Effect of corneal collagen cross linking on crystalline lens clarity graded by Pentacam Nucleus Staging Software

doi:10.21203/rs.3.rs-2959432/v1

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Research Article

Effect of corneal collagen cross linking on crystalline lens clarity graded by Pentacam Nucleus Staging Software

https://doi.org/10.21203/rs.3.rs-2959432/v1

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published 31 Dec, 2022

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Background

to describe the effect of ultraviolet rays dissipated during corneal collagen crosslinking on cataract development in keratoconus patient in Cairo, Egypt.

Methods

We performed a descriptive prospective study that will assess the influence of uneventful corneal collagen crosslinking in management of keratoconus on the crystalline lens clarity in one hundred Eye by oculus pentacam nucleus staging (PNS) for patients attending the specialist eye hospital at the military medical complex of Kobri el Kobba in collaboration with Al-Azhar university hospitals diagnosed from January 2021.

Results

Our study reported that corneal collagen crosslinking has a highly significant effect in developing lens opacities specially the older age and small AC depth and reported also its affection on visual acuity.

Conclusion

Corneal collagen cross linking as a method of stabilizing keratoconus progression results in significant changes and increase in the densitometry of the crystalline lens which is a problem that increase the risk in the development of cataract, this is particularly in patient more exposed to ultraviolet rays and pre CXL high lens densitometry.

Collagen crosslinking

Crystalline lens graded

Pentacam Nucleus Staging Software

Ectasia of the cornea is a worldwide disease affecting one every 2000 of young patients ⁽¹⁾.

Keratoconus makes significant affection of the corneal curvature, lead to astigmatism which reduce the visual acuity by image distortion, sensitivity to light and glare ⁽²⁾.

According to the stage of the keratocnous and the progression can be managed by different options. If it’s stable, the idea is to correct the vision. If it is progressing, the main goal of management is to stop the progression ⁽³⁾.

Keratoconus affect the corneal shape and leads to distortion and stromal thinning, so the traditional methods in management as soft CL and glasses are available only in the early stages. ⁽²⁾.

In moderate to severe stage of keratoconus, rigid gas permeable CL is the main method to improve the vision by creating a tear pool between it and the cornea, which neutralize the aberrations created by keratoconus ⁽³⁾.

The main gold standard minimally invasive procedure to stop the progression of keratoconus is corneal collagen crosslinking ⁽⁴⁾.

Dresden protocol for CXL involves the removal of the corneal epithelium followed by application of riboflavin solution to the de-epithelialized cornea for thirty minutes then the cornea is ultraviolet-A irradiated for another thirty minutes⁽¹⁾.

Another option for improving the vision is to implant a small curved PMMA rings in corneal stroma to flatten the curvature of the cornea, which is called corneal rings ⁽²⁾.

The last option in management too thin cornea is completely replacing the all layer (penetrating keratoplasty) or partial layers (lamellar keratoplasty) with new healthy donor tissue ⁽⁵⁾.

Some studies reported that exposure of guinea pigs to ultraviolet rays A develops nuclear cataract ⁽⁶⁾.

Previously, ophthalmologists classified the grades of cataract according to old subjective method of classification called (LOCS III) into nuclear, cortical and posterior subcapsular but it depends on individuals evaluation ⁽⁷⁾.

So, in this study we used the Pentacam high resolution (HR) and Scheimpflug anterior segment imaging system as a newly evolved objective method for assessment of lens clarity which give numerical values away from the other old subjective one ⁽⁷⁾.

Pentacam nucleus staging is a newly evolved method of grading that taking a series of images of the nucleus, forming a sample of the nucleus and determine its optical density according to the idea of light scattering, generating a grade of cataract from zero to five ⁽⁸⁾.

Scheimpflug photography and densitometric image analysis are very precise techniques for light scattering measurement in the anterior segment of the eye. Crystalline lens become thicker, loose its clarity and their tissue-specific light scattering increases either with age or suspected to some factors that accelerate the process of losing its clarity⁽⁹⁾.

study design

This is a descriptive prospective study that detected the impact of UVA rays dissipated during collagen corneal cross linking using Dresden protocol for keratoconic corneas on the crystalline lens clarity graded by PNS.

Setting and participants

This is a descriptive prospective study that assessed the effect of UVA rays dissipated from corneal collagen cross linking of keratoconic corneas on crystalline lens clarity by a newly evolved method of grading called pentacam nucleus staging.

The study performed on one hundred eyes of a patients attending Kobri El Koba military hospital in collaboration with faculty of medicine, Al Azhar University.

Patients were enrolled in our study of both gender with a clear lens, without previous history of ocular surgery, diagnosed from January 2021 till July 2022.

Procedure

Full assessment of the patients is performed before surgery after taking written informed consent.

Assessment include complain, its onset and duration, past medical history, macular function test and color discrimination, Pupillary light reflex, direct and consensual, Corrected and uncorrected distance visual acuity, Slit-lamp assessment, Fundoscopy to rule out posterior segment pathology affecting the anterior segment, Assessment of the keratoconus using oculus pentacam HR and Scheimpflug imaging by using oculus pentacam (pentacam nucleus staging).

The inclusion criteria was age 15–40 years, both gender with no prior ocular disease, clear cornea devoided from any corneal dystrophy and degenerations, keratoconus confirmed by pentacam, post Lasik keratectasia, clear crystalline lens grade 0 according to pentacam nucleus staging (PNS).

While the exclusion criteria were age more than 40 years and less than 15 years, uncontrolled diabetes, autoimmune disorders, congenital lens opacities, early faint lens opacities approved by pentacam, Occupational radiation (radiologist, dentist…etc.), Previous operation other than refractive procedure, Any type of corneal pathology as corneal degeneration and corneal dystrophy.

Ocular examination

complete ocular examination of all patients include, corrected and un corrected visual acuity by log MAR chart, color vision ,amsler grid, pupillary function, dilate the pupil by three drops of cyclopentolate, fundus examination, check the clarity of the crystalline lens to exclude any type of lens opacities.

Investigation performed

Pentacam HR type 70900 SN 98129080 was used in the study to evaluate the keratoconus and detection of the clarity of the crystalline lens through its densitometry by schiempflug imaging, schiempflug imaging was done preoperitavily,1st month and 3rd month after cross linking.

Technique of corneal collagen crosslinking

In this study we used the Epi off Dresden protocol for CXL and involves removal of the corneal epithelium to about 8mm zone by soaking the epithelium with alcohol the removal it by PRK blade, Imbibition of riboflavin 0.1% isotonic (vibex ®) used in my study every 5 minutes, Application of UV rays of 8mm spot diameter (OVEDRO KXL ® 11001018 KXL 1603082016) of UV-A light exposure of wavelength λ370nm 3mw/Cm2 for 30 minutes to be the total energy received 5.4 j/cm2, the distance of the device from the eye is 5cm, Application of isotonic riboflavin every 5 min during UV application and Then contact lens applied and the patient prescribed antibiotic eye drops, non-steroidal eye drops and artificial tears for 1week then prednisolone ED for two weeks then Fluca ED for 2 months. Following up the patients by slit lamp examination for corneal clarity and epithelial healing and contact lens removal 6 day post operatively. 1st month and 3rd month post-operative intervals follow up by PNS densitometry.

Statistical analysis

In this study we used specific measures to get the statistical analysis of the collected data.

All of the data collected and managed for statistical analysis by (IBM SPSS) VERSION 23.

The quantitative data presented into mean, standard deviations and ranges.

The qualitative variables formed in the form of numbers and percentages.

Paired t-test used for comparison between the quantitative and parametric data.

ANOVA test used in comparison between more than two groups.

Assessment of the relation between two quantitative measures in the same group by spearman correlation.

The p-value was considered significant if P > 0.05: Non significant P < 0.05: Significant < 0.01: Highly significant.

Ethical consideration

This descriptive prospective study was conducted after the approval of the research ethics committee at al Azhar university at 5/12/2020, All patients received complete explanation of the nature and the purpose of the study, an informed consent was obtained from all participants in the research before inclusion, all names of the participants were hidden and replaced by numbers to maintain their privacy and confidentiality of the data and Data were not used for any other purpose.

The age distribution as shown in (Table 1) range 15–40 years old with mean SD (27.48 ± 6.30), while one hundred eyes of fifty patient included in the study 27 (54.0%) were male and 23 (46.0%) were female patient.

Table (1)

Showing age and gender distribution in this study

		No. = 50
Age	Mean ± SD	27.48 ± 6.30
Age	Range	15–40
Sex	Female	23 (46.0%)
Sex	Male	27 (54.0%)

All of the patient shared a common complain which is diminution of vision without past medical history, but some of the patient presented with past ocular history of refractive surgery (LASIK) 20%. By examination 20% of the patient has past ocular history of refractive surgery show LASIK flap (Table 2).

Table (2)

Table show history and examination data of the cases

		No.	%
Complain	Diminution of vision	100	100.0%
Past medical history	NAD	100	100.0%
Past ocular history	NAD	80	80.0%
Past ocular history	Lasik	20	20.0%
Anterior segment of the eye	NAD	80	80.0%
Anterior segment of the eye	Lasik flap	20	20.0%
Posterior segment of the eye	NAD	100	100.0%

One hundred eyes participated in the study fifty of them right and fifty of them left. Visual acuity ranging from 0.3–0.9 with mean SD (0.54 ± 0.15) (Table 3).

Table (3)

Showing the distribution of the eyes and their range and mean of visual acuity

		No. = 100
Eye	OD	50 (50.0%)
Eye	OS	50 (50.0%)
Visual acuity	Mean ± SD	0.54 ± 0.15
Visual acuity	Range	0.3–0.9

Corneal thinnest location, anterior chamber depth and Lens densitometry

Pre corneal thinnest location range from 399–565 with mean SD 457.38 ± 31.60. Anterior chamber depth range from 2.5–4 with mean SD 3.20 ± 0.33. Lens densitometry range from 5.3–10.1 with mean SD 7.42 ± 0.94 (Table 4).

Table (4)

Corneal thinnest location, anterior chamber depth and Lens densitometry

Pre		No. = 100
Corneal thinnest location	Mean ± SD	457.38 ± 31.60
Corneal thinnest location	Range	399–565
Anterior chamber depth	Mean ± SD	3.20 ± 0.33
Anterior chamber depth	Range	2.5–4
Lens denistometry	Mean ± SD	7.42 ± 0.94
Lens denistometry	Range	5.3–10.1

This study show highly significant increase in the lens densitometry 1st month post operatively by mean SD 8.37 ± 1.04 and 3rd month by 8.51 ± 1.03 (Table 5).

Table (5)

Showing effect of cxl 1st and 3rd month on lens densitometry, range of zero PNS 0 to 11.5 denistometry

Lens denistometry	Pre	1month	3 month	Test value•	P-value	Sig.
Lens denistometry	No. = 100	No. = 100	No. = 100	Test value•	P-value	Sig.
Mean ± SD	7.42 ± 0.94	8.37 ± 1.04	8.51 ± 1.03	360.409	0.000	HS
Range	5.3–10.1	6.3–11.1	6.4–11.5	360.409	0.000	HS
Difference	--	0.94 ± 0.53	1.09 ± 0.46
Paired t-test	--	17.890	23.748
P-value	--	< 0.001 (HS)	< 0.001 (HS)

The study revealed that there is a direct relation between age and pre-operative densitometry (Table 6).

Table (6)

Showing relation revealed in the study

	Lens denistometry
	Pre		Post 1month		Post 3 month
	r	P-value	r	P-value	r	P-value
Age	0.361^*	0.010	0.411^**	0.003	0.420^**	0.002
Visual acuity	0.122	0.227	0.009	0.928	-0.049	0.630
Pre corneal thinnest location	0.031	0.759	-0.321^**	0.001	-0.338^**	0.001
Pre Anterior chamber depth	-0.202^*	0.044	-0.088	0.383	-0.131	0.194

There is a highly significant changes in the visual acuity after 1st m and 3rd m in relation to the changes in densitometry as shown in (Table 7)

Table (7)

Showing the visual acuity changes after 1st m and 3rd m in relation to the changes in denistometry

Visual acuity	Pre	1month	3 month	Test value•	P-value	Sig.
Visual acuity	No. = 100	No. = 100	No. = 100	Test value•	P-value	Sig.
Mean ± SD	0.29 ± 0.12	0.38 ± 0.18	0.33 ± 0.14	51.499	0.000	HS
Range	0–0.5	0–1	0–0.7	51.499	0.000	HS
Difference	--	0.09 ± 0.10	0.04 ± 0.07
Paired t-test	--	8.689	4.888
P-value	--	< 0.001 (HS)	< 0.001 (HS)

The study results revealed that there is significant relation between the the densitometry and the affection of log MAR visual acuity as shown in (Table 8)

Table (8)

Table showing significant direct relation between the increase in lens denistometry and changes in log MAR visual acuity

Difference of visual acuity	Difference of lens denistometry
	1month		3 month
	r	P-value	r	P-value
1 month	0.569**	0.000	--	--
3 months	--	--	0.537**	0.000

This is the first study to evaluate the effect of corneal collagen cross-linking on the human crystalline lens clarity graded by the newly evolved objective method of grading which is pentacam nucleus staging densitometry in an Egyptian population and its effect on the visual acuity.

Cataract divided into three main types nuclear, cortical, and sub capsular ⁽¹⁰⁾.

Haag, Sieber, and Heßling divided the risk factors into acquired factors and congenital factors ⁽¹¹⁾.

Acquired factors include smoking and alcohol consumption, exposure to radiation, vitamin and protein deficiency, high blood pressure, increasing age ⁽¹⁰⁾.

Radiation in the wavelength categorized into different ranges as UVC (100–280 nm), UVB (280–315 nm), UVA (315–400 nm), and visible light (380–80) nm ⁽¹¹⁾.

Kamari documented that Ultraviolet rays cause lens opacification by oxidative stress, phototoxicity of crystalline proteins which lead to apoptosis ⁽¹²⁾.

Thirty seven percent of UVA radiation at 340 nm is absorbed by the cornea, 14% by the aqueous humor, and 48% by the lens ⁽¹³⁾.

In general by time exposure to UVA and UVB spectrum lead to decrease in lens transparency ⁽¹¹⁾.

Cataract cause visual impairment by absorption and scattering of light in the eye lens ⁽¹⁴⁾.

Many studies reported that there’s a great association between cataract development and ultra violet rays exposure wish support my study results.

Miyashita et al. (2019) ⁽¹⁵⁾ have reported that ultraviolet (UV) radiation to be a main risk factor for cataract development.

Giblin et al. ⁽¹⁵⁾ previously reported that long-term exposure to low-dose UVA induce nuclear cataract (NUC) in a guinea pig model in his animal experiment ⁽¹⁵⁾.

Miyashita et al. (2019) ⁽¹⁵⁾ reported in his study that there is a significant association between UV exposure and posterior sub capsular cataract development.

Delavar also reported that there is a significant relation between the race living in regions with different UV intensities exposure and cataract development ⁽¹⁶⁾.

His study found less association between the highest exposures of ambient UVR and cataract development than previously reported studies which is against my study results.

Cécile Delcourt et al. set many of Studies in France and North Africa and his studies revealed there is a direct significant effect of ultra-violet rays and cataract development which go with my study results ⁽¹⁷⁾.

McCarty et al. made several studies in Australia and USA but Australian studies revealed increased risk of cortical cataract development subtypes than in the United States studies ⁽¹⁸⁾.

Delavar et al. found no association between lifetime average times outdoors exposure to UV and cataract risk which is against my study ⁽¹⁶⁾.

While Delcourt et al. have found decreased or no risk which go against my study and the other old studies ⁽¹⁹⁾.

Most research regarding in vivo experiments is performed with rodents, especially rats, pigs and cows ⁽²⁰⁾.

Söderberg, Michael, and Merriam reported that irradiation dosage to induce cataracts in rat eyes with a wavelength of 300 nm is 2.2 kJ/m2 ⁽²¹⁾

Olsen made his experiments on porcine eyes which is anatomically very close to the human eye ⁽²²⁾.

Haag, Sieber, and Heßling performed an experiment on porcine lens ex-vivo which irradiated with wavelengths 311 nm (UVB) and 370 nm (UVA) which revealed that UVB has a very cataractogenic effect on crystalline lens ⁽¹¹⁾

The dark field method ranks UVA radiation as more cataractogenic than UVB radiation which go with my study ⁽²³⁾

Hessling, Spellerberg, and Hoenes studied the irradiation in vitro the crystalline lens of rodent animals and his study revealed the significant effect of UVR on cataract development and bacterial growth during the 24 h experiment duration despite the usage of GVPC (Glycine-vancomycin-polymyxin-cycloheximide agar) and intense irradiation ⁽²⁴⁾.

Another impact might be the overall experiment time because lens tissue degenerates after 5 h after lens extraction ⁽²⁵⁾

There are a lot of newly evolved method of grading and early detection methods of cataract away from the old one that depend on the inspection of the lens color and the evaluation of the ophthalmologist such as slitlamp evaluation by LOCS classification.

Previously a lot of studies performed by scientists supporting my study to depend on new methods for grading and early detection of cataract away from the old one.

Haag, Sieber, and Heßling reported that Cataract formation starts earlier on a molecular basis, so it can be detected earlier by fluorescence methods ⁽¹¹⁾.

New objective method applied for evaluation are slit lamps fluorescence measurements, and chromatographic procedures and Dark field images which depend on the amount of light scattering⁽¹¹⁾

So there is a great interest of the scientist nowadays to measure the degree of the light scattering during its pathway in the lens to get the degree of the cataract on objective numerical value.

So I depended in my study on grading the nuclear density on a newly objective method for grading (PNS) away from the old subjective methods of cataract grading (LOCS3) that’s depending on the color of the nucleus and the examiner experience.

Kim et al. used also pentacam nucleus staging for cataract grading which is consistent with my study as an objective method of grading to detect the changes in the lens clarity depending on measuring the degree of light scattering ⁽²⁶⁾.

Nixon also used PNS to grade the pre-operative cataract and linked it with the phaco-emulsification parameters used during the phaco-emulsification especially in eyes with high grades of cataract ⁽²⁶⁾.

That’s supporting the aim of the study to use this method of grading of the lens clarity away from the old methods.

Another support for this grading method used in my study, Pei et al. agreed that Pentacam Scheimpflug densitometry is a good objective clinical parameter for judging a patient’s visual impairment resulting from light scattering caused by lens opacification ⁽²⁷⁾.

My study revealed that there is a significant association between ultraviolet rays exposure during corneal collagen crosslinking as a method of haulting the progression of keratoconus may be due to denaturation of lens protein and apoptosis of lens cells fibers as Kamari reported in his study in 2019 which is powerful support of my study.

Mostly the energy dissipated from UVA during CXL lead to phototoxicity which lead to increase in the grade of nuclear cataract.

When the light pass throw the lens opacities of the nuclear cataract lead to light scattering which affect the visual acuity and the quality of vision, this may explain my study results in which there is decrease in visual acuity 1st and 3rd month post crosslinking as Gakamsky documented in his study.

Strengths and limitations

There is multiple drawbacks in my study the small sample size, the all attention was paid to only one type of cataract which is the nuclear one without taking in consideration the other type of cataract, the short duration of follow up.

Unfortunately, my study did not collect direct information on sun protection. Darker iris colors, such as green, hazel, and dark brown, which were associated with a slight increased risk of cataract when compared to blue irises, and also our study did not have information on cataract subtype.

I recommend giving more attention to this worldwide ophthalmological problem and making more studies about the effect of ultraviolet rays on development of cataract either during crosslinking or ultraviolet rays exposure outdoors or medical stuff exposed to ultravioletrays

Corneal collagen cross linking as a method of treating keratoconus results in significant changes and increase in the densitometry of the crystalline lens which is a problem that increase the risk in the development of cataract this is particularly in patient more exposed, to ultraviolet rays and pre CXL high lens densitometry so we recommend after this study the necessity to good screening for patient preoperatively by taking history to know the patient more subjected to UV rays and the AC depth and pre operatively lens densitometry to adjust the parameters of the duration and the total energy delivered to the cornea during CXL.

Ethics approval and consent to participate

This study was approved by the ethics committee of the universidad delrosari under the reference cvo 005 717-cv1069 and conducted according to the tenets of the helsinki declaration. Informed consent to participate was obtained from the parents or legal guardian in all cases.

Availability of data and materials

The data that support the findings of this study are available from the corresponding

Author, AEF, upon reasonable request.

Funding

No funding

Authors’ contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis. The first draft of the manuscript was written by all authors and also commented on previous versions of the manuscript. all authors read and approved the final manuscript.

Acknowledgements

We thank the participants for participating in the study.

Consent for publication

Not applicable.

Competing interests

The authors report no conflicts of interest in this work

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No competing interests reported.

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Effect of corneal collagen cross linking on crystalline lens clarity graded by Pentacam Nucleus Staging Software

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