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A Physiological Model to Measure Effects of Age on Lenticular Accommodation and Spherical Aberration in Chickens

¹ From the School of Optometry, University of Waterloo, Waterloo, Ontario Canada; and the ² Department of Neuroscience, University of Pittsburgh, Pittsburgh, Pennsylvania.

	Abstract

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PURPOSE. To assess physiological accommodative function of intact intraocular lenses, as measured by focal length changes, in chickens of various ages.

METHODS. Eyes of white leghorn chickens, aged 0 days (hatchlings), 7 days, 14 days, 6 weeks, 1 year, and 2 years, were enucleated and the backs of the globes, except for the ciliary nerve and ganglion, were removed. The ciliary nerve and ganglion were suctioned into the tip of a suction electrode, and lenses were optically scanned before, during, and after accommodation. Accommodation was elicited by delivery of 30-Hz electrical pulses.

RESULTS. For all age groups, lenticular focal lengths for stimulated eyes were significantly shorter than for relaxed eyes, indicating that accommodation had been induced. Lenticular accommodative amplitudes decreased significantly with age, with reduced function occurring between 0 and 7 days and again between 14 days and 1 year. Although accommodation was associated with an increased spherical aberration in all age groups, the increase was significant only in some age groups.

CONCLUSIONS. Results showing reduction of lenticular accommodation concomitant with increasing age suggest that in spite of major differences in anatomy and physiology of the accommodative mechanism, chickens may become presbyopic. Results showing high amounts of nonmonotonic spherical aberration in hatchling lenses suggest inherently poor optics in these birds.

	Introduction

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The avian eye differs both anatomically and physiologically from human and other mammalian eyes. For example, in birds, the iris and ciliary muscles are striated. However, similar to those in mammals, avian ciliary muscles are innervated by postganglionic ciliary nerves, which themselves receive input from the parasympathetic oculomotor (III) nerve at the ciliary ganglion.¹ Most avian eyes undergo accommodation through direct manipulation of the lens, due in part to various evolutionary structural differences; the ciliary processes are much larger, and the diameter of the lens is augmented by the presence of a ring of columnar epithelial cells at the equatorial periphery called the annular pad. Lenses are soft and malleable, and the corneoscleral sulcus, which exists as a consequence of the scleral ossicles, permits a greater range of movement. Together, these structures make it possible for contraction of the ciliary muscle to directly squeeze the lens, resulting in changes to lenticular surface curvatures and an increase in refractive power. This configuration contrasts markedly with the typical mammalian (human) eye in which the accommodative mechanism is indirect. Specifically, the effect of contraction of the ciliary muscle is transmitted indirectly to the lens through relaxation of suspensory ligaments.

Although it has been well established that the lens plays a major role in vertebrate accommodation, its optical properties during accommodation have been difficult to assess, partly because the lens is located within the eye. Some investigators have examined the lens during accommodation using whole-field electrical stimulation,^{2 3 4} pharmacologic agents,⁵ and a zonule-stretching apparatus.⁶ But, because these artificial in vitro techniques involve detachment of the ciliary nerve, accommodation is elicited by means of a mechanism other than that which is present in vivo. Recent evidence shows that the chicken lens contains actin and myosin in addition to other contractile proteins, indicating that the lens may not play the passive role during accommodation that has been ascribed to it.⁷ Moreover, there is evidence showing that receptors for acetylcholine, a neurotransmitter that elicits contraction of skeletal muscle at neuromuscular junctions, are present in the lens.⁸ Although it is probable that acetylcholine is not involved in an active contraction of the lens, the potential for pharmacologic or whole-field electrical stimulation to directly affect lens in an unknown manner renders these methods inappropriate.

In a study by Glasser et al.,⁴ optical properties of the lens in vivo were examined during electrical stimulation of the Edinger-Westphal nucleus, the part of the brain that signals accommodation. Retinoscopy and keratometry were used to measure changes to the total power of the eye and to corneal curvatures, respectively, and therefore, lenticular optics was not directly measured but was instead, inferred. Moreover, because the lens was enclosed by the remainder of the eye, changes to optical quality of the lens during accommodation could not be measured. This study was undertaken to develop a physiological accommodation model with which optical changes to the intact chicken lens can be measured directly and concomitantly with accommodation that has been induced through a natural in vivo pathway—that is, by electrical stimulation of the ciliary nerve.

The cause of presbyopia, the decline in accommodation that is associated with age, is controversial, with a body of evidence showing that compromise to one, some, or all the individual accommodative components may play a role. A recent study by Priolo et al.⁹ shows significant change in chicken lens morphology with age. The in situ accommodation model described herein has therefore also been used to assess the effect of age on the functional optics and spherical aberration (SA) of the lens. The chicken is the ideal animal model with which to test optical properties of the lens during accommodation, because the chicken possesses a direct accommodation mechanism, as mentioned earlier.

	Methods

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White leghorn chickens (Gallus domesticus) were obtained on the day of hatching and were killed the same day (0 days) or after 7 days, 14 days, or 6 weeks. Chicks not immediately used were reared in stainless-steel chicken brooders for a maximum of 14 days. After 2 weeks, birds to be kept for 6 weeks were moved to a room with the floor covered with wood shavings. All chicks were fed chick starter and water ad libitum. Fluorescent lighting in the room was set to an artificial diurnal (14-hour light–10-hour dark) schedule. In addition, 1- and 2-year-old birds were obtained from the Poultry Research Center at the University of Guelph. All chickens were obtained and cared for according to the Guidelines of the Canadian Council on Animal Care and therefore their management adhered to the ARVO Statement for the Use of Animals in Ophthalmic and Vision Research.

Chickens were killed by decapitation and eyes were removed while submerged in oxygenated (95% O₂:5% CO₂) Tyrode’s saline (TS: 134 mM NaCl, 3 mM KCl, 20.5 mM NaHCO₃, 1 mM MgCl₂, 3 mM CaCl₂). The posterior portion of each globe was removed, except for a wedge containing the ciliary nerves and ganglion. Eyes were pinned to a washer (Sylgard; Dow Corning, Midland, MI) and were placed into a silicon base mold that formed the bottom of a chamber. The chamber was completed by fitting the base mold with a rectangularly shaped glass tube, with a second, smaller, open-ended tube attached to one of the glass piece walls. A handmade suction electrode, with silver chloride wires and various diameters of Tygon tubing tips to allow for a tight fit with the ciliary ganglion, was passed through the open-ended tube, and the ciliary ganglion was suctioned into the pipette tip. The rest of the open-ended tube was filled with petroleum jelly to act as a temporary plug. The chamber was filled with 8% (vol/vol) fetal bovine serum in TS to visualize the refracted beams and to neutralize the optical effects of the cornea.

Lenses were scanned using a redesigned scanning laser monitor.¹⁰ In brief, a low-power helium-neon laser beam was passed up through a small circular window at the bottom of the scanner, at various motor-controlled x–y coordinates from the center. The chamber, consisting of the mold and rectangular glass piece, and containing the eye, was placed in a slot above the laser, and beams were captured by digital cameras. Before scanning, the optical axis of the lens (beam vertical or slope of beam equal to 0) was determined by a computer program (ScanTox, ver. 1.4.48; Harvard Apparatus, Hollingston, MA) also responsible for controlling the position of the laser and for calculations of back vertex focal lengths (BVFLs). Eyes were scanned at various eccentricities from the optical axis, and BVFLs were recorded and stored on the computer. The back vertex for each lens was predetermined from a camera image.

For each eye, lenses were scanned before stimulation, with stimulation, then finally in a poststimulation relaxed state, and the data collected represented, respectively, the resting, accommodating, and recovering states of the eye. Stimulus pulses were typically 0.3 msec at 30 Hz, with current held between 0.1 and 0.15 mA for eyes from young chickens, or 10 times this current for 1- and 2-year-old chickens. These parameters were chosen on the basis of previous work¹¹ involving one of the authors. Measurements were made for maximal iridial contractions, as assessed by eye before scanning. Step sizes were selected to ensure that the number of beams passing through the eye was relatively consistent, regardless of age (or size) of the chicken. Step sizes were 0.10 mm, 0.13 mm, 0.15 mm, and 0.24 mm for 0-, 7-, and 14-day-old and 6-week-old chickens respectively, and 0.29 mm for both 1- and 2-year-old chickens (Table 1) . During collection of the data, the three most central rays were omitted to avoid spurious variability associated with sutures, areas of disruption where the lens fibers meet at the anterior and posterior poles.

	Results

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Effects of Age and Accommodation
Although eyes were scanned at consistent step sizes (see the Methods section and Table 1 ), within each age group, eyes showed a range of iridial aperture sizes, inherently, as well as associated with accommodation, which made variations in the number of eccentric points scanned across the lens difficult to control for (Table 1) . Comparison of beam number ranges shows that the range differences in younger chickens were at least double those of the 1- and 2-year old chickens (Table 1 , compare range of 12–18 in hatchlings to range of 12–14 in 1- and 2-year-olds). Nevertheless, the mean number of eccentric points scanned across the lens was more or less consistent with age, although this was not tested for. In relaxed eyes, both before and after stimulation, the mean number of beams passing through the pupil ranged from 13 to 16, with slightly lower means (13 and 14) in eyes from chickens 6 weeks old and older (Table 1) . During accommodation, the mean number of eccentric points was closer, ranging from 11 to 13. No trend was observed: The smallest means (11 and 12) occurred in eyes from hatchlings and 6-week-old chickens, respectively.

Without corrections for pupil size, the BVFLs in lenses from hatchling chicks before stimulation averaged to 19.76 ± 0.47 mm (SEM; Table 2 ). The mean BVFL decreased with accommodation, averaging 15.05 ± 0.51 mm, and then increased to 19.43 ± 0.47 mm in the poststimulus state. In 7-day-old chickens, the average BVFL in lenses was slightly longer, beginning at 20.28 ± 0.29 mm in the prestimulus state, decreasing to 17.02 ± 0.37 mm during accommodation, and increasing up to 20.09 ± 0.28 mm during the poststimulus state. In 14-day-old chickens, mean BVFLs were 23.27 ± 0.35 mm, 19.35 ± 0.35 mm, and 22.84 ± 0.33 mm, in eyes in the prestimulus, stimulated, and poststimulus states, respectively. BVFLs in 6-week-old chickens were much longer, with averages of 29.15 ± 0.37 mm, 25.55 ± 0.44 mm, and 28.94 ± 0.36 mm in the prestimulus, stimulated, and poststimulus states, respectively. In eyes from 1-year-old chickens, mean BVFLs were 30.22 ± 0.29 in eyes before stimulation, 28.89 ± 0.39 mm during accommodation, and 29.93 ± 0.27 mm after stimulus. In 2-year-old chickens, the BVFLs were slightly shorter, with means of 29.96 ± 0.51 mm, 28.58 ± 0.47 mm, and 29.72 ± 0.50 mm, in the prestimulus, stimulated, and poststimulus states, respectively.

View larger version (20K): [in this window] [in a new window]   Figure 1. Mean BVFLs (±SEM), adjusted for constant aperture size, of lenses from chickens aged 0, 7, and 14 days (d); 6 weeks (w); and 1 and 2 years (y), for each accommodative state. Some error bars are covered by points on the graph. Within each age group, mean BVFLs denoted by asterisks were significantly shorter than those not marked (P < 0.05; one-way repeated measures ANOVA with Bonferroni multiple-comparison test). Note age-associated increases in mean BVFLs.

Before assessment of lenticular accommodative function, all lenticular BVFLs were converted to diopters or vergences (assuming thin lens in water, n_w = 1.33; see the Methods section). Changes during accommodation were quantified by subtracting dioptric values of the prestimulated state from those of the stimulated state. Analysis of the accommodative amplitudes as a function of chicken age revealed an age-associated reduction in the mean amount of accommodation (Fig. 2) , an indication that chickens become presbyopic. Specifically, lenticular accommodation in hatchlings was significantly greater than in all other age groups, and means in 7- and 14-day-old chickens were significantly greater than in 1- and 2-year-old chickens (P = 0.000; one-way ANOVA with HSD Tukey test). The mean lenticular accommodative amplitude in 6-week-old chickens, at an intermediate level between that in 14-day-old chickens and those in 1- and 2-year-old chickens, was not significantly different from either group. Accommodative amplitudes observed during recovery, calculated by subtraction of dioptric values in the poststimulated state from those in the stimulated state, showed exactly the same trend (P = 0.000; one-way ANOVA with HSD Tukey test; data not shown).

View larger version (14K): [in this window] [in a new window]   Figure 2. Mean change in accommodation (±SEM), from prestimulus to stimulated state, as a function of age. Means denoted by the same letters are statistically similar (P > 0.05; one-way ANOVA with HSD Tukey test). Note reduction in the amount of accommodation concomitant with increasing age, with significant reductions occurring at 7 days and again at 1 year.

View larger version (25K): [in this window] [in a new window]   Figure 3. Mean BVFLs (±SEM) of lenses from young chickens aged (A) 0, (B) 7, and (C) 14 days, plotted as a function of eccentricity. Each data point represents a mean of a minimum of three values measured at that eccentricity. Lenses were optically scanned before (squares), during (triangles), and after (circles) stimulation. Note that for all accommodative states, hatchling lenses showed nonmonotonic SAs, whereas SAs were monotonic and clearly negative in lenses of 7- and 14-day-old chickens.

View larger version (21K): [in this window] [in a new window]   Figure 4. Mean BVFLs (±SEM) of lenses from older chickens aged (A) 6 weeks, (B) 1 year, and (C) 2 years, plotted as a function of eccentricity. Each data point represents a mean of a minimum of three values measured at that eccentricity. Lenses were optically scanned before (squares), stimulation (triangles), and after (circles) stimulation. Note reduced accommodative responses in 1- and 2-year old chickens.

View larger version (18K): [in this window] [in a new window]   Figure 5. Mean parabolic A-coefficient (±SEM) representing SAs in lenses from chickens aged 0, 7, and 14 days (d); 6 weeks (w); and 1 and 2 years (y). Some error bars are covered by points on the graph. Means denoted by asterisks were significantly greater than those of the same accommodative state from 1- and 2-year old chickens (P < 0.05; one-way ANOVA with HSD Tukey). Within each age group, means denoted by dots were significantly greater than those of the prestimulus state (P < 0.05; one-way repeated measures ANOVA with Bonferroni t-tests).

Given that a highly nonmonotonic SA can be an indication of poor optical quality, the degree of nonmonotonicity for each scan, defined herein as the variation from the expected BVFL defined by the best-fitting parabola, was calculated as the deviation or mean sum of squares, from its best-fitting parabola. To account for disparity in aperture size, nonmonotonicity was calculated for the same number of points,⁶ representing approximately 61% of the pupil diameter of a stimulated eye in all age groups (Fig. 6) . Use of a two-way repeated measures ANOVA revealed that nonmonotonic deviation was affected by both age (P = 0.000) and accommodation (P = 0.007), with significant interaction between the two factors (P = 0.000). Specifically, in all accommodative states, nonmonotonic deviations in hatchling lenses were significantly greater than in all other age groups (P < 0.05; one-way ANOVAs with HSD Tukey tests), an indication that lenticular optical quality in these hatchlings was inherently poor. Analysis of the degree of nonmonotonicity as a function of accommodation revealed an increase in hatchlings and 6-week-old chickens (P < 0.05; one-way repeated measures ANOVA with Bonferroni multiple-comparison test), an indication that accommodation was associated with worsening optical quality only in some age groups. Again, no trend was observed in accommodation-associated changes in deviation.

View larger version (17K): [in this window] [in a new window]   Figure 6. Mean deviation or nonmonotonicity (± SEM) in lenses from chickens aged 0, 7, and 14 days (d); 6 weeks (w); and 1 and 2 years (y). Some error bars are covered by points on the graph. Asterisks: significantly greater deviations compared with all other age groups (P < 0.05; one-way ANOVAs with HSD Tukey tests). Within each age group, means denoted by dots were significantly greater than those of the prestimulus state (P < 0.05; one-way repeated measures ANOVA with Bonferroni t-tests).

	Discussion

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To the best of our knowledge, this is the first study to show an adverse effect of age on lenticular accommodative function in chickens, with reduction in lenticular accommodation associated concomitantly with increasing age, a characteristic of presbyopia. Although age-matching of chickens to humans has not been analyzed, it must be noted that chickens are precocial birds, opening and using their eyes the day of hatching. Hens usually begin laying eggs by the end of 5 months, an indication that 1- and 2-year-old chickens may be comparable to middle-aged humans. Because chickens older than 2 years were not available, whether even older chickens would show further reduction in lenticular accommodation capability or an absence of accommodative response altogether, remains unknown. It should be noted that although lenticular accommodation was reduced in older chickens, it was not at an insignificant level. These chickens were still able to accommodate, just not to the extent that was possible by younger chickens. It should also be noted that the effect of age on corneal accommodation is not known.

As with humans, it is also difficult to determine the cause of presbyopia in chickens. Changes in the accommodative amplitude may be due to biophysical changes to the lens, weakening of the ciliary muscle, or both. It must be noted that hardening of the lens, whether due to changes in thickness or an increase in lenticular protein concentrations, would have an effect on the ciliary muscle, with requirements of greater ciliary muscle function. As reported herein, lenticular focal lengths in 2-year-old chickens were slightly shorter, although not significantly, than those in 1-year-old chickens, which raises an intriguing possibility that with more samples or with even older chickens, lenticular focal lengths would shorten with increasing age. Physiologically, this is possible if growth of the lens is accompanied by an increased protein accumulation, causing an increase in refractive index and/or thickening of the lens. If this were to occur, it would be an indication that the refractive index of the lens had increased and that the ciliary muscle could have been affected because of the increased effort required to squeeze a less flexible or thicker lens. It should be noted that in human eyes, the suspensory ligaments play an indirect role during accommodation, and therefore age-related changes to the ligaments could contribute to presbyopia. Given that this anatomic structure is not a component in avian accommodation, its contribution to the presbyopia observed in this study was eliminated. However, if presbyopia is a function of changes in lens consistency and/or ciliary muscle contractibility, then the avian model of presbyopia presented herein may have some relevance to human presbyopia.

The changes in accommodative amplitude in the current study correlate well with the results of Glasser et al.,⁴ which showed lenticular accommodative changes of approximately 10 D in 4-week-old birds. Estimates of the change in accommodation in 4-week-old chickens in the current study would fall somewhere between approximately 6 and 10 D (estimate from Fig. 2 ). Differences in dioptric values may be accounted for by variations in chicken strain and environments in which the chickens were raised. In their study, Glasser et al. suggested that the 10-D change in accommodation they observed was probably not the true extent of lenticular accommodation in the chick, because of backward movement of the lens, mediated by loss of intraocular pressure (IOP) and removal of the vitreous, and because they had previously measured greater accommodative amplitudes using 0.011% nicotine stimulation.

It remains unknown whether the arguments expressed by Glasser et al. held true in the current work. The degree of backward movement of the lens, if any, was not assessed. Thus, it is possible that backward movement of the lens occurred in the current experiments, caused by removal of the back of the globe. However, there were several differences in this study that may have helped to alleviate loss of IOP. Vitreous was not removed, and the eye was placed near the bottom of the chamber. Hence, some IOP may have been recovered by the volume of TS weighing down on the vitreous and, through it, on the lens. In addition, eyes from hatchlings underwent corneal accommodation (data not shown), which is an IOP-dependent process that requires 15 to 20 mm Hg IOP.¹³ Together, these observations suggest that in hatchling eyes at least, the minimum IOP criterion was met and that IOP loss was attenuated. Finally, it should be noted that BVFLs were measured for the maximum iridial contraction inducible by a physiological paradigm and that the great amount of accommodation observed pharmacologically may be an extremely artificial circumstance. Although the lens is capable of generating the amount of accommodation observed, this accommodative amplitude may not be observed naturally or in vivo.

As expected, resting lenticular focal lengths in young chickens increased as a function of age (Fig. 1) , presumably in association with axial elongation of the eye. However, these focal lengths, as reported herein, are slightly longer than those reported by Priolo et al.,⁹ who examined optical properties of excised chickens lenses in vitro as a function of age. This difference is probably attributable to the isolation of the lens in the previous study, where disruption of the anatomic structures supporting the lens in vivo causes changes to the shape of the lens. "Rounding up" of the lens once it has been free of its supporting anatomy has been shown by Glasser et al.⁴ In addition, a more recent and sensitive version of the scanning laser monitor was used in the current study, which may have contributed to the differences observed between the two studies. However, regardless of the differences, the patterns for lenticular focal length distribution as a function of age between the two studies are similar.

The finding that the hysteresis effect was significant only in 2-year-old chickens must be interpreted cautiously. It could be an indication that the lenticular function is detrimentally affected in older chickens. However, because poststimulus focal lengths were collected to ensure that stimulation of the ciliary had no optical or physiologically deleterious effects, the recovery time between the end of collecting data for stimulated eyes to the beginning of collection of poststimulus focal lengths was not controlled for. Presumably, longer recovery times would result in smaller differences between pre- and poststimulus focal lengths.

An advantage in the use of the physiological in vivo accommodation model described herein is its usefulness in directly measuring the effects of age and accommodation on lenticular SA. As reported, after 7 days, lenticular SAs became monotonic (Figs. 3 4 6) and negative, an observation that is in keeping with other reports.^{5 9} It should be noted that high amounts of negative SA may not necessarily result in poor vision, because the amount and type of SAs at the cornea currently remain unknown. However, although it is possible that the effects of the cornea may act to counter the negative SAs observed in the lens, it is less likely that the erratic nature and clearly high amount of nonmonotonicity exhibited by hatchling lenses, regardless of accommodative state (Figs. 3 6) , can be compensated for by the cornea. Taken together, the results indicate that the lens was not fully developed at this age.

It remains unclear whether the high degree of SAs observed in some stimulated lenses arose because of changes to the shape of the lens or because of changes to the refractive index of the lens. Given that focal lengths were measured for "distant" objects (collimated light), it may be expected that accommodation would be associated with degradation of optical quality. That the greatest increases in SA and degree of nonmonotonicity were observed in hatchlings may be related to the observation that hatchlings also showed the greatest accommodative ability. Although it must be noted that an age-associated trend was not observed for SA and nonmonotonicity, SAs in stimulated lenses were greater than in their unstimulated counterparts in all age groups, although only significantly so in some of the age groups.

Accommodation in some birds also includes a corneal component. In chickens and pigeons, changes to the cornea can account for up to half of the total amount of accommodation,¹⁴ whereas, in hooded mergansers, lenticular accommodation plays a dominant role,² especially when these diving ducks are in water and power from the cornea is neutralized. It must be noted that although the corneal contribution was not measured in this study, the cornea may play a significant role to chicken vision during accommodation. Whether its effect on SA, if it exists, is synergistic with the lens during accommodation, working to improve optical quality, or is deleterious is not known.

	Acknowledgements

 
The authors thank Trefford Simpson, Denise King, and Kelley Moran for helpful discussions; Trevor German, Robin Jones, and Andrew Nowinski for technical assistance and the staff at the University of Guelph Poultry Research Center.

	Footnotes

 
Supported by a grant from the Natural Sciences and Engineering Research Council of Canada (JGS) and an Ontario Graduate Scholarship (VC).

Submitted for publication June 11, 2001; revised August 24, 2001; accepted September 10, 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: Jacob G. Sivak, School of Optometry, University of Waterloo, 200 University Avenue West, Waterloo, Ontario, Canada N2L 3G1; jsivak{at}sciborg.uwaterloo.ca.

	References

Top Abstract Introduction Methods Results Discussion References

 

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3. Sivak, JG, Hildebrand, TE, Lebert, CG, et al (1986) Ocular accommodation in chickens: corneal versus lenticular accommodation and effect of age Vision Res 26,1865-1872[Medline][Order article via Infotrieve]
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5. Glasser, A, Howland, HC (1995) In vitro changes in back vertex distance of chick and pigeon lenses: species differences and the effects of aging Vision Res 35,1813-1824[Medline][Order article via Infotrieve]
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This Article Abstract Full Text (PDF) Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Choh, V. Articles by Meriney, S. D. Search for Related Content PubMed PubMed Citation Articles by Choh, V. Articles by Meriney, S. D.