Surgical Retina

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Editor
Masahito Ohji
Department of Ophthalmology
Shiga University of Medical Science
Otsu, Shiga, Japan

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Contents

1 Epiretinal Membranes and Macular Pseudoholes������������������������������������������������������� 1

Jen-Hsiang Shen, Wei-Chi Wu, and Chi-Chun Lai
2 Vitreomacular Traction Syndrome����������������������������������������������������������������������������� 23
Yusuke Ichiyama and Masahito Ohji
3 Macular Holes��������������������������������������������������������������������������������������������������������������� 27
Daniele Veritti, Valentina Sarao, Carla Danese, and Paolo Lanzetta
4 Myopic Foveoschisis and Macular Hole Retinal Detachment����������������������������������� 45
Kazunari Hirota and Akito Hirakata
5 Diabetic Retinopathy: Surgical Aspects��������������������������������������������������������������������� 55
Xuejing Chen and Michelle C. Liang
6 Retinal Detachment and PVR������������������������������������������������������������������������������������� 67
Peiquan Zhao
7 Cavitary Optic Disc Maculopathy������������������������������������������������������������������������������� 77
Nieraj Jain and Mark W. Johnson
8 Coloboma of the Choroid��������������������������������������������������������������������������������������������� 87
Andrew Carey and J. Fernando Arevalo
9 Intraocular Cysticercosis��������������������������������������������������������������������������������������������� 93
Gopal Lingam and Tarun Sharma
10 Basic Principles in 23-, 25-, and 27-Gauge Pars Plana Vitrectomy ����������������������� 101
Andreas Ebneter, Weng Onn Chan, and Jagjit Singh Gilhotra
11 Robot-Assisted Retinal Surgery: Overcoming Human Limitations����������������������� 109
K. Xue, T. L. Edwards, H. C. M. Meenink, M. J. Beelen, G. J. L. Naus,
M. P. Simunovic, M. D. de Smet, and R. E. MacLaren

v
About the Editor

Masahito Ohji, MD, graduated from Osaka University in 1983. He is currently Professor
and Chairman of the Department of Ophthalmology, Shiga University of Medical Science,
Japan. He has more than 200 peer-reviewed international publications and several book
chapters to his credit. He is the treasurer of the Asia Pacific Vitreoretinal Society, a trustee
of the Japan Ophthalmology Society, and an executive committee member of the Club Jules
Gonin. Dr. Ohji has received several awards, including Achievement Award and Senior
Achievement Award from the American Academy of Ophthalmology, International
Gold Award from the Chinese Ophthalmological Society, and Tano Lecture and Achievement
Award from the Asia-Pacific Academy of Ophthalmology.

vii
‘Retina Atlas’ series includes the following 9 Volumes:

1. Retinal Imaging
2. Retinal Vascular Disorders
3. Macular Disorders
4. Surgical Retina
5. Inflammatory and Infectious Ocular Disorders
6. Hereditary Chorioretinal Disorders
7. Pediatric Retinal Diseases
8. Ocular Oncology
9. Trauma in Retina

ix
 Epiretinal Membranes and Macular
Pseudoholes 1
Jen-Hsiang Shen, Wei-Chi Wu, and Chi-Chun Lai

1.1 Introduction In 1977, Gass proposed a classification as follows: (1) grade

0 (cellophane maculopathy), in which a translucent epiretinal
1.1.1 Epiretinal Membrane (ERM) membrane is not associated with distortion of the inner retina;
(2) grade I (crinkled cellophane maculopathy), in which the
Epiretinal membrane usually occurs in patients over inner retinal surface is distorted by a thin membrane; and (3)
50 years old and could be seen in 10–30% of the general grade II, in which the membrane is thicker, with a distinct gray-
population over 70 years old. Bilateral involvement is pres- ish appearance, and in which it obscures underlying vessels and
ent in 20% of these patients. Eighty percent of these mem- causes marked distortion of the retina (Table 1.1) [15].
branes are idiopathic, while about 20% are secondary to The management of ERM includes observation and vit-
previous retinal detachment, vascular, or inflammatory reti- reoretinal surgery. Most ERMs are with stable clinical
nal diseases [1–5]. course, but VA deterioration and intolerable metamorphopsia
The initial presenting visual acuity is usually fair, and the may still occur. Surgery is advised to patients: VA deterio-
progression is usually slow [6, 7]. rates under 20/100–20/50 or worse and/or intolerable meta-
Epiretinal membrane and its pathogenesis had first been morphopsia [9, 16].
reported by Iwanoff in 1865 [8]. However, most of the
advances on etiopathogenesis and management took place
from the 1980s. 1.1.2 Macular Pseudohole (MPH)
Historically, epiretinal membrane had also been called as
primary retinal folds, cellophane maculopathy, surface wrin- Macular pseudohole (MPH) originates from contraction of
kling retinopathy, preretinal macular fibrosis, macular epiretinal membrane (ERM), and it is typically round and
pucker, wrinkling of the internal retinal surface, interno-­ reddish under biomicroscopy (Fig. 1.1a, b). Patients’ initial
retinal fibrosis, and vitreoretinal interface changes [9]. visual acuity (VA) is often fair, but metamorphopsia may still
The pathogenesis of ERM was believed to be discontinu- exist in some patients. MPH could be seen in 8–20% of eyes
ity of the internal limiting membrane (ILM). Glial cells may with ERM [17].
proliferate onto the inner retinal surface. The collagen fibrils MPH was first described by Arthur W. Allen, Jr., an
of the cortical vitreous may tangle with the proliferation and American ophthalmologist, and John Donald MacIntyre Gass,
together form firm vitreoretinal attachment [9–11]. Epiretinal a Canadian-American ophthalmologist in 1976. They reported
membrane in case with prior retinal break or detachment four patients having a hole in an epiretinal ­membrane overlying
often had retinal pigmented epithelium (RPE) component
and sometimes had pigmented appearance [12–14]. Table 1.1 Epiretinal membrane grading proposed by Gass [15]
Grade Description
0; cellophane Translucent epiretinal membrane is not
J.-H. Shen maculopathy associated with distortion of the inner retina
Department of Ophthalmology, Chang-Gung Memorial Hospital, I; crinkled cellophane Inner retinal surface is distorted by thin
Linkou, Taiwan maculopathy membrane
W.-C. Wu · C.-C. Lai (*) II Thicker membrane with a distinct grayish
Department of Ophthalmology, Chang-Gung Memorial Hospital, appearance, and in which it obscures
Linkou, Taiwan underlying vessels and causes marked
College of Medicine, Chang-Gung University, Tauyuan, Taiwan distortion of the retina

© Springer Nature Singapore Pte Ltd. 2019 1

M. Ohji (ed.), Surgical Retina, https://doi.org/10.1007/978-981-13-6214-9_1
2 J.-H. Shen et al.

a b

c d

e
1 Epiretinal Membranes and Macular Pseudoholes 3

Fig. 1.1 (a) This is a right eye fundus from a 66-year-old male patient. insidious onset. Fundoscopy showed yellow-grayish thick ERM with
This color fundus picture shows central round reddish hole-like mild distortion of retinal surface and small vessels. Radial retinal folds
structure with contractile epiretinal membrane (ERM). Minimal vessel could all be also appreciated. Red-free photography was not taken
tortuosity could also be observed on the contractile ERM. (b) This is during this time point. (e) After 2 years of follow-up, the yellow-
the same fundus of (a) under red-free filter. We could observe the more grayish thick ERM with mild distortion of retinal surface and small
evident contractile folds around macula. (c) OCT image from two vessels. Radial retinal folds could all be also appreciated. The ERM
different patients showed macular pseudoholes with straight edges and was relatively stable. However, the VA deteriorated from 0.4 to 0.3 in
stretched edges. (d) This was the left eye of a 53-year-old female. She Snellen chart. Red-free photography was not taken during this time
complained of progressively blurred vision in the left eye with point

the macula that mimicked a macular hole. In two patients, the of the cortical vitreous may tangle with the proliferation and
clinical course was stable. One patient progressed to full-thick- together form firm vitreoretinal attachment [9–11].
ness macula hole. One patient had spontaneous peeling of ERM can occur in eyes with posterior vitreous detach-
epiretinal membrane and hole closure. All of the patients had ment (PVD) or no PVD yet. In 1977, Foos showed the inter-
normal or nearly normal visual acuity at first presentation. Three nal limiting membrane (ILM) is especially thin over larger
patients had a slight fluorescence in the base of the hole in fluo- posterior retinal vessels [22, 23]. In these locations, discon-
rescein angiography (FA). The fluorescence is less than in true tinuity of ILM may occur, and glial cells may proliferate
macular holes and not present in lamellar macular holes [18]. onto the inner retinal surface. The collagen fibrils of the cor-
Due to advancement of optical coherence tomography tical vitreous may tangle with the proliferation and together
(OCT), the characteristics and morphology of macular form firm vitreoretinal attachment [9–11]. Foos also raised
pseudohole had been redefined. In 2004, Haouchine et al. that retinal ischemia and inflammation may produce enzy-
assessed 40 MPH cases and summarized a steepened foveal matic destruction of ILM integrity and induce glial prolif-
pit combined with thickened foveal edges and a small foveal eration [22, 23].
pit diameter as the features of the MPH. Central foveal Michels also summarized the hypothesis in patients with
­thickness was normal or slightly increased (167 ± 42 μm). PVD already [9]:
Mean perifoveal thickness was greater than normal
(363 ± 65 μm) [19]. Intraretinal split was considered to be 1. Full-thickness retinal breaks with liberation of retinal pig-
only lamellar macula hole at that stage. ment epithelial (RPE) cells into the vitreous cavity
In 2008, Gupta, Sadun, and Sebag demonstrated ERM 2. Disruption of the ILM, followed by proliferation of glial
with multifocal contraction tends to result in retinal edema cells onto the inner retinal surface
and intraretinal cystoid space [20]. In 2012, Michalewska 3. Mechanical damage to the optic nerve head, where
et al. were the first to find all subtypes of non-full-thickness ILM is attenuated or absent, followed by glial cell
macular hole (NFMH) belong to the same entity of macu- proliferation
lopathy due to ERM, internal limiting membrane (ILM), or 4. Intraocular hemorrhage or inflammation, or both, that,
hyaloid contraction [21]. in turn, introduces other cells capable of proliferation
In 2013, Gaudric et al. reviewed 54 eyes with MPH using [24, 25]
the Cirrus SD-OCT (Carl Zeiss Meditec, Dublin, California,
USA). They found 24 (44%) eyes had vertical foveal pit and Epiretinal membrane in case with prior retinal break or
straight, smooth edges on the OCT scan corresponding to detachment often had retinal pigmented epithelium (RPE)
centripetal contraction of the ERM. Nevertheless, 30 (56%) component and sometimes had pigmented appearance [12–
other eyes exhibited some degree of stretching and cleavage of 14]. Several factors have been associated with formation of
the foveal pit edge resulting from asymmetrical tangential macular epiretinal membrane after retinal reattachment
traction of the ERM between multiple epicenters of contraction. surgery [9]:
Thus, they proposed some lamellar macular holes (LMH)
might be a subcategory of macular pseudohole (MPH). 1. Increasing patient age [26]
2. Low preoperative visual acuity [26]
3. Total retinal detachment [27]
1.2 Etiopathogenesis 4. Preoperative evidence of epiretinal membrane formation
elsewhere in the eye [26]
1.2.1 ERM 5. Vitreous hemorrhage [28, 29]
6. Drainage of subretinal fluid and multiple perforations
The pathogenesis of ERM was believed to be discontinuity [27, 29]
of the internal limiting membrane (ILM). Glial cells may 7. Intraoperative complications including vitreous
proliferate onto the inner retinal surface. The collagen fibrils loss [29]
4 J.-H. Shen et al.

There are two hypothesized sources of contraction: myo- Table 1.2 Etiologies of epiretinal membrane
fibroblasts and contraction of vitreous fibrils [30, 31]. Study ERM etiology
Vascular leakage and intraretinal edema could be seen in Michels [9] Previous retinal detachment in 46 eyes (62%)
cases with thick epiretinal membrane and retinal distortion. Idiopathic in 9 eyes (12%)
Developmental in 4 eyes (5%)
FA can detect chronic leakage in about 20% of cases, but Previous cataract extraction in 3 eyes (4%)
these leakages did decrease overtime [9]. Previous uveitis, vitreous hemorrhage,
In 1981, Kampik and coworkers published the ultrastruc- photocoagulation, penetrating injury, other
tural findings in 56 eyes with epiretinal membranes. kinds of surgery in 12 eyes (16%)
Poliner et al. [32] Idiopathic in 61 eyes (69%)
Myofibroblast-like cells are seen in 91% of these eyes. RPE
Previous retinal detachment in 27 eyes (31%)
cells were identified only in eyes with retinal detachment with Yazici et al. [31] Idiopathic in 61 eyes (69%)
massive preretinal proliferation (MPP) (11 of 11 cases) or Previous retinal detachment in 27 eyes (31%)
prior retinal detachment (11 of 23 cases). Fibrous astrocytes Idiopathic in 125 eyes (43%)
and fibroblasts were observed in 44 (79%) and 43 (77%) eyes, Diabetic retinopathy in 107 eyes (37%)
Retinal vein occlusion in 28 eyes (10%)
respectively. In eyes (n = 23) with prior retinal detachment, the Uveitis in 12 eyes (4%)
percentage rose to 83% and 61%, respectively [31]. Previous retinal detachment in 5 eyes (2%)
In 1982, Michels released a series of 74 cases. Forty-six Other pathologies in 16 eyes (5%)
eyes (62%) had prior retinal reattachment surgery. Nine cases
(12%) were otherwise healthy eyes with PVD. Two eyes (3%)
Table 1.3 Etiopathogenesis of macula pseudoholes (MPH)
were considered developmental, while two eyes (3%) were
Study Etiopathogenesis
considered acquired type in young patients. Fifteen eyes
Allen and Gass [18] Centripetal contraction of ERM
(20%) had history of uveitis, damage from a penetrating Gaudric et al. [33] Centripetal force between eccentric
injury, vitreous hemorrhage, or prior photocoagulation or epicenters
surgery not related to retinal detachment. In the membranes Michalewska et al. [20] Hyperreflective linear structure, either
removed, he identified the following components: epiretinal membrane, thickened internal
limiting membrane, or hyaloids could be
the common cause of all types of
1. Pigment epithelial cells non-full-thickness macular holes (NFMH)
2. Fibrous astrocytes
3. Macrophage
4. Fibrocytes Table 1.4 Type of pseudohole features and epiretinal membrane con-
traction [34]
5. Microfilaments and extracellular collagens
Pseudohole feature ERM contraction
In a more recent report by Yazici et al. in 2011, the major- Straight foveal edge Smooth ERM, contracted around pseudohole,
(n = 24) causing radial retinal folds that converged
ity of ERM remained to be idiopathic in most eyes (43%) toward the edge of the membrane, thus
[32]. However, it is very difficult to compare these epidemi- revealing the centripetal forces of contraction
ology studies, because the difference in patient population (n = 18)
may influence these results greatly (Table 1.2). Complex pattern fold (n = 4)
Smooth, no visible folds (n = 2)
In summary, the pathogenesis of ERM was believed to be Stretched edge with Multiple epicenters of contraction,
discontinuity of the ILM. Glial cells may proliferate onto the partial cleavage of asymmetric distortion Eversion of foveal edge
inner retinal surface. The collagen fibrils of the cortical inner and outer (n = 22)
vitreous may tangle with the proliferation and together form retina (n = 30) Smooth with few folds (n = 4)
More or less radial (n = 4)
firm vitreoretinal attachment. ERM can occur in eyes with
posterior vitreous detachment (PVD) or no PVD yet. The
grading of ERM still follows the Gass classification as grades force of epiretinal membrane in 1976 [18]. There are two
0, I, and II (Table 1.1). The pathology exam showed the studies to support this assumption, and they provided more
component of ERM as pigment epithelial cells, fibrous detailed proposals [21, 34] (Table 1.3).
astrocytes, macrophage, fibrocyte, microfilaments, and Some pseudoholes have stretched edge or intraretinal
extracellular collagens. cleavage that could not be simply explained by one center
of centripetal contraction. Thus, Gaudric et al. studied the
en face OCT images of 54 eyes with MPH. They found 24
1.2.2 MPH eyes with straight edges and 30 eyes with stretched edges
(Table 1.4 and Fig. 1.2). They found MPH with straight
There is currently no published histopathologic report of a edges often had smooth ERM, contracted around pseudo-
macular pseudohole [34]. The pathogenesis of macular hole hole, causing radial retinal folds that converged toward the
was initially proposed by Allen and Gass to be the contraction edge of the membrane, revealing the centripetal forces of
1 Epiretinal Membranes and Macular Pseudoholes 5

Fig. 1.2 (a) High-resolution

optical coherence a
tomography (OCT) showed
thickened ERM and central
macula edema with
intraretinal split, on both
horizontal section (a) and
vertical section (b). (b)
High-resolution optical
coherence tomography
(OCT) showed thickened
ERM and central macula
edema with intraretinal split,
on both horizontal section
(a) and vertical section (b)

b
6 J.-H. Shen et al.

Table 1.5 Characteristics of ERMs on SD-OCT analysis [35] 1 day were also administered. After 1.5 months
ERM Pseudohole eyes (n = 27) postoperatively, follow-up OCT showed removal of ERM
Typical tractional ERM 24 and ILM on central macula, on both horizontal section
Atypical epiretinal tissue 0 (Fig. 1.3a) and vertical section (Fig. 1.3b).
Combined 3 After 2.5 months postoperatively, the intraretinal split
subsided and initial restoration of foveal depression
Table 1.6 Proposed stages of macular pseudoholes [36] could be observed (Fig. 1.4a, b). After 6.5 months
Stages Number Definition postoperatively, the anatomical improvement had been
1 14 No cleavage stable (Fig. 1.5a, b).
2a 13 Localized cleavage not crossing fovea After 2 years of follow-up, the macula seemed flat with-
2b 9 Localized cleavage crossing fovea out recurrence of ERM. The VA was stable at 0.4. On the
3b 14 Diffuse cleavage OCT, the retinal layers also showed adequate segmentation.
Please note the remnant of ERM on the superior aspect of
contraction. They also noted MPH with stretched edges macula. The ERM did not extend to the parafoveal region.
often had multiple epicenters of contraction and asymmet- Please also note there were some epiretinal hyperreflectivi-
ric distortions [34]. ties on the horizontal section, but these spots did not form
On the other hand, Michalewska et al. championed that contractile ERM (Fig. 1.6a–d).
not only epiretinal membrane could produce this contraction.
They proposed that hyperreflective linear structure-like
epiretinal membrane, thickened internal limiting membrane, 1.3.2 Examples of Secondary ERM
or hyaloids could be the common cause of all types of non-­
full-­thickness macular holes [21]. We demonstrate some cases of secondary ERM here. The
Besides these two theories, Schumann et al. analyzed the first case was the left eye of a 29-year-old female. She suf-
properties of epiretinal membrane of 27 eyes with MPH in fered from poorly controlled diabetes mellitus. Proliferative
2015. They confirmed the majority of ERM are typical trac- diabetic retinopathy with tractional epiretinal membrane and
tional ERM [35] (Table 1.5). vitreous hemorrhage. The second case was the left eye from
In 2016, Tomaya et al. proposed three stages of macular a 74-year-old female with prior proliferative diabetic reti-
pseudoholes: no cleavage (stage 1), localized cleavage (stage nopathy with panretinal photocoagulation scars. Tractional
2) that does or does not cross the central fovea (stage 2b and membrane over disc and nasal side retina and yellow-grayish
2a, respectively), and diffuse cleavage (stage 3) (Table 1.6). contractile macular ERM could be seen. The third case was
This reflected different levels of stretching and foveal mor- the left eye from a 74-year-old female with prior prolifera-
phology distortion [36]. tive diabetic retinopathy with pan-retinal photocoagulation
scars. Tractional membrane over disc and nasal side retina
and yellow-grayish contractile macular ERM could be seen.
1.3 Clinical Features High-resolution OCT showed thickened ERM with attenua-
tion of the foveal pit. No remaining macular ERM could be
1.3.1 A Typical Case of ERM seen post-operatively. The contractile wrinkling had also
been gone (Fig. 1.7).
This was the left eye of a 53-year-old female. She com-
plained of progressively blurred vision in the left eye with
insidious onset. Fundoscopy showed yellow-grayish thick 1.3.3  resenting Age, VA, and Laterality
P
ERM with mild distortion of retinal surface and small ves- in ERM
sels. Radial retinal folds could all also be appreciated
(Fig. 1.1d). She had been observed for 2 years and had rela- Epiretinal membrane usually occurs in patients over 50 years
tive stable clinical course with best-corrected VA deteriorat- old and could be seen in 10–30% of the general population
ing from 0.4 to 0.3 (Fig. 1.1e). High-resolution optical over 70 years old. Bilateral involvement is present in 20% of
coherence tomography (OCT) showed thickened ERM and these patients. Eighty percent of these membranes are
central macula edema with intraretinal split, on both hori- idiopathic, while about 20% are secondary to previous retinal
zontal section (Fig. 1.2a) and vertical section (Fig. 1.2b). detachment, vascular, or inflammatory retinal diseases [1, 5]
However, due to this worsening, the patient requested for (Table 1.2). The initial presenting visual acuity is usually fair,
operation. Microincisional sutureless 23G vitrectomy with 20/50, or better, and the progression is usually slow [5–7].
double peeling with triamcinolone acetonide (TA) staining In 1982, Sidd et al. published a series of 98 eyes in 89
was performed. Air tamponade with head-positioning for patients, with 83 more than 50 years old. Sixty eyes (60/98,
1 Epiretinal Membranes and Macular Pseudoholes 7

Fig. 1.3 (a) After

1.5 months postoperatively, a
follow-up OCT showed
removal of ERM and ILM
on central macula, on both
horizontal section (a) and
vertical section (b). The
central foveal thickness
decreased markedly, and
the intraretinal splitting
lessened. Please also note
very thin ILM still evident
on the side close to optic
nerve head. We preferably
perform limited ILM
peeling in our cases. (b)
After 1.5 months b
postoperatively, follow-up
OCT showed removal of
ERM and ILM on central
macula, on both horizontal
section and vertical
section. The central foveal
thickness decreased
markedly, and the
intraretinal splitting
lessened. Please also note
very thin ILM inferiorly
and residual ERM-ILM
superiorly. We preferably
perform limited ILM
peeling only in our cases
8 J.-H. Shen et al.

Fig. 1.4 (a) After 2.5 months

a
postoperatively, the
intraretinal split subsided, and
initial restoration of foveal
depression could be observed.
(b) After 2.5 months
postoperatively, the
intraretinal split subsided, and
initial restoration of foveal
depression could be observed

b
1 Epiretinal Membranes and Macular Pseudoholes 9

Fig. 1.5 (a) After 6.5 months

postoperatively, the
a
anatomical improvement had
been stable. There was no
more foveal cystic change,
and the segmentation of
retinal layers was well-­
defined. (b) After 6.5 months
postoperatively, the
anatomical improvement had
been stable. There was no
more foveal cystic change,
and the segmentation of
retinal layers was
well-defined

61%) had initial presenting VA 6/12 (20/40) or better. Nine In 1988, Appiah, Hirose, and Kado reviewed 395 eyes in
patients had initial bilateral epiretinal membrane, and a sec- 324 eyes with idiopathic premacular gliosis. The mean age
ond eye became involved in one initially unilateral patient of onset in these patients was 64.6 years old. Initial visual
during the follow-up period. Sixteen of 74 eyes (21%) had acuity was 20/40 or better in 214 eyes (54.2%), 20/50 to
fluorescein leakage into the macula [7]. 20/100 in 136 eyes (34.4%), and poorer than 20/100 in 45
eyes (11.4%).
10 J.-H. Shen et al.

a b

Fig. 1.6 (a) After 2 years of follow-up, the macula seemed flat without also showed adequate segmentation. Please note the remnant of ERM
recurrence of ERM. There was also no retinal folding. (b) After 2 years on the superior aspect of macula. The ERM did not extend to the para-
of follow-up, the macula seemed flat without recurrence of ERM. There foveal region. Please also note there were some epiretinal hyperreflec-
was also no retinal folding. (c, d) After 2 years of follow-up, the macula tivities on the horizontal section, but these spots did not form
seemed flat without recurrence of ERM. On the OCT, the retinal layers contractile ERM