Changes in the Ocular Surface Index after 25-Gauge Pars Plana Vitrectomy Using an Ocular Surface Analyzer

doi:10.21203/rs.3.rs-3105863/v1

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Changes in the Ocular Surface Index after 25-Gauge Pars Plana Vitrectomy Using an Ocular Surface Analyzer

https://doi.org/10.21203/rs.3.rs-3105863/v1

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Purpose

The purpose of this study was to analyze the changes before and after 25-gauge pars plana vitrectomy (PPV) using an ocular surface analyzer.

Methods

The medical records of 82 patients and 163 eyes who underwent PPV were reviewed retrospectively. Non-invasive tear film break-up time (NITBUT), lipid layer thickness, meibomian gland loss, and tear meniscus height were measured at before surgery, one month, and three months after surgery. The changes in each index were statistically analyzed. In addition, risk factors that could reduce NITBUT at one month after surgery were analyzed.

Results

One month after surgery, the NITBUT was significantly decreased in the operative eyes compared to before surgery (p = 0.006, paired t-test). Compared with non-operative eyes, NITBUT in operative eyes decreased significantly at one month after surgery (p = 0.006, student t-test). Age (β=-0.248, p = 0.029, multiple linear regression) and preoperative NITBUT (β = 0.357, P = 0.002, multiple linear regression) were identified as significant risk factors associated with the decrease in NITBUT at one month after surgery.

Conclusion

25-gauge PPV can significantly reduce NITBUT at one month after surgery, and the risk factors are age and preoperative NITBUT. This may contribute to the development of dry eye disease after surgery.

Health sciences/Diseases/Eye diseases

Health sciences/Diseases/Eye diseases/Conjunctival diseases

Health sciences/Diseases/Eye diseases/Corneal diseases

Dry Eye Disease

Non-invasive Tear Film Break-up Time

Ocular Surface Analyzer

Ocular Surface Index

Pars Plana Vitrectomy

The Dry Eye Workshop II defined dry eye syndrome as a multifactorial disease of the tears and ocular surface that causes increased tear osmolarity and ocular surface inflammation¹. The prevalence of dry eye disease (DED) varies from 5–35% across different age groups². It is generally more common in women, and various factors such as contact lens wear, diabetes, hypertension, and autoimmune diseases are known to contribute to its development³.

Patients with DED may experience not only simple functional visual impairment, but also subjective decreases in quality of life⁴. To address these problems, many studies have been conducted on the occurrence of dry eye after various ophthalmic surgeries. DED can occur temporarily or permanently after refractive surgery, and an increased incidence has been reported after cataract surgery⁵. Clinically, ophthalmologists encounter patients who complain of dryness of the eyes after not only refractive and cataract surgery, but also vitrectomy. In fact, when symptom scores were measured in patients who underwent retinal surgery, the prevalence of dry eye syndrome increased from 40% in the group that did not undergo surgery to 63% in the group that underwent surgery⁶.

To diagnose DED, a combination of subjective symptoms and objective tests is utilized. Objective tests, such as tear film breakup time measurement and Schirmer test, are employed to evaluate both tear quality and quantity⁷. However, there are limitations to the Schirmer test as it may be difficult to reproduce the actual tear film height due to discomfort caused by the test paper, and the invasive tear breakup time test using fluorescein dye to stain the conjunctiva and observing it under a slit lamp can cause a decrease in tear film stability due to the dye^8,9. In order to overcome these limitations, the importance of various ocular surface indices including noninvasive tear breakup time (NITBUT) has been emphasized recently, and various anterior segment imaging devices for measuring these indices have been introduced and used in clinical practice¹⁰.

To date, there have been no studies on ocular surface indices after 25-gauge pars plana vitrectomy (PPV) using an ocular surface analyzer. Therefore, the purpose of this study is to measure ocular surface indices before and after vitrectomy using an ocular surface analyzer, and to find objective evidence on whether vitrectomy can actually cause dry eye syndrome.

Study design

This study was conducted on 82 participants, totaling 163 eyes, who visited the Department of Ophthalmology at Inje University Busan Paik Hospital and underwent vitrectomy surgery from April 2021 to February 2022. These participants were followed up for at least 1 month. Patients were subjected to examinations using the ocular surface analyzer before surgery, one month, and three months after surgery. Ocular surface analysis was conducted at the same location using the same device for each patient, and four ocular surface indices were measured in both eyes at each time point, except when it is impossible to measure. The ocular surface indices included NITBUT, lipid layer thickness (LLT), meibomian gland (MG) loss, and tear meniscus height (TMH) were measured. Through medical records, we investigated the age, gender, preoperative diagnosis, presence of cataract surgery, number of trocars used during the surgery, and the use of filling material within the eye for each study participant.

Ethics and permissions

The Institutional Review Board of Busan Paik Hospital (BPIRB 2022-04-013-003) approved the study and provided a waiver for informed consent. As a retrospective medical record analysis, there is no risk of harm to the patient, and it does not affect dignity, rights, or welfare. In addition, it is practically impossible to obtain the consent of the subject at this point, and it is applicable to cases where the risk to the subject is extremely low even if the consent is waived. This study followed the Declaration of Helsinki. There are no conflicts of interest related to this study.

Ocular surface index assessments

Each index was automatically measured using the IDRA ocular surface analyzer (IDRA® Ocular Surface Analyzer Device, SBM SISTEMI, UK) to minimize examiner involvement. The following methods were used to measure each index. NIBUT was measured by maintaining the eyes open after a complete blink, reflecting a circular Placido's disk on the cornea, and determining the earliest time at which the Placido's disk collapsed without interference from a blink, indicating the beginning of tear film breakup. LLT was measured by projecting white light onto the cornea and measuring the light reflected from the tear film. The automatic interferometry test of IDRA was used to detect color interference in the lipid layer. The presence of color interference indicated the presence of lipids, allowing for the observation of the lipid layer thickness. A non-glossy white pattern was considered as no lipid. MG loss was calculated as a percentage by observing the degree of absence of MG in the entire lower eyelid plate. This observation was done by inverting the lower eyelid and using an infrared transillumination filter to observe the lower MGs, which have high reflectivity. TMH was measured by detecting the upper and lower tear meniscus in the captured image and measuring the tear meniscus height along the edge of the lower eyelid. (Fig. 1)

Surgical procedures

All surgeries were performed by a single surgeon. Pars plana vitrectomy was performed using a 25-gauge vitrectomy system (CONSTELLATION® Vision System, Alcon Laboratories. Inc., Fort Worth, TX, USA), and 3 or 4 trocars were inserted into the sclera 3-3.5mm away from the limbus for the surgery. When using 3 trocars, they were inserted at 2 o'clock, 10 o'clock, and 4 or 8 o'clock positions, and when using 4 trocars, an additional cannula was inserted. Following the surgery, the trocar sites were closed using non-sutured closure with a scleral depressor. In cases where leakage occurred or gas or silicone oil was used for tamponade, 8 − 0 vicryl sutures were employed for closure and were removed within a week.

Statistical analysis

The statistical analysis was performed using the Statistical Package for the Social Sciences version 22.0 program (IBM Corp., Armonk, NY, USA). A significance level of less than 0.05 was considered statistically significant. To compare the ocular surface indices of the surgical group before surgery, one month after surgery, and three months after surgery, paired t-tests were conducted. Independent t-tests or Mann Whitney U tests were used to compare the ocular surface indices between the surgical group and the non-surgical group at each time point. For investigating factors related to the NITBUT at one month after surgery, simple linear regression analysis was conducted, followed by multiple linear regression analysis for statistically significant variables.

This study included a total of 82 participants and 163 eyes, comprising 40 males and 42 females. The average age of the participants was 60.61 ± 12.82 years. Preoperative diagnoses consisted of retinal detachment (RD) in 25, epiretinal membrane (ERM) in 20, vitreous hemorrhage (VH) in 22, vitreomacular traction syndrome (VMTS) in 5, and macular hole (MH) in 10 patients. Simultaneous vitrectomy and cataract surgery were performed in 45, and the use of filling materials such as gas or silicon oil was in 25, and the average number of trocars was 3.30 ± 0.46. All patients underwent analysis using the IDRA ocular surface analyzer before surgery (baseline). A follow-up period of one month was completed by 69 participants, while 35 participants were followed up for three months, and 22 participants were evaluated at both one and three after surgery. (Table 1)

Table 1

Demographics and clinical characteristics of study participants
Baseline characteristic	Value (n = 82)
Number of eyes	163
Operative	82
Non-operative	81
Sex
Male	40 (51.2)
Female	42 (48.8)
Age	60.61 ± 12.82
Preoperative diagnosis
Epiretinal membrane	20 (24.4)
Macular hole	10 (12.2)
Retinal detachment	25 (30.4)
Vitreous hemorrhage	22 (26.82)
Vitreomacular traction syndrome	5 (6.1)
Operative factor
Simultaneous cataract surgery	45 (54.9)
Use of filling material	25 (30.5)
Number of trocars	3.30 ± 0.46
F/U period
Only 1 month F/U	69
Only 3 months F/U	35
1 month with 3 months F/U	22
Values are presented as number only, mean ± standard deviation, or number (%); F/U = flow up.

The mean of each ocular surface index was compared for the surgical group (operative eyes). The NITBUT decreased from 6.29 ± 1.01 seconds before surgery to 5.90 ± 0.78 seconds one month after surgery, then increased to 6.41 ± 0.76 seconds three months after surgery. The LLT showed a decreasing trend over time, from 66.83 ± 19.57 µm before surgery to 64.17 ± 20.10 µm one month after surgery and 62.42 ± 18.28 µm three months after surgery. The MG loss increased from 45.80 ± 25.67% before surgery to 51.75 ± 26.19% one month after surgery, then decreased to 48.42 ± 27.25% three months after surgery. The THM increased from 0.20 ± 0.09 mm before surgery to 0.21 ± 0.07 mm one month after surgery and increased at 0.22 ± 0.10 mm three months after surgery. We conducted a comparison of the ocular surface index between the surgical group and the non-surgical group (fellow eyes) at various time points. An independent t-test revealed a significant difference, with NITBUT in the non-surgical group being shorter than that in the non-surgical group (p = 0.006, independent t-test). However, there were no significant differences observed in the LLT, MG loss, and THM between the two groups at each respective time point. (Table 2)

Table 2

Comparison of ocular surface indices between operative and non-operative eyes at each observation time
		Baseline	p-value	1 month	p-value	3 months	p-value
NIBUT (sec)	Operative	6.29 ± 1.01 (n = 82)	0.602	5.90 ± 0.78 (n = 69)	0.006*	6.41 ± 0.76 (n = 36)	0.113
NIBUT (sec)	Non-operative	6.20 ± 0.94 (n = 81)	0.602	6.31 ± 0.92 (n = 67)	0.006*	6.11 ± 0.83 (n = 34)	0.113
LLT (µm)	Operative	66.83 ± 19.57 (n = 82)	0.577	64.17 ± 20.10 (n = 69)	0.399	62.42 ± 18.28 (n = 36)	0.623
LLT (µm)	Non-operative	65.09 ± 20.25 (n = 81)	0.577	67.04 ± 19.61 (n = 68)	0.399	64.88 ± 23.03 (n + 34)	0.623
MG loss (%)	Operative	45.80 ± 25.67 (n = 82)	0.975	51.75 ± 26.19 (n = 69)	0.750	48.42 ± 27.25 (n = 36)	0.792
MG loss (%)	Non-operative	45.94 ± 29.28 (n = 81)	0.975	50.34 ± 25.78 (n = 69)	0.750	50.00 ± 22.36 (n = 34)	0.792
TMH (mm)	Operative	0.20 ± 0.09 (n = 82)	0.895	0.21 ± 0.07 (n = 69)	0.579	0.22 ± 0.10 (n = 36)	0.623
TMH (mm)	Non-operative	0.20 ± 0.09 (n = 81)	0.895	0.21 ± 0.07 (n = 68)	0.579	0.21 ± 0.07 (n = 34)	0.623
Values are presented as mean ± SD unless otherwise indicated; NIBUT = non-invasive tear film break-up time; LLT = lipid layer thickness; MG = Meibomian gland; TMH = tear meniscus height; Statistical analysis was performed using independent t-test or Mann Whitney U tests; *p-value < 0.05.

The NITBUT was recorded as 6.29 ± 1.01 seconds before surgery and 5.90 ± 0.75 seconds one month after surgery in surgical group. A paired t-test demonstrated a significant decrease of 0.35 ± 0.83 seconds in the NITBUT one month after surgery compared to the baseline (p = 0.006, paired t-test). However, there was no statistically significant change in the NITBUT between the one-month and three-month follow-up after surgery. LLT, MG loss, and TMH showed no statistically significant differences when compared between preoperative, one-month, and three-month after surgery (Table 3).

Table 3

Comparison of ocular surface indices between each observation time in operative eyes
	Baseline	1month	p-value	1month	3months	p-value	Baseline	3months	p-value
	n = 69			n = 22			n = 35
NIBUT (sec)	6.29 ± 1.01	5.90 ± 0.75	0.006*	5.99 ± 0.68	6.20 ± 0.75	0.322	6.36 ± 1.08	6.39 ± 0.75	0.881
LLT (µm)	66.74 ± 19.54	64.17 ± 20.10	0.250	66.27 ± 20.27	67.73 ± 19.98	0.799	68.29 ± 19.47	63.03 ± 18.17	0.236
MG loss (%)	45.29 ± 26.05	51.75 ± 26.19	0.125	41.73 ± 26.13	49.82 ± 27.02	0.270	41.60 ± 25.41	48.03 ± 27.54	0.275
TMH (mm)	0.20 ± 0.09	0.21 ± 0.07	0.806	0.21 ± 0.07	0.20 ± 0.08	0.440	0.21 ± 0.08	0.21 ± 0.08	0.489
Values are presented as mean ± SD unless otherwise indicated; NIBUT = non-invasive tear film break-up time; LLT = lipid layer thickness; MG = Meibomian gland; TMH = tear meniscus height; Statistical analysis was performed using independent paired t-test; *p-value < 0.05.

An analysis was conducted to evaluate variables that could potentially affect the NITBUT at one month after surgery. Age (β=−0.017, p = 0.035, simple linear regression analysis) and preoperative NITBUT (β = 0.227, P = 0.021, simple linear regression analysis) were identified as statistically significant risk factors. Additional multiple linear regression analysis was performed for these two variables, which showed that both age (β=-0.248, p = 0.029, multiple linear regression analysis) and preoperative NITBUT (β = 0.357, P = 0.002, multiple linear regression analysis) revealed significant risk factors (Table 4).

Table 4

Single and multiple regression analysis of factors associated with NITBUT decrease at one month after vitrectomy
	NITBUT 1 month after 25G PPV
	Single linear regression			Multiple linear regression
Variables	β	SE	p-value	β	SE	p-value
Age	-0.017	0.008	0.035*	-0.248	0.007	0.029*
Sex	0.103	0.186	0.580	-	-	-
Cataract surgery	-0.004	0.200	0.984	-	-	-
Filling material	-0.398	0.299	0.187	-	-	-
Number of trocars	-0.505	0.337	0.139	-	-	-
Baseline NITBUT	0.227	0.096	0.021*	0.357	0.086	0.002*
Baseline LLT	-0.005	0.005	0.275	-	-	-
Baseline MG loss	0.000	0.004	0.920	-	-	-
Baseline TMH	0.780	1.114	0.486	-	-	-
25G PPV = 25-gauge pars plana vitrectomy; NIBUT = non-invasive tear film break-up time; LLT = lipid layer thickness; MG = Meibomian gland; TMH = tear meniscus height; Statistical analysis was performed using single linear regression and multiple linear regression, multiple linear regression was performed only on significant variables in single linear regression.; *p-value < 0.05.

DED is a multifactorial disorder caused by various factors, and it is classified into two main mechanisms: a decrease in tear quantity and an increase in evaporation of the ocular surface¹¹. In the 2017 report of the Tear Film and Ocular Surface Society International Dry Eye Workshop II (TFOS DEWS II), it is recommended to diagnose DED by evaluating scores through surveys targeting individuals with symptoms and assessing tear film homeostasis through the following parameters: NITBUT, osmolarity, ocular surface staining¹. We focused on NITBUT as one of these parameters in our study. We observed a significant decrease in NITBUT one month after surgery, both in repeated measurements within the operative eyes and in comparisons with the non-operative fellow eyes. This indicates that there was an increased instability of the ocular surface, not only compared to the preoperative but also the fellow eye. Furthermore, the eyes undergoing vitrectomy exhibited changes that closely resembled the diagnostic criteria for DES as proposed by TFOS DEWS II¹.

Ghasemi et al have reported a significant decrease in Schirmer's test values at 1 month and 3 months after 23-gauge PPV¹². Additionally, Sato et al have reported a significant increase in corneal and conjunctival fluorescein staining score and TMH one week after performing 25-gauge PPV¹³. We also observed a significant decrease in NITBUT after 1 month of vitrectomy, compared to baseline in operative eyes and non-operative fellow eyes. This was consistent with previous studies. However, the measured parameters such as LLT, TMH, and MG loss showed similar trends but did not reach statistical significance in elucidating the underlying cause.

In previous studies focusing on cataract surgery, most cases of dry eye disease (DED) were found to be transient, lasting approximately 3 months after surgery, with subsequent recovery observed through tear break-up time (TBUT)^14–16. Lee et al have reported a significant increase in OSDI score at 3 months after vitrectomy¹⁷. To confirm this, we also conducted a follow-up at 3 months after surgery to investigate the recovery of DED. Although Recovery of LLT, TMH, and MG losses at 3 months compared to 1 month after surgery was observed, but it was not statistically significant.

Since the reported occurrence of DED after vitrectomy, several studies have investigated the risk factors associated with this condition. Yang et al have identified age as a prominent risk factor¹⁸, while another study reported scleral depression as a risk factor¹⁹. In this study, similar to previous findings, increasing age was found to be a risk factor that could affect the NITBUT value at one month after surgery. Mathers et al. suggested that age-related dry eye may be associated with factors such as tear quantity, evaporation rate, and intraocular pressure²⁰. Damato et al. proposed decreased tear secretion due to fibrotic changes in the lacrimal glands as a contributing factor²¹. These age-related factors contributing to dry eye in the general population are believed to potentially influence the development of DED after surgery as well.

The tear film is composed of the lipid layer, aqueous layer, and mucin layer, which nourish the conjunctival epithelium and cornea, facilitate smooth eyelid movement, and provide the cornea with a high refractive index for optimal optical surface quality. The pathogenesis of DED involves inflammation, cellular apoptosis of lacrimal and conjunctival epithelial cells, and androgen imbalance^22,23. Following vitrectomy, potential causes of DED include direct damage to the corneal epithelium and conjunctiva due to surgery, as well as tear film instability and distribution caused by scleral sutures, conjunctival sutures, incisions, and conjunctival edema after surgery²⁴. Using a 20-gauge vitrectomy probe can cause surgical-induced astigmatism, and using a 23-gauge vitrectomy probe has been reported to cause changes in corneal topography after surgery, although less than with a 20-gauge probe^25,26. Both scleral incision and closure also contribute to the development of DED. Furthermore, the blood flow and edema of corneal tissue associated with vitrectomy can influence the adhesion of the mucin layer on the ocular surface, potentially allowing the infiltration of inflammatory factors. This process can lead to tear gland damage, exacerbating corneal injury²⁷. Additionally, the postoperative medications prescribed for the management after vitrectomy often contain preservatives, which are known to impact the integrity of the corneal epithelium²⁸. Finally, molecular changes following PPV also contribute to the development of DED. Previous studies have demonstrated a reduction in conjunctival goblet cells and mucin protein levels in tears, accompanied by increased cytokine levels after PPV²⁹. These changes can explain the decrease in non-invasive tear breakup time observed in this study following PPV. These factors can contribute to the occurrence of DED after vitrectomy and potentially impact the instability of the tear film. In this study, we targeted surgeries performed using a 25-gauge vitrectomy probe. It is expected that the relative minimal damage to the conjunctiva through sutureless surgery was achieved. However, despite these factors, it is important to note that there was a significant decrease in NITBUT at one month after surgery compared to before surgery and when compared to the non-surgical group. This finding is significant and highlights the impact of surgery on the ocular surface, even with the use of a 25-gauge vitrectomy probe and minimal conjunctival damage.

There are several limitations in this study. Since the patient's subjective symptom score was excluded, it is not known whether the patient actually complained of discomfort due to the decrease in NITBUT. In addition, the sample size is small, and the observation period for all subjects is not the same, so there is a lack of repeated measurements for the same time points. Furthermore, there was a lack of control over conditions other than vitrectomy and cataract surgery. This is considered a challenge that needs to be overcome through large-scale in serial studies.

Nevertheless, this study is the first to investigate the ocular surface index after 25-gauge PPV using an ocular surface analyzer, and it is meaningful that a significant decrease in the NITBUT was observed after surgery. This can be used as objective evidence that 25-gauge PPV can cause DED. Furthermore, It will help clinicians predict the possibility of developing dry eye syndrome after vitrectomy and reduce patients' postoperative discomfort.

Competing interests

The author(s) declare no competing interests.

Data availability statements

All data analyzed during this study are available from the corresponding author on reasonable request.

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Changes in the Ocular Surface Index after 25-Gauge Pars Plana Vitrectomy Using an Ocular Surface Analyzer

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Abstract

Purpose

Methods

Results

Conclusion

Figures

INTRODUCTION

METHODS

Study design

Ethics and permissions

Ocular surface index assessments

Surgical procedures

Statistical analysis

RESULTS

DISCUSSION

Declarations

Competing interests

Data availability statements

References

Additional Declarations

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