A research critique demonstrates your ability to critically read an investigative study.? For this assignment, choose a research

RESEARCH ARTICLE

Macular pigment changes after cataract

surgery with yellow-tinted intraocular lens

implantation

Akira ObanaID 1,2☯*, Yuko Gohto1☯, Ryo Asaoka1☯

1 Department of Ophthalmology, Seirei Hamamatsu General Hospital, Hamamatsu, Shizuoka, Japan,

2 Photochemical Medicine Department, Photon Medical Research Center, Hamamatsu University School of

Medicine, Hamamatsu, Shizuoka, Japan

☯ These authors contributed equally to this work. * [email protected]

Abstract

Purpose

We previously reported that macular pigment optical density (MPOD) levels decreased dur-

ing a long follow-up period after clear intraocular lens (IOL) implant surgery presumably due

to excessive light exposure. We examined changes in MPOD levels in the eyes that

received yellow-tinted IOL implant surgery.

Subjects and methods

This was a prospective, observational study. Fifty-five eyes of 35 patients were studied.

MPOD levels were measured with a dual-wavelength autofluorescence technique on day 4;

months 1, 3, and 6; and years 1 and 2 postoperatively. The average optical densities at 0˚-

2˚ eccentricities (local MPODs) and total volumes of MPOD (MPOVs) in the area within 1.5˚

and 9˚ eccentricities were analyzed.

Results

The mean local MPOD at baseline (on day 4) was 0.79 at 0˚, 0.71 at 0.5˚, 0.68 at 0.9˚, and

0.32 at 2˚. The mean MPOV within 1.5˚ and 9˚ at baseline was 2950 and 18,897, respec-

tively. Local MPOD at 0.9˚ and 2˚ and MPOVs were slightly decreased at month 1 and

increased after that. The increase reached statistical significance in local MPOD at 0.5˚ and

2˚ and MPOVs (Tukey–Kramer test). The changes in MPOV within 9˚ at year 2 [(MPOV on

year 2 − MPOV on day 4) / MPOV on day 4] were from −0.21 to 1.18 (mean and standard deviation: 1.14 ± 0.28). The MPOV of 15 eyes increased more than 10% from the initial value, was maintained within 10% in 21 eyes, and deteriorated more than 10% in only 3

eyes.

Conclusions

Local MPOD and MPOV tended to slightly decrease month 1 postoperatively and gradually

increased after that, but the rates of increases in MPOD levels were small. Yellow-tinted

PLOS ONE

PLOS ONE | https://doi.org/10.1371/journal.pone.0248506 March 25, 2021 1 / 12

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OPEN ACCESS

Citation: Obana A, Gohto Y, Asaoka R (2021)

Macular pigment changes after cataract surgery

with yellow-tinted intraocular lens implantation.

PLoS ONE 16(3): e0248506. https://doi.org/

10.1371/journal.pone.0248506

Editor: Alfred S. Lewin, University of Florida,

UNITED STATES

Received: December 17, 2020

Accepted: February 26, 2021

Published: March 25, 2021

Peer Review History: PLOS recognizes the

benefits of transparency in the peer review

process; therefore, we enable the publication of

all of the content of peer review and author

responses alongside final, published articles. The

editorial history of this article is available here:

https://doi.org/10.1371/journal.pone.0248506

Copyright: © 2021 Obana et al. This is an open access article distributed under the terms of the

Creative Commons Attribution License, which

permits unrestricted use, distribution, and

reproduction in any medium, provided the original

author and source are credited.

Data Availability Statement: All relevant data are

within the paper and its Supporting Information

files.

Funding: The authors received no specific funding

for this work.

IOLs that have a lower transmittance of blue light might be preferable for preserving MPOD

levels after surgery.

Introduction

Visible light (wavelength: approximately 380 to 760 nm) has the potential of inducing retinal

damage [1, 2]. Especially blue light, with wavelengths ranging from 380 to 500 nm, has a high

potential to induce retinal damage because of its higher energy per photon than longer wave-

length lights. In the retina, blue light is absorbed by lipofuscin in the retinal pigment epithelial

(RPE) layer, rhodopsin in the photoreceptor layer, and other chromophores [3–5] and singlet

oxygen and other radical species that damage the RPE and photoreceptors are produced [6].

These photochemical or photooxidative light–tissue reactions occur with low and sustained

irradiation under the threshold value that induces thermal changes [1, 3, 7]. This situation is

called blue light hazard. Acute damage to the retina by accidentally gazing at sun light, arc

welding light, laser light from medical and industrial equipment, and light emission diodes

used in toys has been reported [8–22]. However, the harmfulness of chronic exposure to blue

light of certain wavelengths is still controversial [23–26]. Accumulative photooxidative stress

by blue light theoretically induces chronic changes in the retina, and photooxidative stress is

presumed to be one of the origins of retinal disorders, such as age-related macular degenera-

tion (AMD) [27].

The human crystalline lens becomes yellowish to brown with aging and potentially blocks

harmful blue light [3, 28–30] (Fig 1A). Removal of the crystalline lens by cataract surgery

enhances blue light exposure to the retina (Fig 1B), and this higher level of exposure may have

the potential to progress AMD via increased photooxidative stress [27, 31]. The effects of cata-

ract surgery, however, on AMD development has not been determined because of insufficient

data [32]. On the other hand, the retina has macular pigment (MP) consisting of three caroten-

oids, that is, lutein [(3R,30R,60R)-lutein], zeaxanthin [(3R,30R)-zeaxanthin], and meso-zeaxan- thin [(3R,30S; meso)-zeaxanthin] [33, 34]. The maximum absorption wavelength of MP is 460 nm [35] and MP acts as a filter by absorbing blue light (Fig 1B). It potentially protects against

light-induced oxidative damage in the retina by quenching oxygen radicals [36–38]. Thus, the

Fig 1. A. Transmission of human crystalline lens with age ranged 10 to 70 years old. The data is a personal gift from

Okuno T. Transmission shows a monotonous decrease in blue range with age. B. Transmission curves of +20 diopter

clear intraocular lens (IOL, SA60AT, Alcon Inc.) and yellow-tinted intraocular lenses (SN60AT). Yellow-tinted IOL

blocks blue light. Dotted line indicates the maximum absorption wavelength of macular pigment (460 nm). The data is

a personal gift from Tanito M.

https://doi.org/10.1371/journal.pone.0248506.g001

PLOS ONE Macular pigment changes in eyes with yellow-tinted intraocular lens implants

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Competing interests: The authors have declared

that no competing interests exist.

MP is an important internal defense system in the retina. We previously investigated the

changes in MP in eyes that received cataract surgery with intraocular lens (IOL) implantation.

The results showed that MP levels in the eyes implanted with a clear IOL deteriorated 1 and 2

years after surgery, whereas MP levels in the eyes with a yellow-tinted IOL implantation had

no change. The mechanisms underlying the deterioration of the MP in eyes with a clear IOL

are unknown, but we speculated that a high transmission rate of short wavelength components

with a clear IOL might induce higher exposure of blue light to the MP and cause high con-

sumption of MP carotenoids [39] (Fig 1B). We considered that a yellow-tinted IOL has advan-

tages in preserving the MP. While in contrast, Nolan et al. reported increased MP optical

density (MPOD) levels in the eyes with yellow-tinted IOL implants and unchanged MPOD

levels in the eyes with clear IOLs [40]. Therefore, the changes in MP in the eyes that received

IOL implants are still controversial. In our previous study, we used resonance Raman spectros-

copy (RRS) to measure MP levels, and Nolan et al. used heterochromatic flicker photometry.

RRS is a highly specific method that can measure MPOD levels because this method directly

measures the Raman signal from the MP that is specific to carotenoids. However, RRS allows

counting the total Raman signals from the MP within a diameter of 1 mm of the central fovea.

Actually, the MP was distributed more widely in the macular region, and the importance of

measuring the total amount of MP at the macular region is proposed to investigate the protec-

tive effects of MP [41]. Heterochromatic flicker photometry has been widely used for the inves-

tigation of MP for a long time, but its subjective nature needs subjective cooperation and may

induce some bias. Heterochromatic flicker photometry also measures the MP at limited lesions

of the retina. In contrast, a dual-wavelength autofluorescent technique is an objective tech-

nique. With this technique, not only MPOD at any location of the macular area but also a total

volume of MPOD in the area within any eccentricity can be obtained. A module on the Heidel-

berg SPECTRALIS with MultiColor (Spectralis-MP, Heidelberg Engineering Inc.) equipped

with a dual-wavelength (486 and 518 nm) autofluorescent technique was developed recently,

and the reliability of this device was validated [41–43].

In this study, we measured MPOD levels in eyes implanted with yellow-tinted IOLs 4 days

to 2 years after surgery using the dual-wavelength autofluorescence technique to verify our

previous results.

Subjects and methods

Fifty-five eyes of 35 patients (18 men and 17 women) who underwent cataract surgery at Seirei

Hamamatsu General Hospital between September 2016 and September 2018 were included in

the study (Table 1). Patient ages ranged from 41 to 86 years, and the mean and standard

Table 1. Demographics of the patients.

Male Female

patients 18 17

eyes 27 28

Age range (years) 56–86 41–85

Mean age (SD) (years) 69.0 (8.4) 71.1 (10.3)

No. of eyes implanted the following IOLs

SN60WF 14 19

XY1 9 7

YP2.2 2 2

PCB00V 2 0

SD, standard deviation; IOL, intraocular lens

https://doi.org/10.1371/journal.pone.0248506.t001

PLOS ONE Macular pigment changes in eyes with yellow-tinted intraocular lens implants

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deviation was 71.2 ± 9.6 years. All surgeries were performed by three experienced surgeons (AO, YG, and HS) using the same phaco instrument (Infinity, Alcon Inc.) and operating

microscope (OPMI Visu210/S88, Carl Zeiss, Oberkochen, Germany). The operating technique

was the same reported in the previous study. IOLs were implanted in the capsuler bag in all

eyes. The products of IOLs that were implanted were SN60WF (Alcon Inc., Fig 1B) in 33 eyes,

XY1 (HOYA Corporation) in 16 eyes, YP2.2 (Kowa Company, LtD) in 4 eyes, and PCB00V

(AMO Japan K.K) in 2 eyes. All eyes were free of disorders that could have affected the MPOD

measurements, including corneal and vitreal opacities, and retinal disorders such as vein

occlusion, multiple drusen, and pigment abnormalities in the macula. There was no severe

inflammation postoperatively.

MPOD levels were measured with a SPECTRALIS OCT with MultiColor equipped with a

dual-wavelength autofluorescence technique. The actual measurement was performed in the

same manner as described in previous studies [44–46]. The reference plateau for assumed

absence of MP was set at 9˚ eccentricity. The measurements were performed in eyes under

mydriasis induced by 2.5% phenylephrine hydrochloride and 1% tropicamide. The average

optical densities at 0˚, 0.5˚, 0.9˚, and 2˚ eccentricities (local MPODs) and total MPOD volumes

(MPOVs) in the area within 1.5˚ and 9˚ eccentricities were analyzed. The RRS technique

obtained total Raman counts in the central area with a 1-mm diameter. In order to adjust the

RRS measurement, MPOVs in the area of 1.5˚ were analyzed. Patients were examined on day

4; months 1, 3, and 6; and years 1 and 2, postoperatively. Patients underwent usual ophthalmo-

logical examinations including visual acuity testing and measurement of intraocular pressure

at every time point. Posterior capsule opacification was evaluated with slit-lamp biomicro-

scopy, and no eyes had clinically relevant opacification that could have caused loss of visual

acuity and light transmission for MPOD measurements. It was confirmed verbally that no

patients started to take supplements containing lutein and/or zeaxanthin after surgery.

These prospective case series were approved by the institutional review board of Seirei

Hamamatsu General Hospital (IRB No. 2199). The protocol followed the tenets of the Declara-

tion of Helsinki. All patients provided written informed consent at enrollment.

Statistical analysis

The values of local MPODs at 0˚, 0.5˚, 0.9˚, and 2˚ eccentricities and MPOVs in the areas

within 1.5˚ and 9˚ eccentricities were compared at day 4; months 1, 3, and 6; and years 1 and

2, using a linear mixed model with patients as a random effect (because one or two eyes of a

patient were included) and the Tukey–Kramer test, which considered multiple comparisons.

The linear mixed model is equivalent to an ordinary linear regression in that the model

describes the relationship between the predictor variables and a single outcome variable. How-

ever, standard linear regression analysis rests on the assumption that all observations are inde-

pendent of each other. In the current study, measurements were nested within subjects and

hence were dependent on each other. Ignoring this grouping of the measurements will result

in underestimation of the standard errors of regression coefficients. The linear mixed model

adjusts for the hierarchical structure of the data, modeling in such a way that measurements

are grouped within subjects to reduce the possible bias derived from the nested structure of the

data [47, 48]. Subsequently, these analyses were iterated using only eyes that were subjected to

measurements both at day 4 and year 1 and day 4 and year 2.

In addition, the change rate of MPOV within 9˚ on year 2 was calculated as (MPOV on

year 2 − MPOV on day 4) / MPOV on day 4. The change rates were compared between SN60WF and XY1 using a non-paired t-test.

PLOS ONE Macular pigment changes in eyes with yellow-tinted intraocular lens implants

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All statistical analyses were performed using the statistical programming language R (ver.

3.6.1, The R Foundation for Statistical Computing, Vienna, Austria); StatView, version 5.0;

SAS statistical software (Cary, NC); and Statistical Package for Service Solution (SPSS) soft-

ware, version 26 (IBM SPSS, Chicago, IL); p < 0.05 was considered significant.

Results

The MPOD levels were measured in all eyes on day 4 postoperatively, which was defined as the

baseline value of MPOD levels in each eye. Some eyes failed to receive MPOD measurements

at some time points, and the number of eyes that received MPOD measurements was 49 at

month 1, 51 at month 3, 47 at month 6, 48 at year 1, and 39 at year 2. Local MPOD levels at

four eccentricities and MPOV within two eccentricities for all time points are shown in

Table 2. The differences in local MPOD levels and MPOV between day 4 and year 1, postoper-

atively, were analyzed statistically in 48 eyes of 29 subjects who received MPOD measurements

at year 1 (Table 3). Local MPOD levels increased significantly at year 1 at 0˚, 0.5˚, and 2˚

eccentricities and MPOV within 1.5˚ and 9˚ eccentricities increased significantly at year 1. The

differences in local MPOD levels and MPOV between day 4 and year 2 postoperatively were

also statistically analyzed in 39 eyes of 23 subjects who received MPOD measurements at year

2 (Table 4). A significant increase was observed in local MPOD at 0.5˚ and 2˚ and MPOV

within 1.5˚ and 9˚ eccentricities.

MPOD levels were measured at all time points during a postoperative follow-up period of 2

years in 35 eyes of 22 subjects. Fig 2 shows changes in the mean local MPOD levels in these

eyes. There were no significant changes in local MPOD at 0˚ and 0.5˚ between any two time

points. The local MPOD at 0.9˚ at month 1 was lower than that at day 4, month 6, and years 1

and 2. Local MPOD at 2˚ at month 1 was lower than that at day 4, month 6, and years 1 and 2,

and the differences between month 1 and month 6, year 1, and year 2 were significant. Local

MPOD at 2˚ at year 1 was significantly higher than that at day 4 (Tukey–Kramer test). Figs 3

and 4 show changes in MPOV within 1.5˚ and 9˚, respectively. MPOV within 1.5˚ at year 2

Table 2. Local MPOD levels and MPOV at four eccentricities at all time points.

Day 4 Month 1 Month 3 Month 6 Year 1 Year 2

0˚ Range 0.37–1.39 0.31–1.38 0.44–1.30 0.44–1.48 0.39–1.26 0.45–1.33

Mean (SD) 0.79

(0.21)

0.82

(0.24)

0.82

(0.21)

0.82

(0.23)

0.82

(0.21)

0.80

(0.22)

0.5˚ Range 0.21–1.12 0.25–1.24 0.21–1.21 0.27–1.24 0.24–1.27 0.32–1.24

Mean (SD) 0.71

(0.22)

0.72

(0.22)

0.72

(0.22)

0.72

(0.21)

0.72

(0.22)

0.72

(0.21)

0.9˚ Range 0.21–1.12 0.22–1.05 0.21–1.04 0.25–1.05 0.24–1.05 0.34–1.04

Mean (SD) 0.68

(0.22)

0.66

(0.21)

0.67

(0.21)

0.68

(0.21)

0.69

(0.21)

0.67

(0.20)

2˚ Range 0.06–0.74 0.08–0.68 0.06–0.71 0.09–0.71 0.08–0.72 0.12–0.68

Mean (SD) 0.32

(0.17)

0.33

(0.17)

0.33

(0.17)

0.33

(0.17)

0.34

(0.17)

0.31

(0.14)

MPOV within 1.5˚ Range 846–5352 977–5073 846–5051 1084–4992 1013–5014 1397–4950

Mean (SD) 2950

(1003)

2960

(1010)

2988

(981)

2996

(981)

3042

(1005)

2951

(917)

MPOV within 9˚ Range 4948–42810 4842–71142 4948–41430 5886–42042 7026–42980 7118–37789

Mean (SD) 18,897

(9294)

19,800

(11,724)

19,168

(9300)

19,447

(9340)

19,707

(9374)

17,886

(7628)

SD, standard deviation

https://doi.org/10.1371/journal.pone.0248506.t002

PLOS ONE Macular pigment changes in eyes with yellow-tinted intraocular lens implants

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was significantly higher than that at day 4 and months 1 and 3. MPOV within 1.5˚ at month 1

was significantly lower than that at month 3, year 1 and 2. MPOV within 9˚ at year 1 was sig-

nificantly higher than that at day 4. MPOV within 9˚ at month 1 was significantly lower than

that at month 6, and year 1 and 2. (Tukey–Kramer test).

The change rate of MPOV within 9˚ at year 2 was from −0.21 to 1.18. The mean change rate and standard deviation was 1.14 ± 0.28. We divided change rates into three categories: +1.1 and more, lower than +1.1 and higher than −1.1, and −1.1 and lower. Fifteen eyes had an increased MPOV of >10% from the initial value. The change rates of 21 eyes were within 10%,

and only three eyes had a deteriorated MPOV of more than 10%. The mean change rates of

each IOL product were 0.09 ± 0.02 with SN60WF, 0.23 ± 0.18 with XY1, 0.08 with YP2.2, and −0.04 with PCB00V. There was no significant difference in the mean change rates between SN60WF and XY1 (p = 0.478, non-paired t-test). Statistical analyses were not performed in YP2.2 and PCB00V because of the small number of eyes that were implanted.

Discussion

The present results showed that MPOD levels in the yellow-tinted IOL-implanted eyes tended

to be slightly decreased at month 1 postoperatively and gradually increased after that. The

increase in local MPOD reached statistical significance at 0˚, 0.5˚, and 2˚ at year 1 (Table 3)

and at 0.5˚ and 2˚ at year 2 (Table 4). MPOV within 1.5˚ and 9˚ also increased significantly at

years 1 and 2 (Tables 3 and 4). Twenty-five eyes (64% of the eyes measured MPOD at year 2)

showed higher MPOVs within 9˚ at year 2 than those at day 4, and among them, 15 eyes (38%)

increased the MPOV >10%, whereas only 3 eyes had a deteriorated MPOV of more than 10%.

Table 3. Comparison of MPOD levels between day 4 and year 1 postoperatively.

Day 4 Year 1

Mean Standard deviation Range Mean Standard deviation Range P value Local MPOD

0˚ 0.77 0.21 0.37–1.39 0.82 0.21 0.39–1.26 0.0104

0.5˚ 0.70 0.22 0.21–1.19 0.72 0.22 0.24–1.27 0.0252

0.9˚ 0.67 0.22 0.21–1.12 0.69 0.21 0.24–1.05 0.0924

2˚ 0.32 0.17 0.06–0.74 0.34 0.17 0.08–0.72 0.0029

MPOV within 1.5˚ 2936 1012 846–5352 3042 1005 1014–5014 0.0045

MPOV within 9˚ 18,767 9591 4948–42,810 19,707 9374 7026–42,980 0.0036

Significant values were shown in bold.

https://doi.org/10.1371/journal.pone.0248506.t003

Table 4. Comparison of MPOD levels between day 4 and year 2 postoperatively.

Day 4 Year 2

Mean Standard deviation Range Mean Standard deviation Range P value Local MPOD

0˚ 0.77 0.21 0.37–1.39 0.80 0.22 0.45–1.33 0.313

0.5˚ 0.69 0.22 0.21–1.19 0.72 0.21 0.32–1.24 0.0204

0.9˚ 0.65 0.21 0.21–1.12 0.67 0.20 0.34–1.04 0.135

2˚ 0.29 0.15 0.06–0.74 0.31 0.14 0.12–0.68 0.0188

MPOV within 1.5˚ 2817 973 846–5352 2951 917 1392–4950 0.0086

MPOV within 9˚ 16,991 8504 4948–40,224 17,886 7628 7118–37,789 0.0408

Significant values were shown in bold.

https://doi.org/10.1371/journal.pone.0248506.t004

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Nolan et al. measured MPOD at four eccentricities, i.e., 0.25˚, 0.5˚, 1˚, and 1.75˚, with

flicker photometry at 12 months after surgery in 11 eyes with yellow-tinted IOLs. They con-

firmed the increase in local MPOD levels at 0.25˚ and 0.5˚. The increase in MPOD levels at 1˚

and 1.75˚ did not reach a significant level, but the mean MPOD of these four eccentricities

increased significantly at months 3, 6, and 12. They speculated that the mechanisms for the

increased MPOD were as follows: yellow-tinted IOLs have a lower transmission in the blue

light region than clear IOLs, but the transmission was still higher than that in the human lenses

of elderly people (Fig 1), and the increased visible light irradiation of the retina after cataract

surgery could stimulate enhanced retinal capture of circulating lutein and zeaxanthin, perhaps

due to a mechanism involving increased isomerization of the MP constituents under light

exposure [7]. Because the living human body generally has an autoregulatory system, it seems

reasonable that the increase in MPOD can prevent retinal damage caused by increased short

wavelength visible light intensities and correspondingly higher oxidative stress.

Fig 2. A change in the mean local macular pigment optical density (MPOD) levels in the eyes that had all

measurement data during a postoperative follow-up period of 2 years (35 eyes of 22 subjects). Asterisks indicate a

significant difference (p < 0.05) in local MPOD levels between two time points.

https://doi.org/10.1371/journal.pone.0248506.g002

Fig 3. A change in macular pigment optical density volume (MPOV) within 1.5˚ eccentricity in the eyes that had

all measurement data during a postoperative follow-up period of 2 years (35 eyes of 22 subjects). Asterisks indicate

a significant difference (p < 0.05) in MPOV between two time points.

https://doi.org/10.1371/journal.pone.0248506.g003

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The present results also showed increases in MPOD levels after surgery at some eccentrici-

ties and MPOV, but the increased rates were quite different from those reported in a study by

Nolan et al. In the study by Nolan et al., the increased value of MPOD was 0.16 at 0.25˚ and

0.123 at 0.5˚. The initial MPOD levels at 0.25˚ on week 1 ranged from 0.07 to 0.52 (mean ± SD, 0.28 ± 0.17), and then the increased rate in the mean MPOD at 0.25˚ was 57%. In the present study, the increased rates at year 1 were 6% at 0˚ and 3% at 0.5˚. One possible reason for the

difference in change rates is the different levels of the initial MPOD. Our initial MPOD levels

were high (0.77 at 0˚ and 0.7 at 0.5˚) compared with those of Nolan’s study (0.28 at 0.25˚).

Optical density of 0.7 represents a transmission rate of 17%, wherea

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