Pathological evaluation of postmortem human eyes implanted with a new single-piece hydrophobic acrylic lens

Pathological evaluation of postmortem human eyes implanted with a new single-piece hydrophobic acrylic lens Andrea M. Izak, MD, Liliana Werner, MD, PhD, Suresh K. Pandey, MD, David J. Apple, MD Purpose: To report the pathological findings in 14 human cadaver eyes implanted with a single-piece AcrySof威 (Alcon Laboratories) posterior chamber intraocular lens (IOL). Setting: David J. Apple, MD Laboratories for Ophthalmic Devices Research, John A. Moran Eye Center, University of Utah, Salt Lake City, Utah, USA. Methods: Fourteen human autopsy eyes implanted with a single-piece AcrySof (SA30AL) IOL were evaluated. The eyes were sectioned at the equatorial plane, and the anterior segment containing the IOL in the capsular bag was evaluated from a posterior perspective (Miyake-Apple view) and from an anterior perspective (surgeon’s view) after removal of cornea and iris. They were then processed through paraffin, sectioned, and stained with hematoxylin–eosin, periodic acidSchiff, and Masson’s trichrome and examined under light microscopy. Results: All IOLs had symmetric in-the-bag fixation. Slight decentration was measured in 1 eye, which also had an anterior capsule tear. Grade 1 anterior capsule opacification was present in 9 eyes. No central posterior capsule opacification or posterior capsule folds were observed in any eye. Soemmering’s ring formation was observed in 5 eyes. Zonular stretch caused by different degrees of capsular bag contraction was present in 4 eyes without decentration of the IOL. Conclusions: Analyses of pseudophakic cadaver eyes from the posterior (Miyake-Apple) view, complemented by microscopic analyses, proved useful in the evaluation of IOL–capsular bag interaction. These studies are more important in cases of newly introduced lens designs. J Cataract Refract Surg 2004; 30:1537–1544  2004 ASCRS and ESCRS

T

he 3-piece hydrophobic acrylic AcrySof威 posterior chamber intraocular lens (PC IOL) (Alcon Laboratories) is associated with low rates of postoperative capsule bag opacification in clinical and pathological studies (http://www.ophthalmic.hyperguides.com/tutorials/ cataract/pandey/default.asp).1–7 Some authors attribute this finding to the square-edged optic design of the lens8; others believe that the adhesive properties of the

Accepted for publication November 20, 2003. Reprint requests to Liliana Werner, MD, PhD, John A. Moran Eye Center, Department of Ophthalmology and Visual Sciences, University of Utah, 50 North Medical Drive, Salt Lake City, Utah 84132, USA. E-mail: [email protected].  2004 ASCRS and ESCRS Published by Elsevier Inc.

AcrySof material play an important role in preventing capsular bag opacification.9–13 The manufacturer developed a single-piece lens, all of AcrySof material, that has square optic and haptic edges. The first clinical experiences with this single-piece design have been reported. A study by Caporossi and coauthors14 evaluated aspects of the IOL such as surgical handling, haptic flexibility and resistance, stability in the capsular bag, and biocompatibility. In all cases, the IOL was easily folded, inserted, and unfolded. It remained well centered in the capsular bag, and there were no intraoperative or postoperative complications. Davison15 studied the clinical performance characteristics of models SA30AL and SA60AT of the single0886-3350/04/$–see front matter doi:10.1016/j.jcrs.2003.11.047

LABORATORY SCIENCE: PATHOLOGY OF SINGLE-PIECE HYDROPHOBIC ACRYLIC IOL

piece hydrophobic acrylic lens. He focused on sameday incision competence after implantation, A-constant validation, and optic centration with respect to pupil and capsule anatomy. Postoperatively, the presence of pseudophakic dysphotopsia and glistenings was evaluated. Davison reports that the single-piece hydrophobic acrylic lenses performed well in all aspects. Pseudophakic dysphotopsia occurred in only a few patients with these lenses. Lens exchange, when necessary, is recommended in the early postoperatively period because the adhesive properties of the AcrySof biomaterial make explantation increasingly difficult as time passes. In our center, we recently received the first 14 human eyes obtained postmortem from 10 patients with the new single-piece hydrophobic acrylic IOL design. Analyses of pseudophakic cadaver eyes from the posterior (Miyake-Apple) view, complemented by microscopic analyses, proved useful in evaluating the IOL–capsular bag interaction. The primary purpose of this study was to objectively document the findings of the single-piece hydrophobic acrylic IOL design in human eyes obtained postmortem. It focused on IOL fixation and centration, zonular stretch, anterior capsule opacification (ACO),16,17 posterior capsule opacification (PCO), and Soemmering’s ring formation (http://www.ophthalmic.hyperguides. com/tutorials/cataract/pandey/default.asp)5–7,18,19 according to methods established in our laboratory.

Materials and Methods The entire single-piece AcrySof PC IOL is of the same hydrophobic acrylic biomaterial with an incorporated ultraviolet absorber. The lens has an asymmetric biconvex optic; the refractive index of its material is 1.55. The haptics are modified L-loops. The memory and flexibility of the material allow the haptics to be bent back on themselves, twisted, and contorted to a much greater degree than the haptics of 3-piece lenses. The AcrySof model SA30AL has an optic diameter of 5.5 mm and a total length from haptic to haptic of 12.5 mm. Since January 1988, pseudophakic human eyes obtained postmortem have been submitted to our center in a random fashion from eye banks nationwide. Each eye was received in 10% neutral buffered formalin and was analyzed according to a standard technique established in our laboratory. When the human eyes were received from the eye bank, gross analyses were performed and results noted. Gross measurements of the anterior–posterior, horizontal, and vertical axes of the 1538

eyes, as well as inspection of the shape and size of the pupil, were initially performed. Each eye was then sectioned at the equator and the posterior segment inspected. Then, gross evaluation of the anterior segment from behind (Miyake-Apple view) revealed the presence of the single-piece hydrophobic acrylic lens. The relationship of the IOL to anatomical structures such as the capsular bag (eg, lens fixation, loop position, dimensions of the capsular bag in relation to the loop axis) was evaluated. The axis of PC IOL decentration (when present) was also noted. The IOL decentration at this axis was measured with calipers and expressed in millimeters according to the following formula: Decentration ⫽ y ⫺ x/2, where y and x are the largest and the smallest distance between the IOL optic edge and the inside margin of the ciliary body (ciliary ring), respectively. Posterior capsule opacification was graded in 3 locations (central optic, peripheral optic, and Soemmering’s ring) from 0 to 4 according to an established method using standard photographs.6 Soemmering’s ring formation was scored in each quadrant. The presence of zonular stretch, capsulo-zonularciliary scarring, capsule tears, or posterior capsulotomy (neodymium:YAG [Nd:YAG] laser or surgical) was also noted. The anterior segment of each eye was documented from a posterior or Miyake-Apple view, with photographs taken under an operating microscope (Leica/Wild MZ-8 Zoom Stereomicroscope, Vashaw Scientific, Inc.). The cornea and iris were then removed, and the ACO was graded from 0 to 4 from an anterior or surgeon’s view.17 Gross photographs were also taken under an operating microscope. After gross examination, all globes were sectioned in the pupillo-optic nerve plane, with the cuts oriented parallel to the IOL haptics. This secured the entire IOL in the entire capsular bag. After dehydration and embedding in paraffin, 15 to 20 serials, 3.0 mm thick sections were made from each eye. The sections from each eye were stained with hematoxylin–eosin, periodic acid-Schiff (PAS), and Masson’s trichrome for normal histological evaluation. The sections were examined under a light microscope (Olympus, Optical Co. Ltd.), and photomicrographs were taken for documentation. Anterior capsule fibrosis was scored from 0 to 3 according to the thickness of the fibrocellular tissue attached to the inner surface of the capsulorhexis margin.16 The amount of residual/ regenerative cortical material and cells at the equatorial region of the capsular bag (Soemmering’s ring) and at the level of the posterior capsule was also noted.

Results Table 1 summarizes the gross (macroscopic) findings in the 14 eyes. Gross examination from the Miyake-Apple posterior view revealed in-the-bag fixation (Figure 1, A and B) of all 14 single-piece AcrySof IOLs. Five AcrySof lenses had the loops oriented at the

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Table 1. Macroscopic findings. IOL Loop Position Eye Fixation (O’Clock)

Measured Decentration mm/Location

ACO PCO MA C/P

Soemmering’s Ring Zonular Stretch Grade/Quadrant

Grade/Quadrant

Capsule Tears Capsulo-Zonular-Ciliary Scarring Anterior/Posterior

1

B–B

3–9

—

0

—

1/1

—

—

–/–

2

B–B

10:30–4:30

—

1

—

1/2

1/2

—

–/–

3

B–B

3–9

—

0

—

—

—

—

–/–

4

B–B

3–9

—

1

—

—

—

—

–/–

5

B–B

10:30–4:30

0.26/9 o’clock

0

—

—

—

—

5 o’clock/–

6

B–B

2–8

—

1

—

—

1/4

—

–/–

7

B–B

6–12

—

1

—

—

—

—

–/–

8

B–B

3–9

—

1

—

1/1

—

—

–/–

9

B–B

4–10

—

1

—

—

—

—

–/–

10

B–B

6–12

—

0

—

—

1/4

—

–/–

11

B–B

2–8

—

0

—

1/1

—

—

–/–

12

B–B

1–7

—

1

—

—

—

—

–/–

13

B–B

3–9

—

1

—

—

—

—

–/–

14

B–B

2–8

—

1

—/1

2/4

2/1

—

–/–

ACO ⫽ anterior capsule opacification; B–B ⫽ bag–bag IOL fixation; C ⫽ central; MA ⫽ macroscopically; P ⫽ peripheral; PCO ⫽ posterior capsule opacification

3 to 9 o’clock meridian, 2 at 10:30 to 4:30, 2 at 6 to 12 o’clock, 3 at 2 to 8 o’clock, 1 at 1 to 7 o’clock, and 1 at 4 to 10 o’clock. There was no measured lens decentration in 13 eyes (Figure 1, A). In 1 eye, slight decentration of 0.26 mm was measured at the 9 o’clock position (Figure 1, C and D). Macroscopically, ACO was scored as grade 0 in 5 cases and grade 1 in 9 cases (Figure 2, A and B). No central PCO was observed in any of the 14 eyes. Grade 1 peripheral PCO was observed in 1 case. Soemmering’s ring formation was seen 5 eyes. Three eyes had grade 1 Soemmering’s ring in 1 quadrant, 1 had grade 1 in 2 quadrants, and 1 had grade 2 in all 4 quadrants. Capsule retraction and zonular stretch were absent in 10 eyes. Slight zonular stretch (grade 1) was present in 3 eyes. In 1 of them, zonular stretch was present in 2 quadrants. In 2 eyes, the stretch was present in all 4 quadrants because of capsular bag contraction (Figure 3 A and B). In the last eye, grade 2 zonular stretch was present in 1 quadrant (Figure 3, C). No capsulozonular-ciliary scarring was observed. The only anterior capsule tear observed (eye 5) did not extend toward the equator. It was located at 5 o’clock and was in the eye with IOL decentration (Figure 1, C and D). No posterior capsule tears were noted. No Nd:YAG laser capsulotomies had been performed in any eye analyzed.

Analysis of the posterior segment of the eyes showed 1 peripheral retinal tear at the 12 o’clock position in eye 1. External examination of the eye showed a 360degree scleral buckling element. Scars of laser treatment and cryopexy were seen at the retinal periphery and around the tear. The retina was attached. There was slight elevation of the retina in the macular area related to postmortem changes. The lens was in the bag, with the loops oriented at the 3 to 9 o’clock meridian. The PC IOL was not decentered. No central or peripheral PCO was observed. Grade 1 Soemmering’s ring was present in 1 quadrant. No capsulo-zonular-ciliary scarring or anterior or posterior capsule tears were noted. Scars after laser treatment were also observed in eye 9. In this case, the lens was also in the bag, with the loops oriented at the 4 to 10 o’clock meridian. The IOL was not decentered. No central or peripheral PCO or Soemmering’s ring was noted. No capsulo-zonular-ciliary scarring or anterior or posterior tears were observed. Histopathological evaluation of all 14 eyes confirmed gross (macroscopic) findings. All AcrySof IOLs were implanted in the capsular bag. Microscopic ACO (fibrosis) was grade 0 in 9 eyes and grade 2 in 5 eyes (Figure 4, A and B). In eyes with Soemmering’s ring formation, the barrier effect of the IOL’s square edge (Figure 4, C to F) had prevented migration of residual/

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Figure 1. (Izak) Gross photographs of human eyes obtained postmortem. A: Miyake-Apple posterior photographic technique shows inthe-bag fixation of a single-piece AcrySof IOL with no decentration. There is no PCO or Soemmering’s ring (eye 13). B: Anterior or surgeon’s view of the eye in A. Macroscopically, ACO grade 1 is observed. Miyake-Apple posterior view (C ) and anterior or surgeon’s view (D ) of the eye (eye 5) with lens decentration. The arrows show an anterior capsule tear. Central/peripheral PCO, Soemmering’s ring, and ACO are absent.

regenerative cortical material and lens epithelial cells (LECs) onto the central posterior capsule.

Discussion In the past, improvements in cataract surgery have focused on prevention and eventual eradication of PCO. This is especially important in pediatric eyes, for example, in which the rate of inflammatory response and PCO development after IOL implantation is higher than in adult eyes.20 Study of different forms of opacification of the capsular bag is important as new technology such as pseudoaccommodating IOLs becomes available.21,22 Capsular bag opacification/fibrosis may limit the longterm functioning of these lenses. Posterior capsule opacification has been extensively studied throughout the years in our laboratory. Six factors to reduce PCO were 1540

defined and divided into 2 groups: surgery-related and IOL-related (http://www.ophthalmic.hyperguides.com/ tutorials/cataract/pandey/default.asp). 5–7,18 Surgeryrelated factors are represented by (1) creation of a small continuous curvilinear capsulorhexis (CCC) with the edge on the anterior IOL surface, (2) hydrodissectionenhanced cortical cleanup, and (3) in-the-bag IOL fixation. In this study, all eyes had a CCC performed intraoperatively. Most cases had a CCC smaller than the IOL optic, covering its edge for 360 degrees. Regarding hydrodissection and enhanced cortical cleanup, we did not have means to obtain precise information on the surgical technique in each case. However, the small amount of Soemmering’s ring we observed suggests that the surgeons had performed careful intraoperative cortical cleanup. Creating a CCC in each case helped ensure precise in-the-bag IOL fixation. It is interesting

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Figure 2. (Izak) Gross photographs of human cadaver eyes from the anterior or surgeon’s view. A: Grade 0 ACO (eye 10). B: Grade 1 ACO (eye 2).

that although 1 eye presented with an anterior capsule tear, the mechanical characteristics of the single-piece hydrophobic acrylic design prevented its extension toward the equator. The lens remained fixated in the capsular bag and was only slightly decentered. This IOL design does not exert excess traction in the capsular bag. This was clearly observed in a laboratory study evaluating the capsulorhexis ovaling and stretch of the

capsular bag performed in postmortem human pediatric eyes after the implantation of various rigid and foldable IOLs.23 The single-piece hydrophobic acrylic lens was associated with significantly less capsulorhexis ovaling and capsular bag stretch. The 3 IOL-related factors that prevent PCO are (1) a design that ensures maximum lens optic–posterior capsule contact, (2) square/truncated optic edges, and

Figure 3. (Izak) Gross photographs of human eyes obtained postmortem from the Miyake-Apple posterior view. An overview (A ) and a detail (B ) of a case with capsule contraction (eye 6). C: Grade 2 zonular stretch in 1 quadrant (eye 14).

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Figure 4. (Izak) Photomicrographs of the anterior segment of human eyes obtained postmortem. Grade 0 ACO (A ) and grade 2 ACO (B ) were found in eyes 11 and 9, respectively (PAS stain, original magnification ⫻400). C to F: The barrier effect of the square edge can be observed in eye 7 (Masson’s trichrome stain, original magnification ⫻10 [C and D] and ⫻100 [E and F]).

(3) biocompatibility. The single-piece AcrySof IOL has a planer design; thus, there is no optic–haptic angulation. However, the square optic and haptic edges, in association with the adhesive properties of the biomaterial, probably compensate for the lack of such angulation. The role of the square optic edge as a barrier to LEC migration onto the posterior capsule, and thus 1542

PCO, was originally described with the 3-piece AcrySof IOL. The AcrySof lens was the first commercially available design to have square optic edges; today, other square-edged lenses are available including those made of other biomaterials.24 The PCO prevention effect of the square edge is mainly mechanical. This is an important second line of defense when surgery is not satisfac-

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tory, especially with regard to insufficient cortical cleanup. Hollick and coauthors25 studied and compared the biocompatibility of 3 IOL biomaterials. They found that AcrySof IOLs were associated with lower giant cell counts than poly(methyl methacrylate) (PMMA) and silicone IOLs. The authors believe this might play an important role in eyes with preexisting blood–aqueous barrier damage. Biocompatibility of an IOL can also be considered in relation to the clarity of the anterior and posterior capsules. The barrier effect of the square edge probably plays the most prominent role in preventing PCO. However, the lens edge would not influence the outcome of opacification (fibrosis) of the anterior capsule. Thus, the effect of IOL biomaterial being in contact with the inner surface of the anterior lens capsule is the most important factor. Studies of ACO performed by Werner et al.16,17 demonstrate that the anterior capsule in pseudophakic human eyes obtained postmortem implanted with 3-piece AcrySof lenses remained clearer than anterior capsules in eyes with silicone or PMMA lenses. Up to July 2001, our center accessioned 637 pseudophakic human eyes obtained postmortem that were implanted with the 3-piece AcrySof lens. Our analyses revealed 90% in-the-bag fixation of this design, good centration, and none or minimal decentration. The amount of ACO and central PCO was consistently lower that with other IOL designs available in the United States. Similar analyses performed after launching any new IOL design into the market help us understand the interaction between the design and ocular structures, such as the capsular bag, as well as its influence on the outcome of postoperative complications. However, studies of human eyes obtained postmortem are limited by difficulty in obtaining clinical and surgical information in all cases. In this present study, the first 14 human autopsy eyes implanted with a single-piece AcrySof lens submitted to our center between May 2001 and July 2002 were evaluated. Information on how long the IOLs were in the eyes was not available, but it is unlikely they were in place longer than 3 years. All the IOLs had symmetric in-the-bag fixation. There was minimal measured IOL decentration in only 1 eye, which had an anterior capsule tear that probably accounted for the slight decentration. One might hypothesize that

implantation of a 3-piece lens with rigid haptics, which in general causes different degrees of ovalization of the capsular bag along the loop fixation meridian, would have extended the radial tear. Even in the presence of these complications, no ACO or PCO was observed in this eye. Macroscopic grade 1 ACO was present in 9 eyes. No eye had central PCO or posterior capsule folds. Zonular stretch caused by different degrees of capsular bag contraction without decentration of the IOL was present in 4 eyes. In a rabbit model, Nishi and Nishi26 found that the bulky haptics of the single-piece AcrySof IOL hampered adhesion between the anterior and posterior capsules, and thus capsular bend formation. In a rabbit study performed in our laboratory, we noted that the square edge effect may be absent at the level of the optic–haptic junctions of single-piece lenses. Thus, PCO would be more likely to start at those sites.27 We did not observe central PCO in the 14 human cadaver eyes in the current study. The use of appropriate surgical techniques, combined with the mechanical and adhesives properties of this new IOL design, probably accounted for the good results we obtained. However, accession of a greater number of similar specimens in our laboratory, combined with long-term clinical studies of this IOL design, will confirm these preliminary results.

References 1. Hollick EJ, Spalton DJ, Ursell PG, et al. The effect of polymethylmethacrylate, silicone, and polyacrylic intraocular lenses on posterior capsular opacification 3 years after cataract surgery. Ophthalmology 1999; 106:49–54; discussion by RC Drews, 54–55 2. Casprini F, Tosi GM, Quercioli PP, Caporossi A. Comparison of AcrySof MA30BA and Sensar AR40 acrylic intraocular lenses. J Cataract Refract Surg 2002; 28: 1130–1134 3. Halpern MT, Covert D, Battista C, et al. Relationship of AcrySof acrylic and PhacoFlex silicone intraocular lenses to visual acuity and posterior capsule opacification. J Cataract Refract Surg 2002; 28:662–669 4. Ram J, Pandey SK, Apple DJ, et al. Effect of in-the-bag intraocular lens fixation on the prevention of posterior capsule opacification. J Cataract Refract Surg 2001; 27:1039–1046 5. Ram J, Apple DJ, Peng Q, et al. Update on fixation of rigid and foldable posterior chamber intraocular lenses. Part II: choosing the correct haptic fixation and intraocular lens design to help eradicate posterior capsule opacification. Ophthalmology 1999; 106:891–900

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6. Apple DJ, Peng Q, Visessook N, et al. Eradication of posterior capsule opacification; documentation of a marked decrease in Nd:YAG laser posterior capsulotomy rates noted in an analysis of 5416 pseudophakic human eyes obtained postmortem. Ophthalmology 2001; 108: 505–518 7. Werner L, Apple DJ, Pandey SK. Postoperative proliferation of anterior and equatorial lens epithelial cells. In: Buratto L, Werner L, Zanini M, Apple DJ, eds, Phacoemulsification: Principles and Techniques, 2nd ed. Thorofare, NJ, Slack, 2003; 603–623 8. Nishi O, Nishi K. Preventing posterior capsule opacification by creating a discontinuous sharp bend in the capsule. J Cataract Refract Surg 1999; 25:521–526 9. Nagata T, Minakata A, Watanabe I. Adhesiveness of AcrySof to a collagen film. J Cataract Refract Surg 1998; 24: 367–370 10. Oshika T, Nagata T, Ishii Y. Adhesion of lens capsule to intraocular lenses of polymethylmethacrylate, silicone, and acrylic foldable materials: an experimental study. Br J Ophthalmol 1998; 82:549–553 11. Linnola RJ. Sandwich theory: bioactivity-based explanation for posterior capsule opacification. J Cataract Refract Surg 1997; 23:1593–1542 12. Linnola RJ, Werner L, Pandey SK, et al. Adhesion of fibronectin, vitronectin, laminin, and collagen type IV to intraocular lens materials in pseudophakic human autopsy eyes. Part 1: histological sections. J Cataract Refract Surg 2000; 26:1792–1806 13. Linnola RJ, Werner L, Pandey SK, et al. Adhesion of fibronectin, vitronectin, laminin, and collagen type IV to intraocular lens materials in pseudophakic human autopsy eyes. Part 2: explanted intraocular lenses. J Cataract Refract Surg 2000; 26:1807–1818 14. Caporossi A, Casprini F, Tosi GM, Baiocchi S. Preliminary results of cataract extraction with implantation of a single-piece AcrySof intraocular lens. J Cataract Refract Surg 2002; 28:652–655 15. Davison JA. Clinical performance of Alcon SA30AL and SA60AT single-piece acrylic intraocular lenses. J Cataract Refract Surg 2002; 28:1112–1123 16. Werner L, Pandey SK, Escobar-Gomez M, et al. Anterior capsule opacification; a histopathological study comparing different IOL styles. Ophthalmology 2000; 107: 463–471 17. Werner L, Pandey SK, Apple DJ, et al. Anterior capsule opacification: correlation of pathologic findings with clinical sequelae. Ophthalmology 2001; 108:1675–1681 18. Apple DJ, Peng Q, Visessook N, et al. Surgical prevention of posterior capsule opacification. Part 1. Progress

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From the David J. Apple, MD Laboratories for Ophthalmic Devices Research, John A. Moran Eye Center, Department of Ophthalmology and Visual Sciences, University of Utah, Salt Lake City, Utah, USA. Presented in part at the annual meeting of American Academy of Ophthalmology, Orlando, Florida, USA, October 2002. Supported in part by an unrestricted grant from Research to Prevent Blindness, Inc., New York, New York, USA. None of the authors has a financial or proprietary interest in any material or method mentioned.

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