Indications for penetrating keratoplasty in a tertiary referral centre in ...

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Indications for penetrating keratoplasty in a tertiary referral centre in Canada, 1996–2004 Stephen J. Dorrepaal, MD; Kathy Y. Cao, MD; Allan R. Slomovic, MA, MD, FRCSC ABSTRACT • RÉSUMÉ

Background: The leading indications for penetrating keratoplasty (PKP) have changed over recent years. This study examined the leading indications for PKP and their trends, comparing these with recently published data from other studies, including a report from our centre examining indications from 1986 through 1995. Methods: A retrospective chart review was conducted of all patients who underwent PKP in a single practice at the University Health Network,Toronto Western Hospital, between July 1, 1996, and June 30, 2004. Results: A total of 617 patients underwent 794 PKP operations during the 8-year study period. Sufficient documentation was available to include 777 surgeries from 600 patients in this study. Specific indications for PKP were reported and grouped into 16 categories.The leading indication categories for PKP were regraft (209 cases, 26.9%), pseudophakic bullous keratopathy (PBK) (193 cases, 24.8%), primary corneal endotheliopathies including Fuchs’ endothelial dystrophy (101 cases, 13.0%), anterior keratoconus (93 cases, 12.0%), and viral or postviral causes (41 cases, 5.3%). Regraft, keratoconus, and Fuchs’ endothelial dystrophy each displayed a nonsignificant decreasing trend from 1996 to 2004, and PBK, herpes simplex virus, and mechanical trauma each displayed a nonsignificant increasing trend (p > 0.05 for all). Interpretation: Regraft was the leading indication for PKP at our centre, followed by PBK; these findings were in agreement with data reported in recent literature.The frequency of regraft had increased since a previous study from our centre (1986–1995), and the frequency of PBK had decreased. Contexte : Les principales indications de kératoplastie transfixiante (KPT) ont évolué ces dernières années. Cette étude examine ces indications et leurs tendances, les comparant avec les données récentes publiées dans d’autres études, y compris un compte-rendu de notre centre portant sur les indications de 1986 à 1995. Méthodes : On a examiné rétrospectivement les dossiers de tous les patients qui avaient subi une KPT provenant d’une pratique au centre du University Health Network, du Toronto Western Hospital, entre le 1er juillet 1996 et le 30 juin 2004. Résultats : En tout, 617 patients sont subi 794 KPT dans les 8 années qu’a duré l’étude. La documentation accessible a permis d’inclure dans l’étude 777 chirurgies de 600 patients. Les indications spécifiques de KPT relevées ont été réparties en 16 catégories. Les principales catégories d’indication de KPT furent : le regreffage (209 cas, 26,9 %), la kératopathie bulleuse pseudophakique (KBP) (193 cas, 24,8 %), l’endothéliopathie cornéenne primaire y compris la dystrophie endothéliale de Fuchs (101 cas, 13,0 %), le kératocone antérieur (93 cas, 12,0 %) et les causes virales et postvirales (41 cas, 5,3 %). Le regreffage, le kératocone et la dystrophie endothéliale de Fuchs ont présenté chacun une faible tendance à la baisse dans le délai étudié, alors que la KBP, le virus de l’herpes simplex et le traumatisme mécanique ont présenté une faible hausse (p > 0,05 pour tous). Interprétation : Le regreffage a été la principale indication de KPT à notre centre, suivi de la KBP; ces constatations concordaient avec les données de la littérature récente. La fréquence du regreffage avait augmenté depuis une étude antérieure de notre centre alors que celle de la KBP avait baissé.

From the Department of Ophthalmology, University of Toronto, Toronto, Ont.

Correspondence to: Stephen J. Dorrepaal, MD, 91 Grath Cres., Whitby ON L1N 6N7; [email protected]

Presented at the annual meeting of the Canadian Ophthalmological Society in Edmonton June 24, 2005; poster presentation at the World Cornea Congress V in Washington, DC, April 13–15, 2005

This article has been peer-reviewed. Cet article a été évalué par les pairs.

Originally received March 1, 2006. Revised June 28, 2006 Accepted for publication Aug. 13, 2006

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Can J Ophthalmol 2007;42:244–50 doi: 10.3129/can j ophthalmol.i07-030

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P

enetrating keratoplasty (PKP) is among the most successful forms of tissue transplantation. Worldwide, an estimated 120 000 corneal transplants were performed in the year 2000, making the cornea the most frequently transplanted human tissue at this time.1–3 The leading indications for PKP vary by geographic region and have undergone many changes over recent years.4 We retrospectively studied the indications for PKP in a tertiary ophthalmic referral centre from 1996 to 2004 and compared these with data from other series, including one that reported indications from 1986 to 1995 at the same practice.5

METHODS

A retrospective chart review was conducted of all PKP cases performed by a single ophthalmologist (A.R.S.) over the 8-year period from July 1, 1996, to June 30, 2004 at a tertiary ophthalmic referral centre (the Cornea and External Disease Service at the University Health Network, Toronto Western Hospital). Each patient’s record was retrospectively reviewed, and the indication for each PKP classified according to a standard set of established diagnostic categories.6,7 Primary graft failure was defined as irreversible opacification of a graft occurring within 2 weeks of surgery. Other information collected for each surgery included demographic data, presence or absence of various medical and ocular conditions, preoperative visual acuity, lens status (phakia, aphakia, or type of intraocular lens [IOL]), and associated surgical procedures performed at the time of the PKP operation. In addition, for patients undergoing a corneal regraft in a given eye, the indication for the first graft in that eye was collected. A review of the literature published since 1997 was performed to compare our results with the leading indications for corneal transplantation in other centres. Statistical methods

Linear regression was used to establish both linear trends in the data and the statistical significance of these trends. A p value of 0.05 was considered significant throughout the study. RESULTS

A review of the surgical log indicated that 617 patients underwent a total of 794 PKP operations during the 8-year study period; 777 surgeries (97.9%) from 600 patients had sufficient data available and were included in the study population for analysis. Of these, 385 (49.5%) involved right eyes and 392 (50.5%) involved left eyes. The mean age of patients in the study was 64 years (range 13–98),

with a median age of 70. Descriptive statistics for the 600 corneal transplant recipients are presented in Table 1. Medical comorbidities were recorded according to selfreport at the time of initial patient evaluation at the clinic. The presence of glaucoma was assumed if patients were taking one or more medications to lower intraocular pressure (IOP). The presence of corneal neovascularization and peripheral anterior synechiae were either noted during preoperative examinations or observed intraoperatively. To examine trends, study data were categorized into 8 one-year periods, each beginning on July 1 and ending on June 30 of the subsequent year. An average of 97 (SD 3) PKP operations were carried out at the study centre each year (range 92–102). Both the number of PKP operations performed each year and the average age of patients each year remained stable over the study period. Table 2 presents the number of PKP surgeries performed on each eye during the study period (668 eyes). A total of 69 patients received corneal grafts in both eyes during the study period. During this time, 11 patients had regrafts of both eyes, 16 had regrafts of one eye only, and 42 did not require regrafts in either eye. Specific indications for each PKP were categorized into 16 broad categories, as presented in Table 3. Overall, the leading indication categories for PKP in the study period were regraft (26.9%), pseudophakic bullous keratopathy Table 1—Characteristics of patients receiving penetrating keratoplasty, n = 600 No. of included patients No. of included surgeries Male Female Age, years Mean (SD), male Mean (SD), female Mean (SD), all Median Past medical history Diabetes Hypertension Heart disease Asthma, COPD Thyroid disease Past ocular history Glaucoma Corneal neovascularization Peripheral anterior synechiae Preoperative lens status Phakia Pseudophakic IOL Anterior chamber Posterior chamber Pupil-plane Scleral-fixated Iris-fixated Aphakia

600 777 311 (51.8) 289 (48.2) 59 (20) 69 (17) 64 (19) 70 79 (13.2) 174 (29.0) 83 (13.8) 4 2 ( 7. 0 ) 33 (5.5) 148 (24.7) 119 (19.8) 81 (13.5) 302 (50.3) 132 (22.0) 115 (19.2) 6 (1.0) 5 (0.8) 1 (0.2) 27 (4.5)

Note: Data at time of patient's first penetrating keratoplasty (PKP) surgery, shown here as No. (%) unless otherwise stated; COPD = chronic obstructive pulmonary disease; IOL, intraocular lens.

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(PBK) (24.8%), primary corneal endotheliopathies, including Fuchs’ endothelial dystrophy (13.0%), ectasias and (or) thinnings, including anterior keratoconus (12.0%), and viral and (or) postviral (5.3%). Some major Table 2—Penetrating keratoplasty surgeries performed per eye during the study period Number of procedures per eye

Number of eyes (%)

1 2 3 4 Total

580 (86.8) 71 (10.6) 13 (1.9) 4 (0.6) 668 (100)

PKP indications had a female:male (F:M) sex ratio that showed a female predominance (Fuchs’ 2.88, varicella zoster 2.33, bacterial infection 3.00) while others showed a male predominance (anterior keratoconus 0.52, herpes simplex 0.43, traumatic scarring 0.29, neuroparalytic and (or) neurotropic keratitis 0.20). The F:M ratio for PBK rose to 1.72 from 1.21 in the previous study (1986 to 1995).5 Some major indications had an average (SD) age notably lower than the overall mean age, including anterior keratoconus (38 [15] years) and traumatic scarring (46 [15] years). Fig. 1 presents the trends in the prevalence of 6 of the leading indications for PKP over the study period. None of these trends met statistical significance at the 95% level by linear regression. Regraft, keratoconus,

Table 3—Leading indications for penetrating keratoplasty by category and specific indication, n = 777 Indication category

No. of surgeries (%)

Regraft

209 (26.9%)

Pseudophakic bullous keratopathy Primary corneal endotheliopathies

193 (24.8) 101 (13.0)

Ectasias and (or) thinnings Viral and (or) postviral

93 (12.0) 41 (5.3)

Microbial and (or) postmicrobial

33 (4.2)

Mechanical trauma (nonsurgical)

24 (3.1)

Noninfectious ulcerative keratitis or perforation

20 (2.6)

Aphakic bullous keratopathy Interstitial keratitis Chemical injuries

12 (1.5) 12 (1.5) 7 (0.9)

Stromal corneal dystrophies Congenital opacities Corneal degenerations Other † Total

3 (0.4) 2 (0.3) 2 (0 .3) 25 (3.2) 777 (100.0)

Specific indication

No. of surgeries, %

Graft failure and (or) endothelial decompensation Previous graft rejection No previous graft rejection Unknown if previous graft rejection Allograft rejection Microbial and (or) viral infection Primary tissue failure Trauma and (or) rupture Other causes Pseudophakic bullous keratopathy Fuch's endothelial dystrophy Iridiocorneal endothelial syndrome Congenital hereditary endothelial dystrophy Posterior polymorphous dystrophy Anterior keratoconus Herpes simplex Varicella zoster Other Bacterial Chlamydial Acanthamoeba Fungal Other Traumatic scarring Traumatic corneal edema Traumatic irregular astigmatism Total blood staining of cornea Neuroparalytic and (or) neurotropic

147 (18.9) 7 (0.9) 101 (13.0) 39 (5.0) 47 (6.0) 9 (1.2) 2 (0.3) 2 (0.3) 2 (0.3) 193 (24.8) 93 (12.0) 5 (0.6) 2 (0.3) 1 (0.1) 93 (12.0) 30 (3.9) 10 (1.3) 1 (0.1) 20 (2.6) 6 (0.8) 4 (0.5) 2 (0.3) 1 (0.1) 18 (2.3) 3 (0.4) 2 (0.3) 1 (0.1) 6 (0.8)

Sjogren syndrome Mooren's ulcer Exposure Other Aphakic bullous keratopathy Interstitial keratitis Acid Alkaline Other Granular stromal dystrophy Rieger's syndrome Calcific band keratopathy

2 (0.3) 1 (0.1) 1 (0.1) 10 (1.3) 12 (1.5) 12 (1.5) 3 (0.4) 1 (0.1) 3 (0.4) 3 (0.4) 2 (0.3) 2 (0. 3) 25 (3.2) 777 (100.0)

*Corneal degenerations other than keratoconus and keratoglobus. †

Other indications include post radial keratotomy, glaucoma, cicatricial pemphigoid, electrical injury, contact-lens induced, immunologic-induced corneal melt, lipid keratopathy, post laser, and unknown.

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and Fuchs’ endothelial dystrophy displayed a nonsignificant decreasing trend, and PBK, herpes simplex virus, and mechanical trauma displayed a nonsignificant increasing trend. Overall, first-time regrafts accounted for 64% (134 cases) of the 209 regraft surgeries, second regrafts for 22% (46 cases), third regrafts for 11% (23 cases), fourth regrafts for 2% (4 cases), and fifth regrafts for 1% (2 cases). Table 4 lists the leading indications for the original graft in eyes that had undergone a regraft PKP during the study period. The total number of regrafts in this table is only 178 because 31 of the 209 regrafts performed in the study period were second or third regrafts on a particular

eye in the study period; these PKPs were not included to avoid disproportionately representing these indications. Of the 59 eyes that were regrafted and had PBK as the indication for the original PKP, 35 had an anterior chamber (AC)IOL preoperatively. Twenty-six of these ACIOLs were retained, and 9 were removed at the time of PKP. Surgical characteristics of all 777 PKPs performed are described in Table 5. The majority of patients had no lens surgery performed at the time of their PKP. Associated surgical procedures performed at the same time as the PKP included anterior vitrectomy, goniosynechiolysis, pars plana vitrectomy, and tarsorrhaphy.

Fig. 1—Trends in the leading indications for penetrating keratoplasty, 1996–2004.The R2 statistic summarizes how well the regression line fits the data points.The closer the value is to one, the better the fit.


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INTERPRETATION

We reported the clinical indications for PKP in a single tertiary referral practice during an 8-year period from July 1, 1996, to June 30, 2004. In a previous study examining patients from this practice between January 1986 and December 1995, Liu and Slomovic5 found the leading indications for PKP were PBK (28.5%), regraft (22.3%), keratoconus (10.0%), and Fuchs’ endothelial dystrophy (7.7%). The leading indications for PKP in the current study were regraft (26.9%), PBK (24.8%), Fuchs’ endothelial dystrophy (12.0%), and keratoconus (12.0%). These 4 indications have been widely recognized in the literature, along with corneal scarring, as the leading indications for PKP worldwide.5,8–34 Table 4—Regrafts by original indication, n = 178 Indication Pseudophakic bullous keratopathy Preoperative anterior chamber (AC) IOL ACIOL removed ACIOL retained Herpes simplex virus Traumatic scarring Fuch's endothelial dystrophy Anterior keratoconus Aphakic bullous keratopathy Bacterial Iridiocorneal endothelial syndrome Other* Unknown Total

No. (%) 59 (33.1) 35 (19.7) 9 (5.1) 26 (14.6) 15 (8.4) 12 (6.7) 12 (6.7) 10 (5.6) 8 (4.5) 6 (3.4) 4 (2.2) 20 (11.2) 32 (18.0) 178 (100.0)

*Includes

glaucoma, interstitial keratitis, mucopolysaccharidosis, petroleum-based chemical injury, Reis Bückler's dystrophy, varicella zoster virus, acanthamoeba infection, anterior ocular ischemia due to temporal arteritis, chlamydia, cicatricial pemphygoid, Reiger's syndrome, Salzmann's nodular degeneration, and Sjögren syndrome.

Table 5—Surgical characteristics, n = 777 No. (%) Mean host-bed size, mm Range, mm Lens surgery No lens surgery Phacoemulsification and insertion of PCIOL Removal of ACIOL and insertion of ACIOL ECCE and insertion of PCIOL Removal of ACIOL and insertion of scleralfixated IOL Insertion of scleral-fixated IOL (preoperative aphakia) Other Associated surgical procedures Anterior vitrectomy Goniosynechiolysis Pars plana vitrectomy Tarsorrhaphy

7.75 6–9 440 (56.6) 116 (14.9) 81 (10.4) 38 (4.9) 19 (2.4) 16 (2.1) 67 (8.6) 159 (20.5) 108 (13.9) 29 (3.7) 25 (3.2)

Note: PCIOL is posterior chamber intraocular lens; ACIOL, anterior chamber IOL, ECCE, extracapsular cataract extraction.

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Characteristics of patients included in the current study were similar to those found in 2 other studies by Sit et al20 and Weisbrod et al21 that examined PKP recipients from the same practice between January 1986 and June 1993. We also found that the F:M ratio, the median age, and the percentage of patients with histories of diabetes, hypertension, and glaucoma had each changed by less than 8% relative to the previous study at our centre (1986–1995).5 With respect to preoperative lens status, the percentage of patients who were phakic increased from 43.3% to 50.3%, the percentage of patients with pseudophakia decreased slightly from 44.9% to 43.2%, and the percentage of patients with aphakia decreased from 11.8% to 4.5%, reflecting recent trends in IOL usage. There was little fluctuation in the number of PKPs performed each year due to limitations in both operating room time and donor tissue availability. When comparing the indications for PKP in this study with those reported elsewhere, it must be noted that the indications reported in most centres represent all patients in need of corneal transplant. By contrast, in centres where the number of operations performed each year is restricted, any criteria that prioritize certain patients over others may skew the relative numbers for the reported indications. At our centre, PKPs were performed on a first-come, first-served basis, with the exception of urgent operations necessitated by corneal perforation, impending perforation, or pain. Accordingly, bias was minimized. Regraft was the most common indication in our series. It is also one of the leading indications in many recent studies from North America, Europe, and Asia.5,9,15–19,24,27–32,34 Regraft numbers have increased since a previous study conducted at our centre, although the proportion of regraft recipients receiving their first regraft on a given eye has remained relatively stable over time.5,20,21 The increasing trend in regrafts between the 2 studies is likely due to the increasing number of PKP recipients in the population. The importance of the nonsignificant decreasing trend in regrafts we observed within the present study period is unclear, and it will be interesting to follow this trend in the coming years. In regrafted patients, we found, as have previous studies,5,35 that PBK was the most common indication for the original graft in the same eye. Although 10-year graft survival for PBK eyes has been reported to be as low as 50%, lower than that for keratoconus, herpetic and non-herpetic keratitis, and corneal dystrophies and degenerations, another recent study showed that 10-year graft survival rates of 85% could be obtained if IOL exchange was performed at the same time as PKP36,37 The top 2 indications for regraft in the current study were graft failure and (or) endothelial decompensation and allograft rejection, as was the case in another

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recent study.37 Early treatment of graft rejection episodes may reduce the need for regraft, and it is therefore important that all PKP recipients are well-informed regarding the symptoms of graft rejection so they can contact their ophthalmologist promptly upon symptom presentation. PBK was the 2nd most common indication for PKP in the current study and, as shown in Table 6, has also been a leading indication in recent studies from around the world.5,8,11–17,19,22–27,31,33,34 A slight decline was seen in PBK as an indication since a previous study conducted at our centre, likely due to improvements in IOL designs and cataract surgical techniques. PBK was also increasingly common in women (F:M ratio 1.72 vs. 1.21 previously).5 Fuchs’ endothelial dystrophy and keratoconus were tied as the 3rd leading indication in this study. Keratoconus has recently been reported as the number one indication for PKP in countries such as France, Germany, Israel, New Zealand, and Zimbabwe, although not in the United States or Canada.17,19,25,26,30,33 Genetic factors and climatic effects may play a role in the high prevalence of keratoconus in certain areas. In addition, one study reported preferential

grafting of keratoconus during a time of corneal donor tissue shortage because of a higher success rate.19 Keratoconus favoured males with a F:M ratio of 0.52, similar to the F:M ratio of 0.50 found by Liu and Slomovic.5 Interestingly, a recent review states that keratoconus occurs in all ethnic groups with no male or female preponderance.38 Fuchs’ dystrophy favoured females with a F:M ratio of 2.88, similar to the previous study’s F:M ratio of 3.06.5 Female predominance is a well-established finding in Fuchs’ dystrophy.39 In summary, regraft has become the most common indication for PKP in our centre, followed by PBK, Fuchs’ endothelial dystrophy, and keratoconus. None of the leading indications for PKP showed a significant increasing or decreasing trend over the 8-year study period. Indications for PKP will likely continue to change with duration of practice and an aging population. Studies such as this one are important to monitor the leading PKP indications and their trends and to attempt to anticipate future changes in the field. Sources of support requiring acknowledgement: none declared.

Table 6—Comparison of leading indications since 1997 listed by nationality of study centre Leading indications First author, date

Country

1st

Dorrepaal / Slomovic, 2005 Al-Towerki, 2004 Al-Yousuf, 2004 Tabin, 2004

Canada

Regraft

PBK

2nd

Fuch's and keratoconus (tie)

3rd

Saudi Arabia UK Nepal

Corneal scarring Regraft Corneal scars

PBK or ABK Keratoconus Adherent leukoma

Chaidaroon, 2003

Thailand

Bullous keratopathy

Corneal scars

Corneal degeneration Fuch's endothelial dystrophy Perforation or impending perforation Corneal dystrophy and degeneration

Mendes, 2003

USA

Bullous keratopathy

Price, 2003 Randleman, 2003 Teenan, 2003 Cosar, 2002 Edwards, 2002 Chen, 2001

USA USA UK USA New Zealand Taiwan

PBK Failed graft Endothelial cell failure PBK Keratoconus Corneal scars

Scarring, keratoconus, and dystrophies (3-way tie) Fuch's endothelial dystrophy Bullous keratopathy Keratoconus Regraf t PBK or ABK Regraft

Legeais, 2001 Dobbins, 2000 Inoue, 2000 Maeno, 2000 Mkanganwi, 2000

France USA Japan Canada Zimbabwe

Keratoconus PBK Bullous keratopathy Regraft Keratoconus

Cursiefen, 1998 Chan, 1997 Wong, 1997 Dandona, 1997 Dandona, 1997 Frucht-Pery, 1997 Liu / Slomovic, 1997 Lois, 1997 Ramsay, 1997 Reinhard, 1997

Germany Singapore India India Israel Canada USA Scotland Germany

Keratoconus Regraft Corneal scars Corneal scars Keratoconus PBK PB K Corneal scars Keratoconus

Herpetic infections Fuch's endothelial dystrophy Keratoconus Keratoconus Presumed post measles scarring Corneal scars ABK Regraft Regraft R eg raf t Regraft R e g ra f t Regraft Bullous keratopathy

Keratoconus Keratoconus Dystrophy and regraft (tie) Kerat oconus Regraft Acute necrotizing and ulcerative keratitis Graft failures and PBK or ABK (tie) Keratoconus Nonherpetic keratitis PBK PBK PBK or ABK PBK A c t i v e i n f e c t i o u s k e ra t i t i s ABK Herpetic infections Keratoconus Fuch's endothelial dystrophy Keratoconus Endothelial dystrophies

Note: PBK = pseudophakic bullous keratopathy; ABK, aphakic bullous keratopathy.


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