.00 and 5.00 PM, approximately at the 12 hr of fasting. All the examinations were performed in the same room by the same examiner. Only one measurement was taken for each test during nonfasting and fasting periods. The statistical analysis was performed using SPSS (version 17.0; SPSS Inc., Chicago, IL). As the parameters showed normal distribution according to Kolmogorov and Smirnov method, paired sample t test was used to compare the measurements taken in nonfasting and fasting periods. The variance reported on the data was shown as mean6SD. A P value of 0.05 or lower was accepted as statistically significant.
RESULTS The duration of hunger and dehydration were approximately 3 and 12 hr in nonfasting and fasting periods, respectively. The mean 240
consumption of water during nonfasting and fasting periods were recorded as 1.6360.96 L (0.6–4.0 L) and 2.4360.93 L (1.064.0 L), respectively. There was a significantly increased water intake during the Ramadan fasting period (P,0.001). The mean tear osmolarity values were measured as 285.668.2 mOsm/L and 293.3616.0 mOsm/L, whereas the mean Schirmer I values were 14.866.0 mm and 10.665.3 mm in nonfasting and fasting periods, respectively. Tear osmolarity, OSDI, and Oxford grading scores significantly increased during the fasting period compared with the nonfasting period (P=0.02, P=0.002, and P=0.003, respectively), whereas Schirmer I values decreased (P,0.001) (Table 1). Although the total amount of fluid consumed by each individual increased during fasting in our study, we expected a hyperosmolar state, which was confirmed with the finding of increased tear osmolarity levels after a fluid restriction of 12 hr. None of the patients had osmolarity values above 308 mOsm/L in the nonfasting period, whereas osmolarity increased remarkably above 308 mOsm/L in 4 patients during fasting. When these 4 patients were evaluated individually, Schirmer test scores were significantly lower and OSDI scores were found significantly higher during the fasting period. Intraocular pressure measurements during nonfasting and fasting periods were found as 13.663.0 mm Hg (9–21 mm Hg) and 12.062.3 mm Hg (6–16 mm Hg), respectively, which was statistically significant (P=0.001). There were no significant differences in TBUT (mean TBUT was 8.061.9 and 7.262.1 for nonfasting and fasting periods, respectively; P=0.08) and corneal topography values including Sim K1 and Sim K2, amount of astigmatism, and ocular aberrations obtained by Zernike polynomials. The correlation of the water intake with tear osmolarity during nonfasting and fasting periods was also assessed. Pearson correlation coefficient was found as 20.371 (P=0.05) during nonfasting and interpreted as moderately negatively correlated, whereas this correlation was low during fasting (Pearson correlation coefficient=0.076, P=0.678) (Fig. 1). The correlation of water intake during fasting and the amount of osmolarity difference between 2 time periods was also low (Pearson correlation coefficient=0.086) (Fig. 2). The correlations of tear osmolarity values with TBUT, conjunctival staining with lissamine green, and OSDI scores was low both TABLE 1.
Measurements of Tear Osmolarity and Tear Film Function Tests During Nonfasting and Fasting Periods
Osmolarity (mOsm/L) Mean6SD Range Tear break-up time (sn) Mean6SD Range Lissamine staining (Oxford score) Mean6SD Range Schirmer I test (mm) Mean6SD Range Ocular Surface Disease Index score Mean6SD Range
Nonfasting Period
Fasting Period
285.668.2 276–306
293.3616.0 275–346
0.02
8.061.9 5–12
7.262.1 3–10
0.08
0.0 0–0
0.2860.45 0–1
0.003
14.866.0 4–25
10.665.3 3–20
,0.001
30.0618.8 0–70.8
35.6616.4 0–68.7
0.007
P
Bold values are significant.
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Eye & Contact Lens Volume 40, Number 4, July 2014
FIG. 1. Scatter diagram demonstrating correlation of water intake and tear osmolarity during the nonfasting period.
in nonfasting (r=20.27, r=20.29, and r=20.03, respectively) and fasting periods (r=20.26, r=20.01, and r=20.01, respectively) (P.0.05, for all). However, the correlations of tear osmolarity values with Schirmer I tests were found to be moderate in both nonfasting and fasting periods (r=20.41 and r=20.39, respectively; P=0.02, for both). There was poor negative correlation between nonfasting and fasting tear osmolarity values (r=20.218, P=0.52).
DISCUSSION Ramadan is a time of spiritual reflection, improvement, and increased devotion and worship in Islamic belief. The fasting begins at dawn and ends at sunset. Muslims abstain from eating, drinking, sexual relations, and generally sinful speech and behavior for several hours. Fluid abstinence during religious fasting might reduce salivary and tear secretion resulting in dry mouth and eye symptoms. However, previous studies could not confirm such an
FIG. 2. Scatter diagram demonstrating correlation of water intake and tear osmolarity during the fasting period.
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Tear Film During Religious Fasting association between religious fasting and dry eye.1,4 Kerimoglu et al.1 found no changes in reflex and basal tear measurements values in the 13 hr of hunger during the fasting period. Kayikcioglu et al.4 also showed that religious fasting in the winter season did not seem to affect basal tear secretion and BUT values in healthy individuals. They concluded that fasting people drink considerable amount of water compared with nonfasting people in a limited period between sunset and dawn, and a significant amount of this water intake occurs at the predawn meal just before the sunrise, which seems analogous to water loading and prevents a significant decrease in tear secretion. In this study, tear film parameters were evaluated by several different methods, including tear osmolarity, fluorescein TBUT, LGS (Oxford score), and reflex tear production with Schirmer I test. The OSDI was calculated for each patient to assess the subjective complaints. Tear secretion was reduced and OSDI scores increased after 13 hr of fasting. Mean tear osmolarity was 285.668.2 mOsm/L within a range of 276 to 306 mOsm/L before Ramadan, which increased to 293.3616.0 mOsm/L (275–346 mOsm/L) after 13 hr of fasting. In the study of Lemp et al.,11 the tear osmolarity has been proposed as a best diagnostic method with a ROC curve of 0.89. Tear osmolarity was found to have superior diagnostic performance (with 73% sensitivity and 93% specificity at a cutoff of 312 mOsm/L) compared with tear BUT, corneal staining, conjunctival staining, Schirmer test, and meibomian gland grading. In the study of Versura et al., 12 the cutoff point was given as 308 mOsm/L in people with severe dry eye. In the study of Moore et al.,13 tear osmolarity level above 308 mOsm was accepted as hyperosmolarity. Fortes et al.5 investigated the effect of fluid restriction on tear osmolarity and found significant increase of tear osmolarity from 293 to 305 mOsm/L. The authors reported that tear osmolarity might be used for rapid assessment of hydration status. We have also found an increase from 285.668.2 mOsm/L during the nonfasting period to 293.3616.0 mOsm/L during the fasting period. Although the total amount of fluid consumed by each individual increased during fasting in our study, we expected a hyperosmolar state, which was confirmed with the finding of increased tear osmolarity levels after a fluid restriction of 12 hr. Moreover, when we accepted 308 as the cutoff point in tear osmolarity levels, we observed that 4 of 29 patients had undergone hyperosmolar state. In this study, Ramadan was in August, which is the most tropical summer month in Turkey and hot weather might be the reason for the observed drying effect, although the amount of fluid intake was remarkably higher during Ramadan month. The thin tear film layer accumulates in the upper and lower menisci and spread over the corneal epithelium by every blinking and plays an important role in optical quality. Ocular aberrations were reported to be negatively correlated with ocular tear film stability in previous studies.14–17 Patients with dry eyes have larger optical aberrations than normal eyes do, which was based on the surface irregularity of the cornea in dry eye patients.17 In this study, there was a slight increase in ocular aberrations after 13 hr of fasting; however, the differences were statistically not significant. Koh et al.14 investigated the dynamic changes in tear film in subjects with normal eyes and evaporative dry eyes using a wavefront sensor and optical coherence tomography and observed a significant difference between root mean square of dry eyes and normal eyes 241
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B. E. Koktekir et al. measured after each blink. In the study by Wang et al.,15 wavefront aberrations and visual acuity was proposed to be affected by tear film fluctuation. Montés-Micó et al.16 found that instillation of artificial tears has produced a significant decrease in total, spherical-like and coma-like aberrations. In this study, keratometry values did not differ before and after fasting, which was consistent with the study of Nowroozzadeh et al.,6 which showed no changes in the corneal topography readings between fasting and nonfasting periods. There are few reports in the literature regarding IOP changes during the fasting period. Kerimoglu et al.1 reported that there is a double response in IOP, including a rise in the morning because of predawn meal and more fluid intake and a decrease in the afternoon because of dehydration. Dadeya et al.2 measured IOP four times during the fasting day and found significant differences in all four measurements. Unlikely, Kayikcioglu et al.3 reported no change in IOP during the fasting period. We took only one measurement of IOP, which is in the afternoon, at the 12 hr of fasting and found a significant decrease during the fasting period compared with the nonfasting period. There are some limitations in this study. First, only 1 examination in the afternoon at the end of 12 hr fasting was performed; therefore, the diurnal changes in tear and IOP parameters could not be evaluated. Second, only male subjects were included because the measurements of women might be affected in case of lactation or menstruation; however, dry eye is a disorder that is more frequently observed in female subjects. Third, as the subjects are relatively young, tear film function tests and tear osmolarity might be less affected during fasting compared with elder population, which means that age-related alterations could not be evaluated. The last limitation is the measurement of one eye of each patient because of limited number of osmolarity test kits. In conclusion, fasting significantly decreases tear production and increases tear osmolarity; however, it does not deteriorate corneal topographic parameters and ocular aberrations in healthy subjects.
242
Eye & Contact Lens Volume 40, Number 4, July 2014 REFERENCES 1. Kerimoglu H, Ozturk B, Gunduz K, et al. Effect of altered eating habits and periods during Ramadan fasting on intraocular pressure, tear secretion, corneal and anterior segment parameters. Eye (Lond) 2010;24:97–100. 2. Dadeya S, Kamlesh, Shibal F, et al. Effect of religious fasting on intraocular pressure. Eye (Lond) 2002;16:463–465. 3. Kayikcioglu O, Guler C. Religious fasting and intraocular pressure. J Glaucoma 2000;9:413–414. 4. Kayikcioglu O, Erkin EF, Erakgun T. The influence of religious fasting on basal tear secretion and tear break up time. Int Ophthalmol 1999;22:67–69. 5. Fortes MB, Diment BC, Di Felice U, et al. Tear fluid osmolarity as a severe marker of hydration status. Med Sci Sports Exerc 2011;43:1590–1597. 6. Nowroozzadeh MH, Mirhosseini A, Meshkibaf MH, et al. Effect of Ramadan fasting in tropical summer months on ocular refractive and biometric characteristics. Clin Exp Optom 2012;95:173–176. 7. Srinivasan S, Nichols K. Collecting tear osmolarity measurements in the diagnosis of dry eye. Expert Rev Ophthalmol 2009;4:451–453. 8. van Bijsterveld OP. Diagnostic tests in Sicca syndrome. Arch Ophthalmol 1969;82:10–14. 9. Irkec MT; Turkish OSDI Study Group. Reliability and validity of Turkish translation of the Ocular Surface Disease Index (OSDI) in dry eye syndrome. Invest Ophthalmol Vis Sci 2007;48:E-Abstact 408. 10. Schiffman RM, Christianson MD, Jacobsen G, et al. Reliability and validity of the ocular surface disease Index. Arch Ophthalmol 2000;118:615–621. 11. Lemp MA, Bron AJ, Baudouin C, et al. Tear osmolarity in the diagnosis and management of dry eye disease. Am J Ophthalmol 2011;151:792–798. 12. Versura P, Profazio V, Campos EC. Performance of tear osmolarity compared to previous diagnostic tests for dry eye diseases. Curr Eye Res 2010; 35:553–564. 13. Moore JE, Vasey GT, Dartt DA, et al. Effect of tear hyperosmolarity and signs of clinical ocular surface pathology upon conjunctival goblet cell function in the human ocular surface. Invest Ophthalmol Vis Sci 2011;52: 6174–6180. 14. Koh S, Tung C, Aquavella J, et al. Simultaneous measurement of tear film dynamics using wavefront sensor and optical coherence tomography. Invest Ophthalmol Vis Sci 2010;51:3441–3448. 15. Wang Y, Xu J, Sun X, et al. Dynamic wavefront aberrations and visual acuity in normal and dry eyes. Clin Exp Optom 2009;92:267–273. 16. Montés-Micó R, Cáliz A, Alió JL. Changes in ocular aberrations after instillation of artificial tears in dry-eye patients. J Cataract Refract Surg 2004;30:1649–1652. 17. Montés-Micó R. Role of the tear film in the optical quality of the eye. J Cataract Refract Surg 2007;33:1631–1635.
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