Combined retinal massage and autologous blood covering for persistent macular holes after vitrectomy in high myopia

Abstract

Purpose:

To evaluate the efficacy of retinal massage combined with autologous blood covering in the treatment of persistent macular holes following vitrectomy in eyes with high myopia.

Settings and Design:

Retrospective, consecutive case series in a tertiary eye center.

Methods:

A total of 12 highly myopic eyes with persistent macular holes after vitrectomy and internal limiting membrane peeling received combined retinal massage, air/fluid exchange, autologous blood covering, and gas/silicone oil tamponade. Best-corrected visual acuity, axial length, and optical coherence tomographic images before and after the treatment were compared.

Results:

The mean hole diameter before this intervention was 931.58 ± 244.58 μm (range, 508–1270), and the axial length was 30.39 ± 2.13 mm (range, 27.08–34.64). During the 6-month follow-up period, hole closure was achieved in eight eyes (66.67%). The mean best-corrected visual acuity improved significantly from 1.40 ± 0.50 logarithm of the minimum angle of resolution (logMAR) at baseline to 1.10 ± 0.30 logMAR (P < 0.05). No complications were observed.

Conclusions:

Combined retinal massage and autologous blood covering, which is easy to manipulate, can promote the closure of persistent macular holes after vitrectomy and improve vision in high myopia with an axial length less than 29 mm.

Macular hole (MH) is a common and vision-threatening complication of high myopia with or without retinal detachment.[1,2] Treatment of MHs associated with high myopia is challenging to surgeons because of the unique ocular fundus features in highly myopic eyes, such as the extremely long axis and low contrast. Although the inverted internal limiting membrane (ILM) flap technique improves the rate of MH closure up to 70%–90%,[3,4,5,6,7] its effect on highly myopic MHs is far less satisfactory than that on idiopathic holes due to excessive axial elongation, thinning of the retinal tissue, chorioretinal atrophy, posterior staphyloma, and retinoschisis.

Persistent or recurrent MHs represent a potential risk for retinal detachment in highly myopic eyes after an unsuccessful vitreous surgery.[8] To promote MH closure in high myopia, modified techniques, including autologous ILM transplantation,[9] amniotic membrane application,[10,11,12] lens capsule transplantation,[13] autologous free-flap retinal transplantation,[14] and temporal scleral imbrication,[15] have been used in clinical practice. Retinal massage and autologous blood clot therapy have also been respectively employed in the primary MH surgery.[16,17] Herein, we attempted to evaluate the efficacy of combined retinal massage and autologous blood covering in facilitating the closure of unclosed MHs after vitrectomy.

Methods

Ethical approval

This retrospective, consecutive case series study was approved by the Ethics Committee of Qingdao Eye Hospital (No. 2023-66). The study adhered to the guidelines of the Declaration of Helsinki.

Patients

Medical records of patients who received retinal massage combined with autologous blood covering at Qingdao Eye Hospital from May 2021 to September 2023 for persistent MHs after vitrectomy and ILM peeling were reviewed. Patient inclusion criteria for the combined surgical treatment were high myopia (<-6 D), axial length ≥26 mm, and an unclosed MH 2 months after the primary surgery, with or without retinal detachment. Patients with concomitant diabetic retinopathy, retinal vascular occlusion, vitreous hemorrhage, uveitis, or glaucoma were excluded. Consequently, data of 12 patients (12 eyes) were collected for analyses, including best-corrected visual acuity (BCVA), axial length, and optical coherence tomography (OCT; Optovue Inc., Freemont, CA, USA) findings till 6 months after the intervention. All these patients also received air/fluid exchange and gas/silicone oil tamponade. The central smallest diameter of the hole was taken as the hole size. MH closure was defined as a complete connection of the neuroepithelial MH without bare retinal pigmental epithelium (RPE) on the OCT image.

Surgical procedures

All surgeries were performed by the same experienced surgeon (NC). First, standard three-port, 25-gauge scleral incisions were made (Constellation Vitrectomy System; Alcon Laboratories, Fort Worth, TX, USA). If there was previous silicone oil tamponade, the silicone oil was removed. Triamcinolone acetonide was then injected to identify whether there were residual vitreous cortex and epiretinal membrane. After confirming that there was no residual vitreous cortex around MH and the range of the previous ILM peeling was sufficient, massage was performed with the retina smoothed radially toward MH, starting from the arcades in a centripetal fashion, using a silicone-tipped flute needle. The hole at the needle's handle was blocked with the thumb in case any suction force was generated at the retinal surface. The massage was gentle, avoiding to press the retina against RPE. When the retina was elongated a little from multiple directions, the hole became smaller. No tapping or suction on the hole edge was performed for fear of retinal damage. The fluid was aspirated over the disc, with the eyeball rotated to the nasal side in favor of thorough drainage during air/fluid exchange. Then a drop of autologous blood obtained from the vein was immediately used to cover the hole. Finally, the vitreous cavity was filled with C3F8 (concentration around 14%) or silicone oil [Supplementary Video]. All patients were informed to maintain a prone position for at least 2 weeks after surgery and were followed up at 2 weeks, 1, 3, and 6 months postoperatively.

Statistical analysis

Statistical Package for the Social Sciences 26.0 software (SPSS Inc., Chicago, IL, USA) was used for statistical analysis. Descriptive statistics were used to analyze patient demographics, preoperative characteristics, and surgical outcomes. Continuous variables were reported as mean ± standard deviation, while categorical variables were presented as frequencies and percentages. BCVA values were converted to the logarithm of the minimum angle of resolution (logMAR) values. Counting fingers was assigned 2.3, hand movements 2.6, and light perception 2.9. Paired t-tests were used to compare preoperative and postoperative visual acuities. P <0.05 was considered statistically significant.

Results

The included patients consisted of four males and eight females, with an average age of 59.25 ± 8.35 years (range, 50–74). Before this surgical treatment, the mean axial length was 30.39 ± 2.13 mm (range, 27.08–34.64), the mean hole size was 931.58 ± 244.58 μm (range, 508–1270), and the mean BCVA was 1.40 ± 0.50 (range, 0.82–2.30). Silicone oil was tamponaded in two patients, and gas was used in 10 patients. The baseline clinical features and surgical results are shown in Table 1 and Figs. 1 and 2.

Table 1.

Baseline characteristics of included patients and their surgical results

Patient no.	Age (years)	Sex	Laterality	Lens status	Axial length (mm)	Diameter of MH (μm)	Preop. BCVA	MH retinal detachment	Postop.MH status	Postop. BCVA at 6 months	Tamponade agent
1	54	F	OD	Phakic	28.14	1270	1.40	No	Closed	1.30	C3F8
2	50	F	OD	Aphakic	31.08	1250	2.30	Yes	Closed	1.40	Silicone oil
3	67	M	OD	Pseudophakic	30.96	933	1.40	No	Open	1.22	C3F8
4	74	F	OD	Pseudophakic	30.31	922	1.00	No	Closed	0.82	C3F8
5	52	F	OD	Pseudophakic	34.64	848	1.40	No	Open	1.00	C3F8
6	58	M	OS	Pseudophakic	30.09	508	0.82	No	Closed	0.82	C3F8
7	60	M	OD	Aphakic	32.20	1150	1.40	No	Open	1.22	C3F8
8	53	F	OS	Pseudophakic	30.14	926	0.82	No	Open	0.82	Silicone oil
9	51	F	OD	Aphakic	29.80	770	1.30	No	Closed	0.82	C3F8
10	56	F	OD	Pseudophakic	27.08	578	1.00	No	Closed	0.82	C3F8
11	73	M	OD	Aphakic	27.75	864	1.70	No	Closed	1.30	C3F8
12	56	F	OD	Phakic	32.51	1160	2.30	No	Closed	1.70	C3F8

BCVA=best-corrected visual acuity, F=female, M=male, MH=macular hole, postop=postoperative, preop=preoperative, OD=right eye, OS=left eye

Figure 1.

Funduscopic and optical coherence tomographic images of the macular holes before and after combined retinal massage and autologous blood covering in patients with an axial length <29 mm

Figure 2.

Funduscopic and optical coherence tomographic images of the macular holes before and after combined retinal massage and autologous blood covering in patients with an axial length >29 mm

Postoperatively, MH was closed in eight eyes (66.67%) with a complete neuroepithelium connection, representing type 1 closure. The hole was not sealed, but stayed attached to RPE in four eyes (33.33%) at the last visit. BCVA had significantly improved from 1.40 ± 0.50 logMAR at baseline to 1.10 ± 0.30 logMAR at 6 months (t = 3.90, P < 0.05). The vision was improved in 10 eyes (83.33%) and remained stable in the other two eyes. There were no complications, such as retinal detachment, retinal hemorrhage, and visible RPE damage, during the follow-up period.

The mean axial length and hole size were 31.99 ± 1.96 mm and 964.25 ± 129.69 μm, respectively, in the four eyes with unclosed holes versus 29.60 ± 1.83 mm and 915.25 ± 293.06 μm, respectively, in the eight eyes with hole closure. Although statistical analysis was not performed between the two groups due to the small sample size, it was definite that MHs tended to close in eyes with a smaller eye globe.

Discussion

The surgical strategy for MHs associated with high myopia has been widely recognized with the ILM flap technique,[8] while the management of postoperative persistent MHs remains controversial. For patients who have had ILM peeling, the remedy management is mostly focused on the scaffold-supporting strategy, in which exogenous membranes, such as the amniotic membrane[10,11,12] and the lens capsular flap,[13] are used. The second intervention can become more challenging due to the extremely long axis, neurosensory retinal thinning, and poor contrast even for an experienced surgeon. Moreover, there are concerns about membrane dislocation, local histocompatibility, and abnormal proliferation that may come after the exogenous membrane insertion.

Wang et al.[18] treated refractory MHs, including giant MHs, persistent MHs, and recurrent MHs, via parafoveal retinal massage in combination with autologous blood covering and achieved favorable anatomic results. But only three highly myopic eyes were enrolled, with a mean axial length of 28.35 mm, which was shorter than that in our series (30.39 ± 2.13 mm). All 12 eyes in the current study suffered persistent MHs associated with high myopia. The closure rate of 66.67% reinforces the efficacy of this technique in highly myopic patients.

The use of blood derivatives is not new in ophthalmology as autologous serum and platelet concentrates have already been tested as adjuvants in macular surgery.[19,20,21] The unique biological advantage of a blood clot may lie on the following three aspects. First, the mechanical effect of the clot, which is firmly adherent to the retinal surface, may further contribute to create a sealed interface, preventing the retina from rebounding after the massage and hydration in intraocular fluid. Second, activation of the platelet thrombin receptors releases trophic and growth factors, including platelet-derived growth factor, transforming growth factor-β, basic fibroblast growth factor, vascular endothelial growth factor, epidermal growth factor, and angiopoietin-1, which have the potential to activate a glial response and promote cell proliferation and migration. Third, the blood clot, like the inverted ILM flap, autologous ILM graft, and amniotic membrane, may act as a scaffold for glial proliferation and retinal movement to facilitate hole closure. This glial reaction helps to restore the normal foveal microanatomy. Furthermore, the blood covering technique represents a simple manipulation, not only avoiding the challenging scaffold material harvesting, but also simplifying the scaffold placement during the surgical procedure.

Different from the “scaffold providing” strategy, retinal massage, which does not rely upon stuffing MH with any material, aims to release the tangential tractional force and help the hole shrink quickly by a physical way. It was first described by Alpatov et al.,[22] with a hole closure rate of 92% and 84% of eyes showing excellent tissue approximation at the fovea. Mohammed and Pai[23] and Chakraborty et al.[24] employed this technique for refractory MHs, and the success rate was 100%. Peyman et al.[25] demonstrated a high closure rate in chronic holes using passive suction to the edges of MH, whereas Kumar et al.[17] disclosed acceptable anatomic and functional success rates by tapping MH edges, even in large MHs. Retinal massage seems to be preferred to achieve a type 1 true hole closure rather than using the ILM flap as a scaffold, which usually leads to a type 2 closure with poor visual recovery.[23] The massage makes the retinal tissue more flexible and facilitates the hole closure in the time and distance aspects of tissue healing.

In the current series, nonclosure in one-third of eyes might be attributed to the following conditions. First, the blood covering time was short, which could not cover the whole retinal healing process. Chen et al.[11] treated MHs with human amniotic membrane grafting and blood clot covering, and 83.3% of holes became closed. Besides the shorter axial length (27.36 mm) and smaller holes (641.76 µm), the long covering from the amniotic membrane might contribute to the hole closure. Peng et al.[26] also demonstrated that large MHs in high myopia (mean, 1,472.78 µm) deserved a long scaffold supporting time with nondegradable materials (lens capsular flap). In our series, retinal massage may compensate the short covering of a blood clot and reduce the retinal healing time by making the hole edges closer manually. Second, to reduce the mechanical damage to the fragile and thinning retina, we did not tap the hole edge, although suction and tapping of the hole edge were reported to be beneficial to hole closure.[17,25] With the retinal massage and no passive hole stuffing, the closure was actually the outcome of natural healing of the retina. Thus, sometimes, the time may be inadequate for the healing of an extremely large hole and an elongated eyeball. Third, the biometric parameters of the eyes in this study were less favorable for hole closure. MHs completely closed in patients with an axial length <29 mm, while in patients who failed to achieve closure, the axis was all longer than 30 mm. The axial length might be an indicator for MH closure. Regarding the hole size, however, there was no obvious tendency.

Moreover, we observed significant vision improvement in 83.33% of patients, and no patients experienced decline in vision after the surgical intervention. The reasons are considered as follows. First, the neurotrophic effect of the blood clot can help to sustain the functions of photoreceptors and neuron cells. The simplified surgical procedure might reduce the mechanical and optical toxicity during the surgery. Second, the natural retinal healing without adjuvant stuffing is helpful to light perception and electrical signal transmission in the retinal layers. It was reported that the inverted ILM flap technique was more effective than ILM peeling in anatomic results, but it showed no significant advantage in the postoperative visual outcome.[7,27] The material used to fill or cover the hole may induce glial cell proliferation and scar formation. The approximation of photoreceptors without scarring has the potential to better improve vision since abnormal glial tissue is not formed. Therefore, the technique of retinal massage seems to be more visually rewarding, which is consistent with the opinion of Gu and Qiu.[28] Third, we protected the retina by avoiding simultaneous suction, pressing of RPE, and tapping of the hole edge to minimize the disturbance to the inner retinal layer intraoperatively. Meanwhile, since no adjuvant insertion or subretinal implantation was performed, the central RPE cells were rescued, which contributed to the vision improvement.

The sample size was relatively small due to the low incidence and poor vision prognosis expectation, as well as the retrospective nature of this study. Future prospective and controlled studies with larger sample sizes are warranted to further validate the efficacy of this approach in the treatment of MHs in high myopia.

Conclusion

The technique of retinal massage combined with autologous blood covering can evoke the natural healing process of the retina and facilitate postoperative persistent MHs in high myopia to close when the axial length is less than 29 mm, with the advantages of simplicity, minimal invasion, and cost reduction.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.