Microtropia is an adaptation of binocular vision by a monocular alteration of undefined etiology. There are various theories for its origin, which range from anisometropic refractive defects1 to difficulty in bifoveal fixation or even genetic predisposition.2 The concept of microtropia was introduced by Lang during the International Symposium on Strabismus, celebrated in Giessen in 1966. It is described as a primary ocular deviation of less than 10 prism diopters (PD) associated with harmonious anomalous retinal correspondence and reduced stereopsis.3 This harmonious anomalous retinal correspondence, caused by a cortical adaptation mechanism,4–6 is caused by a minor eccentric fixation in the microtropic eye.5,7 As a result of this, eccentric fixation visual acuity is compromised, causing amblyopia and central suppression scotoma from the fovea to the retinal fixation point, known as Harm's scotoma.8 When this eccentricity increases and the vision disparity exceeds the limits of binocular vision, known as the Panum fusional area, it is eliminated. The abnormal retinal correspondence that is generated due to the adaptation of the visual cortex through the use of neuronal chains is more apparent when the deviation is less than 5 degrees.7 This abnormal binocular adaptation develops at the age of a few months and normally remains unchanged.
To determine the fixation, direct ophthalmoscopy by visuscope is the most common technique used. However, it has its limitations, especially when used on young patients, and proves to be inefficient due to the patients' lack of cooperation. The identification and description of the fixation can occasionally become subjective.
It can be difficult to diagnose microtropia, especially when the angle of deviation is minimal or even inappreciable. Identifying an eccentric fixation in patients with suspected microtropia would be helpful for diagnosis.
Over the past few years, advances in non-invasive retinal image acquisition techniques such as optical coherence tomography (OCT) have contributed to pseudo-histological images of the retina.9 OCT is now present in almost all eye departments, so new applications using this technology could be useful. One possible application is to determine the retinal fixation point of a patient.
The aim of this study was to assess whether OCT could be useful in detecting and documenting fixation in children with microtropia.
Patients and Methods
The study was approved by the research commission board of the University Hospital of Torrevieja (No. CI2016-19), Alicante, Spain, and conducted in accordance with the tenets of the Declaration of Helsinki.
A retrospective, observational, and transversal study was conducted, in which a total of 15 patients with varying degrees of amblyopia from the Ophthalmology/Optometry Department between 2010 and 2016 were included. All patients were diagnosed or suspected of having microtropia because visual acuity was lower than expected and they did not present with stereoscopic vision after the follow-up and treatment of the amblyopic eye.
A control group of 10 eyes without amblyopia or microtropia and with foveal fixation by visuoscopy and stereopsis and normal visual acuity was included. Patients similiar in age to the study group were selected. The eye of the control group was selected at random in case of symmetric refraction or lack of ametropia. The more hyperopic eye was selected in the case of anisometropia.
The presence of ocular deviation was determined by performing a cover–uncover test and, if present, deviation was measured using an alternate cover test with a prism bar. Best corrected visual acuity (BCVA) was measured using a Snellen chart at 6 meters, starting with the non-amblyopic eye. Patients with a visual acuity in the amblyopic eye of 0.7 logMAR or worse were also included and showed a high level of cooperation.
Presence of a central scotoma was determined by performing a 4-PD base-out test.10 Stereopsis was tested with the TNO test, developed by Walraven in 1975. Failure to identify hidden objects in all three first plates (retinal disparity of 1,900 seconds of arc) was considered to be absence of stereopsis.
The retinal fixation point was measured using a visuscope, although it could not be performed successfully on 4 patients due to lack of cooperation. The fixation point was classified by alignment and fixation stability.
Retinal imaging was captured in all eyes using spectral-domain OCT (Cirrus HD-OCT, version 220.127.116.11; Carl Zeiss AG, Oberkochen, Germany), with the Macular Cube 512 × 128 scanning protocol applied. It allows the acquisition of a large amount of information and provides 1,024 points per A-scans per B-scans, with a line width of 47 µm over an area of 6 × 6 mm and a 2.4-second imaging time.
We routinely perform efficiency checks of OCT by using the “performance verification” tool. With this method, we can confirm that both the image of the eye fundus by scanning laser ophthalmoscope and the tomographic image of OCT are aligned.
After positioning the patient correctly, the eye was aligned to the instrument, the refractive error was adjusted (focus adjustment possibility from −20.00 to +20.00 diopters [D]), and the patient was instructed to look into the center of the fixing stimulus presented by the OCT (a green star).
Because of the external observation monitor, it was possible to visualize the patient's fixation in real time. When we observed a stable fixation without random movements, an image was captured. Images were always taken starting with the healthy eye because this leads to increased cooperation and shows the patient what to expect. Several attempts were made to capture images to ensure good repeatability and all patients had a scan quality signal of 7 or better.
After obtaining the image, we identified the foveal center and fixation point. The foveal center was considered to be the anatomical center of the fovea (lowest point of the foveal depression in the horizontal and vertical planes). We considered the retinal fixation point to correspond to the subjective projection of the fixation stimulus in the retina. The distance between both points was measured, in microns, using the metric tool of the OCT system software (Figure 1).
Optical coherence tomography exploration screenshot of a two-dimensional thickness map (patient 8). A 6 × 6–mm area was studied, with the identification of the patient's fixation point (indicated by crosshairs) in the nasal quadrant at 461 µm. The software automatically identifies the foveal center, but it is mandatory to check the patient's actual retinal point of fixation. To achieve this, the system tool is used to show or hide high-resolution images (black square). The foveal center was the lowest point of the foveal depression in the horizontal and vertical planes of the central circular area. The tool bars in the program include a metric tool (black circle), with which the distance between the fixation point and the foveal anatomical center is measured.
Thickness was also measured for both the foveal center and the fixation point of the eye.
After these measurements, a refraction test was performed under cycloplegia, instilling one drop of cyclopentolate 1% every 10 minutes, a total of three times. After 45 minutes had elapsed from the last instillation, a retinoscopy was performed.
All tests were performed by the same optometrist (MAG-G).
Statistical analysis was done using SPSS software (version 22; SPSS, Inc., Chicago, IL).
Given that the different sample sizes were small, the Wilcoxon test was used to compare refractive changes after cycloplegia. Likewise, the corresponding Mann–Whitney U and Kruskal–Wallis tests were used to make non-parametric comparisons among independent samples.
The connection between a reduction in the angles of deviation and fixation was studied using Spearman correlation analyses. The hypotheses tests were bilateral in all cases, with a significance level of 0.05.
The average age of the patients was 8.86 ± 2.60 years (10 female: average age of 8.4 years [range: 5 to 14 years]; 5 male: average age of 9.4 years [range: 6 to 11 years]). The amblyopic eye was the left eye in 73% of cases. Deviation by cover test was detected in 67% of cases, whereas no movement was detected in the rest. Stereopsis was not present in any cases and the 4-PD base-out test determined a central scotoma in all cases.
The spherical equivalent, in spectacles, was +3.60 ± 2.74 and +2.71 ± 2.35 D in the amblyopic and contralateral eye, respectively. No significant differences were observed with respect to the cylindrical component in any case, with an average of −0.71 ± 0.80 D.
Regarding cycloplegic refraction, there was hypo-correction in the average spherical value of 0.90 ± 0.62 D (P < .001).
Hyperopic refraction was present in all but one case. Only one patient presented with myopic refraction, with a spherical equivalent of −1.00 D in the right eye and −0.75 D in the left eye, although the cycloplegic refraction was a spherical equivalent of +1.00 and +1.25 D, respectively. Thirteen percent of cases showed no anisometropia, 40% had anisometropia between 0.13 and 0.50 D, and 47% had anisometropia that was greater than 0.50 D, with the greatest difference being 2.75 D. We only found significant differences between the degree of anisometropia and the spherical equivalent of the amblyopic eye (P = .024; Kruskal–Wallis test).
The BCVA was 0.03 logMAR (range: 0.15 to 0.00 logMAR) in the contralateral eye and 0.18 logMAR (range: 0.7 to 0.05 logMAR) in the amblyopic eye (P < .001, Mann–Whitney U test).
An eccentric fixation of 387 ± 199 µm was observed in the amblyopic eyes using OCT (Figure 2). The eccentric fixation was foveal in only one case, which also presented the greatest deviation (10 PD). A relationship can be determined when this case is excluded (R = 0.550, P = .02) (Figure 3).
(A) Distribution of retinal fixation points (rhombuses) of strabismic eyes superimposed on a background image of the central macular area. The coordinates (0, 0) were considered to be the anatomical center of the fovea. The deviation of each fixation point is expressed in prism diopters. N = nasal; T = temporal (B) Cross-section of the optical coherence tomography scan corresponding to the upper image. The retinal thickness at the fixation point is specified in cases 4 and 6.
The relationship between deviation and eccentric fixation in amblyopic eyes as determined with optical coherence tomography. Except in the case of foveal fixation, it is noted that the greater the eccentric fixation, the greater was the ocular deviation.
Superonasal eccentricity was more frequent (57%), followed by nasal (29%) and inferonasal (14%). The average deviation was 3.73 ± 3.34 PD. All contralateral eyes presented central foveal fixation, which is defined as the fixation situated within the foveal pit, without exceeding 102 µm (0.29°).11
No relationship was found to exist between the deviation and cycloplegic spherical equivalent, although a weak relationship was found between visual acuity and the cycloplegic spherical equivalent (R = .371, P = .173). A relationship was also found between visual acuity and the eccentric fixation and, more precisely, between visual acuity and retinal thickness at the fixation point. The greater the eccentricity and retinal thickness were, the lower the visual acuity was (R = 0.465, P = .081 and R = 0.529, P = .043, respectively).
Cases that did not present movement during a cover test presented an average eccentric fixation of 283 ± 66 µm, compared to 439 ± 235 µm in cases where deviation was present, indicating a small statistically significant difference (P = .055, Mann– Whitney U test) (Figure 4).
Box plot comparing eccentric fixation in patients not presenting deviation “with identity” (n = 5) to those patients presenting deviation “without identity” (n = 10). Lower eccentricity values and less disperse values can be observed in the group not presenting with a deviation during the cover test.
Fixation by visuscope could be determined in 10 of 15 cases, presenting as stable nasal in 8 cases and unstable nasal in only 1 case. Fixation was described as foveal using visuoscopy in only one case, although a superonasal eccentric fixation of 286 µm was measured with OCT.
Fixation could not be measured by visuscope in the patient with the greatest prismatic deviation, but a foveal fixation was observed on OCT.
The average foveal thickness was 216 ± 19 µm, with no significant differences between the amblyopic and contralateral eye. The average foveal thickness in the fixation area of the amblyopic eye was 266 ± 42 µm.
In the control group (4 female and 6 male; average age of 9 years [range: 6 to 12 years]), the mean refractive error was spherical equivalent +3.03 ± 1.87 D and BCVA was 0.02 logMAR (range: 0.00 to 0.09 logMAR). A foveal fixation in the OCT images was observed in all cases, with a deviation from the anatomical center of the fovea of less than 100 µm and always inside the foveal pit.
The concept of microtropia has usually been associated with small-angle strabismus. On occasion, its classification has depended on the type of macular fixation (foveal or eccentric). In cases in which the retinal correspondence is normal and there is foveal fixation, the term “monofixation syndrome” was introduced.12
Other authors have also used the term microtropia in cases in which the eccentric fixation coincides with the angle of deviation, without observing movement during the cover test. These cases have been classified as strabismus “with identity,” whereas those cases that presented movement during the cover test1 have been classified as strabismus “without identity.” In our study, 10 patients presented movement during the cover test, whereas the 5 remaining patients did not.
We found only one case in which fixation was foveal and, curiously enough, presented the highest deviation. This indicates that the case was not true microtropia, but rather a small angle endotropia (or “monofixation syndrome”) because foveal fixation cannot exist in true microtropia. When the eccentric fixation and angle of deviation coincide, no movement is detected while performing the cover test, thereby presenting a stable eccentric fixation with no changes observable.1 Our results show a lower eccentricity in these cases. In cases in which movement was observed with the cover test, the eccentricity was more variable. Tomaç et al.13 observed some instability in fixation in these cases, which accounts for the movement during the cover test.
Different methodologies for determining retinal fixation have been proposed, with the most standardized being observation using a visuscope, a modification of the direct ophthalmoscope, developed by Cüppers. There have been variations of this technique that have been shown to be efficient in children.14 New techniques for retinal studies have permitted the development of instruments that can determine the area of macular fixation with a high degree of precision. The scanning laser ophthalmoscope (SLO; Rodenstock, Munich, Germany), developed in the 1970s, has been used in various studies on young patients with strabismus and amblyopia,15,16 detecting foveal fixation in the amblyopic eyes with the best visual acuity. Advances in this technology, such as the MP-1 Retinal Microperimeter (Nidek Technologies, Padua, Italy), provide analysis of both fixation and fixation stability over time and are excellent tools for studying young amblyopic and strabismic patients.17,18 A reduced fixation instability in anisometropic and amblyopic eyes of children, more so with abnormal stereopsis, has been demonstrated through microperimetry.19,20
Dickmann et al.21 studied sensitivity and fixation in eyes with strabismic amblyopia and refractive amblyopia, according to the classification of Fujii et al.,22 and found that macular sensitivity was always greater in the contralateral eye, as measured by OCT. However, they did not find significant differences in fixation between the amblyopic and contralateral eye, as measured by microperimetry.21 Significant differences were also found between the macular thickness of the strabismic and contralateral eye,21 which differs from the results obtained in our study. This could be due to the fact that the measurement was taken at the fovea without observing the whole macular area, or because we did not introduce the correction of ocular magnification induced by axial length, according to the Littmann formula.23 However, no differences greater than 7.3% were found due to significant refractive defects.24
In our study, the eyes of the control group showed foveal fixation in all cases, and these findings were the same in the contralateral eyes of the study group. The fixation stimulus presented by OCT coincides with, or is close to, the instrument optical axis, although this could only be measured exactly through the optical bench.
Using OCT to determine eccentric fixation has been previously reported in macular retinal pathologies,25 such as a case of bilateral macular coloboma in a 4-year-old patient,26 but there are no references in the literature to OCT localization studies in young patients with amblyopia or strabismus.
OCT use on children is becoming an important observational method, contributing significant advantages to the detection and evaluation of retinal pathologies, as well as to anatomical studies of the macula and retinal nerve fiber layer.27,28 The use of manual observation techniques has also been attempted on children from 3 years of age with good results.29
The small experimental sample size and the study design (observational and retrospective) limit the results. Furthermore, comparison with a gold standard or reference test, such as microperimetry, would be of value.
The instability of fixation in amblyopic or strabismic eyes is another important bias factor to be considered. OCT performs a fast capture that is a few seconds in duration and small movements of fixation during the scan can be present.
OCT is not designed to assess patterns of retinal fixation. There are different fixation stimuli of current OCTs, and there are serious concerns about the real alignment of stimulus with the OCT system, both of which could also have affected our results. A study to determine the “normal” range of fixation as measured by different OCTs is also necessary, with consideration of the fixation stimulus alignment within the optical system.
To our knowledge, this is the first case in which OCT has been used for this purpose. OCT can aid in the detection of eccentric fixation and provide a relative degree of location of the retinal fixation point. According to our results, OCT can play an important role in the detection and measurement of eccentric fixation in eyes with microtropia, providing a high sensitivity compared to other methods.
- Helveston EM, Von Noorden GK. Microtropia: a new defined entity. Arch Ophthalmol. 1967;78:272–281. doi:10.1001/archopht.1967.00980030274003 [CrossRef]
- Cantolino SJ, Von Noorden GK. Heredity in microtropia. Arch Ophthalmol. 1969;81:753–757. doi:10.1001/archopht.1969.00990010755001 [CrossRef]
- Lang J. Microtropia. Arch Ophthalmol. 1969;81:758–762. doi:10.1001/archopht.1969.00990010760002 [CrossRef]
- Jennings JA. Anomalous retinal correspondence: a review. Ophthalmic Physiol Opt. 1985;5:357–368. doi:10.1111/j.1475-1313.1985.tb00680.x [CrossRef]
- Herzau V. How useful is anomalous correspondence?Eye (Lond). 1996;10:266–269. doi:10.1038/eye.1996.56 [CrossRef]
- Lang J. Anomalous retinal correspondence update. Graefes Arch Clin Exp Ophthalmol. 1988;226:137–140. doi:10.1007/BF02173301 [CrossRef]
- Wong AM, Lueder GT, Burkhalter A, Tychsen L. Anomalous retinal correspondence: neuroanatomic mechanism in strabismic monkeys and clinical findings in strabismic children. J AAPOS. 2000;4:168–174. doi:10.1016/S1091-8531(00)70008-5 [CrossRef]
- Harms H. Location and quality of suppression in strabismic patients [article in German]. Graefes Arch Clin Exp Ophthalmol. 1937;138:149–210. doi:10.1007/BF01854538 [CrossRef]
- Huang D, Swanson EA, Lin CP, et al. Optical coherence tomography. Science. 1991;254:1178–1181. doi:10.1126/science.1957169 [CrossRef]
- Irvine SR. Amblyopia ex anopsia: observations on retinal inhibition, scotoma, projection, light difference discrimination and visual acuity. Trans Am Ophthalmol Soc. 1948;46:527–575.
- Rohrschneider K, Becker M, Schumacher N, Frendrich T, Völcker HE. Normal values for fundus perimetry with the scanning laser ophthalmoscope. Am J Ophthalmol. 1998;126:52–58. doi:10.1016/S0002-9394(98)00065-8 [CrossRef]
- Parks MM. The monofixation syndrome. Trans Am Ophthalmol. 1969;67:609–657.
- Tomaç S, Sener EC, Sanaç AS. Clinical and sensorial characteristics of microtropia. Jpn J Ophthalmol. 2002;46:52–58. doi:10.1016/S0021-5155(01)00470-1 [CrossRef]
- Cooper J, Gelfond I, Carlson PE, Campolattaro B, Wang F. Comparison of eccentric fixation measurements using the streak target of an ophthalmoscope and a traditional visuoscopy target. J Pediatr Ophthalmol Strabismus. 2005;42:89–96.
- Siepmann K, Reinhard J, Herzau V. The locus of fixation in strabismic amblyopia changes with increasing effort of recognition as assessed by scanning laser ophthalmoscope. Acta Ophthalmol Scand. 2006;84:124–129. doi:10.1111/j.1600-0420.2005.00550.x [CrossRef]
- Kelly JP, Weiss AH, Zhou Q, Schomode S, Dreher AW. Imaging a child's fundus without dilation using a handheld confocal scanning laser ophthalmoscope. Arch Ophthalmol. 2003;121:391–396. doi:10.1001/archopht.121.3.391 [CrossRef]
- Barrio-Barrio J, Olmo Jiménez N, Caire JM. Fixation analysis in amblyopia and strabismus: preliminary study with the MP-1 microperimeter [article in Spanish]. Boletín de la Sociedad Oftalmológica de Madrid. 2006;46.
- Carpineto P, Ciancaglini M, Nubile M, et al. Fixation patterns evaluation by means of MP-1 microperimeter in microstrabismic children treated for unilateral amblyopia. Eur J Ophthalmol. 2007;17:885–890. doi:10.1177/112067210701700603 [CrossRef]
- Subramanian V, Jost RM, Birch EE. A quantitative study of fixation stability in amblyopia. Invest Ophthalmol Vis Sci. 2013;54:1998–2003. doi:10.1167/iovs.12-11054 [CrossRef]
- Birch EE, Subramanian V, Weakley DR. Fixation instability in anisometropic children with reduced stereopsis. J AAPOS. 2013;17:287–290. doi:10.1016/j.jaapos.2013.03.011 [CrossRef]
- Dickmann A, Petroni S, Perrota V, et al. A morpho-functional study of amblyopic eyes with the use of optical coherence tomography and microperimetry. J AAPOS. 2011;15:338–341. doi:10.1016/j.jaapos.2011.03.019 [CrossRef]
- Fujii GY, de Juan E Jr, Sunness J, Humayun MS, Pieramici DJ, Chang TS. Patient selection for macular translocation surgery using the scanning laser ophthalmoscope. Ophthalmology. 2002;109:1737–1744. doi:10.1016/S0161-6420(02)01120-X [CrossRef]
- Littmann H. Determination of the real size of an object on the fundus of the living eye [article in German]. Klin Monbl Augenheilkd. 1982;180:286–289. doi:10.1055/s-2008-1055068 [CrossRef]
- Knighton RW, Wang F, Gregori G, et al. Calibration of fundus images using spectral domain optical coherence tomography. Ophthalmic Surg Lasers Imaging. 2008;39(4 suppl):S15–S20.
- Oh IK, Oh J, Kim SW, Huh K. Fixation and photoreceptor integrity in optical coherence tomography. Optom Vis Sci. 2012;89:E1000–E1008. doi:10.1097/OPX.0b013e31825da30d [CrossRef]
- Abe K, Shirane J, Sakamoto M, et al. Optical coherence tomographic findings at the fixation point in a case of bilateral congenital macular coloboma. Clin Ophthalmol. 2014;21:1017–1020. doi:10.2147/OPTH.S63593 [CrossRef]
- Salchow DJ, Hutcheson KA. Optical coherence tomography applications in pediatric ophthalmology. J Pediatr Ophthalmol Strabismus. 2007;44:335–349.
- Alasil T, Keane PA, Sim DA, Tufail A, Rauser ME. Optical coherence tomography in pediatric ophthalmology: current roles and future directions. Ophthalmic Surg Lasers Imaging Retina. 2013;44(6 suppl):S19–S29. doi:10.3928/23258160-20131101-04 [CrossRef]
- Gerth C, Zawadzki RJ, Héon E, Werner JS. High-resolution retinal imaging in young children using a handheld scanner and Fourier-domain optical coherence tomography. J AAPOS. 2009;13:72–74. doi:10.1016/j.jaapos.2008.09.001 [CrossRef]