Anterior segment changes with age and during accommodation measured with partial coherence interferometry

ARTICLE

Anterior segment changes with age and during accommodation measured with partial coherence interferometry Alexis Tsorbatzoglou, MD, PhD, Ga´bor Ne´meth, MD, Noe´mi Sze´ll, MD, Zsolt Biro´, MD, PhD, Andra´s Berta, MD, PhD, DSc

PURPOSE: To evaluate anterior segment alterations with age and during accommodation in different age groups. SETTING: Department of Ophthalmology, Medical and Health Science Center, University of Debrecen, Debrecen, Hungary. METHODS: Fifty-three subjects (101 normal eyes) were enrolled in this study and divided into 3 age groups: younger than 30 years (Group 1), between 31 years and 44 years (Group 2), and older than 45 years (Group 3). The total amplitude of accommodation was determined with a defocusing technique, and anterior segment measurements were performed by partial coherence interferometry. RESULTS: Group 1 comprised 32 eyes; Group 2, 37 eyes; and Group 3, 32 eyes. The total amplitude of accommodation decreased with age (P<.0001). With the target position at infinity, the lens thickness (LT) and anterior segment length (ASL) increased and the anterior chamber depth (ACD) decreased significantly with age (P<.0001). During accommodation in the youngest group, the mean change in LT was 36.3 mm/diopter (D) and in ACD, 26.7 mm/D. The mean accommodationinduced ACD change was 0.08 mm G 0.06 (SD) in Group 1, 0.064 G 0.087 mm in Group 2, and 0.03 G 0.06 mm in Group 3 (P Z .0004). The mean LT change during near fixation was 0.109 G 0.063 mm in Group 1, 0.103 G 0.136 mm in Group 2, and 0.006 G 0.05 mm in Group 3 (P<.0001). The mean ASL change during accommodation was 0.029 G 0.037 mm, 0.039 G 0.114 mm, and 0.023 G 0.051, respectively (P<.0001). CONCLUSIONS: In addition to forward movement of the anterior lens surface with age, the posterior surface moved backward. Alterations in LT and ACD sufficient for a unit of refractive power change during accommodation might be smaller than previously thought. Anterior shifting of the lens may also participate in the accommodative response. J Cataract Refract Surg 2007; 33:1597–1601 Q 2007 ASCRS and ESCRS

Accommodation is defined as a dynamic change in the overall refractive power of the eye during near fixation. Despite extensive investigations, the exact nature of human accommodation remains controversial. Helmholtz1 was the first to provide a comprehensive description of the accommodative mechanism. He proposed that during near fixation, ciliary muscle contraction relaxes the zonules around the entire lens equator. As a result of the release of zonular tension, the lens diameter decreases and the curvature of the anterior lens surface increases and moves forward, resulting in increased refractive power of the eye. Fincham2 showed that during accommodation the increase in lens thickness (LT) is greater than the Q 2007 ASCRS and ESCRS Published by Elsevier Inc.

decrease in anterior chamber depth (ACD), suggesting that the posterior lens surface moves backward with accommodation. However, recent alternative theories question the original concept of accommodation. Schachar3,4 postulates that ciliary muscle contraction causes relaxation of the anterior and posterior zonules only, while the equatorial zonules exert increased tension on the lens. This produces slight displacement of the lens equator toward the sclera, which flattens the peripheral lens surface and increases the curvature of the central anterior and posterior lens surfaces. Conversely, Coleman5,6 suggests the role of the pressure difference between the aqueous and vitreous body in the accommodative mechanism. Recent studies 0886-3350/07/$dsee front matter doi:10.1016/j.jcrs.2007.05.021

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suggest that changes in corneal curvature7,8 and eye elongation9,10 during near fixation also participate in the mechanism of accommodation. The age-related changes that underlie presbyopia are also not fully understood. Some studies suggest that hardening of the crystalline lens11,12 or an increase in lens thickness and diameter13 with age causes presbyopia. Others believe that the predominant cause is extralenticular, such as age-related changes in the angle of the zonular attachments to the lens,14 a decrease in ciliary body movement,15 or reduced elasticity of the choroid.16 Because of these unsolved questions, the topic of accommodation and presbyopia remains a focus of research. However, few studies in the literature,17–19 all with small sample sizes, have evaluated accommodation-induced changes in anterior segment parameters using partial coherence interferometry (PCI). At present, PCI is one of the most precise methods of biometric measurement.20,21 The purpose of our study was to evaluate anterior segment alterations with age and during accommodation in different age groups using PCI. SUBJECTS AND METHODS This single-center prospective study was performed at the Department of Ophthalmology, University of Debrecen, Hungary. After the nature of the procedures was fully explained, informed consent was obtained from the subjects. The research was conducted in accordance with the Declaration of Helsinki and the ethical standards of the local ethics committee. One hundred one normal eyes of 53 subjects were enrolled in the study. Subjects were divided into 3 age groups: younger than 30 years (Group 1), between 31 years and 44 years (Group 2), and older than 45 years (Group 3). Exclusion criteria were best corrected distance visual acuity worse than 20/20; refractive error greater than 1.00 diopter (D); anterior or posterior segment pathology; history of contact lens wear; medication that might affect pupil diameter; and history of ocular laser treatment, trauma, or eye surgery. The total amplitude of accommodation was measured with defocusing (minus-lenses-to-blur technique). With the contralateral eye occluded, subjects were asked to look

Accepted for publication May 25, 2007. From the Departments of Ophthalmology, Medical and Health Science Center, University of Debrecen (Tsorbatzoglou, Ne´meth, Berta), and Kene´zy Gyula Hospital (Sze´ll), Debrecen, and St. Imre Hospital (Biro´), Budapest, Hungary. No author has a financial or proprietary interest in any material or method mentioned. Corresponding author: Alexis Tsorbatzoglou, MD, Department of Ophthalmology, University of Debrecen, Nagyerdei Boulevard 98, H-4012 Debrecen, Hungary. E-mail: [email protected].

with the study eye at the smallest legible line on a standard illuminated distance visual acuity chart. Concave lenses were added in front of the distance correction in 0.25 D steps. The subjects reported when they could no longer see the smallest legible line in sharp focus. The minus lens power added over the distance correction was recorded as the amplitude of accommodation. Anterior segment measurements, such as ACD, LT, and anterior segment length (ASL Z ACD C LT), were performed with the ACMaster (Carl Zeiss) using the PCI method. All subjects were seated; the study eye was fixated on a defined target with the fellow eye occluded to prevent convergence movements during measurements. To correct spherical equivalent of refractive errors, internal corrective spherical lenses were positioned in the optical path, providing essentially emmetropic conditions for the procedure. The anterior segment parameters were measured first with target position at infinity, after which an internal 3.00 D minus lens was added for near fixation. Ten measurements were taken for the distance target and near target, and changes in the anterior segment parameters were calculated by subtracting the mean values measured during distance fixation from the mean values measured during accommodation. Statistical analysis was performed using MedCalc for Windows software (version 9.1.0.1). The data were indicated descriptively (means, standard deviations, medians, and interquartile ranges). The normality of the data was checked with the D’Agostino-Pearson test. Because the normality of the data was rejected (P!.05), a nonparametric test was used (Kruskal-Wallis). The associations between values were calculated with the Spearman rank correlation. A P value of 0.05 was considered significant.

RESULTS The mean age of the 53 subjects was 39.0 years G 12.7 (SD) (range 16 to 71 years). Group 1 comprised 32 eyes; Group 2, 37 eyes; and Group 3, 32 eyes. The mean refractive error was 0.05 G 0.13 D in Group 1, 0.03 G 0.32 D in Group 2, and C0.21 G 0.19 D in Group 3. The total amplitude of accommodation measured with the defocusing technique was 4.63 G 2.06 D, 2.9 G 2.9 D, and 0.69 G 0.46 D, respectively. The differences between groups were significant (P!.0001). Table 1 shows the anterior segment parameters with the target position at infinity. The anterior chamber was significantly deeper in Group 1 than in the other 2 groups (P!.0001). The baseline LT and ASL increased significantly with age (P!.0001 and P Z .002, respectively). Table 2 shows the alterations in anterior segment parameters induced by near fixation. The ACD changes during accommodation decreased with age (P Z .0004) (Figure 1). The LT changes induced by physiological accommodation also decreased with age (P!.0001) (Figure 2), as were the changes in ASL (P!.0001). Statistically significant correlations were detected between subject age and ACD shifts (r Z 0.332, P Z .001),

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Table 1. Anterior segment parameters with target position at infinity. Parameter ACD (mm) Mean G SD Median IR LT (mm) Mean G SD Median IR ASL (mm) Mean G SD Median IR

Group 1

Group 2

Group 3

3.578 G 0.278 3.632 0.323

3.324 G 0.277 3.347 0.375

3.242 G 0.23 3.283 0.364

3.776 G 0.188 3.778 0.281

4.04 G 0.269 4.109 0.397

4.313 G 0.237 4.385 0.233

7.355 G 0.279 7.402 0.412

7.364 G 0.211 7.394 0.372

7.556 G 0.237 7.562 0.382

P Value !.0001

!.0001

.002

ACD Z anterior chamber depth; ASL Z anterior segment length; IR Z interquartile range; LT Z lens thickness

LT changes (r Z 0.486, P Z .0001), and ASL alterations (r Z 0.327, P Z .001). DISCUSSION Measurement of the anterior segment parameters such as ACD, LT, and ASL is indispensable to understanding the mechanism of accommodation and development of presbyopia. These parameters can be measured with different techniques such as ultrasound (US) biometry, high-resolution magnetic resonance imaging, US biomicroscopy, Scheimpflug imaging, anterior segment optical coherence tomography, and PCI. Partial coherence interferometry has proved to be more precise in ocular biometry than standard US, and its reproducibility is excellent.20,21 We used the ACMaster for our PCI measurements. The device enables measurement of anterior segment parameters using physiological stimulus. Moreover, in contrast to US techniques, the

eye being measured accommodates during the procedure, off-axis measurement is impossible, and no corneal applanation is caused by direct contact. The crystalline lens changes during one’s lifetime, with the LT increasing and ACD decreasing.22–24 Our data correlate well with these facts. It is also known that the age-dependent thickening of the lens is mainly caused by the increase in the anterior and posterior cortical layers.23 In accordance with Dubbelman et al.,23 and contrary to Koretz et al.,22 we showed that the ASL also increases with age. This means that the increase in the axial thickness of the crystalline lens is greater than the decrease in ACD, suggesting that the posterior lens surface moves backward with age. In the present study, a mean increase in LT (0.109 mm) and a mean decrease in ACD (0.08 mm) were found in young subjects during accommodation using a 3.00 D target. Our results represent a 36.3 mm/D

Table 2. Changes in anterior segment parameters induced by physiological accommodation. Parameter ACD changes (mm) Mean G SD Median IR LT changes (mm) Mean G SD Median IR ASL changes (mm) Mean G SD Median IR

Group 1

Group 2

Group 3

P Value .0004

0.08 G 0.06 0.09 0.062

0.064 G 0.087 0.054 0.106

0.03 G 0.06 0.022 0.039 !.0001

0.109 G 0.063 0.119 0.085

0.103 G 0.136 0.091 0.157

0.006 G 0.05 0.014 0.034

0.029 G 0.037 0.018 0.027

0.039 G 0.114 0.008 0.053

0.023 G 0.051 0.006 0.023

!.0001

ACD Z anterior chamber depth; ASL Z anterior segment length; IR Z interquartile range; LT Z lens thickness

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0,3 0,2

mm

0,1 0,0 -0,1 -0,2 -0,3 16-30 YEARS

31-44 YEARS

45-71 YEARS

Figure 1. Anterior chamber depth changes induced by a 3.00 D stimulus integrated in the device. Box plots with medians (lines), interquartile ranges (boxes), ranges (whiskers), outliers (circles), and extreme values (squares) (P Z .0004).

mean change in LT and 26.7 mm/D mean change in ACD if we assume a linear relation per diopter of accommodation. The ACD alterations correlate well with the optical coherence tomography data of Baikoff et al.25 but are smaller than findings in previous studies.19,26–30 However, the ACD and LT changes in the other studies were mainly measured by methods that are less accurate than PCI. Our data suggest that the alterations in LT and ACD sufficient for a unit of refractive power change during accommodation are smaller than previously thought. However, one limitation of our study is that the true accommodative state of the fellow eye was not measured simultaneously. Therefore, we cannot distinguish accommodation from pseudoaccommodation, nor can we exclude the possibility that the 3.00 D stimulus did not result in 3.00 D true accommodative response, which may affect our results. 0,5 0,4 0,3

mm

0,2 0,1 -0,0 -0,1 -0,2 -0,3

16-30 YEARS

31-44 YEARS

45-71 YEARS

Figure 2. Lens thickness changes induced by a 3.00 D stimulus integrated in the device. Box plots with medians (lines), interquartile ranges (boxes), ranges (whiskers), outliers (circles), and extreme values (squares) (P!.0001).

The mean LT changes during accommodation using the 3.00 D target were 0.103 mm in subjects between 31 years and 44 years old and 0.109 mm in the youngest group. The similar alterations can be explained by the fact that the accommodative responses were similar in the 2 groups. Using 3.0 D stimulus, the accommodative effort was maximum in subjects between 31 years and 44 years and submaximum in the youngest subjects. (The accommodative amplitude measured with the defocusing technique was 2.90 D in Group 2 and 4.63 D in Group 1). Despite the similar LT changes, the ACD decreased to a smaller degree (62% of LT change) and ASL increased to a greater degree (38% of LT change) in the 31- to 44-year group than in the youngest group (ACD change 73% of LT change; ASL change 27% of LT change). Moreover, we found a small decrease in ACD (mean 0.03 mm) and ASL (mean 0.023 mm) during the accommodative effort in the oldest group, while the LT remained practically unchanged (mean 0.006 mm). Dubbelman et al.23 found that thickening of the crystalline lens during accommodation is mainly caused by thickening of the nucleus and that cortical layers do not play a role in the process. Their data also show that with accommodation, thickening of the nucleus is uniform. Despite symmetrical thickening of the nucleus, we found that the decrease in the ACD was greater than the increase in the ASL. These results can be explained by the hypothesis that the crystalline lens thickens and moves forward simultaneously during accommodation. In addition, Koeppl et al.18 found that pharmacologic ciliary muscle contraction in young eyes and presbyopic phakic eyes induces a forward shift of the lens. Vilupuru and Glasser31 report small forward movement of the midline of the lens in monkey eyes during Edinger-Westphal–stimulated accommodation. Dubbelman et al.23 found significant anterior movement of the human lens during accommodation. Their data also suggest that the forward movement of the lens contributes to the increase in refractive power of the human eye during near fixation. Moreover, we found that with age, the proportion of near fixation–induced anterior pole forward movement and posterior pole backward movement changed from 73% and 27%, respectively, to 62% and 38%, respectively, supporting the hypothesis that a decrease in anterior lens shift may participate in the mechanism of presbyopia. However, a previous study32 questioned the role of anterior shift of the crystalline lens during voluntary accommodation. Further studies are needed to measure the possible movement of the anatomical center of the crystalline lens during accommodation, investigate the amount of this anterior shift, and determine whether the shift is enough to cause a significant increase in refractive power.

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In conclusion, our data suggest that in addition to thickening of the anterior surface of the lens, the posterior surface also thickens and moves backward with age. We found that alterations in LT and ACD sufficient for a unit of refractive power change during accommodation might be smaller than previously thought. Our results suggest that forward movement of the lens also contributes to the increase in refractive power of the eye during physiological accommodation. We cannot exclude the possibility that a decrease in this forward lens shift plays a role in the mechanism of presbyopia. REFERENCES 1. Helmholtz H. Ueber die Accommodation des Auges. Albrecht von Graefes Arch Ophthalmol 1855; 1(2):1–74 2. Fincham EF. The mechanism of accommodation. Br J Ophthalmol Monogr Suppl 1937; 8 3. Schachar RA. Cause and treatment of presbyopia with a method for increasing the amplitude of accommodation. Ann Ophthalmol 1992; 24:445–447, 452 4. Schachar RA. Zonular function: a new hypothesis with clinical implications. Ann Ophthalmol 1994; 26:36–38 5. Coleman DJ. Unified model for accommodative mechanism. Am J Ophthalmol 1970; 69:1063–1079 6. Coleman DJ. On the hydraulic suspension theory of accommodation. Trans Am Ophthalmol Soc 1986; 84:846–868; Available at: http://www.pubmedcentral.nih.gov/tocrender.fcgi? iidZ124642; Accessed June 1, 2007 7. Pier scionek BK, Popio1ek-Masajada A, Kasprzak H. Corneal shape change during accommodation. Eye 2001; 15:766–769 8. Yasuda A, Yamaguchi T, Ohkoshi K. Changes in corneal curvature in accommodation. J Cataract Refract Surg 2003; 29:1297– 1301 9. Drexler W, Findl O, Schmetterer L, et al. Eye elongation during accommodation in humans: differences between emmetropes and myopes. Invest Ophthalmol Vis Sci 1998; 39:2140–2147 10. Mallen EAH, Kashyap P, Hampson KM. Transient axial length change during the accommodation response in young adults. Invest Ophthalmol Vis Sci 2006; 47:1251–1254 11. Heys KR, Cram SL, Truscott RJW. Massive increase in the stiffness of the human lens nucleus with age: the basis for presbyopia? Mol Vis 2004; 10:956–963; Available at: http://www. molvis.org/molvis/v10/a114; Accessed June 1, 2007 12. Glasser A, Campbell MCW. Biometric, optical and physical changes in the isolated human crystalline lens with age in relation to presbyopia. Vision Res 1999; 39:1991–2015 13. Strenk SA, Strenk LM, Koretz JF. The mechanism of presbyopia. Prog Retin Eye Res 2005; 24:379–393 14. Koretz JF, Handelman GH. How the human eye focuses. Sci Am 1988; 259:92–99 15. Tamm E, Croft MA, Jungkunz W, et al. Age-related loss of ciliary muscle mobility in the rhesus monkey; role of the choroid. Arch Ophthalmol 1992; 110:871–876 16. van Alphen GWHM, Graebel WP. Elasticity of tissues involved in accommodation. Vision Res 1991; 31:1417–1438

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17. Drexler W, Baumgartner A, Findl O, et al. Biometric investigation of changes in the anterior eye segment during accommodation. Vision Res 1997; 37:2789–2800 18. Koeppl C, Findl O, Kriechbaum K, Drexler W. Comparison of pilocarpine-induced and stimulus-driven accommodation in phakic eyes. Exp Eye Res 2005; 80:795–800 19. Bolz M, Prinz A, Drexler W, Findl O. Linear relationship of refractive and biometric lenticular changes during accommodation in emmetropic and myopic eyes. Br J Ophthalmol 2007; 91:360– 365 20. Vogel A, Dick HB, Krummenauer F. Reproducibility of optical biometry using partial coherence interferometry; intraobserver and interobserver reliability. J Cataract Refract Surg 2001; 27:1961–1968 21. Drexler W, Baumgartner A, Findl O, et al. Submicrometer precision biometry of the anterior segment of the human eye. Invest Ophthalmol Vis Sci 1997; 38:1304–1313 22. Koretz JF, Kaufman PL, Neider MW, Goeckner PA. Accommodation and presbyopia in the human eye – aging of the anterior segment. Vision Res 1989; 29:1685–1692 23. Dubbelman M, Van der Heijde GL, Weeber HA, Vrensen GFJM. Changes in the internal structure of the human crystalline lens with age and accommodation. Vision Res 2003; 43:2363–2375 24. Lege BAM, Haigis W, Neuhann TF, Bauer MH. Age-related behavior of posterior chamber lenses in myopic phakic eyes during accommodation measured by anterior segment partial coherence interferometry. J Cataract Refract Surg 2006; 32:999– 1006 25. Baikoff G, Lutun E, Ferraz C, Wei J. Static and dynamic analysis of the anterior segment with optical coherence tomography. J Cataract Refract Surg 2004; 30:1843–1850 26. Dubbelman M, van der Heijde GL, Weeber HA. Change in shape of the aging human crystalline lens with accommodation. Vision Res 2005; 45:117–132 27. Beauchamp R, Mitchell B. Ultrasound measures of vitreous chamber depth during ocular accommodation. Am J Optom Physiol Opt 1985; 62:523–532 28. Storey JK, Rabie EP. Ultrasoundda research tool in the study of accommodation. Ophthalmic Physiol Opt 1983; 3:315–320 29. Ostrin L, Kasthurirangan S, Win-Hall D, Glasser A. Simultaneous measurements of refraction and A-scan biometry during accommodation in humans. Optom Vis Sci 2006; 83:657–665 30. Ostrin LA, Glasser A. Comparisons between pharmacologically and Edinger-Westphal-stimulated accommodation in rhesus monkeys. Invest Ophthalmol Vis Sci 2005; 46:609–617 31. Vilupuru AS, Glasser A. The relationship between refractive and biometric changes during Edinger-Westphal stimulated accommodation in rhesus monkeys. Exp Eye Res 2005; 80:349–360 32. Glasser A. Accommodation: mechanism and measurement. Ophthalmol Clin North Am 2006; 19(1):1–12

First author: Alexis Tsorbatzoglou, MD, PhD Department of Ophthalmology, University of Debrecen, Debrecen, Hungary

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