Choroidal Perfusion after Macular Surgery in Myopic Traction Maculopathy

Abstract

Myopic traction maculopathy (MTM) is a vision-threatening condition associated with high myopia, posing public health concerns due to the global rise in the prevalence of myopia. MTM encompasses various pathological changes, including foveoschisis, macular hole formation, and retinal detachment, which can lead to irreversible vision loss if not detected or managed early. Understanding choroidal perfusion, particularly in highly myopic eyes, is crucial because the choroid undergoes changes such as thinning and reduced perfusion, which may influence the onset and severity of myopic maculopathy. This chapter explores the importance of choroidal perfusion in MTM and its role in guiding surgical interventions. This chapter investigates two key hypotheses: the impact of various surgical approaches on the postoperative choroidal vascularity index (CVI) and the correlation between the CVI and postoperative visual outcomes following current surgical techniques. This chapter discusses the advantages and limitations of CVI, future research directions, and potential therapeutic implications.

1. Introduction

Myopic traction maculopathy (MTM), a vision-threatening condition due to high myopia (HM) considered an eye with an anteroposterior axial length of ≥26.5 mm or more, has received considerable attention for its timely diagnosis and management, as it leads to multiple retinal pathologies if untreated on time [1]. Pathologic myopia (PM), which is defined as the progressive deterioration of chorioretinal tissue owing to scleral elongation and posterior staphyloma (PS) development, is characterized by the existence of myopic lesions in the back of the eye consistent with chorioretinal atrophy, choroidal neovascularization (CNV), and slow vitreomacular traction (VMT) linked to the progressive emergence of different MTM manifestations in approximately 30% of high myopia cases with the common occurrence of PS [2]. The global prevalence of myopia has been steadily increasing globally, making MTM an emerging public health issue [3]. The World Health Organization estimates that by 2050, approximately 50% of the world’s population will be affected by myopia, with nearly 10% of patients suffering from HM [4]. HM is a significant contributor to legal blindness in industrialized nations, and its prevalence has steadily increased in recent decades. Projections suggest that by 2050, it could affect nearly one billion individuals. Studies analyzing regional and temporal trends have observed a sharp increase in myopia cases worldwide, particularly in East and Southeast Asia, affecting approximately 80–90% of the population, with up to 20% suffering from HM [5]. In the United States, nearly 2% of the general population aged between 12 and 54 years is estimated to be affected by HM, underscoring the need to focus on preventive measures and treatment strategies [6]. These approaches aim to prevent vision loss and blindness caused by PM. Notably, in Japan, PM is identified as the fifth leading cause of blindness, while in China (among people over 40 years of age), it ranks as the second leading cause [7]. As the prevalence of myopia increases, so does the incidence of associated complications, such as MTM, making it essential to understand the disease mechanisms and optimize treatment strategies.

MTM is explained in numerous forms by different researchers, ranging from retinal thickening resembling macular schisis (MS) to foveoschisis (FS), foveoretinal detachment (FRD), and shallow macular detachment (MD) [8]. The first mention of “retinomacular schisis” was by Phillips in 1958 [9], who described posterior retinal detachment (RD) without a macular hole (MH) in patients with myopic staphyloma, suggesting traction as the cause. In 1999, Takano and Kishi used optical coherence tomography (OCT) for anatomical characteristics, which they refer to as “foveal retinomacular schisis” [10]. Panozzo et al. introduced the term “myopic traction maculopathy,” which affects 9–34% of HM patients with PS [11]. Shimada et al. [12] described the stages of macular FS that lead to FRD through an outer lamellar macular hole (O-LMH). Ruiz-Medrano et al. [13] provided a comprehensive classification of myopic maculopathy, including MTM as a tractional aspect [13]. Parolini et al. proposed a novel MTM staging system (MSS) that defines it as a progressive disease starting with inner MS (I-MS) and culminating in MD, reflecting the dynamic nature of the condition [14].

The current understanding is that MTM with all these pathological changes may result in a spectrum of different and very complex clinical manifestations with distinct OCT structural phenotypes, including isolated macular thickening without schisis (Figure 1a), extrafoveal MS (Figure 1b), myopic MS (Figure 1c), MS with inner lamellar macular hole (I-LMH) (Figure 1d), localized or extensive FRD (Figure 1e), inner LMH (Figure 1f), inner LMH with epiretinal membrane (ERM) (Figure 1g), full-thickness macular hole (FTMH) (Figure 1h), and posterior pole or more extensive MH-related rhegmatogenous RD (MHRD) (Figure 1i) [15], all of which can severely impair visual function [11, 14, 16]. As MTM progresses, it can lead to irreversible vision loss, emphasizing the importance of early detection and intervention.

Figure 1.

Different stages of myopic traction maculopathy (a) Schisis-like thickening of the macula nasally to the fovea. (b) Extrafoveal schisis-like thickening of the macula with epiretinal membrane proliferation (ERM). (c) Elevated macular foveoschisis (FS) with tractional elongation of Henle’s nerve fiber layer. (d) Macular FS and severe tractional elongation of Henle’s nerve fiber layer with an inner lamellar macular hole (I-LMH). (e) Magnified image of macular foveoretinal detachment with ERM and schisis-like thickening on the nasal side; there is subretinal retinal fluid. (f) Highly myopic eye with I-LMH. (g) Complex FRD and I-LMH with inner and outer schisis-like thickening of the macula and some hyaloidal remnants on the nasal side. (h) High-definition horizontal line 12 mm image of a very elevated macular FS with a full-thickness macular hole (FTMH) and severe traction of Henle’s nerve fiber layer. (i) Spectralis B-scan examination consistent with retinal detachment and confirmed presence of FTMH (not shown); deep and irregular scleral staphyloma is depicted.

MTM pathogenesis is multifactorial and involves tangential retinal traction and combined anteroposterior traction induced by VMT, vitreomacular adhesions, vitreous cortex remnants, PS, and epiretinal membrane (ERM) proliferation [17, 18]. The internal limiting membrane (ILM), retinal vascular microfolds, and paravascular vitreal adhesions may also contribute to its pathogenesis [19, 20, 21]. In highly myopic eyes, the choroid undergoes changes, including thinning and reduced perfusion, which have been linked to the onset and severity of myopic maculopathy [22]. Thus, assessing choroidal circulation in patients with MTM can offer valuable insights into disease progression and treatment response, thereby aiding the development of targeted therapeutic approaches.

Currently, the optimal stage for patients with MTM to benefit the most from surgical intervention remains uncertain. Some researchers have proposed that surgery should be considered in all cases of MTM where there is a risk of sight-threatening complications or when such complications are already evident [23, 24]. However, some experts recommend a wait-and-see approach for patients in the early stages, advising at least six months of observation [25], as there is a chance of spontaneous remission [26]. Surgery is necessary in cases of reduced visual acuity, symptomatic FS and FRD, full-thickness macular holes (FTMHs), or RS with a schisis pattern resembling a champagne flute [17, 27]. To address RS, the primary goal is to release traction forces from the front of the retina and to counteract the posterior elongation force caused by the staphyloma. Surgical treatment options for this condition include pars plana vitrectomy (PPV) with or without internal limiting membrane (ILM) peeling or macular buckling (MB) [28, 29]. However, the selection of surgical methods could influence postoperative outcomes such as the integrity of the choroidal circulation. Understanding the consequences of various surgical approaches on choroidal perfusion is essential for optimizing visual outcomes in patients with MTM.

Moreover, while best-corrected visual acuity (BCVA) is a commonly used measure to evaluate visual function, it may not fully encompass the intricacies of visual performance influenced by changes in choroidal perfusion. Recent studies have indicated that choroidal perfusion might be evaluated using the choroidal vascularity index (CVI), which has been linked to various visual outcomes beyond BCVA, including contrast sensitivity, central macular thickness (CMT), and microperimetry [1, 30]. Therefore, investigating the correlation between the CVI and visual outcomes can offer a more comprehensive assessment of visual function in patients with postoperative MTM, leading to improved management and enhanced patient care.

This chapter aimed to examine the importance of choroidal perfusion in MTM and its role in guiding surgical intervention. We will explore two key hypotheses: first, the impact of various surgical approaches on postoperative CVI and second, the correlation between CVI and visual outcomes beyond BCVA following surgical interventions. Through a comprehensive analysis of peer-reviewed literature and the exploration of these hypotheses, we aimed to enhance the comprehension of MTM management and ultimately improve patient outcomes for this serious eye condition.

2. Pathophysiology of myopic traction maculopathy

MTM development has been attributed to two distinct groups of forces exerting influence on the retina: preretinal and subretinal factors [31]. Preretinal factors include forces that generate centrifugal and tangential traction on the retina, such as incomplete posterior vitreous detachment (PVD), VMT, and ERM. However, subretinal factors involve forces that induce centrifugal traction on the retina, such as the deformation of the scleral eyewall. If either group of forces surpasses the retina’s limited elasticity, which is constrained by small retinal vessels, a thickened or stiffened ILM, or vitreous remnants, it can potentially cause damage to the retina [20, 27, 32, 33]. Understanding the pathophysiology of MTM is crucial for developing effective management strategies to preserve vision in affected individuals. The pathophysiology of MTM is multifactorial and involves several interrelated mechanisms.

2.1 Posterior vitreous detachment

PVD is linked to serious ocular conditions, such as retinal tears, rhegmatogenous RD, vitreous hemorrhage, MHs, and VMT syndrome, as reported in multiple studies [34, 35, 36, 37, 38, 39, 40]. Retinal complications associated with PVD are more commonly observed in individuals with HM than in those without HM [12, 17, 27, 40, 41, 42, 43, 44]. As a result, it is presumed that PVD advancement differs between highly myopic and nonhighly myopic eyes. The vitreous humor in highly myopic eyes tends to liquefy, leading to PVD [45]. The occurrence of partial or complete PVD was identified as a contributing factor to the increased development of traction, particularly in myopic eyes compared with emmetropic eyes [46, 47]. Moreover, highly myopic eyes were found to exhibit the formation of a specific gap termed the posterior precortical vitreous pocket (PPVP) between the vitreous cortex, which is in contact with the ILM, and the vitreous itself, which could mimic the effects of PVD [47]. PVD is rare in eyes with MTM, but the reason for this has not been determined [48, 49, 50]. Prior investigations employing different techniques to study the posterior vitreous revealed that PVD occurs at an earlier age in individuals with HM than in those without HM (nonhighly myopic patients) [46, 47, 51, 52]. Until the advent of swept-source optical coherence tomography (SS-OCT), precise visualization of the posterior vitreous was not feasible [53, 54, 55].

A study conducted by Itakura et al. [47] utilized SS-OCT and demonstrated that both partial and complete PVD occur earlier in highly myopic patients than in nonhighly myopic patients. However, their investigation did not include a detailed classification of the subtle progression of partial PVD, although they had a three-stage classification system for partial PVD that covered paramacular, perifoveal, and peripapillary PVD [56]. Additionally, Takahashi et al. [57], employing ultrawide field SS-OCT, reported various abnormal PVD patterns specific to the PM. More recently, among highly myopic patients aged ≥60 years, PVD tended to occur at a younger age in women than in men [58]. Therefore, to gain a better understanding of the situation, it is crucial to compare the status of PVD between patients with and without high myopia using cohorts matched for age and sex. Furthermore, a more intricate classification of partial PVD stages is necessary.

2.2 Bruch’s membrane and choroidal changes

HM is strongly associated with various retinal and macular complications, including FS, FRD, and MHs, which are partly caused by vitreous traction. MTM has been demonstrated to occur in approximately 9.0–34.4% of highly myopic eyes with PS [10, 16]. Approximately 10% of highly myopic eyes have macular Bruch’s membrane (BM) defects, which could be closely linked to other chorioretinopathies [59]. The BM is a 2–4 μm-thick acellular sheet positioned between the choroid and RPE [60]. The BM serves as a barrier between the retinal pigment epithelium (RPE) and choriocapillaris. In addition to spatially separating the retinal and choroidal compartments, BM potentially plays a biomechanical role in supporting the shape and form of the eyeball. For eyes with myopia, there is a hypothesis suggesting that axial elongation could be influenced by BM production in the retro-equatorial region [61]. Regarding chorioretinopathy, scientists have discovered that macular BM abnormalities could serve as a distinctive feature in cases of patchy atrophy or myopic CNV, leading to foveal atrophy [62, 63]. Additionally, the presence of a dome-shaped macula (DSM) appears to be significantly associated with macular BM defects [64]. The root cause of these BM abnormalities appears to be related to increased tension within the membrane; however, the precise underlying mechanism remains unclear. Similarly, the myopization process and development of fundus lesions in highly myopic eyes pose a challenge to elucidate [65].

The vascular choroid supplies nutrients and a high concentration of oxygen to the outer layers of the retina [66]. This vascular network is crucial for maintaining homeostasis and normal functioning of the outer layers of the retina, including the RPE. Changes in the choroid structure may indicate the presence of an underlying disease. To effectively assess the condition of the choroid in both healthy and diseased retinas, clinicians often rely on choroidal thickness measurements in their research [67]. However, it is important to note that choroidal thickness alone has limitations as it cannot fully characterize the vascular flow between the stromal and luminal vascular regions.”

2.3 Foveoschisis

During MTM progression, the earliest change in the retina is known as retinoschisis (RS). When it involves the macula, it is termed MS; when it involves only the fovea, it is called FS [68] (Figure 2). These changes occur in approximately 8–34% of individuals diagnosed with PM [10, 16, 69]. This condition was first described by Calbert Phillips in 1959 when he observed localized posterior RD occurring over a PS without a detectable MH. He speculated that conditions such as FS may explain this RD [70].

Figure 2.

Macular foveoschisis with extensive tractional elongation of Henle’s nerve fiber layer, foveal thinning, inner and outer schisis-like retinal thickening, and epiretinal membrane (ERM) on the temporal side.

The term “myopic foveoschisis” was introduced by Takano and Kishi in 1999. They described it as the splitting of the macular inner retinal layers, resulting in a thinner outer layer and thicker inner layer [10]. In 2003, Baba et al. found a correlation between FS and PS, suggesting that FS may be due to scleral protrusion, which surpasses the stretching capacity of the retina [16]. Benhamou et al. characterized FS as a thickening of the outer retinal layer, with perpendicular columns of tissue bridging the outer and inner layers known as tractional elongation of Henle’s layer [18]. This progressive separation of the retinal layers appears as long, straight, and highly reflective lines at the fovea and throughout the RS area when observed using OCT [71]. FS is often accompanied by other OCT features, such as ERMs, detachment of the ILM, retinal microfolds, defects in the ellipsoid zone (EZ) line, paravascular micro holes, inner or outer LMHs, FTMHs, and chorioretinopathy [72]. According to Wu et al. [69] OCT images of myopic FS or early-stage MTM reveal splitting of the neurosensory retina into two distinct layers. One layer is a thin outer retinal layer positioned on the RPE, and the other is a thicker inner retinal layer [69].

Various classifications have been proposed for FS. Shimada et al. suggested five categories of outer FS based on its location and extension: no apparent FS (S0), extrafoveal FS (S1), foveal FS (S2), foveal FS without involvement of the entire macula (S3), and FS with complete macular involvement (S4) [27]. In contrast, Fujimoto et al. and Ceklic et al. classified FS based on the location of the splitting of the retina into inner, outer, or both inner and outer FS [71, 73]. The exact cause of myopic FS remains uncertain; however, several factors have been proposed to contribute to its development, including posterior vitreous traction, reduced ILM flexibility, inflexibility of retinal vessels, presence of an ERM in conjunction with elongation of the axial length (AXL), and retinal stretching due to staphyloma [18, 21, 69, 74].

2.4 Foveoretinal detachment

FS can progress to FRD over time (Figure 3), but its progression is generally slow. In some instances, FS may remain stable or even improve if traction on the retina is spontaneously relieved [75]. According to Gaucher et al., myopic FS can trigger the formation of ERMs, FRD, MH, LMH, and MHRD, which are usually responsible for the dramatic deterioration of the patient’s BCVA [17]. A study conducted by Shimada et al. monitored 207 highly myopic eyes for a minimum period of 24 months. They observed a decrease or complete resolution of FS in 3.9% of the eyes, while 11.6% of the eyes exhibited progression from FS to FRD or more advanced stages of MTM. Notably, eyes with more extensive FS tend to experience a higher likelihood of progression than those with less extensive FS [27].

Figure 3.

Magnified macular image of moderately elevated foveoretinal detachment (FRD) with thinning of the foveal roof and outer schisis-like macular thickening and evidence of epiretinal macular proliferation.

Another study conducted by the same authors [12] categorized the stages of progression from FS to RD by using OCT.

• Stage 1: Characterized by irregularity in external retinal layer thickness with localized retinal elevation.

• Stage 2: The development of an outer lamellar macular hole (O-LMH) occurs either in the foveal or extrafoveal region and is associated with a small RD.

• Stage 3: The O-LMH increases vertically and horizontally, separating the column-like structures within the RS layer, with concurrent enlargement of the RD.

• Stage 4: RD further enlarges, and the RS resolves.

These findings shed light on the possible evolution of FS to more severe conditions such as FRD, O-LMH, I-LMH, FTMH, and MHRD, highlighting the importance of close monitoring in eyes with high myopia.

2.5 Lamellar macular hole

LMH is characterized by irregularities in the foveal contour, where there is a defect in the inner retina with or without splitting within the retinal layers [76]. In some instances, there may be disruptions in the outer retinal layers, including the external limiting membrane (ELM) and EZ [77, 78, 79, 80, 81, 82]. LMHs can be further classified into two types: inner LMHs (I-LMHs), characterized by the splitting of the inner foveal layers (Figure 4), and outer LMHs (O-LMHs), characterized by the splitting of photoreceptors [14] (Figure 5). However, the mechanisms underlying LMH formation are subject to ongoing debate in the scientific community. The emergence of OCT has enabled the identification of structural changes associated with LMH, such as ERMs and VMT [81, 83, 84]. Govetto et al. observed two distinct morphologies of LMHs and proposed that they may arise through either a tractional process or degenerative evolution [85]. More recently, Hubschman et al. redefined LMH-related lesions as “LMH,” “ERM with foveoschisis,” and “macular pseudohole,” supporting the hypotheses of both tractional and degenerative evolutionary pathways [86].

Figure 4.

Inner lamellar macular hole (I-LMH) with nasal epiretinal macular proliferation; automated red and blue segmentation lines in this horizontal B-scan partial-thickness macular hole indicate tissue irregularities.

Figure 5.

Complex localized foveoretinal detachment (FRD) with evidence of outer lamellar macular hole (O-LMH), there is evidence of outer schisis-like macular thickening and vitreomacular traction.

In nonmyopic eyes, LMH is associated with two types of ERM: conventional ERM, commonly found in macular pucker, appearing as a highly reflective line overlying the retinal nerve fiber layer (RNFL) with tractional properties, and atypical ERM, which is a thicker membrane delineated by a highly reflective line filled with moderately reflective material that lacks tractional properties [80]. In eyes with HM, the clinical progression of LMHs is characterized by increased complexity and instability due to the presence of intricate forces, including the adherent posterior hyaloid, ERM, rigid ILM, PS, and the occurrence of macular RS [87, 88, 89, 90].

The stability of myopic LMH is a subject of ongoing debate. Dell’Omo et al. conducted a retrospective observational case series of 44 myopic eyes with LMH and found that they were often linked with ERMs and LMH-associated epiretinal proliferation (LMHEP). Over time, they observed both morphological and functional stability in these patients [89]. In contrast, Frisina et al. performed a retrospective observational longitudinal study of 40 myopic eyes affected by LMH and pseudoholes. They discovered that myopic LMHs, particularly those associated with atypical ERMs, represent a more severe condition than those associated with conventional ERMs. Moreover, they observed that myopic LMHs may not be stable and may progress to FTMH [91]. In conclusion, understanding LMH variations and progression is crucial for better outcomes and requires advancements in imaging technology.

2.6 Macular hole and macular hole retinal detachment

Myopic FTMH is an advanced stage of MTM that is associated with significant visual impairment [92] (Figure 6). Ikuno et al. [93] observed 44 eyes with myopic FS and noted that its natural progression typically advanced from RS to MH and then to MHRD (Figure 7). The status of the fovea was identified as a prognostic indicator for the success of surgical interventions, such as vitrectomy and ILM peeling, with better surgical outcomes observed in the RS group and poorer outcomes in the MH group [93]. According to Jo et al. [94], myopic MH can be classified into two types: the “flat type” and the “schisis type.” The “flat type” closely resembles idiopathic macular holes (IMHs) and typically does not progress to MHRD. On the other hand, the “schisis type” is characterized by a tall and straight-sided configuration with a sharp angle at the top, forming an acute-angled edge that is shorter than the base diameter. The “schisis type” is associated with a higher risk of developing MHRD.

Figure 6.

Irregular full-thickness macular hole (FTMH) with moderate schisis-like thickening of the macula due to tractional elongation of Henle’s nerve fiber layer and epiretinal traction on the nasal border of the hole.

Figure 7.

Full-thickness irregular macular hole and retinal detachment associated with a shallow posterior staphyloma.

2.7 Different stages of MTM and clinical manifestations

Previously, MTM grading was not commonly practiced and primarily relied on clinical examination using slit-lamp biomicroscopy or fundus photographs. Some classification systems based on fundus photography, such as the International Photographic Classification Grading System, exist [95]. However, with the widespread adoption of OCT machines in clinical settings, the diagnosis of MTM has become increasingly accurate.

Parolini et al. introduced the Myopic Traction Maculopathy Staging System (MSS), which classifies MTM into two evolutionary patterns based on OCT images. They also determined the average time of progression of MTM, confirmed a decline in visual acuity with advancing stage, and observed a correlation between MTM staging and age. They investigated the pathogenesis of MTM by describing various centrifugal forces acting on the retina and fovea, counteracting the centripetal forces exerted by Müller cells, the external limiting membrane (ELM), and the ILM that maintain retinal integrity. Based on these theories, Parolini et al. outlined two evolutionary patterns in MTM: retinal and foveal patterns. Retinal patterns evolve from inner MS (I-MS) or inner and outer MS (IO-MS) in stage 1 to predominantly outer MS (O-MS) in stage 2 and then progress to MS with macular detachment (MS-MD) in stage 3 and eventually to MD in stage 4. Conversely, the foveal patterns evolved from a normal foveal profile in stage a to I-LMH in stage b and finally to FTMH in stage c. The presence of O-LMHs and any epiretinal abnormalities are additional findings associated with each pattern and are denoted in the MSS as “O” and “+”, respectively. Moreover, Parolini et al. observed a gradual reduction in the mean MTM evolution as it progressed from stages 1 to 2 (20 months), stages 2 to 3 (12 months), and stages 3 to 4 (3 months), with BCVA decreasing as the stages advanced. Additionally, they found a correlation between MTM stage and patient age [14].

In 2019, Ruiz-Medrano et al. proposed the ATN classification system that combines clinical examinations and OCT findings to categorize MTM. This system classifies MTM based on macular appearance (atrophic, A), presence of traction observed on OCT (tractional, T), and the presence or history of neovascularization (neovascularization, N) [13, 96]. The ATN classification accounts for tractional and neovascularization-related changes and has demonstrated high consistency and agreement among different observers [97]. Precise pathological staging of MTM plays a crucial role in making well-informed decisions regarding the optimal timing of surgical intervention for both the affected and fellow eyes [98].

3. Surgical approaches in myopic traction maculopathy

The historical development of the ab externo approach to MTM dates back to 1930, before the formal definition of MTM. The initial concept involved reinforcing the posterior sclera to prevent the progressive elongation of the myopic eye. Various materials, such as fascia lata [12], donor sclera [99], and lyodura (derived from processed cadaver dura mater) [100], have been used for this purpose. A modified posterior scleral reinforcement (PSR) technique was proposed by Snyder and Thompson and further refined by several researchers [100, 101, 102, 103, 104]. Additionally, the MB technique, introduced by Schepens et al., is considered the primary surgical approach for treating MTM [105].

3.1 Macular/scleral buckling

MB in combination with scleral imbrication has proven to be an effective treatment that significantly enhances the surgical success rate of MH-associated macular degeneration. MB is essential for alleviating both anteroposterior traction resulting from PS and tangential traction exerted by the vitreous cortex [106, 107]. The rationale behind MB was to counteract pathological posterior bulging and stretching of the sclera, particularly in eyes with pronounced PS, which is a significant risk factor for MTM development [108, 109]. The evolution of macular buckling is shown in Figure 8. For a considerable period of time, the ab externo approach was overshadowed by the ab interno approach. However, in the 2000s, the MB technique made a comeback with the use of sponges or solid silicone exoplants, resulting in a high rate of reattachment [107, 110]. The MB technique was reported in 2009 by Ward to effectively control axial myopia by shortening the AXL in HM, exhibiting better visual outcomes than PPV [111], and was regarded as the gold standard for treating MTM when compared to the ab interno approach, as per Alkabes and Mateo’s 16-year review of MB for MTM [112].

Figure 8.

The evolution of macular buckling with historical depiction.

3.2 Pars plana vitrectomy

PPV is currently considered the gold standard treatment for MTM, resulting in maintenance and improvement of vision in most cases [16, 113]. The most commonly employed surgical approach for MTM involves PPV with complete ILM removal, a procedure known as ILM peeling (ILMP) [33, 114]. The introduction of surgical techniques such as ILMP and laser treatment around the edges of the MH yielded promising anatomical results with success rates of up to 90% but limited functional recovery [115, 116, 117, 118]. However, MH occurs in approximately 5–28.6% of eyes that have undergone PPV with ILMP for the treatment of MTM, resulting in unfavorable visual outcomes even after a repeated surgical procedure [28, 87, 93, 119, 120, 121, 122, 123, 124, 125, 126, 127, 128, 129, 130]. Recently, a novel approach called fovea-sparing internal limiting membrane peeling (FSIP), described by Shimada et al. [120], has emerged in the scientific community (Figure 9). This technique aims to prevent postoperative MH formation after surgery by preserving the foveal Müller cell cone [121]. Shimada et al. [120] compared the FSIP and complete ILMP groups. The study showed a relatively higher occurrence of MH formation in the complete ILMP group; however, this difference was not statistically significant. Additionally, there was no substantial improvement in postoperative BCVA in the FSIP group compared to that in the complete ILMP group. However, subsequent studies with larger sample sizes reported contrasting results. These studies revealed a significant difference in postoperative BCVA [121] and CMT [131] between the two groups. Furthermore, various outcome measures were explored to compare the complete ILMP and FSIP groups. PPV combined with ILM has been effective in relieving major traction in some cases [33, 114]. However, postoperative FTMH can develop in up to 28.6% of cases [121]. To overcome these complications, FSIP has gained attention [120, 121, 131, 132, 133, 134], and this approach is not entirely free from FTMH formation, particularly because of the vulnerability of the thin fovea to mechanical forces during surgery [131]. To address larger or persistent FTMH, an alternative method known as the inverted internal limiting membrane flap (ILMF or modified ILMF) has been utilized [134, 135]. According to Lin and Yang, both the FSIP technique and the combined FSIP and ILMP technique demonstrated the ability to enhance both BCVA and central macular thickness (CMT). Nevertheless, none of the 35 eyes in the modified ILMF group developed postoperative MH after surgery. In contrast, in the FSIP control group, two eyes experienced immediate MH development after surgery, and one eye had a delayed occurrence of MH [136].

Figure 9.

Intraoperative image of the fovea-sparing internal limiting membrane peeling approach.

Furthermore, different intravitreal tamponades, such as gas and silicone oil (SO), were combined with PPV. Although SO showed a higher anatomical success rate than gas, several authors have reported unsatisfactory functional outcomes [137, 138]. PPV was subsequently adopted for the treatment of RS, MS, and RD without MH. However, PPV has limitations, such as the limited power of tamponades due to the configuration of the PS, the potential weakening of an already fragile retina through ILM peeling, and difficulties in visualizing atrophic changes in the myopic choroid. Consequently, the success rate of PPV in MTM remains variable across different studies, leading to ongoing debates regarding its use in such cases [23, 139, 140, 141, 142].

3.3 Combined vitrectomy and macular buckling

The combination of MB and vitrectomy allows simultaneous treatment of tangential and anteroposterior tractions of the MTM [29]. MTM management has evolved over the years, and combined vitrectomy and MB surgery have emerged as promising treatment approaches [143]. Vitrectomy was performed to address anteroposterior traction caused by the vitreous. To counteract tangential force, the surgeon peels the ILM, achieves complete PVD from the optic nerve and macula, and removes the ERM if present [93, 119, 127, 144]. In cases where there are recent or unsuccessful macular tractional changes despite vitrectomy, attention should be given to the third component of the tractional force acting at the macula, the staphyloma-related scleral-retinal mismatch. In such instances, an MB is necessary to provide support for the staphyloma [29, 145, 146]. Although further research and long-term follow-up studies are warranted to validate these findings, the combination of vitrectomy and MB surgery holds great potential as a comprehensive treatment option for effectively managing MTM.

4. Choroidal vascularity index

CVI has gained popularity as a convenient and noninvasive measure owing to its simplicity and calculation method [147, 148, 149]. The CVI can be derived from enhanced OCT images by using digital binarization and quantification techniques [150, 151]. Unlike choroidal thickness, the CVI provides a more comprehensive assessment of choroidal structure by capturing both vascular and stromal changes. Numerous studies have associated changes in the CVI with the development and progression of various retinal diseases [147, 152, 153]. CVI can detect specific microcirculatory alterations in the retina [154, 155, 156] and is associated with visual function after vitrectomy [157]. Given that retinal diseases often involve multiple processes affecting the choroid, such as inflammation, edema, and leakage, the CVI has been proposed as a potentially valuable biomarker for evaluating the integrity of the choroidal vascular network [152, 158]. Moreover, earlier investigations have demonstrated that the CVI remains unaffected by factors such as AXL, blood pressure, and intraocular pressure, making it a reliable measurement [159].

4.1 Methodology applied to calculate the CVI and its clinical relevance

Initially, the CVI was computed using a horizontal B-scan that passed through the fovea, and it subsequently became a widely adopted conventional method in numerous studies found in the literature. Agrawal et al. demonstrated that the scanning area, whether subfoveal, total macular, or central macular, does not influence the final CVI results in healthy individuals [160]. Therefore, a single subfoveal scan could reliably represent the posterior pole. Furthermore, the type of OCT scan, whether swept-source (SS) or spectral-domain (SD), had no impact on the CVI values [161].

The CVI values were calculated based on macular images obtained using SD-OCT. High-resolution 9-mm horizontal OCT-B images were chosen and imported into ImageJ analysis software (version 1.53, http://imagej.nih.gov/ij/). These images are initially converted into an 8-bit format and adjusted using the Niblack automatic local threshold. Next, the subfoveal choroid area was manually selected from 750 μm nasal to 750 μm temporal in the horizontal plane from the foveal center and from the RPE-Bruch membrane to the scleral border in the vertical plane. The total choroidal area (TCA) was measured using an adaptable geometric polygon tool. Subsequently, the stromal vascular tissue area was determined by counting the number of white pixels, whereas the luminal area (LA) at the enhanced choroid was calculated by applying the threshold tool and quantifying the number of dark pixels. Finally, the dark-to-light pixel ratio is expressed as a percentage and defined as CVI, as previously described by Agrawal et al. [148, 152].

CVI is derived by taking the ratio of LA to the total choroidal area (TCA), and it is expressed as a percentage [162]. This parameter offers a distinct opportunity to acquire information about choroidal perfusion, as it precisely mirrors the vascular alterations in the choroid [1]. CVI is calculated as follows: CVI = (luminal area/total choroidal area) × 100.

CVI is usually expressed as a percentage, representing the proportion of the choroid occupied by the blood vessels. The protocol study method for the binarization method is shown in Figure 10.

Figure 10.

Method used for quantifying the CVI in healthy myopic eyes. (a) Binarized image designed to depict the intraretinal structure and choroidal vascular layers in greater detail in a healthy, highly myopic eye with an axial length of 29.2 mm. (a1) Magnified image within the yellow square showing binarized processing of the subfoveal choroidal vascular stroma and luminal vascular visualization of the subfoveal choroidal vessels to obtain a choroidal vascularity index (CVI) of 64.2%. The selected subfoveal area of choroidal flow is clearly delineated by the white-yellow dotted line. (b) Binarized processing of choroidal flow in a healthy highly myopic eye with an axial length of 30.2 mm. (b1) Enhanced choroidal vessel visualization yielding a CVI of 62.3% inside of the magnified image within the white-yellow dotted line clearly delineating a CVI of 62.3%. (c) Binarized image corresponding to a healthy, highly myopic eye with an axial length of 29.7 mm in the control group. (c1) The white and yellow dotted lines depict the binarized choroidal flow area selected to calculate the CVI. The CVI was 63.4% inside the selected choroidal flow area in the magnified image depicting the selected area for the CVI measurements.

4.2 Clinical relevance and role of the CVI in assessing choroidal vascular changes in MTM

CVI has proven to be informative in determining the condition of the choroidal vasculature across various disease and treatment scenarios [163, 164, 165, 166, 167, 168]. Reliable quantitative metrics, such as the CVI, have been devised to diagnose, categorize, and track retinal disorders [169]. An increase in the CVI can result from an increase in the number of blood vessels or the diameter of choroidal blood vessels in a specific area [152]. Hayreh [170] demonstrated that the submacular choroidal supply is susceptible to general chronic ischemic conditions such as AMD because of the multiple watershed zones of the short posterior ciliary arteries in the choroid. The clinical implications of the CVI could be significant and warrant further investigation in subsequent studies [170]. Conversely, a decrease in the CVI at baseline might indicate choroidal ischemia in patients with macular disorders such as AMD or diabetes. In contrast, the CVI can be used to determine an increase in choroidal vascularity in cases of posterior uveitis or central serous chorioretinopathy. Moreover, the CVI can serve as a valuable tool for monitoring the treatment response and disease resolution [152]. MTM is a progressive condition that has been classified into four stages [171, 172]: stage 1, MF; stage 2, FRD; stage 3, myopic MHs; and stage 4, MHRD. Employing noninvasive techniques, such as CVI estimation, to monitor disease and treatment outcomes could significantly enhance the management of MTM [173]. In a case series conducted by Quiroz-Reyes et al., which included eyes with MTM, patients with more advanced disease stages tended to exhibit lower CVIs [1].

5. CVI alteration after surgery in myopic traction maculopathy

Numerous studies have established a connection between the CVI and the development and progression of various diseases, including genetic, retinal, and macular conditions [149, 152, 153]. These investigations suggest that the CVI can serve as a distinctive indicator of retinal diseases. Since retinal diseases involve multiple factors, such as inflammation, edema, and leakage, the CVI has been suggested as a potential marker because it reflects the changes that affect the integrity of the vascular network within the highly blood-supplied retinal structure known as the choroid [152, 158]. Consequently, quantifying vascular factors is believed to accurately represent the ongoing disease pathogenesis.

In a previous study [1], we investigated the CVI as a potential biomarker of myopic traction maculopathy (MTM). In this investigation, data were collected from normal eyes in the control group, one being a healthy emmetropic eye and the other a healthy highly myopic eye, with an intervention group consisting of four patients with MTM related to high myopia. The findings revealed that the CVI was significantly lower in the disease group than in the control group. This suggests that the CVI may indicate disease pathology in MTM, and a lower CVI in diseased eyes could be linked to choroidal vascular defects caused by PM or surgical procedures, potentially influencing the manifestation, progression, and functional outcomes in different stages of surgically resolved MTM. Preoperative patient characteristics were mostly similar and directly comparable, except for visual acuity, which was expected to be poor in the disease group. The study found differences in TCA and CVI between normal subjects and MTM patients; however, among the surgical groups, the CVI was similar for the surgical patients. However, the CVI proved to be a useful noninvasive biomarker, distinguishing patients in the MTM group from those in the healthy control group. It has been reported that age and the CVI are inversely related in healthy eyes, and the study showed an inverse correlation between the CVI and ILM surgical techniques, suggesting that this procedure may not favor better long-term visual recovery in patients with MTM [174]. Nevertheless, surgical intervention significantly improved visual acuity in all participants.

In conclusion, this study highlights the potential of the CVI as a biomarker for MTM and its significance in differentiating healthy eyes from eyes with MTM. Further research is needed to explore and quantify the CVI in myopic subjects to better understand its implications in high myopia.

From the surgical experience of the author, representative and complex clinical cases of highly myopic eyes in which macular surgery was performed at different stages of MTM with the corresponding long-term postoperative and enhanced binarized OCT imaging evaluation and CVI calculations are shown in Figure 11.

Figure 11.

Surgical cases. (a) Preoperative OCT findings consistent with myopic foveoschisis (FS) due to macular and schisis-like thickening of the inner and outer retinal layers at the macula. (a1) Binarized image of the preoperative myopic FS in a symptomatic, highly myopic patient. This is a very complex FS with outer and inner retinal layer-like thickening, tractional elongation of Henle’s layer, and a very thin superficial foveal layer. This preoperative binarized image showed a CVI index of 64.6% between the normal range among the normal controls. (a2) After a 31-month follow-up, the center of the macular region appeared thinner, with a normal foveal profile and without evidence of a macular hole (MH). OCT biomarkers, such as a normal foveal contour and internal and outer neuroretinal lines with total restoration of the central subfoveal ellipsoid zone (EZ), were observed. (a3) Postoperative long-term binarized image with a CVI of 53.3% lower than the mean control value. (b) Preoperative myopic FS in a symptomatic, highly myopic patient. This FS exhibited outer retinal layer-like thickening, tractional elongation of Henle’s layer, and epiretinal membrane (ERM) proliferation mainly over the temporal side of the macula. (b1) Preoperative binarized image showing a CVI index of 61.9%. (b2) Long-term postoperative horizontal B-scan with an almost normal foveal profile and diffuse thinning of the retina layers over the temporal side, no evidence of outer or inner retinal layer thickening, and final vision of 20/60. (b3) The long-term postoperative CVI calculated from the binarized image was 49.6% lower than that of healthy myopic controls. (c) Preoperative image of the right eye exhibiting chronic myopic foveoretinal detachment (FRD) with subretinal fluid, inner and outer retina layer-like thickening in a symptomatic highly myopic eye of 28.8 mm of axial length, and a very thin superficial foveal layer. (c1) Preoperative CVI was 63.2%. (c2) Corresponding long-term postoperative horizontal B-scan depicting diffuse atrophic thinning of the retinal layers and evidence of FRD flattening without ERM remnants. (c3) The CVI calculated from the binarized image was 49.6% in the last enhanced binarized image calculation. (d) Highly myopic eye with posterior staphyloma (PS) in a very symptomatic patient. Evidence of a full-thickness myopic macular hole (FTMH) with severe tractional elongation of Henle’s layer and thickening of the outer layers of the macula without evidence of macular detachment. (d1) Preoperative enhanced-definition binarized image of the corresponding highly myopic patient with FTMH showed a CVI of 61.8%. (d2) Postoperative long-term structural evaluation showed a flat macula with a recovered foveal profile, external limiting membrane (ELM) line lucency defect, and a well-preserved RPE layer. (d3) The long-term perfusion evaluation showed a CVI of 47.8% lower than the mean CVI of the healthy control eyes. (e) The 9 mm high-definition horizontal b-scan depicts full-thickness macular hole (MH)-related retinal detachment (RD). (e1) Corresponding preoperative enhanced-definition image showing a preoperative CVI of 59.7% in this 28.8 mm axial length highly myopic eye with a two-week evolution of very symptomatic MHRD. (e2) Corresponding postoperative image depicting a recovered foveal profile with diffuse retinal thinning and well-defined outer retinal markers. (e3) The corresponding long-term postoperative CVI in this enhanced binarized image was calculated as 45.9%, lower than that in the healthy myopic control eyes.

5.1 Advantages of the choroidal vascularity index

1. CVI enables the use of noninvasive imaging techniques such as OCTfor measurement, allowing patients to undergo assessments without the need for invasive procedures or contrast agents.

2. CVI shows promise in detecting early changes in ocular diseases, such as AMD and diabetic retinopathy, before significant symptoms or vision loss become apparent.

3. CVI offers a quantitative measurement, facilitating an objective and standardized evaluation of choroidal vascularity. This aspect is valuable for monitoring disease progression and gauging treatment response.

4. The CVI may aid in distinguishing between various ocular disease subtypes, leading to more precise diagnoses and personalized treatment plans.

5.2 Limitations of the choroidal vascularity index

1. Inadequate normative data: owing to its recent emergence as a biomarker, the CVI lacks sufficient normative data across diverse populations and ethnic groups. This limitation poses challenges for the accurate interpretation of the CVI values and their universal application.

2. Measurement variability: the CVI measurements can be affected by various factors, including image quality, segmentation algorithms, and observer differences. These variables may have led to inconsistent results.

3. Limited disease specificity: although the CVI can be valuable in detecting changes in choroidal vascularity, it may not offer specific insights into other retinal or optic nerve abnormalities associated with certain ocular conditions.

5.3 Comparison with other biomarkers

1. Compared with CMT, the CVI focuses on evaluating choroidal vascularity instead of retinal thickness. The CVI offers additional information about the health of the choroid and may provide complementary insights beyond what CMT can reveal in the context of retinal diseases.

2. CVI and retinal nerve fiber layer (RNFL) thickness are widely used biomarkers; however, they serve different purposes. While the RNFL thickness is commonly used in glaucoma evaluation, the CVI provides valuable information about choroidal vascular changes, which are not assessed by RNFL thickness measurements. Each biomarker had its own significance within its respective area of focus.

3. When comparing CVI with visual acuity (VA), it is evident that while VA measures a person’s ability to see, CVI is a quantitative biomarker that offers more detailed information about vascular changes in the choroid. By incorporating the CVI along with the VA, healthcare professionals can potentially enhance the accuracy of diagnosing and monitoring various ocular diseases.

6. Future directions

The investigation of MTM and its link to choroidal perfusion via the CVI has yielded valuable insights into the underlying mechanisms and clinical characteristics of this condition. Nonetheless, several aspects require further inquiry to advance our understanding and enhance patient care.

1. Longitudinal investigations: longitudinal studies to observe the progression of MTM and its relationship with changes in the CVI over time could provide crucial information about the natural history of the disease and identify potential risk factors for its progression.

2. Genetic and environmental influences: delving into the impact of genetic and environmental factors on the development and progression of MTM and their association with the CVI may provide insights into individual susceptibility and possible preventive measures.

3. Advancements in imaging: leveraging advancements in imaging technology, such as OCT-A and indocyanine green angiography (ICGA), may open new avenues for studying choroidal perfusion and its relevance to MTM. Combining various imaging modalities can yield comprehensive data on choroidal vascular changes.

4. Therapeutic interventions: investigating the effects of different treatment approaches, including pharmacological agents, intravitreal injections, and surgical methods, on CVI and MTM progression may lead to the development of more effective therapeutic strategies.

5. Collaborative large-scale studies: collaborative efforts involving multiple centers and patient cohorts could lead to larger-scale studies, strengthen the statistical significance of findings, and improve the generalizability of results.

6. Animal models: developing animal models that mimic the pathophysiology of MTM and enable the assessment of choroidal perfusion may provide additional insights into the disease mechanisms and potential treatment targets.

7. Comparison with other retinal diseases: comparing the CVI alterations in MTM with other retinal diseases, such as AMD or diabetic retinopathy, may help identify specific patterns of choroidal perfusion unique to MTM.

8. Functional correlations: investigating the functional implications of the CVI alterations and their relationship with VA and other functional outcomes in patients with MTM could aid clinicians in prognostication and treatment decision making.

7. Conclusions

In conclusion, this chapter presents a comprehensive overview of MTM, emphasizing the importance of choroidal perfusion assessed through the CVI evaluation. Through discussions on various topics, including the pathophysiology of MTM, its different stages, clinical manifestations, and surgical approaches, we have gained a better understanding of this complex condition. The introduction of the CVI calculation as a noninvasive and quantitative tool for evaluating choroidal vascular changes has demonstrated promising clinical relevance and broadens the knowledge of MTM. It offers valuable information about the vascular status, potentially assisting in early diagnosis and prognostication. Moreover, alterations in the CVI have been observed after surgery, suggesting its potential role as a prognostic indicator of surgical outcomes. However, much remains to be explored in the field of MTM and choroidal perfusion. Further research is crucial to unravel the intricacies of this condition and its correlation with the CVI. Longitudinal studies, the exploration of genetic and environmental factors, advancements in imaging techniques, and comparative analyses of other retinal diseases represent promising future directions. By addressing these research gaps and continuing to investigate the relationship between MTM and CVI, we can pave the way for a more precise diagnosis, improve patient management, and enhanced treatment strategies, ultimately improving the quality of life of individuals affected by this sight-threatening condition.

Acknowledgments

We express our deep appreciation to the technical staff of the Retina Department at Oftalmologia Integral ABC (Nonprofit Medical and Surgical Organization), Mexico City, Mexico, affiliated with The Postgraduate Study Division at the National Autonomous University of Mexico.

Conflict of interest

The authors declare no conflicts of interest.

Funding

No funding or grant support was received for this study.

Acronyms and abbreviations

AMD	age-related macular degeneration
ATN	classification system for myopic maculopathy including atrophic (A), tractional (T), and neovascular (N) components
AXL	axial length
BCVA	best-corrected visual acuity
BM	Bruch’s membrane
CMT	central macular thickness
CNV	choroidal neovascularization
CVI	choroidal vascularity index
DSM	dome-shaped macula
ELM	external limiting membrane
ERM	epiretinal membrane
EZ	ellipsoid zone
FSIP	foveal-sparing internal limiting membrane peeling
FRD	foveoretinal detachment
FS	foveoschisis
HM	high myopia
I-MS	inner macular schisis
ILMF	inverted internal limiting membrane flap technique
ILM	internal limiting membrane
ILMP	internal limiting membrane peeling technique
I-LMH	inner lamellar macular hole
IMH	idiopathic macular hole
I-MS	inner macular schisis
LMHEP	lamellar macular hole-related epiretinal proliferation
LCA	luminal choroidal area
LMHEP	lamellar macular hole-associated epiretinal proliferation
LogMAR	logarithm of the minimum angle of resolution
MD	macular detachment
MH	macular hole
MS	macular schisis
MS-MD	macular schisis with macular detachment
MSS	myopic traction maculopathy staging system
MHRD	macular hole-related retinal detachment
MTM	myopic traction maculopathy
OCT	optical coherence tomography
OCT-A	optical coherence tomography angiography
O-LMH	outer lamellar macular hole
O-MS	outer macular schisis
PPV	pars plana vitrectomy
PPVP	posterior precortical vitreous pocket
PM	pathologic myopia
PSR	posterior scleral reinforcement
PS	posterior staphyloma
RNFL	retinal nerve fiber layer
RPE	retinal pigment epithelium
RS	retinoschisis
RD	retinal detachment
SD-OCT	spectral-domain OCT
SO	silicon oil
SS-OCT	swept source OCT
SCA	stromal choroidal area
SRF	subretinal fluid
TCA	total choroidal area
VA	visual acuity
VMT	vitreomacular traction