Introduction

High myopia is a common cause of blindness in many countries. It is becoming a more serious problem globally due to changes in the life style and the environment.[1–4] There are many types of changes in myopic eyes, leading to severe visual loss. Posterior staphylomas are one of these changes, and they develop at the end stage of pathologic myopia. Staphylomas are frequently associated with different types of retinochoroidal atrophy [5], and they generally develop after 40-years-of-age. Posterior staphylomas are observed in 90% of the eyes of individuals ≥50-years with pathologic myopia.[6] It is known that a staphyloma can cause a severe stretch of the outer wall of the eye[5] which leads to pathological changes that cannot be detected by conventional ophthalmological examinations in the early stages.

A tessellated fundus is another common characteristic of myopic eyes.[6–8] In healthy human eyes, it has been shown that a tessellated fundus represents an area where the choroid is thin.[9] In pathologically myopic eyes, the retinal pigment epithelium (RPE) and choroid are thinner due to a stretching and expansion of the posterior surface of the eye.[5,10] A tessellated fundus is observed at a younger age than a posterior staphyloma [6–8], and it was recently classified as category 1 in the five categories of myopic maculopathy. They were followed by diffuse chorioretinal atrophy (category 2), patchy atrophy (category 3) and macular atrophy (category 4).[11] Because 10% of the cases in category 1 were reported to progress to category 2 in 12 years [11], some of the tessellations at a younger age might be involved in pathologic retinochoroidal alterations and/or staphylomas in the advanced stage of pathologic myopia.

There are several types of staphylomas present in highly myopic eyes. Curtin classified staphylomas into ten categories based on their location.[8] However to the best of our knowledge, there has not been a study determining the locations of the tessellation in the fundus and whether they are related to other myopic changes. Considering the increasing prevalence of myopia and its association with serious retinochoroidal changes, it is important to know more about tessellated fundi.

Thus, the purpose of this study was to determine the location of the tessellation in the fundus of young healthy subjects and to determine whether the location was correlated with the degree of optic disc tilt, the area of the optic disc including the conus, and the axial length (AL).

Methods

Classification of lesions in tessellated fundus

The fundi of all subjects were photographed using the same digital fundus camera with a 45 degree view (TOPCON 3D OCT-1000 MARK II, Topcon). The tessellated fundus lesions were classified into 5 primary types based on Curtin’s classification of the location of the posterior staphylomas, viz., in the posterior pole, macula, peripapillary, nasal, and inferior.[8] We classified the tessellated fundi into corresponding areas such as the whole area, temporal area, peripapillary area, nasal area, and inferior area. We also had an additional location, the intra-temporal area, because several eyes had inferior tessellations with or without foveal lesions. In the end, we classified the tessellated fundus into 8 groups (Fig 1); no tessellation (NO), temporal (T), infra-temporal (IT), inferior (I), nasal (N), peripappilariy (PP), whole (W), and unclassified (U) tessellations. The classifications were made by 2 independent masked examiners. If the raters disagreed, they discussed the reasons for their classification with a third rater, and the final classification was determined by an agreement of at least two of the three graders. If an agreement was not reached, the eye was placed in the unclassified group.

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Fig 1. The location of the tessellation using red channel images.

Fundus images were exchanged with the split channel command (red) by Image J software to enhance the clarity of the tessellations. The location of the lesions associated with the tessellation was classified based upon Curtin’s classification.

https://doi.org/10.1371/journal.pone.0156842.g001

Results

We studied 126 right eyes of 126 individuals. The mean ± standard deviation age was 26.0 ± 4.1 years ranging from 22.0 to 40.0 years, and 85 were men (67.5%). The mean refractive error (spherical equivalent) was -4.71 ± 3.41 diopters (D) with ranging from -14.25 to 4.50 D, and the mean of the AL was 25.43 ± 1.45 mm rainging from 22.3 to 30.4 mm. The mean optic disc tilt was 37.01 ± 17.45 pixels rainging from 4.77 to 80.77 pixels. The mean area of the optic disc plus conus was 2798.89 ± 906.9 pixels rainging from 1478.7 to 7331.4 pixels. The complete dataset is available in S1 Dataset.

Comparisons of axial length, optic disc tilt, and area of optic disc plus conus among groups

We compared ocular findings in eyes with tessellation to eyes without tessellation. The AL of the IT group (P <0.001) and W group (P = 0.01) were significantly longer than that in the NO tessellation group (Fig 2A). The area of the optic disc plus conus in the T group (P = 0.01), IT group (P <0.001), and PP group (P = 0.001) were significantly larger than that in the NO tessellation group (Fig 2B). The optic disc tilt in the IT group was significantly larger than that in the NO group (P = 0.01), the I group (P = 0.03), the N group (P = 0.03), and the PP group (P = 0.03; Fig 2C).

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Fig 2. Multiple comparisons of the axial length, area of optic disc plus conus, and optic disc tilt among groups.

(A) The AL of the IT group (P <0.001) and W group (P = 0.01) were significantly longer than that in the NO tessellation group. (B) The area of the optic disc plus conus in the T group (P = 0.01), IT group (P <0.001), and PP group (P = 0.001) were significantly larger than that in the NO tessellation group. (C)The optic disc tilt in the IT group was significantly larger than that in the NO group (P = 0.01), the I group (P = 0.03), the N group (P = 0.03), and the PP group (P = 0.03).

https://doi.org/10.1371/journal.pone.0156842.g002

The mean AL of the IT group (P <0.001) and the W group (P = 0.01) were significantly longer than that of the NO group (Fig 2A). The mean area of the optic disc plus conus in the T group (P = 0.01), IT group (P <0.001), and PP group (P = 0.001) were significantly larger than the area in the NO group (Fig 2B). The optic disc tilt of the IT group was significantly larger than in the NO group (P = 0.01), I group (P = 0.03), N group (P = 0.03), and PP group (P = 0.03; Fig 2C).

Discussion

Our results showed that the tessellations were located in specific regions of the fundus with the infra-temporal location most frequent followed by the para-papillary location. Because we could not find earlier reports on the locations of the tessellations, we compared our results to the locations of posterior staphylomas which are relatively common in eyes with pathologic myopia. If these locations are similar, a closer relationship of the two pathologies might be possible.

Curtin reported that the posterior staphylomas were located in the posterior pole in 55% of the cases, in the macular area in 8.4% of the cases, in the peripapillary area in 1.5% of the cases, in the nasal area in 4.9% of the cases, in the inferior area in 2.6% of the cases, and in compound areas in 27.6% of the cases (subtypes of posterior pole type).[8] For tessellations, the prevalence of the W (whole) type which corresponds to the posterior pole type of staphyloma was 13.4% while Curtin’s posterior pole type was 55%. The prevalence of the T (temporal) type of tessellation was 14.6% which corresponds to the 8.4% of the macular type of posterior staphyloma. Thus, the prevalence of the posterior type of tessellation was lower than the posterior pole type of staphylomas, 13.4% vs 55.0% + 27.6%. In addition, Hayashi et al reported that the prevalence of the posterior pole type of staphyloma was 26.6% and the macular type was 51.7% which are far more prevalent than the other types[7], but similar to that of Curtin’s distribution. The tessellations in this study and the staphylomas in those studies were found mainly in the posterior pole of the eye. However, the frequency of each at a specific location is different, and it was difficult to compare them because of the design of the studies. For example, Hayashi et al investigated hospital-based subjects with visual disturbances while we studied young healthy eyes.

McBien et al followed a large number of normal adults for 2 years and reported that a progression of myopia by an elongation of AL was quite frequent even in adults.[14] So, a remodeling or changing of the structure of eye including localized thinning of the retinochoroidal tissue may occur continuously with increasing age even in adults. Because tessellations become evident at a younger age than posterior staphylomas [7], some of the tessellations at a younger age may progress to posterior staphylomas in eyes with pathological myopia. However, further cohort studies for a longer period are needed to examine this issue.

In general, posterior staphylomas becomes evident after 40-years-of-age.[5] Our results showed that tessellations were most common in the posterior pole as do staphylomas.[7,8] These findings suggest that the localized remodeling of the retinochoroidal tissues leading to a posterior staphyloma may start at a younger age. There is no definite border between a posterior staphyloma and a tessellated fundus, thus these two changes may belong to the same disease spectrum.[7] To obtain a definitive answer on whether tessellations can progress to posterior staphyloma, it will be necessary to perform longitudinal cohort studies.

Our results showed that the AL length was significantly longer in eyes with the infra-temporal type and the whole type of tessellation. Because tessellations are supposedly due to a localized thinning of the RPE/choroid associated with scleral thinning [9], the scleral wall in the tessellated area may be more vulnerable to intraocular pressure than adjacent areas. Thus, this area would easily expand outward. Because the AL is measured as the distance between the cornea and the foveal area, it can be longer in eyes with tessellations within the foveal area than in eyes with tessellations away from the fovea.

Myopic eyes tend to have tilted optic discs [15,16], larger optic disc plus conus area [17,18] than non-myopic eyes. It is clinically important that tessellations were present in the peripapillary area because myopia is a significant factor associated with glaucoma. For example, the degree of optic disc tilt in eyes with infra-temporal tessellation was significantly larger than those in eyes with no tessellation, those with inferior tessellation, nasal tessellation, and peri-papillary tessellations. An optic disc usually tilts laterally, thus the structural changes of the lateral area by tessellations or staphylomas can enhance the optic disc tilting positively, while the changes in the nasal area can do that negatively.

Another issue of tessellated fundi is their relation to the conus.[17,18] A conus is an important myopic change and is supposedly caused by an excessive stretching of the parapapillary area.[19] The present results showed that those eyes with the temporal type, infra-temporal type, and peripallilay type had significantly larger areas of the optic disc plus conus than those with other locations of the tessellations. They are consistent with the idea that both a tessellated fundus and conus are formed by an unusual stretching of the wall of the eye. It is possible that these eyes will further deteriorate into myopic/glaucomatous optic damage. This information should be important in evaluating glaucoma in myopic eyes.

There are several limitations in this study. The sample size was not large enough to detect slight but significant differences between each group. While, the fact that some of the differences reached statistical significance indicates that the findings are sound. Second, we classified the location of tessellations in a subjective way. Although it was classified by two or three independent masked examiners and the inter-rater agreement in the classification of the location of the tessellations was high, new method to classify it objectively would most likely classify it more accurately. Third, this was a cross sectional study, so conclusions on longitudinal effects cannot be made. Fourth, this was a study for young Japanese population. Thus, the present findings may not be applicable to other ethnic groups.

In conclusion, we found that there were specific locations of the tessellations in young healthy eyes. Some of these locations are important sites for making diagnosis of diseases such as myopia and glaucoma. Because their locations were similar to that of posterior staphylomas, the distribution of the locations will be important not only for the diagnosis but also for predicting and preventing the changes in highly myopic eyes.

Supporting Information

Acknowledgments

The authors thank Professor Duco Hamasaki of Bascom Palmer Eye Institute, University of Miami, FL, for providing critical discussions and suggestions to our study and editing of the final manuscript.