Comparison of tear MMP9 with Schirmer’s test in ocular surface disorders &amp; formulation of a treatment algorithm based on the results

doi:10.21203/rs.3.rs-4294558/v1

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Comparison of tear MMP9 with Schirmer’s test in ocular surface disorders & formulation of a treatment algorithm based on the results

https://doi.org/10.21203/rs.3.rs-4294558/v1

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Purpose: To correlate the tear levels of MMP9 with Schirmer’s test in patients with Ocular surface disorder (OSD) & to evaluate treatment with lubricants, steroids and anti-inflammatory drugs based on MMP-9 results.

Methods: 100 eyes with OSD underwent Schirmer’s test & MMP9 estimation. All cases were evaluated on ocular symptomology score (OSS). Association of MMP-9 results with three groups of dry eyes, improvement in objective and subjective parameter in Group I(MMP-9 positive) and Group II(MMP-9 negative) with lubricants and need for additions steroids & Cyclosporine was evaluated.

Results: Out of 100 eyes, 40 eyes tested positive for MMP9. MMP9 positive patients had a mean Schirmer’s value of 12.85 + 7.07 as against MMP9 negative patients who had a mean value of 19.18 + 8.941. 80% were MMP9 positive in severe, 55.6% in moderate and only 22.5% with normal tear secretion were MMP9+ve. No definite Association was found between MMP9 positivity and OSS (chi square test: p>0.05). All MMP9 positive patients were started on lubricants. At 06 months, 85% eyes were continued on lubricants. In 6 eyes (15%) an addition of steroids/Cyclosporine was needed. All patients who were MMP9 negative were started on lubricants, at of 06 months, 96.7% eyes (58 eyes) were continued on lubricants. In 2 eyes (3.3%), addition of Steroid/Cyclosporine was needed.

Conclusion: Results show a trend to evaluate all cases of OSD with MMP- 9 test and treat them depending on results of this test. There is also a case for starting steroids early in cases which are MMP-9 positive.

Ocular surface disorder (OSD)

Schirmer’s test

Matrix metalloproteinase (MMPs)

Ocular symptomology score (OSS)

Ocular surface disorder (OSD) is a prevalent condition that can lead to considerable vision impairment, excessive ocular watering, and acute ocular discomfort¹. Ocular surface inflammation is virtually always present because of desiccation-related epithelium stress, regardless of the exact mechanism underlying OSD. Schirmer’s Test has been the corner stone in the diagnosis of OSD².However, despite its popularity based on its economy and ease of administration, it suffers from some limitations like its lack of accuracy and standardization³. Additionally, an assessment with Tear Film Breakup Time (TBUT)⁴and staining of ocular surface with Rose Bengal and Fluorescein is needed. TBUT needs instillation of a topical anaesthetic agent which may destabilize the tear film. Staining techniques are unable to differentiate OSD from other causes of staining ^4–6.

Epithelial stress as in cases with ocular surface disorders leads to elevated expression of Matrix metalloproteinase (MMPs) which are proteolytic enzymes. Elevated levels of the biomarker MMP- 9 are observed in OSD and also mirror the severity of clinical manifestations in these cases^7–10. Elevated levels of this biomarker can not only be correlated with severity of OSD but also can be used to quantify the inflammatory damage to the ocular surface.

This study aims to address gap in knowledge by attempting to establish MMP-9 estimation as a credible alternative to the Schirmer’s test in the diagnosis and management of OSD. Also demonstration of elevated inflammatory markers in OSD may also lead to newer management protocols using anti-inflammatory drugs as primary options in the treatment of this common and vexing disease.

This pilot study was carried out in a tertiary Ophthalmic center over a three-year period. It was a prospective observational study. After clearance from Institutional Ethics committee, all consecutive cases of clinically symptomatic ocular surface disorder were included in this study. All patients with ocular allergy were excluded. All patients with severe dry eye (Schirmer’s < 2 mm) and poor ocular surface were also excluded. Patients with corneal disorders affecting tear film were also excluded. The objectives were to correlate the tear levels of matrix metalloproteinase 9 (MMP 9) with values on Schirmer’s test in patients with ocular surface disorders & to evaluate the status of patients on follow up after treatment with lubricants, steroids and anti-inflammatory drugs based on MMP-9 results. There was no previous existing study to estimate the sample size. Hence, being a pilot study, a minimum of 100 eyes were proposed to be taken for evaluation.

All patients underwent Schirmer’s test & MMP9 estimation at onset of the study and only Schirmer’s test after six months of treatment. Schirmer’s test was done using commercially available Schirmer’s strips. The strips were folded at 5mm margins and inserted in lower fornix at the junction of inner 2/3rd and outer 1/3rd of lids. Patients were told to keep eyes open in an environmentally controlled room and readings were taken at 5 min as the mm of paper which was wetted. Subgroups were made based on Schirmer’s test levels based on DEWS-2007¹¹ and evaluated at onset of study and at 6 months as Dry eye values

Mild - Schirmer’s value 10–15

Moderate - Schirmer’s value 5–10

Severe - Schirmer’s value 2–5

The MMP-9 test was done using InflammaDry (Quidel Corporation, USA) kits, where a sponge from the kit was used to collect tears & then placed in the kit and a buffer solution was used to detect presence or absence of elevated MMP-9 levels as detected by lines on the kit. Patients were divided into two groups depending on whether MMP9 results were positive (Group I) or negative (Group II). All cases were evaluated on ocular symptomology score(OSS)²² ranging from 0–4 at onset of study and at 6 months.

No symptoms
Minimal symptoms, duration less than 4 hours daily
Moderate symptoms, duration more than 4 hours daily
Severe symptoms relieved by medications
Severe symptoms affecting daily activities

All cases were started on Topical preservative free lubricants Eye Drop Genteal (Novartis, USA) 6 times a day & were reviewed at 01, 03 and 06 months. In non or poor responders, the frequency of lubricants was increased and in cases with no improvement, topical steroids eye drop Fluromethalone 0.1% (FML, Alcon Geneva, Switzerland) one drop four times a day were started. The drug was tapered titrating with the patient’s response. Any patient initially improving with FML and showing recurrence of symptoms on tapering was started on Eye drop Cyclosporin 0.05% (Cyclomune, Allergan USA) twice a day for minimal 03 months. Improvement was defined as two step increase in Schirmer’s value or OSS improvement by two steps. Deterioration/ No response was defined as less than one step increase in Schirmer’s value or less than one step increase in OSS value.

Analytic objectives were

Association of MMP-9 results with three dry eye groups as per Schirmer’s test.
Improvement in objective and subjective parameter in Group I(MMP-9positive) & Group II(MMP-9negative) with lubricants.
Need for change in medicines in Group I&II by adding Eye Drop FML and Eye Drop Cyclomune.

100 eyes were enrolled, out of which 40 eyes tested positive for MMP9. (Fig 1) The mean age of the patients enrolled in the study was 60.26 yrs with a range of 34-82 yrs. The mean age of the patients in Group I (with MMP9 positive) was 58.05 while those in Group II (with MMP9 negative) was 61.73. The difference in their means was not significantly different. A total of 42 males and 58 females were inducted. Out of the 40 patients with MMP9 positivity, 22 were females and 18 were males.

Group I patients had a mean Schirmer’s value of 12.85 + 7.07 as against Group II patients who had a mean value of 19.18 + 8.941. The difference in the means was 6.33 (p value < 0.001). Thus, MMP9 positive patients had a significantly lower Schirmer’s value. (Table 1)

Out of the 5 patients with severe dry eye, 80% were positive for MMP9. 55.6% of moderate dry eye patients were positive for MMP9 whereas only 22.5% of patients with normal tear secretion tested positive for MMP9. The association between severity of Schirmer’s category and MMP9 positivity was significant (p<0.05). Thus, a greater proportion of MMP9 positive patients had higher severity of dry eye, as measured with Schirmer’s test.

There was a positive Association between the pre-treatment OSS severity and severity of Schirmer’s test, as demonstrated by Chi Square test with a significance of <0.01. Out of the 40 eyes with normal Schirmer’s test, 19 (47.5%) had a OSS score of 2. Whereas, 10 of 27 eyes (37%) with moderate Schirmer’s test and 4 of 5 (80%) eyes with severe Schirmer’s test had a OSS of 3. Also, all the 4 eyes (100%) with OSS score of 4, had moderate Schirmer’s test. (Fig 2)

Out of the 40 patients with positive MMP9, only 2 (5%) had an OSS of 4, whereas 18 patients (45%) had a score of 3, 16 patients (40%) had a score of 2 and 4 patients (10%) had a score of 1. 85% of the MMP9 positive patients thus had moderate OSS values. (Fig 3) No definite Association was found between MMP9 positivity and OSS (chi square test: p>0.05). Thus, MMP9 positivity does not necessarily confer a high OSS. This goes on to suggest that seemingly asymptomatic patients may be diagnosed and treated based on MMP9 positivity.

20 eyes (50%) of MMP9 positive group having higher severity of OSS moved to lower grades of OSS after treatment for 06 months. 2 eyes (5%) had no symptoms (OSS=0) at the end of 6 months. (p>0.05). Out of the total of 40 eyes with MMP9 positive, 10 eyes (25%) improved by two step or more at the end of 6 months. (Fig 4)

All 4 eyes (10%) of MMP9 positive group of the severe Schirmer’s category moved to lower grades of Schirmer’s after treatment for 06 months. 21 eyes (52.5%) had normal Schirmer’s at the end of 6 months treatment as against 9 eyes (22.5%) at the start of treatment. (difference is statistically significant: chi square test: p<0.05) Also, out of the total of 40 eyes with MMP9 positivity, as many as 10 eyes (25%) improved by at least two steps in Schirmer’s value at the end of 6 months. All eyes having severe OSS (OSS of 4) pretreatment moved to lower groups after 06 months. The difference in change of OSS between pre and post treatment is statistically significant by chi square test. 27 eyes (45%) had two step improvements of their OSS score at 06 months

38 eyes (63.3%) of MMP9 negative group had normal Schirmer’s test at the end of 06 months treatment with only lubricants. 1 eye (1.7%) had severe Schirmer’s category at onset of treatment which rose to 2 eyes (3.3%) at the end of 6 months treatment (p<0.05). Out of the total of 60 eyes with MMP9 negative, as many as 28 eyes (46.7%) improved by at least two steps in Schirmer’s value at the end of 6 months.

All patients who were MMP9 positive were started on lubricants. At the end of 06 months, 85% eyes (34 eyes) displayed sufficient improvement so as to warrant continuation of treatment only with lubricants. In 6 eyes (15%), the exacerbated severity warranted an addition of steroids & Cyclosporine. (Tab 2) All patients who were MMP9 negative were started on lubricants only, at the end of 06 months, 96.7% eyes (58 eyes) displayed sufficient improvement so as to warrant continuation of treatment only with lubricants. In 2 eyes (3.3%), the exacerbated severity warranted an addition of Steroids & Cyclosporine. (Tab 2)

Dry Eye Workshop report¹¹ had described OSD as a complex disorder of tears and the ocular surface which has multiple causes and leads to symptoms like foreign body sensation, visual acuity affection with unstable tear film which may harm the ocular surface¹.

Diagnosis of dry eye disease can’t be made on symptoms alone as same can be seen with a variety of ocular surface conditions. Approximately half of all patients with symptoms suggestive of dry eye have been shown to have objective signs ^12–15. The standard i.e. Schirmer’s test is notoriously inaccurate and non-reliable ^16–18.

In various studies, OSD is shown to be associated with elevated MMP-9 in the tears. MMP-9 levels in moderate to severe OSD have been shown to mirror clinical findings⁸. Sambursky and O’Brien⁹ in their study showed MMP-9 levels ranged from 3 to 40 ng/ml in tears. Based on this estimation, InflammaDry (Quidel Corporation, USA) immunoassay is positive if levels of MMP-9 are > 40 ng/mL in tears to supplement the diagnosis of dry eye disease.

Sambursky et al¹⁰ published a multicentric clinical trial with 143 patients with dry eye and 63 controls. In the study, InflammaDry was found to be 85% sensitive, 94% specific, it also had 73% negative predictive value of & 97% positive predictive value for clinical dry eye^10,19.

A total of 100 eyes were enrolled in our study, out of which 40 eyes tested positive for MMP9.This is similar to study conducted by Messmer et al²⁰, where, out of 101 eyes tested for MMP-9, 21.8% were MMP-9positive. Also, in 40.4% dry eye patients & 5.6% of controls, MMP-9 had a value > 40 ng/ml in tear film. Lanza et al²¹, reported 39% of dry eye patients turned up to be MMP-9 positive similar to our results.

In this study, MMP-9 positive patients had mean Schirmer’s value of 12.85 ± 7.07 as against MMP-9 negative patients who had a mean value of 19.18 ± 8.941. Thus, patients with MMP9 have a significantly lower Schirmer’s value suggestive of an inverse relation between the two variables. We also found that MMP9 positive patients had a greater severity of dry eye with Schirmer’s test. 80% patients with severe dry eye were positive for MMP9. Similarly, 55.6% of moderate dry eye patients were positive for MMP9 whereas only 22.5% with normal tear secretion were MMP9positive. The association between severity of Schirmer’s category and MMP9 positivity was significant.

Messmer et al²⁰ reported that, Schirmer’s test results were < 10 mm in 72.3% of dry eye patients and only 5.5% controls. Positive MMP-9 results were seen in 43.2% of patients with Schirmer’s < 10 mm & 44.4% of patients with Schirmer’s < 5 mm. Negative MMP-9 results were seen in 90.6% patients with normal Schirmer’s. Correlation of reduced Schirmer’s & MMP-9 positive result was significant statistically (P < 0.001). These are in line with our study.

In the present study, there was a positive association between the pre-treatment OSS severity and severity of Schirmer’s test, as demonstrated by Chi Square test with a significance of < 0.01. Out of the 40 eyes with normal Schirmer’s test, 19 (47.5%) had a OSS score of 2. Whereas, 10 of 27 eyes (37%) with moderate Schirmer’s test and 4 of 5 (80%) eyes with severe Schirmer’s test had a OSS of 3. Also, all the 4 eyes (100%) with OSS score of 4, had moderate Schirmer’s test. No definite association was found between MMP9 positivity and pretreatment OSS (chi square test: p > 0.05). This goes on to suggest that seemingly asymptomatic patients may be diagnosed and treated based on MMP9 positivity.

Schirmer’s test has a strong association with pre-treatment OSS while MMP9 does not. This result comes as an enigma due to the fact that MMP9 has a association with the categorization of tear film dysfunction as per Schirmer’s, and one would have expected it to be extrapolated to OSS. Messmer et al²⁰ reported a mean OSDI score of 48.2 in dry eye cases in comparison to 10 in controls. Association of Positive MMP-9 results with the OSDI score was statistically significant (P < 0.001). Increased severity of disease correlates with MMP9 positive results i.e 6.8% MMP9 positive with < 12 OSDI score, 25 positive with 13–22 OSDI score, 28.6% positive with 23–32 OSDI score & 37.1% positive with 33–100 OSDI score.

Anti-inflammatory management in OSD has been studied extensively ^23–25 with varied criteria and success matrix. Most of these have concluded that all patients don’t respond similarly to these therapies. Since MMP-9 is an inflammatory mediator of ocular surface^26–27, its elevation detects the presence of inflammation. Thus, MMP-9 test may differentiate patients based on underlying etiology (inflammatory versus non-inflammatory). MMP-9positive results can also give an indication if a patient will have a satisfactory response to anti-inflammatory therapy & help the clinicians decide the line of therapy accordingly.

In the present study, all eyes were treated with topical preservative free lubricants as a pre-treatment protocol. 50% eyes of MMP9 positive group having higher severity of OSS (of 3 and 4) moved to lower grades of OSS after treatment for 06 months. 2 eyes (5%) had no symptoms (OSS = 0) at the end of 6 months. However, the difference in results was not statistically significant. Also, out of 40 eyes with MMP9 positives as many as 10 eyes (25%) improved by two steps at the end of 6 months which, was significant.

In MMP9 positive group, all 4 eyes of the severe Schirmer’s category moved to lower grades of Schirmer’s after treatment for 06 months. 21 eyes (52.5%) had normal Schirmer’s at the end of 6 months treatment as against 9 eyes (22.5%) at the start of treatment. Also, out of the total of 40 eyes, 33 eyes (82.5%) improved by at least two steps in Schirmer’s value at the end of 6 months which was significant as decided in pre-treatment protocol. 6 eyes (15%) required a change of treatment with addition of corticosteroids. This is comparable to results by Aragona et al²⁸ where topical corticosteroids were used in treatment which significantly decreased tear film MMP-9 and led to improvement of signs and symptoms of OSD. Pflugfelder et al²⁹ had a slightly different result where a topical corticosteroid produced clinically significant results mainly in severe disease.

In MMP9 negative group, eyes were treated with topical preservative free lubricants. 38 eyes (63.3%) shifted to normal Schirmer’s category at the end of 06 months against 31eyes (51.7%) at beginning of treatment. Also, one eye (1.7%) had severe Schirmer’s category at onset of treatment which rose to two eyes (3.3%) at the end of 6 months treatment (the difference in results are statistically significant). As many as 27 eyes (46.7%) improved by at least two steps in Schirmer’s value at the end of 6 months which was taken as significant improvement. In MMP9 negative group, all eyes having severe OSS (OSS of 4) pre-treatment moved to lower groups after 06 months. 27 eyes (45%) had at least one step improvement of their OSS score at 06 months which was considered significant.

In MMP9 positive group, all patients were initially started on treatment with topical lubricants. At the end of 06 months, 6 eyes (15%) required an additional medication (topical steroid/Cyclosporin) to alleviate symptoms. In MMP9 negative group, at the end of 06 months, as many as 96.7% eyes (58 eyes) displayed sufficient improvement/ static disease activity so as to warrant continuation of treatment only with lubricants. In 2 eyes (3.3%), the severity warranted an addition of one or more drugs (topical steroids/Cyclosporin).

In the present study, there seems to be a benefit in adding steroids early to eyes which were MMP-9 positive and most of the eyes which were MMP-9 negative showed good subjective and objective response to topical lubricants only. MMP-9 results can help in segregating patients with OSD into groups who will benefit with early anti-inflammatory treatment and those who probably need only lubricants as shown in the flowchart in Fig. 5. It also may be useful to follow up to see if treatment has been working and to guide the further treatment protocols.

In conclusion, a pilot study in cases of OSD with Schirmer’s test (Objective criteria) and OSS (Subjective criteria) was compared with MMP-9 levels. MMP-9 positive eyes were found to be associated with a worse Schirmer’s score though not with poorer OSS scores. All eyes were started on lubricants and after 06 months, in MMP9 positive group, there was a statistically significant improvement in both OSS and Schirmer’s values with lubricants. However, a clinically significant number of patients needed steroids in addition to lubricants. Similarly, at 06 months, in MMP9 negative group, there was a statistically significant improvement in both parameters on only lubricants. These results show a trend that there is a case of evaluating all cases of OSD with MMP-9 test and treating them depending on results of this test. There is also a case for starting steroids early in cases which are MMP-9 positive.

Declaration Of Conflicting Interests: The Authors declare that there is no conflict of interest

Declaration of funds: No funds/grants in any kind have been received by authors/Institution for this study from any third party.

Author Contribution

S.G. and S.S.- wrote main manuscriptS.B., A.M.,A.S.- prepared figures, tables and algorithmsAll authors reviewed the manuscript

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Table 1- Mean Schirmer values in Group I and II

Number of eyes

Mean

Sch value

Std. Deviation

Std. Error Mean

MMP9 +

MMP9 -

12.85

19.18

7.069

8.941

1.118

1.154

Table 2 -Summary of initial treatment and treatment at 06 months

GROUP 1
Initial Treatment	Treatment after 06 months
HPMC: 100% (n=40)	HPMC: 85% (n=34)
	HPMC plus Steroids: 15% (n=6)

GROUP II
Initial Treatment	Treatment after 06 months
HPMC only : 100% (n=60)	HPMC: 96.7% (n=58)
	HPMC plus Steroids: 3.3% (n=2)

No competing interests reported.

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Comparison of tear MMP9 with Schirmer’s test in ocular surface disorders & formulation of a treatment algorithm based on the results

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Abstract

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INTRODUCTION

MATERIAL AND METHODS

RESULTS

DISCUSSION

CONCLUSION

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Author Contribution

References

Tables

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