August 1999
Volume 40, Issue 9
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Eye Movements, Strabismus, Amblyopia and Neuro-ophthalmology  |   August 1999
Dynamic Accommodation and Myopia
Author Affiliations
  • Helena M. Culhane
    From the Department of Optometry, University of Bradford, Richmond Road, Bradford, West Yorkshire, United Kingdom.
  • Barry Winn
    From the Department of Optometry, University of Bradford, Richmond Road, Bradford, West Yorkshire, United Kingdom.
Investigative Ophthalmology & Visual Science August 1999, Vol.40, 1968-1974. doi:https://doi.org/
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      Helena M. Culhane, Barry Winn; Dynamic Accommodation and Myopia. Invest. Ophthalmol. Vis. Sci. 1999;40(9):1968-1974. doi: https://doi.org/.

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Abstract

purpose. Accommodative effort during nearwork is thought to be a causative factor in the development of myopia. It has been proposed that an anomaly in autonomic control may be a precursor to the development of myopia. In the present study the closed-loop accommodation response after variations in fixation period was investigated in emmetropes, early-onset myopes and late-onset myopes to determine characteristics of reflex accommodation for each refractive group.

methods. Closed-loop accommodation responses were measured in a group of emmetropes (n = 7), early-onset myopes (n = 7), and late-onset myopes (n = 7) by use of a dynamic tracking infrared optometer. A variation in fixation period (10 seconds, 60 seconds, and 180 seconds) before an accommodative step was used to stimulate the accommodation control mechanism differentially.

results. Group results of accommodative response times showed that late-onset myopes were significantly affected by the duration of fixation before the change in stimulus vergence. Accommodative response times after 3 minutes of sustained near vision were significantly longer than those observed for other groups for the near-to-far condition. Reaction time appears to be independent of refractive grouping, prior fixation period, and direction of step change.

conclusions. Late-onset myopes showed significantly extended accommodation response times after a sustained near vision task that was demonstrable under well-controlled experimental conditions. The extended response times observed in the present study were consistent with previous reports of refractive shifts in late-onset myopes and early-onset myopes and provide a corollary between reflex and adaptive components of the accommodation response. Potential mechanisms are discussed in an attempt to explain the resultant hysteresis under closed-loop viewing conditions.

The association between sustained nearwork requiring high levels of ocular accommodation and the development of myopia has been well documented. 1 2 Epidemiologic studies have also shown a correlation between the amount of nearwork and the onset and subsequent progression of myopia. 3 4 As a result of these observations, the increased accommodative effort required during nearwork has been proposed as a causative factor in the development of myopia. However, the relationship between accommodative demand and myopia is complex, because there is invariably a link between the hereditary basis of myopia and environmental factors. Both genetic 5 and environmental considerations 6 may therefore influence the development of myopia, although the relative significance of each of these determinants remains uncertain. 
Animal 7 and human 8 studies indicate that myopia is caused by an increase in the axial component of the eye that is not neutralized by a concomitant change in corneal curvature. It has been suggested that corneal curvature and refractive error development are not related, because the cornea reaches adult curvature by the age of 3 years. 9 However, the exact nature of the structural changes that occur in the posterior segment of a myopic eye remains a matter of conjecture, with a number of models proposed. 10  
The development of myopia in the older eye generally has no clear hereditary basis 1 and provides an opportunity to identify the interaction between ocular accommodation and its environment, because the onset of myopia is usually associated with increased occupational demands. Although there is no consensus regarding the basis for development of myopia, there is increasing awareness that prolonged and frequent close work is associated with the type of myopia that emerges relatively late in life (>15 years). 1 11 This type of refractive error is classified as late-onset myopia (LOM), 12 which is generally assumed to be environmental in origin rather than caused by hereditary influences. 1 If performing sustained nearwork is a significant factor in the development of myopia, it should be possible to demonstrate variations in the characteristics of the accommodative response for different refractive groups. 
In the absence of visual cues the accommodation mechanism adopts an open-loop resting position that is known as tonic accommodation (TA). Several studies have used measures of TA to differentiate between refractive groups, because the open-loop accommodative level may indicate differences in the neurologic input to the ciliary muscle. 13 14 It has been shown that LOMs have a more distant TA than early-onset myopes (EOMs), emmetropes (EMMs), or hyperopes (HYPs). 13 The speed of accommodation regression back to a person’s TA subsequent to opening the accommodation loop has also been investigated. 15 The time course of regression has been used to specify the magnitude of accommodative adaptation or“ hysteresis” induced by a particular closed-loop task. 11 These measures of post-task open-loop adaptation have been used to provide an insight into the characteristics of ciliary muscle innervation for the closed-loop accommodative response. 11 13 14 15  
Variations in the accommodation response have also been reported between refractive groups under static closed-loop conditions. For example, myopic children have been shown to accommodate significantly less to real targets than emmetropic children. 16 Measurement of stimulus–response curves in university students showed that LOMs have a shallower stimulus–response gradient than EOMs, EMMs, and HYPs. 12 Significant differences among refractive groups have also been found in measures of amplitude of accommodation, with LOMs having the largest amplitude followed by EOMs, EMMs, and HYPs. 17  
Recent work has shown LOMs and EOMs to be significantly more susceptible to nearwork-induced transient myopia (0.36 D and 0.34 D, respectively) after a 10-minute period of sustained near vision than EMMs (0.09 D) or HYPs (0.01 D). 18 This nearwork-induced transient myopia was found to have a much slower decay back to the baseline distance refractive error in LOMs compared with EOMs (time constant: LOMs, 63 seconds; EOMs, 35 seconds). It is clear that myopes show increased adaptation under closed-loop conditions. However, the method used did not allow measurement of accommodation during the initial reflex blur-induced phase of the response. 18  
Few studies have been published on the characteristics of reflex closed-loop accommodation dynamics as a function of refractive group. 19 20 21 22 The results of these studies do not provide a consensus about refractive group–dependent effects on reflex dynamic accommodation. 
A refraction-dependent trend was reported for accommodative reaction times with HYPs (431 msec) demonstrating the longest time followed by MYPs (393 msec), and EMMs (327 msec). 19 Accommodative velocity was also found to be faster for EMMs (5.69 D/t) than either MYPs (2.84 D/t) or HYPs (1.47 D/t). 19 Conversely, it has been reported that accommodative reaction time is significantly increased in MYPs relative to HYPs and that the speed of the accommodative response is slower in MYPs in a sample of 128 students aged between 10 and 19 years. 20 Continuous ultrasonic biometry in 12 EMMs and 12 MYPs demonstrated that the response time for negative accommodation was faster than for positive accommodation in both EMMs and MYPs. 21 In addition, the response times for MYPs were faster than for EMMs for 2-D and 4-D stimulus steps, but slower for a 6-D stimulus step. In contrast, Schaeffel et al. 22 found no relation between accommodative peak velocity and refractive state in a sample of 19 subjects. The apparently contradictory findings may be caused in part by inappropriate classification of myopia (studies have tended to classify myopia as a single group irrespective of the age of onset or the state of progression 23 ) and differences in method among the studies. 
To demonstrate differences in reflex closed-loop accommodation, it is necessary to consider carefully the characteristics of the control system to allow suitable viewing conditions to be used. In the young accommodating eye the parasympathetic and sympathetic components of the autonomic nervous system provide the central and peripheral control processes that ensure the accuracy of the accommodation response. 2 Control of accommodation is mediated primarily by parasympathetic input to ciliary smooth muscle. 24 However, evidence exists supporting sympathetic innervation of ciliary muscle. 25 26 27 28 It has been proposed that a precursor to the development of myopia may be an anomaly in the autonomic control of near vision. 29  
Although several studies have identified differences in the characteristics of accommodation between refractive groups under open-loop conditions, there is no evidence to indicate that differences in reflex accommodation performance are observed under solely closed-loop dynamic conditions. Investigation of the temporal closed-loop accommodation response offers the opportunity to determine the characteristics of reflex accommodation for different refractive groups in the presence of variable external loads. 
The purpose of this study was to investigate the characteristics of reflex closed-loop accommodation after variations in prior fixation period for EMMs, EOMs, and LOMs. 
Methods
Twenty-one visually normal observers participated in the study. Observers were equally divided into three refractive groups: EMMs, spherical equivalent refractive error between −0.50 D and +0.50 D; EOMs, spherical equivalent refraction more than −0.50 D, age of onset before 14 years; and LOMs, spherical equivalent refraction more than− 0.50 D, age of onset 16 years or older. Mean age, spherical equivalent refraction, and gender division for each refractive group are shown in Table 1 . All subjects had corrected visual acuity of at least 6/6 in each eye and wore their habitual distance refractive correction throughout the experimental trials. 
Reflex dynamic accommodation was recorded monocularly (right eye) using a dynamic tracking continuously recording infrared optometer (Fourward Optical Technologies, San Marcos, TX). 30 The instrument tracks the horizontal and vertical position of the first Purkinje image to ensure that the optometer remains on-axis during recording of accommodation. Recordings of accommodation can be made with the optometer that are free from eye movement artifacts over a range of ±5°. The optometer has a resolution of 0.1 D and is based on the Scheiner principle. 30 The analogue output from the optometer was fed into a digital storage oscilloscope (model 1604; Gould, Cleveland, OH) which was connected to an online computer through an interface (IEEE-488). Continuous recording was performed at a sampling rate of 102.4 Hz. 
A three-dimensional visual stimulus deflector system was used to change the vergence of the accommodation stimulus. This Badal stimulus optometer allowed stimulus vergence to be modulated without changing stimulus size, position, or luminance by movement of a telecentric lens in the optical path. 31 The lens was controlled by a frequency generator which could be used to input square waves at a range of amplitudes and temporal frequencies. Subjects viewed a high-contrast photopic (30 candela (cd)/m2) Maltese cross through the Badal stimulus optometer. They were instructed to fixate on the intersection of the Maltese cross and to keep the stimulus clear during the experimental trials. 
In an attempt to stimulate differentially the components of the accommodation control system, three fixation times (10 seconds, 60 seconds, and 180 seconds) were used before the introduction of a 2-D step change in stimulus vergence. Stimuli were presented in 2-D vergence steps over a range of 2 to 4 D after fixation for one of the periods indicated above. The stimulus was placed at a vergence of 2 D or 4 D, which requires a significant parasympathetic effort. Because the sympathetic input is known to have an extended time course, 29 a range of fixation times is necessary if the contribution of this component of the aggregate response is to be considered. Approximately 60 observations were made per stimulus change for each fixation period to calculate individual and group mean reaction and response times. Individual subject data were collected over several experimental sessions to allow stimulus presentation to be randomized and to avoid crossover adaptation effects between fixation periods. 
Reaction and response times were calculated from the step data (Fig. 1) . Reaction time is defined as the period before a change in accommodation response level is observed after a change in stimulus vergence. 32 Response time is the period measured from the end of the reaction time to the point at which the accommodation response achieves a steady level. 32 Comparisons were made using multiple analysis of variance between refractive grouping, direction of motion—that is, far-to-near (2–4 D) or near-to-far (4–2 D) and fixation time before the introduction of a step in stimulus vergence. 
All experimental procedures conformed to the recommendations of the declaration of Helsinki. 
Results
Reaction Time
The means and standard deviations of the reaction times for each refractive group after the three prior fixation periods are shown in Table 2 . The LOMs showed a significant difference in reaction time for the far-to-near target modulations after 10 seconds’ prior fixation, compared with those recorded after 60 seconds’ (P = 0.013) and 180 seconds’ (P < 0.001) fixation. The EMMs and EOMs showed no significant interaction of reaction times with direction of target movement or prior fixation period. Overall, no significant difference was found between refractive groups for reaction time and prior fixation period. 
Response Times
The mean response times for each refractive group as a function of prior fixation period and target vergence modulation are shown in Table 3 . Typical accommodative traces are shown in Figure 2 for EMMs that are consistent with previous reports on accommodation dynamics 33 34 and for LOMs for 10 sec and 180 sec prior fixation period. There was a notable increase in response time in the LOMs for near-to-far changes in target vergence as the prior fixation period increased. The LOMs showed a significant time-dependent element in response times for near-to-far target modulation after 10 seconds’ and 60 seconds’ prior fixation compared with those recorded after 180 seconds (P < 0.001 and P = 0.001, respectively). The near-to-far response time recorded for LOMs after 180 seconds’ prior fixation is also significantly greater than the response time to the same experimental condition for both EMMs and EOMs. A significant difference also exists between response times for the LOMs to a near-to-far and far-to-near target modulation after 180 seconds’ prior fixation (P < 0.001). 
The EOMs showed a significantly shorter response time for far-to-near modulation after 10 seconds’ prior fixation compared with those recorded after 60 seconds and 180 seconds (P < 0.001 and P = 0.002, respectively) and also a significant difference in response times for near-to-far target modulation after 10 seconds’ and 180 seconds’ prior fixation (P = 0.014). The EMMs showed no significant interaction in response times with direction of target movement and prior fixation period. The relatively small sample inevitably reduced the power of the statistical analysis, yet significant differences were still shown. 
Figure 3 shows more clearly the variation in accommodative response times for the three fixation periods for each refractive groups for directional changes in target modulation. 
Discussion
Reaction and response times of the EMMs and EOMs in the present study, under monocular viewing conditions, are consistent with previous reports of accommodation dynamics in adults. 33 34 The reaction time is approximately 250 msec and appears to be independent of step direction and prior fixation period. Step changes in stimulus vergence for all refractive groups after fixation periods less than 1 minute produced a completed accommodation response in approximately 1 second, which is likely to be mediated by the fast-acting parasympathetic branch of the autonomic mechanism. 
Accommodation responses for LOMs were found to be significantly affected by the duration of fixation before the change in stimulus vergence. Responses after 10 seconds of fixation before the stimulus step were in the normal range of values and similar to those observed in EMMs and EOMs. However, the accommodative responses after the 3-minute task were significantly longer than those observed in the other refractive groups for the near-to-far condition, indicating an adaptive component to the response. 
The initial reflex accommodation response is driven by blur-induced changes that occur with step shifts in stimulus vergence. The accommodation control mechanism then acts to optimize retinal image contrast. Under closed-loop conditions this reflex action limits the potential for accommodative adaptation to a zone within the ocular depth-of-focus, 35 and any adaptation effect is therefore likely to be small in magnitude. In addition, the duration of post-task adaptation is short under closed-loop viewing until the necessity for feedback is removed. When the accommodation response falls within the envelope of the depth-of-focus, it may then be possible to identify the adaptive shift in the response. 18  
Under open-loop conditions there have been reports 13 36 indicating a significant magnitude of adaptation in LOMs after sustained near tasks, because the response is not constrained by retinotopic factors. However, natural viewing is a closed-loop activity, and it is therefore necessary to consider the potential for variation in control of accommodation for different refractive groups under habitual viewing conditions. 
Recent evidence suggests that closed-loop post-task adaptation after sustained near vision results in a small but significant shift in distance refractive error in both LOMs and EOMs, although different time constants between the groups were observed. 18 The post-task adaptation reported is within the normal ocular depth-of-focus 35 and represents a shift in the baseline distance refractive error after a rapid initial reflex accommodation response that acts to minimize retinal blur. The method and instrumentation used did not allow initial response times to be determined, because the sampling period was too long to record this aspect of accommodation. The small but significant refractive shift reported for LOMs and EOMs under closed-loop conditions is consistent with the extended response times observed in the present study, providing a corollary between the reflex and adaptive components of the accommodative response. 
Previous studies have been equivocal on the relationship between response dynamics and refractive error. 19 20 21 22 This may be in part because of inappropriate classification of refractive error but is likely to be confounded by the use of inappropriate or inconsistent fixation periods before the step in stimulus vergence. 19 20 21 22 A recent study 23 suggested that anomalies of accommodation associated with myopia may be analyzed more effectively by classifying myopia in terms of progression rather than in relation to age of onset. The LOMs in the present study were all progressing myopes, which may have facilitated a positive result. 
We have demonstrated that a relationship between response times and refractive error exists but is only evident under well-controlled experimental conditions. It is not clear whether the differences observed in reflex closed-loop responses represent a primary anomaly or merely occur as an indirect consequence of differences in accommodative gain. When TA is modeled by slow, leaky integrators, the reduced gain observed in myopes tends to lead to an increase in TA. 37 Open-loop hysteresis therefore represents a symptom of accommodation inaccuracy. The extended response times reported in the present study under reflex closed-loop conditions may represent an additional symptom of accommodative inaccuracy in LOMs. 
Correction of LOMs with lenses requires subjects to exercise a greater accommodative effort for near vision compared with the uncorrected state. Furthermore, the lag of accommodation at near is known to be greater in LOMs, 12 23 resulting in retinal defocus, which may be a myogenic factor. The process of active emmetropization has been shown to detect and compensate for focusing errors, but intervention may disrupt this mechanism. 38 The hysteresis that may occur with increased parasympathetic activity, in the absence of adequate inhibitory sympathetic activity and the effects of retinal defocus, may induce an additional increase in the level of manifest myopia. Recent mathematical modeling supports the development of myopia over a period when related to sustained nearwork. 39  
Post-task hysteresis has been reported previously 11 to be greater in LOM and is confirmed by the results of the present study. Sustained near vision requiring high levels of parasympathetic input should stimulate the inhibitory sympathetic mechanism 29 and prevent accommodative adaptation. It has been suggested that a deficit in inhibitory sympathetic innervation may be a factor that predisposes subjects to accommodative adaptation and may act as a precursor to the development of myopia. It is interesting to speculate that subjects in the LOM group may not have this inhibitory input and may therefore demonstrate adaptation under both open- and closed-loop stimulus conditions. 
The relationship between post-task hysteresis and the development of myopia is unknown, but the mechanism has to be related to the increase in vitreous chamber depth, because this component is the principal determinant of myopia. Previous evidence has been presented showing an increase in vitreous chamber pressure during accommodation in monkeys and humans. 40 The increase in intraocular pressure has been suggested to cause the increase in vitreous chamber depth and thus in axial myopia. 41 The extended duration of parasympathetic tone subsequent to prolonged nearwork, observed in the LOMs, 36 and the chronic accommodative hysteresis caused by slower response times may support this mechanism of axial elongation. In a study in kittens 42 it has been demonstrated that small chronic amounts of accommodation can cause axial elongation. 
It is clear that further investigations are required before any unambiguous conclusions can be drawn on potential precursors to and the mechanism of myopic development. Longitudinal studies on accommodation dynamics and adaptation combined with biometric data may provide further insight into the long-term consequences of sustained visual tasks. There is also a need to obtain a better understanding of the precise function and action of autonomic innervation in ocular accommodation, which may be achieved using pharmacological methods. 
 
Table 1.
 
Demographic and Clinical Data
Table 1.
 
Demographic and Clinical Data
Group Mean Age (y) Mean Spherical Equivalent Refraction (D) Gender
EMM 23.00 ± 2.65 +0.10 ± 0.33 1 Man, 6 women
EOM 22.43 ± 2.30 −4.50 ± 1.83 2 Men, 5 women
LOM 23.57 ± 1.90 −2.02 ± 0.96 4 Men, 3 women
Figure 1.
 
Typical accommodation trace for a far-to-near (2–4 D) step change in stimulus vergence illustrating reaction time (a) and response time (b).
Figure 1.
 
Typical accommodation trace for a far-to-near (2–4 D) step change in stimulus vergence illustrating reaction time (a) and response time (b).
Table 2.
 
Reaction Times for Each Refractive Group after Three Prior Fixation Periods
Table 2.
 
Reaction Times for Each Refractive Group after Three Prior Fixation Periods
Step Modulation EMM EOM LOM
10 sec 60 sec 180 sec 10 sec 60 sec 180 sec 10 sec 60 sec 180 sec
2–4D 0.25 ± 0.05 0.25 ± 0.02 0.25 ± 0.06 0.31 ± 0.03 0.24 ± 0.01 0.31 ± 0.14 0.18 ± 0.07 0.26 ± 0.11 0.32 ± 0.08
4–2D 0.22 ± 0.07 0.21 ± 0.06 0.20 ± 0.05 0.29 ± 0.09 0.22 ± 0.08 0.24 ± 0.02 0.21 ± 0.09 0.25 ± 0.09 0.19 ± 0.06
Table 3.
 
Response Times for Each Refractive Group as a Function of Prior Fixation Period
Table 3.
 
Response Times for Each Refractive Group as a Function of Prior Fixation Period
Step Modulation EMM EOM LOM
10 sec 60 sec 180 sec 10 sec 60 sec 180 sec 10 sec 60 sec 180 sec
2–4D 0.76 ± 0.18 1.00 ± 0.17 1.12 ± 0.39 0.95 ± 0.18 1.35 ± 0.14 1.28 ± 0.18 1.28 ± 0.10 1.28 ± 0.35 1.29 ± 0.39
4–2D 0.76 ± 0.16 1.10 ± 0.47 1.18 ± 0.37 0.93 ± 0.22 1.09 ± 0.38 1.19 ± 0.35 0.88 ± 0.20 1.34 ± 0.50 2.12 ± 0.28
Figure 2.
 
Typical accommodation traces for EMMs and LOMs after 10 (left) and 180 (right) seconds’ prior fixation for near-to-far (4–2 D) target modulation. Zero time indicates the introduction of a step change in stimulus vergence.
Figure 2.
 
Typical accommodation traces for EMMs and LOMs after 10 (left) and 180 (right) seconds’ prior fixation for near-to-far (4–2 D) target modulation. Zero time indicates the introduction of a step change in stimulus vergence.
Figure 3.
 
Mean response time for each refractive group for the three prior fixation periods (10, 60, and 180 seconds).
Figure 3.
 
Mean response time for each refractive group for the three prior fixation periods (10, 60, and 180 seconds).
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Figure 1.
 
Typical accommodation trace for a far-to-near (2–4 D) step change in stimulus vergence illustrating reaction time (a) and response time (b).
Figure 1.
 
Typical accommodation trace for a far-to-near (2–4 D) step change in stimulus vergence illustrating reaction time (a) and response time (b).
Figure 2.
 
Typical accommodation traces for EMMs and LOMs after 10 (left) and 180 (right) seconds’ prior fixation for near-to-far (4–2 D) target modulation. Zero time indicates the introduction of a step change in stimulus vergence.
Figure 2.
 
Typical accommodation traces for EMMs and LOMs after 10 (left) and 180 (right) seconds’ prior fixation for near-to-far (4–2 D) target modulation. Zero time indicates the introduction of a step change in stimulus vergence.
Figure 3.
 
Mean response time for each refractive group for the three prior fixation periods (10, 60, and 180 seconds).
Figure 3.
 
Mean response time for each refractive group for the three prior fixation periods (10, 60, and 180 seconds).
Table 1.
 
Demographic and Clinical Data
Table 1.
 
Demographic and Clinical Data
Group Mean Age (y) Mean Spherical Equivalent Refraction (D) Gender
EMM 23.00 ± 2.65 +0.10 ± 0.33 1 Man, 6 women
EOM 22.43 ± 2.30 −4.50 ± 1.83 2 Men, 5 women
LOM 23.57 ± 1.90 −2.02 ± 0.96 4 Men, 3 women
Table 2.
 
Reaction Times for Each Refractive Group after Three Prior Fixation Periods
Table 2.
 
Reaction Times for Each Refractive Group after Three Prior Fixation Periods
Step Modulation EMM EOM LOM
10 sec 60 sec 180 sec 10 sec 60 sec 180 sec 10 sec 60 sec 180 sec
2–4D 0.25 ± 0.05 0.25 ± 0.02 0.25 ± 0.06 0.31 ± 0.03 0.24 ± 0.01 0.31 ± 0.14 0.18 ± 0.07 0.26 ± 0.11 0.32 ± 0.08
4–2D 0.22 ± 0.07 0.21 ± 0.06 0.20 ± 0.05 0.29 ± 0.09 0.22 ± 0.08 0.24 ± 0.02 0.21 ± 0.09 0.25 ± 0.09 0.19 ± 0.06
Table 3.
 
Response Times for Each Refractive Group as a Function of Prior Fixation Period
Table 3.
 
Response Times for Each Refractive Group as a Function of Prior Fixation Period
Step Modulation EMM EOM LOM
10 sec 60 sec 180 sec 10 sec 60 sec 180 sec 10 sec 60 sec 180 sec
2–4D 0.76 ± 0.18 1.00 ± 0.17 1.12 ± 0.39 0.95 ± 0.18 1.35 ± 0.14 1.28 ± 0.18 1.28 ± 0.10 1.28 ± 0.35 1.29 ± 0.39
4–2D 0.76 ± 0.16 1.10 ± 0.47 1.18 ± 0.37 0.93 ± 0.22 1.09 ± 0.38 1.19 ± 0.35 0.88 ± 0.20 1.34 ± 0.50 2.12 ± 0.28
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