Introduction

As a treatment for end-stage renal disease, renal transplantation has been increasingly used in patients with chronic renal failure, improving patients’ survival chances. However, subsequent long-term use of glucocorticoids and immunosuppressants after renal transplantation significantly increases the incidence of drug-induced cataract (DIC), which seriously affects the visual function of kidney transplant recipients [1, 2]. Children are more susceptible to DIC than adults [3]. If left untreated, this may lead to deprivation amblyopia in children, resulting in lifelong disability. Many drugs, such as corticosteroids, phenothiazines, myotics, and cytostatics [4], can cause DIC. Among these, corticosteroids are the most common, accounting for approximately 14–16% of all cataracts [5]. Moreover, long-term use of immunosuppressants such as cyclosporine after renal transplantation can also cause lens opacity [1].

Phacoemulsification combined with intraocular lens (IOL) implantation is an effective means of treating cataracts. Because of its high efficacy, it has become the first choice for cataract surgery [6, 7]. Owing to the development of IOLs, cataract surgery has evolved from visual restoration surgery to refractive surgery [8]. Patients with post-transplantation tend to be young and have high standards for visual quality. However, only a small amount of literature has reported the different results and long-term postoperative complications after phacoemulsification combined with single-focus IOL implantation in these patients, while the literature on the implantation of multi-focus IOL is rarely reported [9, 10]. Therefore, owing to complex systemic conditions and the lack of reporting, we were conservative in the selection of IOL, all of which chose single-focus IOL. The aim of this study is to analyze the ocular characteristics and discuss the efficacy and postoperative complications of phacoemulsification combined with IOL implantation of renal transplant recipients in detail, intending to provide a reference for whether to consider the implantation of multi-focal IOL from the perspective of surgical effects and long-term complications.

Materials and methods

Patients

This retrospective cohort study enrolled patients after renal transplantation who underwent phacoemulsification and IOL implantation at the Ophthalmology Department of the First Affiliated Hospital of Sun Yat-sen University between July 2018 and September 2022 as the observation group, and age- and sex-matched control patients with senile cataracts during the same period as the control group. The primary diseases of the kidney transplant recipients included IgA nephropathy (five cases), nephrotic syndrome (three cases), chronic glomerulonephritis (three cases), hydronephrosis caused by urinary calculi (two cases), tubular interstitial nephritis (one case), hypertensive nephropathy (one case), and trauma (one case). When progressed to end-stage renal disease, defined as a glomerular filtration rate of less than 15 ml/min, kidney transplantation was considered the optimal treatment. Before phacoemulsification, it was ensured that patients in the observation group were in good general condition and that the control levels of serum creatinine and blood urea nitrogen were relatively normal. All patients had a minimum follow-up period of 6 months after surgery. Patients with a history of diabetes and long-term exposure to radioactive substances were excluded from the study. Further, patients with glaucoma, keratopathy, retinopathy, ocular trauma, or high astigmatism requiring a toric IOL were excluded. We also excluded patients who used high-end IOL or specialized IOL. The study was approved by the Ethics Committee of the First Affiliated Hospital of Sun Yat-sen University in China and complied with the tenets of the Declaration of Helsinki for Biomedical Research Involving Human Subjects. Written informed consent for publication was obtained from the patients after an explanation of the nature and possible consequences of the study.

The observation and control groups underwent phacoemulsification combined with IOL implantation under local anesthesia. All operations were performed by the same experienced surgeon. The diameter of the capsulorhexis should be strictly controlled during continuous curvilinear capsulorhexis operations. The lens nucleus was emulsified and removed using the Infiniti or Centurion (Alcon Laboratories, Fort Worth, TX, USA) phacoemulsifier, followed by irrigation/aspiration to remove the cortex. A 360-degree polish of the lower surface of the anterior capsule was performed using an irrigation/aspiration probe and the Fluid-jet technique was used to polish the posterior capsule [11]. Owing to the complex systemic conditions, we were conservative in the selection of IOLs. Moreover, based on patient preferences and our comprehensive evaluation of the patients, we chose a hydrophobic aspheric single-focus IOL (AcrySof SA60WF; Alcon, Geneva, Switzerland). The Barrett Universal II formula was used to calculate IOL placement parameters. All patients were followed up at 1 week, 1 month, and 6 months after operation.

Examinations

Ophthalmic examinations included best corrected visual acuity (BCVA) measurement, intraocular pressure (IOP) measurement, slit-lamp examination, fundus examination, corneal endothelial cell examination, optical biometry using the IOLMaster 700 (Carl Zeiss AG), optical coherence tomography (Heidelberg Engineering), and dry eye examination including tear film break-up time (BUT), Schirmer’s I test, and fluorescein staining.

Indicators of observation

Indicators, including BCVA, IOP, retinal nerve fiber layer (RNFL) thickness, corneal endothelial cell density, and ocular biometric parameters, were measured. Before surgery, lens opacity was evaluated using the cataract opacity grading system (LOCS III) [12] and classified as cortical, nuclear, or posterior subcapsular. During the postoperative follow-up, BCVA, dry eye condition, and postoperative complications (glaucoma, anterior chamber inflammation, corneal edema, anterior capsular opacification [ACO], posterior capsular opacification [PCO], capsular contraction, and cystoid macular edema) were observed.

Based on the area and degree of opacification of the capsule, we scored the ACO for each eye [13] and graded the PCO according to the visual examination combined with the views of Kucuksumer et al. [14]. The grading of ACO and PCO is shown in Table 1. Besides, images of the anterior segment after mydriasis 6 months after surgery were imported into ImageJ software to measure the area of the capsulorhexis area and evaluate capsular contraction.

Table 1 The grading of ACO and PCO
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Statistical analysis

SPSS software (v26.00; IBM Corp., Armonk, NY, USA) was used for statistical analysis. Normally distributed variable data were presented as mean ± standard deviation, non-normally distributed variable data were presented as median and interquartile range, and attribute data were presented as percentages. The t-test was used for normally distributed data, the Mann–Whitney U test was used for non-normally distributed or rank data, and the chi-square test was used for attribute data. Taking the incidence of PCO as the primary outcome measure, the sample size was calculated to be 52 cases using PASS software (v21.0.3; NCSS, LLC, Kaysville, Utah, USA). All parameters were compared for statistical significance (P < 0.05).

Results

We enrolled 25 eyes of 16 patients with cataracts after renal transplantation and 30 eyes of 21 control patients. The observation group included 19 eyes from 12 men and 6 eyes from 4 women. The patients’ average age was 47.5 ± 11.3 years, with ages ranging from 28 to 65 years. The control group included 18 eyes from 12 men and 12 eyes from 9 women. The patients’ average age was 53.1 ± 4.0 years, with ages ranging from 43 to 58 years. The observation group received allograft kidney transplantation for chronic renal failure between 2005 and 2021 with long-term maintenance administration of glucocorticoids and immunosuppressants, including prednisone 10–20 mg/day or methylprednisolone 4–16 mg/day, tacrolimus 2–7 mg/day or cyclosporine 200–300 mg/day, and mycophenolate mofetil 0.72–2 g/day. Medication was administered for 6–180 months, with the average duration being 55.5 ± 52.1 months.

Demographic and general ophthalmic examination

The observation and control groups were matched by age and sex. No statistically significant differences were observed in preoperative BCVA, preoperative IOP, preoperative or postoperative central corneal thickness (CCT); however, differences in RNFL thickness were statistically significant (P = 0.013). Table 2.

Table 2 Demographic and general ophthalmic examination
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The preoperative and postoperative corneal endothelial cell density of the observation group were higher than that of the control group (P = 0.001; P = 0.001, respectively). The differences between the preoperative and postoperative values were calculated to assess the loss of corneal endothelial cells. As shown in Table 2, there was no statistically significant difference in the reduction of corneal endothelial cells between the two groups (P > 0.05).

Type of cataract

The difference in type of lens opacity between the two groups was statistically significant (P = 0.002). The most common type of cataract after renal transplantation was posterior subcapsular, whereas cortical was the most common type in the control group. Table 3.

Table 3 The type of cataract
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Comparison of ocular biometric parameters

Statistically significant differences in △K, white-to-white, and keratometry values at the vertical axis (KV) were observed between the two groups (P < 0.05). Table 4.

Table 4 Comparison of ocular biometric parameters
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Postoperative BCVA

Compared with preoperative results, the BCVA of the renal transplantation and control groups significantly improved 1 week, 1 month, and 6 months after surgery (P < 0.05), whereas no statistically significant difference in BCVA was observed between the two groups at any time point (P > 0.05). Table 5.

Table 5 The postoperative BCVA between the 2 groups
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Postoperative dry eye and postoperative complications

No statistically significant differences in BUT, Schirmer’s I test, or incidence of dry eye were observed between the two groups during follow-up 6 months after surgery (P > 0.05). Regarding postoperative complications, the grade of ACO and PCO in the renal transplantation group were significantly lower than those in the control group (P = 0.048; P = 0.006, respectively). Figure 1 shows the anterior segment with typical ACO in our study, while Fig. 2 shows typical PCO.

Fig. 1
figure 1

Examples of typical anterior capsular opacification grading in this study. a Grade 0, b Grade I, c Grade II, d Grade III. (Grade IV was not observed in this study.)

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Fig. 2
figure 2

Examples of typical posterior capsular opacification grading in this study. a Grade 0, b Grade I, c Grade II, d Grade III. (Grade IV was not observed in this study.)

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In addition, the incidence of a requirement of neodymium-doped yttrium aluminum garnet (Nd: YAG) laser capsulotomy to restore the capsule transparent in the renal transplantation group was significantly lower than that in the control group (P = 0.032), and the capsulorhexis area was significantly smaller (P = 0.007). In addition, secondary glaucoma occurred in two eyes (8.0%) in the renal transplantation group; no other postoperative complications, such as corneal edema, macular cystoid edema, or IOL deviation, were observed in either group. No severe anterior chamber inflammatory reactions occurred after phacoemulsification, and no special treatment such as intravenous steroid anti-inflammatory therapy or subconjunctival injection of anti-inflammatory drugs was administered. Table 6.

Table 6 Comparison of postoperative dry eye and postoperative complications
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Discussion

Cataracts are one of the most common blinding eye diseases and greatly impact vision. Factors affecting the metabolic environment in the eye, as well as systemic diseases, can cause turbidity of the lens and lead to cataracts [8, 15]. After renal transplantation, long-term use of multiple systemic drugs, especially glucocorticoids and immunosuppressants, can lead to an increased incidence of cataracts (20–45%) [16,17,18]. Currently, some studies have discussed the results of cataract surgery in patients with renal transplantation, but the surgical efficacy and postoperative long-term complications have not been comprehensively discussed [9, 10, 19, 20]. Therefore, we intended to conduct a complete study on the ocular clinical features, long-term vision prognosis, and postoperative complications of these patients. Compared with previous reports, our study found that the degree of ACO and PCO, as well as the incidence of Nd: YAG laser capsulotomy were lower in cataract patients after kidney transplantation.

In contrast to other published studies on cataracts after renal transplantation, we conducted a more detailed study on the postoperative complications of phacoemulsification in patients after renal transplantation. When patients were followed up for 6 months to 3 years after phacoemulsification, we found significantly lower degrees of ACO and PCO in the renal transplantation group and a low probability of a requirement of Nd: YAG laser capsulotomy to restore the capsule transparent (4%), suggesting that residual lens epithelial cells in the renal transplantation group were less likely to proliferate, migrate, or differentiate after phacoemulsification combined with IOL implantation [21], which we suspected was affected by the use of glucocorticoids and immunosuppressants. There have been relevant studies on the effects of glucocorticoids on the proliferation of lens epithelial cells. Jin Yao et al. stated that glucocorticoids can inhibit TGF-β2-induced migration of human lens epithelial cells [22], and P J McDonnell et al. found that a group of drugs, including glucocorticoids, had the ability to inhibit the proliferation and migration of lens epithelial cells in vitro which could be used to prevent the formation and development of PCO [23]. It is well known that glucocorticoids promote the formation of posterior subcapsular cataracts, however, the occurrence of PCO after cataract surgery is a complex process. The use of glucocorticoids can reduce postoperative intraocular inflammation which can clinically reduce the degree of PCO [24]. In addition to the effects of glucocorticoids, several immunosuppressants, including cyclosporin A, have also been proven to inhibit the proliferation and differentiation of lens epithelial cells, thereby reducing the organization and turbidity of the capsule [25, 26].

The results showed that the preoperative and postoperative corneal endothelial cell counts in the renal transplant group were higher than those in the control group, but there was no significant difference in the reduction of corneal endothelial cells between the two groups. Therefore, we can speculate that phacoemulsification will not cause excessive damage to corneal endothelial cells in renal transplant patients and will not bring additional burden to corneal endothelial cells. For types of lens opacities, statistically significant differences were observed between the two groups. Consistent with previous studies, the predominant type of cataract caused by long-term use of glucocorticoids and immunosuppressants after transplantation was posterior subcapsular [10, 16, 27]. Additionally, differences in ocular biological parameters between the two groups were compared using the IOLMaster 700. The transverse diameter of the cornea in renal transplantation patients in this group may be smaller, and the KV may be larger. The difference in ocular biological parameters between the two groups may also be related to the small sample size. The results showed that other ocular biological parameters in patients with cataracts after renal transplantation were not significantly different from those in the control group.

As in previous studies [10], patients after renal transplantation showed a significant improvement in BCVA at each time point after phacoemulsification compared with that before surgery. Moreover, the visual prognosis of patients with cataracts after kidney transplantation did not differ from that of control patients. Therefore, phacoemulsification combined with IOL implantation was suspected to be effective in these patients.

The results showed a mild degree of ACO in patients following renal transplantation, while the postoperative capsulorhexis area of the observation group was significantly smaller than that of the control group. We suspect that although we performed standardized procedures in phacoemulsification and strictly controlled the capsulorhexis diameter to 5.5 mm, the capsulorhexis method that we used was artificial continuous circular capsulorhexis, which would inevitably produce errors and thus affect the area of the capsulorhexis after surgery. In our future studies, we will use femtosecond laser-assisted capsulotomy to ensure the consistency of the area of the capsulorhexis during the operation, so that the postoperative capsulorhexis area is no longer affected by the size of the capsulorhexis during phacoemulsification.

The preoperative and postoperative RNFL of patients in the renal transplantation group was thinner than that in the control group, though all values were within the normal reference range [28]. One patient had increased IOP in both eyes after phacoemulsification but did not present before surgery. This complication was caused by an imbalance between the generation and discharge of atrial water at the trabecular mesh in patients who used hormones for a long time [29]. This patient had increased IOP at the 6-month follow-up after surgery; we believe that this was not related to surgery, but rather to the increased resistance to outflow of the aqueous humor caused by long-term use of glucocorticoids [30]. Through the timely intervention of IOP, the patient’s visual function was not seriously damaged. In addition, no corneal or macular cystoid edema was observed. No severe anterior chamber inflammatory reactions after phacoemulsification occurred in either group, and no special treatment such as intravenous steroid anti-inflammatory therapy or continuous subconjunctival injection of anti-inflammatory drugs was administered. Therefore, we believe that phacoemulsification combined with IOL implantation is generally safe for patients following renal transplantation.

For patients with post-transplantation, we primarily chose to implant a single-focal IOL with a single function but definite efficacy. This was because of the general instability of their general condition, as well as the lack of literature reports on postoperative efficacy and long-term complications of this procedure in these patients. However, patients receiving these implants are usually young and have high visual quality requirements; therefore, an increasing number of patients prefer multi-focal IOL. Our study confirmed that phacoemulsification combined with IOL implantation is generally safe and effective in patients with cataracts after renal transplantation under the premise of proper IOP management. The incidence of complications, such as postoperative capsular organization, turbidity, and the incidence of Nd: YAG laser capsulotomy, is greatly reduced. Moreover, severe IOL deviations are rare in these patients after phacoemulsification, which avoids adverse visual experiences such as glare caused by the projection of multi-focal lens diffraction rings when external light enters the eye [31, 32]. However, the influence of hormonal drugs on the occurrence of glaucoma should be considered, and regular follow-ups are required to monitor IOP after surgery.

This study inevitably has some limitations. Owing to the capsulorhexis method we used being artificial continuous circular capsulorhexis, there will be some errors. In our future studies, we will use femtosecond laser-assisted capsulotomy to ensure the consistency of the capsulorhexis area during the operation, so that the postoperative capsulorhexis area can more accurately reflect the postoperative capsular organization and contraction. Besides, we will further conduct prospective studies to collect baseline data on the dry eye before surgery to better analyze the postoperative dry eye conditions of the two groups.

In conclusion, the type of lens opacity in patients after renal transplantation was mostly posterior subcapsular. Postoperative visual acuity recovered well, and the incidence of postoperative complications such as capsular opacification and the incidence of a requirement of Nd: YAG laser capsulotomy was lower. Our study suggests that phacoemulsification combined with IOL implantation is safe and effective, and that patients with cataracts after renal transplantation can be considered for implantation of multi-focal IOL under the condition of regular postoperative follow-up. This provides a reference for clinicians on IOL selection for similar patients.