Abstract
Purpose:
To record and evaluate the reliability parameters (fixation loss (FL) %, false positive (FP) %) and global indices (mean sensitivity (MS), mean deviation (MD), pattern standard deviation in dB) in three visual field test sessions within two weeks to assess the learning effect in normal healthy subjects and POAG patients and comparison of learning effect gender wise and age wise in primary open-angle glaucoma (POAG) patients.
Methods:
This study was a prospective observational study. An oculus visual field testing was done and analyzed in 30 eyes of POAG patients and 30 eyes of normal healthy subjects in three visits.
Results:
There were 16 (53.3%) males and 14 (46.6%) females in the POAG group and 16 (53.33%) males and 14 (46.66%) females in the normal healthy subject group. A significant difference in data change between each visit in FL, FP, MD, MS was found though the difference was more pronounced in the second visit than in the third visit. The pattern standard deviation does not change significantly in subsequent visits in both groups. Gender wise and age wise no significant difference was found in the POAG group.
Conclusion:
Significant improvement in reliability parameters and global indices with each subsequent visit in both the POAG group and normal patients signifies the importance of learning effect on these parameters and the need to perform at least three tests to get the baseline perimetry chart, especially in POAG patients, while in normal subjects, second perimetric result can be accepted. It was also concluded that the learning effect is not influenced by age and gender.
Keywords: Global indices, learning effect, perimetry, reliability parameters
Glaucoma is a group of diseases where there is cupping and atrophy of the optic nerve head (ONH) and loss of retinal ganglion cells that result in visual field loss and are frequently related to the level of intraocular pressure. The early detection of glaucoma is a vital objective in clinical management so that visual function and quality of life are preserved as the patients with early glaucoma often remain undiagnosed until progression to advanced stages.[1] Nearly half of glaucoma patients remain undiagnosed and half of the diagnosed patients have advanced glaucomatous changes at the time of diagnosis. Since the glaucoma-related vision loss is permanent, adequate treatment with follow-up monitoring can slow the progression and prevent blindness in most cases. Therefore, it becomes more important to increase reliability in our monitoring process with limited resources.
However, progression from first onset to significant loss of vision is slow, usually taking many years. Therefore, it is vital to be able to follow patient’s vision over time in order to detect and quantify changes.[2]
Presently, there are two categories of methods by which glaucoma is identified and monitored—structural and functional tests. Optic disc photography and structural tests like scanning laser tomography and optical coherence tomography (OCT) help to assess the changes in the structure of the retinal nerve fiber layer and/ONH that could indicate the damage.[3] The reasons are still unclear as to why the correlation between these measurements and patients’ vision is weak.[4] Therefore, recording patients’ functional vision accurately is essential for managing glaucoma and is now also the focus of glaucoma research.
Modern perimeters are capable of providing threshold estimates from a number of predefined test locations. So, it gets easy to detect visual field sensitivity losses by comparison of each individual’s point wise threshold sensitivity estimates with population of age-matched normal individuals.[5] Automated perimetry is the gold standard for glaucoma identification and monitoring. Its results have high measurement variability, which may be random or nonrandom. Uniform and good examination procedures should be used to produce usable recordings.[6] It is assumed that individual experience affects the results of perimetry, and it is still largely a subjective test that depends on a lot of factors such as reliability indices (fixation loss (FL), false positive (FP), and false negative parameters), which reflects the extent to which participant is compliant to given instruction. Learning is an important artifact in many psycho physical tests. Several studies have shown that healthy individuals,[7] glaucoma suspects, or confirmed glaucoma patients[8] can exhibit learning effects with repeated visual field test (VFT).[9,10] This effect was also found in short-wavelength automated perimetry,[11] flicker perimetry,[12] and frequency double perimetry.[13]
The possible factors related to learning effect have been studied such as age, race, gender, and previous experience.[14,15] Quite a few studies have been done to know the correlation of education with the learning effect.[16] Also, few recent studies have evaluated the association between the reliability indices and cognitive impairment in glaucoma patients. It stated that since the cognitive decline is associated with reduced Visual field (VF) reliability so screening of cognitive ability is important in the evaluation of VF progression in glaucoma patients.[17]
In our study, we evaluated the learning effect in VFT, so that we can determine as to how many VFT sessions should be administered to primary open-angle glaucoma (POAG) patients as well as normal subjects to get the appropriate baseline perimetry results. We compared the learning effect in POAG patients and normal healthy subjects in terms of improvement in reliability parameters and global indices in subsequent visits. Also, we compared the learning effect gender wise, i.e., males and females and age wise in <40 years and ≥40 years age group in POAG patients. Till now, no known study in the past has evaluated the comparison of learning effect in POAG and normal subjects in subsequent visits.
Our study aims to know the parameters which affected the learning experience of the population undergoing standard automated perimetry (SAP). Various studies were done in past to assess the learning effect in developed nations, but there have been no significant studies reflecting the assessment in developing nations like India, where resources are limited by financial constraints and reduced accessibility to tertiary eye care facilities. Due to the drastically increasing number of glaucoma cases, it becomes important to identify and monitor these cases efficiently so as to get optimum use of limited resources without affecting the quality of management.
Methods
The study was carried out at a tertiary care center in Prayagraj from December 2019 to December 2020, after seeking clearance from the institutional ethical committee.
Study design
This study was a prospective observational study done on POAG patients and normal healthy subjects. A total of 30 eyes of POAG patients and 30 eyes of normal healthy subjects were examined. POAG suspects were those whose fundus showed characteristic disc changes with or without an increase in intraocular pressure. Prior to enrollment for the study, proper consent was taken.
Selection of cases
Inclusion criteria: ▪An adult aged between 20 and 60 years with no previous threshold visual field tests done ▪No hearing or cognitive impairment ▪Best-corrected visual acuity (BCVA) of 6/9 or better in the eye to be studied.
Exclusion Criteria: ▪Unco-operative participants ▪BCVA < 6/9 ▪Pre-existing retinal pathology like diabetic or hypertensive retinopathy, venous occlusion, etc., ▪Pupillary diameter of less than 3 mm and more than 6 mm.
Baseline evaluation: All participants at the time of inclusion in study had undergone the baseline evaluation as complete systemic examination, detailed medical history, and ocular examination. The family history of glaucoma, treatment history, and educational status of participants was recorded.
Fundus examination for evaluation of optic disc and measurement of central corneal thickness by specular microscope was done. VFT was performed in all participants by Oculus Twinfield Version 3.18r925 using 24-2 glaucoma FAST threshold strategy. Visual field examination was done three times in any one of the eyes chosen randomly in participants of both groups of normal healthy subjects and POAG suspects, which fulfilled the inclusion criteria. The same software and machine parameters were used every time for both groups of participants. Also, all readings were taken at an almost similar time of day in the same environment in comfortable seating for participants by the same observer. Similar neutral instructions regarding proper visual field testing were given verbally in easy local language according to the participants’ level of education and understanding.
All particular details like age, sex, and refractive status were filled carefully. The constant supervision of participants undergoing perimetry was done by the same examiner. The fixation was maintained by the electronic eye fixation control system in perimeter throughout the test as the reliability of visual field largely depends on quality of eye fixation. All participants underwent SAP on glaucoma FAST threshold strategy on area 24-2 with target stimulus of iii, white on white with proper refractive correction. A record was kept on each visit which included FL%, FP%, mean sensitivity (MS), range of mean deviation (MD), and pattern standard deviation (PSD). The reliability of results was assessed after a thorough review of reliability and global indices for both healthy normal subjects and POAG patients. [Figs. 1 and 2]
Figure 1.
Visual field of a 54-year-old male with POAG: a) 1st visit, b) 2nd visit, and c) 3rd visit. Reliability indices and global indices, except pattern standard deviation, showed continuous improvement till the third visit
Figure 2.
Visual field of a 28-year healthy subject: a) 1st visit, b) 2nd visit, and c) 3rd visit. Reliability indices and global indices, except pattern standard deviation, showed continuous improvement till the second visit
We assessed the improvement in the mean of FL, FP, MS, MD, PSD in subsequent visits in all participants. We then evaluated POAG patients gender wise to know the difference in the learning effect of males and females. We assessed the learning effect age-wise into <40 years and >40 years of age groups in POAG patients.
The learning effect was assessed as the improvement in FLs and FP, which meant a decrease in FLs and FP along with an increase in MS and decrease in MD in subsequent VFT. We used paired t-test to know the improvement of parameters between visits 1 and 2 and between visits 2 and 3. We compared the learning effect in our study groups using P values to determine whether it was significant or not.
Statistical analysis
Statistical analysis was performed using IBM SPSS V 22.0 for window software. We used paired t-test to know the improvement of parameters between visits 1 and 2 and between visits 2 and 3. A P value of < 0.05 was considered significant.
Results
We had a total of 30 eyes from the POAG group and 30 eyes of normal healthy subjects. Changes in reliability parameters (mean FL, mean FP) and global indices (MS and mean PSD) were noted between each visit in both groups [Table 1]. Mean FL (%) values on visits 1–3 were 11.3 ± 5.6, 4.3 ± 4.8, and 0.7 ± 2.1, respectively, in POAG and 5.5 ± 5.9, 1.1 ± 2.7, and 0.4 ± 1.3, respectively, in healthy subjects. The mean FP values in POAG group were 7 ± 5.2, 2.7 ± 3.4, and 0.4 ± 1.2 and in healthy subject were 4.6 ± 5.6, 1.2 ± 3.2, and 0.9 ± 2.0, respectively, in three visits. The mean values of MS on visits 1, 2, and 3 were 20.5 ± 3.4, 22.5 ± 3.2, and 23.8 ± 2.8 in POAG and 25.07 ± 1.5, 27.6 ± 1.2, and 27.9 ± 1.3, respectively, in healthy subjects. Also mean values of MD for both POAG group and normal subjects in three visits were 11.1 ± 2,7, 9.2 ± 2.5, 7.8 ± 1.9, and 7.1 ± 0.8, 4.5 ± 0.8, 4.2 ± 0.8, respectively [Fig. 3]. Changes in the POAG group between each visit were significant and were more pronounced between the first and second visit, while in normal subjects, significant improvement was seen up to the second visit. We also found more significant changes in the POAG group as compared to normal healthy subject. Changes in mean PSD in the POAG group were 4.3 ± 1.0, 4.0 ± 0.7, and 3.7 ± 0.7, respectively, and in normal healthy subjects were 3.7 ± 0.8, 3.6 ± 0.6, and 3.6 ± 0.5, respectively, in three visits. Though changes in PSD were found in both the groups, the difference was not significant (<0.001).
Table 1.
Reliability parameters and global indices on visit 1, visit 2, and visit 3 in POAG and healthy subjects
| Parameters | Groups | Visit 1 | Visit 2 | Visit3 | Change in parameters between visit 3 and visit 1 (%) | P between visit 1 and 2 | P between visit 2 and visit 3 | P between visit 1 and visit 3 |
|---|---|---|---|---|---|---|---|---|
| Mean fixation loss | POAG | 11.3±5.6 | 4.3±4.8 | 0.7±2.1 | −10.6±5.4 | <0.0001 | 0.0001 | <0.0001 |
| Normal subject | 5.5±5.9 | 1.1±2.7 | 0.4±1.3 | −5.1±5.2 | <0.0001 | 0.07 | <0.0001 | |
| Mean false positive | POAG | 7±5.2 | 2.7±3.4 | 0.4±1.2 | −6.6±5.0 | <0.0001 | 0.0001 | <0.0001 |
| Normal subject | 4.6±5.6 | 1.2±3.2 | 0.9±2.0 | −3.6±4.7 | 0.001 | 0.6 | 0.0003 | |
| Mean of mean deviation | POAG | −11.1±2.7 | −9.2±2.5 | −7.8±1.9 | 3.2±1.8 | <0.0001 | <0.0001 | <0.0001 |
| Normal subject | −7.1±0.8 | −4.5±0.8 | −4.2±0.8 | 2.8±1.1 | <0.0001 | 0.1 | <0.0001 | |
| Mean of mean sensitivity | POAG | 20.5±3.4 | 22.5±3.2 | 23.8±2.8 | 3.2±1 | <0.0001 | <0.0001 | <0.0001 |
| Normal subject | 25.07±1.5 | 27.6±1,2 | 27.9±1.3 | 2.8±1.1 | <0.0001 | 0.10 | <0.0001 | |
| Mean pattern standard deviation | POAG | 4.3±1.0 | 4.0±0.7 | 3.7±0.7 | −0.6±1.1 | 0.06 | 0.8 | 0.3 |
| Normal subject | 3.7±0.8 | 3.6±0.6 | 3.6±0.5 | 0.04±0.8 | 0.46 | 0.55 | 0.4 |
Figure 3.
Bar diagram showed improvement in the mean of MD in subsequent visits in the POAG group, while in the normal healthy volunteer group, there was no improvement after visit 2
In the POAG group, total number of participants below 40 years were 12 (40%) and above 40 were 18 (60%). The mean age of <40 years was 29.8 ± 5.9 years and >40 years was 57.0 ± 4.9 years. The number of female participants was 14 (46.66%) and male participants was 16 (53.33%). We observed the changes in the mean of reliability parameter and global indices in both the genders but found no significant difference gender wise [Table 2]. We also observed the changes in these parameters in both the age groups (<40 years and >40 years) and did not find any significant difference [Table 3].
Table 2.
Changes in the mean of reliability parameters and global indices in subsequent visits in both gender participants of the POAG group
| Parameters | Female (n=14) | Male (n=16) | Gender-wise difference of change in v3-v1 P | ||||||
|---|---|---|---|---|---|---|---|---|---|
|
|
|
||||||||
| Data value | Data change in v3-v1 | V2-v1 P | V3-v2 P | Data | Data change v3-v1 | V2-v1 P | V3-v2 P | ||
| FL% | |||||||||
| FL 1 | 11.2±5.9 | 10.3±5.9 | 0.001 | 0.01 | 11.3±5.5 | 10.8±5.5 | <0.0001 | 0.004 | 0.8 |
| FL2 | 4.7±5.3 | 4.0±4.4 | |||||||
| FL3 | 0.9±2.4 | 0.5±2 | |||||||
| FP (%) | |||||||||
| FP1 | 7.5±5.0 | −7.2±4.7 | 0.005 | 0.03 | 6.5±5.4 | −6.0±5.3 | 0.02 | 0.02 | 0.5 |
| FP2 | 2.7±3.8 | 2.6±3.2 | |||||||
| FP3 | 0.2±1.0 | 0.5±1.3 | |||||||
| MS (dB) | |||||||||
| MS1 | 20.8±3.3 | 3.0±1.1 | <0.0001 | 0.002 | 20.3±3.6 | 3.4±2.2 | 0.0004 | 0.0006 | 0.5 |
| MS2 | 22.9±2.9 | 22.1±3.6 | |||||||
| MS3 | 23.8±2.4 | 23.8±3.2 | |||||||
| PSD (dB) | |||||||||
| PSD1 | 4.2±0.9 | −0.4±0.9 | 0.1 | 0.6 | 4.4±1.2 | −0.8±1.3 | 0.2 | 0.09 | 0.3 |
| PSD2 | 3.9±0.6 | 4.1±0.9 | |||||||
| PSD3 | 3.8±0.3 | 3.6±0.9 | |||||||
FL1, FL2, FL3=mean of fixation losses (%) at visits 1, 2, and 3, FP1, FP2 and FP3=mean of false positive (%) at visits 1, 2, and 3, MS1, MS2 and MS3=mean of mean sensitivity (dB) at visits 1, 2, and 3, PSD 1, PSD2, and PSD3=pattern standard deviation (dB) at visits 1, 2, and3
Table 3.
Changes in the mean of reliability parameters and global indices in subsequent visits in both age groups of POAG
| Parameters | < 40 years age group (n=12) | >40 years age group (n=18) | Gender-wise difference of change in v3-v1 P | ||||||
|---|---|---|---|---|---|---|---|---|---|
|
|
|
||||||||
| Data value | Data change in v3-v1 | V2-v1 P | V3-v2 P | Data | Data change v3-v1 | V2-v1 P | V3-v2 P | ||
| FL% | |||||||||
| FL 1 | 11.4±6.6 | 10.7±6.3 | 0.002 | 0.01 | 11.2±5.0 | −10.5±4.9 | <0.0001 | 0.003 | 0.9 |
| FL2 | 4.9±5.4 | 4.0±4.4 | |||||||
| FL3 | 0.6±2.3 | 0.7±2.1 | |||||||
| FP (%) | |||||||||
| FP1 | 7.5±5.8 | −6.8±5.5 | 0.008 | 0.04 | 6.6±4.8 | −6.4±4.8 | <0.0001 | 0.01 | 0.8 |
| FP2 | 3.5±3.7 | 2.2±3.2 | |||||||
| FP3 | 0.6±1.5 | 0.2±0.9 | |||||||
| MS (dB) | |||||||||
| MS1 | 22.6±3.2 | 3.5±2.1 | 0.001 | 0.006 | 19.1±2.8 | 3.08±1.58 | <0.0001 | 0.0007 | 0.4 |
| MS2 | 24.7±2.6 | 21.0±2.8 | |||||||
| MS3 | 26.2±2.1 | 22.2±2.0 | |||||||
| PSD (dB) | |||||||||
| PSD1 | 4.6±1.2 | −0.8±1.5 | 0.3 | 0.1 | 4.2±0.9 | −0.53±0.9 | 0.06 | 0.3 | 0.4 |
| PSD2 | 4.2±0.9 | 3.8±0.6 | |||||||
| PSD3 | 3.8±0.5 | 3.7±0.8 | |||||||
FL1, FL2, FL3=mean of fixation losses (%) at visits 1, 2, and 3, FP1, FP2, and FP3=mean of false positive (%) at visits 1, 2, and 3, MS1, MS2, and MS3=mean of mean sensitivity (dB) at visits 1, 2, and 3, PSD 1, PSD2, and PSD3=pattern standard deviation (dB) at visits 1, 2, and 3
Discussion
In visual field tests like all psychological tests, it is common to get variability in responses. This variation could be random or nonrandom. Random variability is because of the nature of the visual system and testing process, while nonrandom variability is due to pupil size, media opacity, treatment, or progression of glaucoma. The performance effect is also a nonrandom variation. These could be positive or negative, leading to improvement or deterioration of the visual field test. Inferring results on learning effect on a single participant is impossible as random fluctuations are also present. VFTs are also influenced by number of other factors like age, environment, skill of technician, concentration, co-operation, fatigue, understanding, pupil diameter, etc.
Aulhorn and Harms[18] in 1967 first discussed the perimetric learning observed in healthy subjects when they underwent repeated perimetry. In past studies (Katz,[19] Bickler Bluth[20]), it has been shown in a large proportion of glaucoma and also in normal subjects that the first session is unreliable on the visual field test. As perimetry is the only test for the documentation of functional loss in glaucoma, it is very important to get a baseline field for the subsequent follow up. We assessed the factors which are affected by the learning effect to know how many subsequent fields are required to get the baseline field. We analyzed our data in three different ways—first by comparing POAG patients with normal subjects in terms of improvement in reliability parameters and global indices, second comparing learning effects gender wise in POAG patients, and third, by comparing learning effects in different age groups <40 and >40 years in POAG patients.
In our study, we excluded the unreliable results and took only the test results that came with reliability parameters under the reliable range set by the manufacturer of our perimeter, i.e., FL <20% and FP <33%. Since we examined our participants in a short time interval of 2 week, there are least chances of glaucoma progression or glaucoma therapy affecting our VFT results. Also, we studied our participants on different days for different sessions, so there is less scope for fatigue effect to influence our test results. We performed a field test on one eye in one session so that other eye tests could not become participants’ second perimetric experience. Previous studies have shown that field results deteriorated by a long session of test as compared to shorter test duration.
We performed our tests on the FAST threshold strategy so that long tiring tests do not cause fatigue and worsening of field results. We chose the same environment, same machine with the same parameters, and the same examiner who supervised all perimetry sessions to avoid variations in test results as it is evident from past studies that environment and technician skills influence test results. Patients’ decision making on whether to respond to a stimulus presented is also affected significantly by perimetrist’s instructions; therefore, we gave a neutral set of basic instructions on how to perform the test correctly in their easy local language. Confounding factor like age was excluded by the simple random selection of patients.
We studied learning effects on both normal healthy subjects and POAG patients. The mean age of both groups was found to be similar. The FLs and FP error were found to be more in glaucoma participants as compared to normal subjects. We recorded significant improvement in reliability parameters and global indices in the POAG group in both second and third visits, while significant improvement was found up to the second visit in the normal subject. Also, the improvement was more pronounced between the first and second visits in the POAG group as compared to second and third visits, but it continued to improve till the third visit signifying the importance of learning in perimetry. Normal subjects displayed almost similar improvement till second experience, which means that they learned to correct their FLs and FP errors mostly by the second visit. Similar to our study, Tiwari US et al.,[21] found significant improvement in reliability indices in POAG patients. Aydin[16] on normal population found similar results in the second test session since they performed VFT on both eyes in single session so actually their second session was subject’s third perimetric experience. Werner et al.[22] and D.P.E. Castro et al.[23] studied improvement in global indices and found similar results in POAG patients and normal subjects, respectively. The learning effect takes place in perimetry examinations as the participants become more familiar with subsequent sessions. The retention of the increased sensitivity beyond the third examination may also continue in a small fraction of participants, but since the improvement was small, as shown in past studies also, we did not perform tests after the third test session.
Mean MD was found to improve by 3.2 db in POAG and 2.8 db in normal subjects. This improvement was found to be more in POAG patients as compared to normal subjects. To our knowledge, no study till now has been done to compare the learning effects in POAG and normal subjects. PSD was recorded to be almost similar in all test sessions in both POAG and normal subjects with low standard deviation, which meant that the variations in retinal sensitivity remained almost the same in all tests.
On comparing the data of reliability parameters and global indices gender wise, we found that the improvement was significant and similar in subsequent visits in both males and females in POAG patients in all parameters. Studies done in past which are similar to our results are from A. Heijl[24] and Kulze et al.[15] done on POAG patients. G. Marra[25] also found no difference in learning effect gender wise. On evaluating the parameters age wise, we did not find any statistically significant difference. This is contradictory to the finding of A. Aydin[16] who found changes in all parameters to be more in the older age group. Also, in CIGTS,[26] the authors found a significant correlation between the variability of age and MD, while Kulze et al.[15] found the results similar to our study showing no difference in learning based on age or sex.
From our study, we observed that the learning effect continued till the third test session in the POAG group so it becomes more important to get at least three visual field tests done before considering a field report to be baseline VFT. And in normal healthy subjects, it was observed that the reliability parameters and global indices continue to improve after the second test, but the change is not statistically significant so if the second VFT is set as baseline then it can be accepted. Despite so many studies, it is still unpredictable to comment on a small fraction of the population who show continued learning even after five test sessions as discussed by A. Heijl,[7] while a few participants do not improve at all in subsequent visits.
The present study has a few drawbacks like the small sample size to conclude the result on a larger population, but the strength of our study was that we have normal subjects as a control, and this is the only study from this part of India.
Conclusion
Since SAP is a psychophysical test and due to large variability in results subject wise in different types of study designs, it is still not possible to predict exactly the amount of learning effect. We found that reliability parameters and global indices improved more significantly in POAG participants as compared to healthy subjects till third visual field test. Also, the learning effect was similar in both males and females, and no significant difference in improvement was found age wise. These results can vary with different study designs and different demographic distributions of participants. Still, it is must to perform at least three SAP tests to get the baseline perimetry chart, especially in POAG patients, while in normal subjects, second perimetric results can be accepted.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
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