Purpose
To investigate the nature and characteristic features of deposits causing opacification of intraocular lenses (IOLs) based on the examination of clinical findings using scanning electron microscopy (SEM) and energy-dispersive x-ray spectroscopy (EDX) analysis.
Design
Retrospective, observational case series.
Methods
This is a multicenter study of 6 hydrophilic acrylic IOLs (Lentis LS-502-1; Oculentis GmbH, Berlin, Germany) with a hydrophobic surface that were explanted from 5 patients because of opacification. Three patients had an uncomplicated phacoemulsification. One patient underwent combined phacoemulsification and pars plana vitrectomy for retinal detachment and later silicone oil endotamponade owing to redetachment. The last patient had a pars plana vitrectomy and silicone oil instillation combined with phacoemulsification for tractive retinal detachment and diabetic retinopathy. The explanted lenses were submitted to our laboratory and were examined by SEM and EDX in order to identify the morphologic features and the composition of the deposits.
Results
SEM and EDX analyses confirmed the presence of calcific deposits in the interior of the opacified hydrophilic IOLs, with a pattern showing the formation of lumps on the surface. The lumps were due to subsurface formation of calcium phosphate crystalline deposits. The crystallite clusters seemed to diffuse from the IOL interior to the surface.
Conclusions
We demonstrated the calcification pattern of the hydrophilic IOL (Lentis LS-502-1) with a hydrophobic surface. Although hydrophilic acrylic lenses have a hydrophobic surface, the development of calcification is a possible threat initiating from the hydrophilic subsurface of the IOLs.
Modern hydrophilic intraocular lens (IOL) opacification owing to calcification is a serious complication after an uneventful cataract surgery, leading to IOL explantation. Calcification of hydrophilic acrylic IOLs takes place through the deposition of calcium phosphate crystallites, either on the IOL surface or within the optic material, or both, depending on the hydrophilic acrylic IOL designs. In an earlier investigation including the 4 major hydrophilic IOL designs, Hydroview, Memorylens, SC60B–OUV, and Aqua-Sense, we have demonstrated the deposition of calcium phosphate crystallites in the IOLs. Hydroxyapatite, the thermodynamically most stable calcium phosphate, was the predominant crystalline phase. The formation of calcium deposits may be attributed to the fact that aqueous humor is supersaturated with respect to a number of calcium phosphate phases. As calcification of hydrophilic acrylic lenses seems to be a multifactorial phenomenon, and the exact mechanism is unknown, we suggested that one of the main factors that may be involved in the pathophysiology of this problem is related to the surface hydroxyl groups of the polyacrylic materials. These groups, mostly ionized at physiological pH, facilitate nucleation and further growth of calcium phosphate crystallites. The newer design of hydrophilic acrylic IOLs consists of the combination of a hydrophilic acrylic body with a hydrophobic surface, in order to avoid primary calcification. However, as the exact combination of the factors leading to calcification of the lenses are still unknown, sporadic studies demonstrated that the calcification appears to be a potential complication of these modern hydrophilic acrylic IOL designs with hydrophobic surfaces. Herein, we present the analysis of 6 hydrophilic IOLs with hydrophobic surfaces. All IOLs were explanted owing to significant visual impairment. This study was carried out in an effort to further contribute to a better understanding of the mechanism of acrylic IOL calcification.
Methods
This is a retrospective, observational case series of 6 IOLs (Lentis LS-502-1; Oculentis GmbH, Berlin, Germany) that were explanted from 5 patients owing to opacification. All patients underwent surgical procedures and IOL implantation at the University Hospital of Regensburg, Germany, between November 2009 and April 2011. All IOL explantations and exchanges were performed at the same hospital between November 2011 and March 2013. The study was approved by the ethical committee of the University Hospital of Regensburg, Germany. In accordance with the Declaration of Helsinki, informed consent was obtained from all participants after explanation of the purpose and nature of the investigation.
The calcified IOLs ( Table 1 ) were surgically explanted and examined by scanning electron microscopy (SEM; Leo Supra 35V; Carl Zeiss, Oberkochen, Germany) equipped with an energy-dispersive x-ray analysis unit (EDX; Quantax; Bruker, Berlin, Germany) with Si detector and resolution of 129 eV. The IOLs were covered by a few atomic layers of graphite in a carbon coating device (SCD500; Bal-tec, Schalksmuhle, Germany) to make them conductive. Internal calibration standards were used for the semiquantitative analysis of the test specimens. IOLs were examined on both their surfaces (one at a time) following their immobilization on aluminum slabs covered with a conductive carbon double-stick tape. The cross section was observed in special holders following their dissection with a scalpel. Line scan analysis was performed for the elemental analysis of formations and the respective identification. In calcium phosphate formations the calcium and phosphorus peaks were easily distinguished and the positions at which the calcified deposits were located were marked.
| IOL No. | Date Implanted | Date Explanted | Intraocular Days | Date Packaged | IOL Type | Patient’s Date of Birth | Eye |
|---|---|---|---|---|---|---|---|
| 1 | 12/15/2010 | 3/14/2013 | 820 | 4/23/2013 | Lentis LS-502-1 | 2/16/1936 | OS |
| 2 | 2/9/2011 | 5/21/2012 | 467 | 4/23/2013 | Lentis LS-502-1 | 2/16/1936 | OD |
| 3 | 3/4/2011 | 11/16/2011 | 257 | 4/23/2013 | Lentis LS-502-1 | 7/20/1955 | OD |
| 4 | 11/12/2009 | 8/24/2011 | 650 | 4/23/2013 | Lentis LS-502-1 | 11/24/1940 | OD |
| 5 | 4/18/2011 | 12/7/2012 | 599 | 4/23/2013 | Lentis LS-502-1 | 5/21/1925 | OS |
| 6 | 4/12/2011 | 8/16/2012 | 492 | 4/23/2013 | Lentis LS-502-1 | 9/9/1949 | OS |
Case 1 (Lens Numbers 1 and 2)
A 74-year-old male patient had an uneventful phacoemulsification with implantation of Lentis LS-502-1 (Oculentis GmbH) IOLs in the left eye in December 2010 and in the right eye in February 2011. The patient had a medical history of hypertension, atrial fibrillation, chronic obstructive pulmonary disease, diabetes, and renal failure. He presented 16 months after surgery of the right eye and 27 months after surgery of the left eye with a marked decrease in visual acuity (20/25 to hand motion in the left eye and 20/40 to 20/80 in the right eye), which developed over a period of 2 months. The IOLs were explanted and a hydrophobic IOL was implanted in both eyes.
Case 2 (Lens Number 3)
A 55-year-old male patient with a medical history free of systemic conditions was submitted to phacoemulsification and implantation of a Lentis LS-502-1 (Oculentis GmbH, Berlin, Germany) IOL combined with vitrectomy for rhegmatogenous retinal detachment in the right eye. Two months later he returned to the clinic with recurrent retinal detachment owing to proliferative vitreoretinopathy and was submitted to silicone oil injection. In November 2011, 8 months after implantation of the IOL and 6 months after silicone oil injection, the IOL was explanted during silicone oil removal owing to opacification. Visual acuity was 20/80 before and 1 year after IOL exchange and silicone oil removal.
Case 3 (Lens Number 4)
A 69-year-old male patient with a history of hypertension and cardiac arrhythmia had an uneventful phacoemulsification with implantation of Lentis LS-502-1 (Oculentis GmbH, Berlin, Germany) IOL in the capsular bag of the right eye. The IOL was explanted 22 months postoperatively owing to opacification that caused a decrease in visual acuity from 20/40 to hand motion.
Case 4 (Lens Number 5)
An 82-year-old male patient had an uneventful phacoemulsification with implantation of a Lentis LS-502-1 (Oculentis GmbH) IOL in the capsular bag. The patient had a medical history of hypertension, atrial fibrillation, and coronary heart disease. The IOL was explanted 20 months postoperatively owing to optic opacification and a decrease in visual acuity to 20/40 with strong visual symptoms.
Case 5 (Lens Number 6)
A 62-year-old female patient had a pars plana vitrectomy and silicone oil instillation combined with phacoemulsification and implantation of a Lentis-LS-502-1 (Oculentis GmbH) IOL for tractive retinal detachment and diabetic retinopathy. The patient had a history of diabetes, renal failure, renal anemia, and hypertension. After 13 months the silicone oil was removed. After removal of the silicone oil a capsulotomy was performed. The IOL was explanted 3 months later owing to opacification. Visual acuity was 20/200 before IOL explantation and stabilized at 20/60 1 year after IOL exchange.
The interval between the initial cataract surgery and the onset of the lens opacification was 257–820 days. One of the patients was found to develop bilateral IOL opacification. Two of the patients underwent combined pars plana vitrectomy and silicone oil instillation combined with phacoemulsification and IOL implantation, 1 for retinal rhegmatogenous detachment and the other for tractive retinal detachment and diabetic retinopathy. Most of the patients had some systemic disease. Four patients had systemic hypertension, 2 had atrial fibrillation, 2 had renal failure, 2 had type II diabetes, 1 had chronic obstructive pulmonary disease, 1 had coronary heart disease, 1 had cardiac arrhythmia, 1 had renal anemia, and 1 patient had a disease-free medical history. The systemic diseases of the patients are summarized in Table 2 .
| Patient No. | Hypertension | Atrial Fibrillation | COPD | Diabetes | Renal Failure | Cardiac Arrhythmia | CHD | Renal Anemia |
|---|---|---|---|---|---|---|---|---|
| 1 | + | + | + | + | + | − | − | − |
| 2 | − | − | − | − | − | − | − | − |
| 3 | + | − | − | − | − | + | − | − |
| 4 | + | + | − | − | − | − | + | − |
| 5 | + | − | − | + | + | − | − | + |
The substances used during surgery were diluted epinephrine solution for pupil dilation at the beginning of the procedures (adrenaline 1:1000; Infectopharm) and a cohesive viscoelastic for capsulorrhexis and lens implantation (Healon; AMO).
Results
Case 1 (Lens Numbers 1 and 2)
Examination of opacified IOL number 1 showed lumps on the anterior surface of the lens due to subsurface formation of calcium phosphate deposits (∼10 μm). The solid deposits (most probably clusters of apatite crystals, the size of which is of the order of few tens of nanometers) of crystallite clusters seem to form a front migrating from the IOL interior to the surface, hence the protruding globules on the surface ( Figure 1 ).
The calcified clusters were present throughout the surface. EDX microanalysis confirmed the composition of the mineral underlying bumps as calcium phosphate, as can be seen in Figure 2 .
It should be noted that no calcium phosphate surface deposits were identified on the IOL surface. The formation of calcific deposits took place exclusively in the interior of the IOLs. The morphologic examination of a cross section of IOL number 1 is shown in Figure 3 .
In this low-magnification picture the entire lens cross section is shown. To the left is the posterior surface of the lens. As can be seen, clusters of calcific deposits appear to form from the posterior surface extending to the interior (the formation at a depth of ∼18 μm from the back side is shown). The morphology of the formation shown at ∼18 μm is shown in Figure 4 .
Prismatic crystallites with sizes reaching 500–600 μm and microscopic (20–40 nm) crystallites of hydroxyapatite can be seen ( Figure 4 ). The formations appeared to advance from the back to the front side of the IOL, as seen in Figure 5 .
As can be seen, the amount of formations (clusters of nanocrystallites) is reduced closer to the front side (left side of the image), in agreement with the observation of higher proximity to the anterior surface of the IOL of crystallite clusters. It seems that the formation of calcium phosphates took place throughout the thickness of the IOL, the density being relatively reduced to the anterior surface side. The time of implantation (820 days) apparently was sufficient for the almost uniform formation of calcific deposits in the interior of the lens.
It should be noted that near the surface it seems that the formations of the calcific clusters were smaller in size (<200 nm). Apparently, the crystallites formed near the surface were not allowed either to grow to larger sizes or to aggregate, forming the large clusters exhibited in the back side.
At the interior of the IOL cross section, large plate-like formations were found and were identified as calcium phosphates. The plate-like crystals and their size suggested the formation of octacalcium phosphate (OCP), which is a precursor phase to the formation of hydroxyapatite, as shown in Figure 6 .
The OCP crystallites shown in Figure 6 seem to have been formed more recently than the deposits in the front surface, owing to the continuous feed with the corresponding ions of the aqueous humor, and there was not sufficient time for their conversion into the thermodynamically more stable hydroxyapatite. Hydroxyapatite crystallites were identified further in the bulk of the IOL, at larger penetration depths with respect to the posterior surface.
The examination of IOL number 2 also showed the formation of subsurface deposits. Detail of the globules showed that they consisted of dense formations of ∼50–70 nm size.
The cluster formations on the surface were denser in comparison with the formations of IOL number 1, as seen in SEM Figure 7 .
The surface microanalysis of the entirety of IOL number 2 is shown in Figure 8 . As can be seen, the presence of the strong peaks of Ca and P suggest the high concentration of calcium phosphate mineral salt in this lens.
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