Significant Nonsurgical Risk Factors for Endophthalmitis After

Signiﬁcant Nonsurgical Risk Factors for Endophthalmitis after Cataract Surgery: EPSWA Fourth Report

Jianghong Li,1 Nigel Morlet,2 Jonathon Q. Ng,1 James B. Semmens,1 and Matthew W. Knuiman,1 for Team EPSWA3

PURPOSE. Endophthalmitis remains a devastating complication ostoperative endophthalmitis remains a devastating out- of cataract surgery, despite improved methods of prophylaxis Pcome after cataract surgery, despite improved methods of and surgical technique. The current study was conducted to prophylaxis, surgical technique, and treatment. This complica- identify sociodemographic, environmental, and clinical risk tion causes significant morbidity and distress and often severe 1–5 factors for the development of postoperative endophthalmitis, visual impairment or blindness. using population-based administrative data from Western Aus- The reported incidence of endophthalmitis after cataract 2–28 tralia. surgery varies considerably around the world (Table 1). Occurring about once every 500 operations, the relatively low METHODS. The Western Australian Data Linkage System identi- incidence of endophthalmitis makes it difficult to identify the fied all patients who underwent cataract surgery, along with risk factors clearly.3,29 Previous studies of risk factors were those in whom postoperative endophthalmitis subsequently limited by using only data from individual hospitals and centers developed, from 1980 to 2000 inclusive. Cases of endoph- or groups of surgeons.30–33 This results in a low number of thalmitis were cross-referenced with other sources and vali- cases and reduced external validity, making it difficult to com- dated by medical record review. After selection and prelimi- pare results. nary analysis of potential risk factors, multivariate logistic Our purpose was to identify and quantify a range of risk regression modeling was used to estimate odds ratios for the factors for the development of postoperative endophthalmitis selected variables. using the Western Australian Data Linkage System as part of the Western Australian Safety and Quality of Surgical Care RESULTS. Over the 21 years, 210 cases of endophthalmitis oc- 29,34,35 curred after 117,083 cataract procedures, yielding a cumulative Project. The significant advantage of our Data Linkage System is that it completely encompasses a geographically incidence rate of 1.79 per 1000 procedures. The incidence of isolated and generally stable population of 1.9 million people, endophthalmitis decreased for extracapsular extraction over providing reliable denominators for our statistical model. the whole period, but not for phacoemulsification over the Previous studies have focused primarily on surgical vari- recent 12 years. There was no risk-adjusted difference in the ables as risk factors for postoperative endophthalmitis.30–33 incidence rate of endophthalmitis for the various cataract sur- Several studies have reported a significant reduction in the gery procedure types. However, a significantly higher risk was incidence of endophthalmitis after the transition from intracap- found in patients aged over 80 years, in having surgery in sular to extracapsular extraction.3,9,11,29 However, despite the private hospitals, and to a lesser degree in having same-day introduction of the phacoemulsification technique of cataract surgery and surgery in winter. Cataract surgery with lacrimal or surgery, heralding the advent of small incision, sutureless sur- eyelid procedures dramatically increased the risk of endoph- gery, and the widespread adoption of same-day surgery, it thalmitis. remains controversial whether these changes have had any 3,5 CONCLUSIONS. It may be possible to reduce the incidence rate of impact on the rate of endophthalmitis. Also, the potential postoperative endophthalmitis by almost 80% with a system- influence of social, demographic, and environmental risk fac- atic approach to the management of elderly patients, hospital tors have received little attention to date. Because these un- stay, and clinical protocols. (Invest Ophthalmol Vis Sci. 2004; charted risk factors may confound the effect of surgical technique on endophthalmitis, the overall importance of surgical 45:1321–1328) DOI:10.1167/iovs.03-1000 factors remains unknown. This study addresses the paucity of knowledge about sociodemographic, environmental factors (such as the timing and From the 1School of Population Health, The University of Western location of surgery), and comorbidities that may contribute to Australia, Crawley, Western Australia, Australia; and the 2Department the development of endophthalmitis. of Ophthalmology, Royal Perth Hospital, Perth, Western Australia, Australia. 3Additional members of the Endophthalmitis Population Study of METHODS Western Australia (EPSWA) team are listed in Appendix B. Supported by Australian National Health and Medical Research Ethics Approval Council Project 110250. Submitted for publication September 9, 2003; revised January 4 Approvals for accessing patient health records were obtained from the and 11, 2004; accepted January 14, 2004. University of Western Australia Ethics Committee, the Confidentiality Disclosure: J. Li, None; N. Morlet, None; J.Q. Ng, None; J.B. of Health Information Committee of the Western Australian Depart- Semmens, None; M.W. Knuiman, None ment of Health, and individual hospitals. The research was conducted The publication costs of this article were defrayed in part by page in accordance with the Declaration of Helsinki. charge payment. This article must therefore be marked “advertise- ment” in accordance with 18 U.S.C. §1734 solely to indicate this fact. Data Selection Corresponding author: James B. Semmens, School of Population Health, The University of Western Australia, 35 Stirling Highway, Craw- All cataract operations in Western Australia, including same-day sur- ley, Western Australia 6009; [email protected]. gery, can be performed only in licensed facilities. These facilities, or

Downloaded from iovs.arvojournals.org on 10/01/2021 1322 Li et al. IOVS, May 2004, Vol. 45, No. 5

TABLE 1. Previously Published Incidence Rates of Endophthalmitis after Cataract Surgery

Number of Incidence Reference Location Period Procedures (per 1000) Notes

Population studies Semmens et al.3 (2003) Australia 1980–1998 94,653 1.99 *† Montan et al.6 (2002) Sweden 1998 54,666 1.06 ‡† Versteegh and Van7 (2000) Netherlands 1996–1997 71,028 1.52 * Wegener et al.8 (1998) Denmark 1994–1995 951 0.00 ‡ Norregaard et al.9 (1997) Denmark 1985–1987 19,426 3.14 *† Javitt et al.10 (1994) USA 1986–1987 57,103 0.77 *§࿣ Javitt et al.11 (1991) USA 1984 324,032 1.36 *§ Multicenter studies Versteegh and Van7 (2000) Netherlands 1996–1997 33,750 1.16 *† Schmitz et al.12 (1999) Germany 1996 340,633 0.78 *† Desai et al.13 (1999) United Kingdom 1997 15,787 1.65 *†‡ Desai14 (1993) United Kingdom 1990 (1 week) 998 3.00 †‡ Fisch et al.15 (1991) France 1988–1989 26,731 3.23 †‡ Single center studies Mayer et al.16 (2003) United Kingdom 1991–2001 18,191 1.65 *† Riley et al.17 (2002) New Zealand 2000 488 2.05 †‡ Eifrig et al.4 (2002) USA 1995–2001 21,972 0.36 *†¶ Yorston et al.18 (2002) Africa 1999 1,800 0.00 ‡ Ernest et al.19 (2000) Czech Republic 1990–1999 13,247 2.57 Colleaux and Hamilton20 (2000) Canada 1994–1998 13,886 0.72 *† Bohigian21 (1999) USA 1985–1996 19,269 0.62 *† Aaberg et al.2 (1998) USA 1990–1994 18,530 0.92 *¶# Somoni et al.5 (1997) Canada 1989–1996 13,285 2.41 *† Chitkara and Smerda22 (1997) United Kingdom 1987–1991 1,552 1.93 * Stanila23 (1996) Romania 1990–1995 759 3.95 de Gottrau and Leuenberger24 (1994) Switzerland 1983–1992 6,954 1.15 * Kattan et al.25 (1991) USA 1984–1989 23,625 0.72 *¶# Kattan et al.25 (1991) USA 1976–1982 7,552 0.93 *¶# Fahmy26 (1975) Denmark 1964–1974 4,498 5.33 *† Allen and Mangiaracine27 (1974) USA Not stated 36,000 0.86 † Christy and Lall28 (1973) Pakistan 1957–1972 77,093 4.96 †

Studies were not included if cataract surgery numbers were not provided to enable calculation of cumulative incidence. * Retrospective designs. † Endophthalmitis defined clinically. ‡ Prospective design. § Endophthalmitis defined according to International Classification of Diseases codes and not validated clinically. ࿣ Study population consisted of a 5% random population sample. ¶ Studies originated from the same center. # Endophthalmitis defined as culture positive microbiological specimens.

hospitals, are required by law to submit morbidity data for each patient Selection of the Variables for Statistical Analysis discharge, and this information provides the core data set of the Western Australian Data Linkage System. Using record linkage, data Age was stratified into two groups: younger than 80 years, or 80 years from all patient discharges enabled us to identify all patients who old or older. Preliminary analysis indicated that age as a continuous underwent cataract surgery in Western Australia from 1980 to 2000 variable, or divided into four groups (0–49, 50–59, 60–69, and 70–79 inclusive. Records were selected using the International Classification years) had no significant effect on the risk of development of postop- for Diseases (ICD) procedure codes for cataract surgery: ICD-9 and erative endophthalmitis. ICPM for 1980 to 1987; its modification, ICD-9-CM for 1988 to 1998; Patients were classified as residing in metropolitan or country areas (rural and remote) according to the postcode of their residential and ICD-10-AM for 1999 forward (Appendix A).36–40 The data set consisted of all hospital admissions for patients who had cataract address in the Health Zone classification system of the Western Aus- surgery during the study period. The ICD diagnosis codes for endoph- tralian Department of Health. Although there were 359 procedures thalmitis were used to identify patients with an admission for endoph- (0.3% of 117,083) for which we had no postcode information to thalmitis after cataract surgery as summarized in Appendix A. determine residential area, none were cases of endophthalmitis. Health insurance type was coded into three categories: public Data Validation (public patients), private (privately insured patients), and other. Pa- tients covered by workers’ compensation, motor vehicle injuries, or All cases of postoperative endophthalmitis cases were cross-referenced veteran (returned military service personnel) insurance schemes were with specific clinical databases located in the Departments of Micro- classified as private because these patients were treated privately. biology and Anesthetics at Royal Perth Hospital (Western Australia, The Dartmouth-Manitoba adaptation of the Charlson Index of co- Australia). Two vitreoretinal subspecialists managed almost all cases of morbidity was used to measure patient comorbidity (Appendix A).42 endophthalmitis at some point. To ensure further complete case iden- The presence of comorbidity was defined by the coding of any of the tification we reviewed their surgical logbooks over the 21-year period. 17 conditions from the Charlson Index at either the index admission All potential endophthalmitis cases were then validated by medical for cataract surgery, or any hospital admission within the previous record review.41 Three cases of endophthalmitis were excluded from year. Comorbidity was included in the final model as a dichotomous the analysis because of inadequate clinical data. variable after preliminary analysis had shown that the results remained

Downloaded from iovs.arvojournals.org on 10/01/2021 IOVS, May 2004, Vol. 45, No. 5 Risk Factors for Endophthalmitis after Cataract Surgery 1323

unchanged, regardless of whether comorbidity was analyzed as a age (80 years and older) was an important risk factor for continuous or dichotomous variable. Record linkage to the Western developing endophthalmitis after cataract surgery, indepen- Australian Cancer Registry also allowed identification of patients with dent of other risk factors, including comorbidity (OR 1.50; 95% a cancer diagnosis before or during the cataract surgery admission. CI 1.13–1.99). No significant association was found between Cancer diagnosis was also used as a dichotomous indicator. gender, comorbidity, health insurance type, or the locality of We differentiated hospital of surgery into private versus public and the patient’s residence and the risk of endophthalmitis. rural versus metropolitan. Public hospitals were subdivided into metropolitan public, rural public, and teaching public hospitals. Hospital Hospital of Cataract Surgery of surgery was also differentiated according to the cumulative number of cataract operations performed over the 21-year period. One hospital More cataract procedures were performed in private hospitals had performed 21% of all cataract procedures and was classified as the and metropolitan hospitals than in public hospitals and hospi- largest hospital. The next group of hospitals was classified as large with tals in rural areas. Large hospitals performed two thirds of all 2000 or more procedures, medium with 1000 or more, and small cataract surgeries. hospitals with less than 1000. Fourteen hospitals were excluded from Procedures performed in private hospitals had a signifi- the analysis because they had each coded less than 10 cataract proce- cantly higher risk of postoperative infection than did those dures and because of the nature of the hospitals (for example, provid- performed in public hospitals (OR 2.38; 95% CI 1.32–4.27). ing only maternity or psychiatric care) we suspected coding errors. No However, hospital location, the type of public hospital (met- cases of postoperative endophthalmitis originated from these hospi- ropolitan versus teaching) or the volume of cataract surgery tals. performed at each hospital had no effect on the incidence rate Length of hospital stay for cataract surgery was categorized into five of endophthalmitis. groups (same day and 1, 2–5, 6–7, and 8 or more days) after prelimi- Same-day cataract surgery was performed in 43% of the nary analysis showed that a continuous variable or other groupings had cases and 40% of the others. Most inpatient procedures had a no effect on the outcome. length of stay of 1 to 3 days (Table 2, Fig. 1A). Despite a steady Surgical technique was differentiated into three categories—intra- decline in the length of stay since 1980, 22% of cataract capsular, extracapsular/phacoemulsification, and other cataract extrac- operations in 2000 were still performed with inpatient admis- tion/lens-related procedures—because analysis revealed no significant sion, with an average length of stay of 1 day (Fig. 1A). difference in the mean incidence rate of endophthalmitis between Patients undergoing same-day cataract surgery were more phacoemulsification and extracapsular procedures, or between other prone to development of endophthalmitis than those with cataract extraction and lens-related procedures. inpatient stays of 2 to 5 days, but over the 21 years of data the Timing of surgery was analyzed according to the year and season of difference did not achieve statistical significance (OR 1.42, 95% the admission date for surgery. Seasons were defined according to CI 0.95–2.13, P ϭ 0.09). However, for the period 1990 to 2000, those in the Southern Hemisphere: winter, June to August; spring, the risk associated with same-day surgery was statistically sig- September to November; summer, December to February; and au- nificant (OR 1.62, 95% CI 1.01–2.61, P ϭ 0.047). The differ- tumn, March to May. ence between the entire 21 years’ and the latter 10-years’ results was due to the virtual nonexistence of same-day surgical Statistical Analysis procedures before 1990 (Fig. 1B). We found no other interactions between year of surgery Patients who underwent cataract surgery and had postoperative en- and length of hospital stay. There was no trend effect of the dophthalmitis were classified as cases, and those who underwent length of hospital stay on the outcome. The higher risk ob- surgery but did not have endophthalmitis were others. Analyses were served with a prolonged hospital stay of eight or more days performed on computer (SPSS; SPSS Science, Chicago, IL; and Stata; represents delayed discharge due to the development and Stata Corporation, College Station, TX).43,44 A multivariate logistic treatment of endophthalmitis during the same admission as regression model (referred to as the model) was used to estimate odds that for cataract surgery. ratios (OR) and 95% confidence intervals (CI) for each risk factor. Analysis was based on the procedure as the unit of analysis, with adjustment for possible clustering of multiple procedures in a patient. Surgical Characteristics The clustering adjustment used generalized estimating equations, There was a decline in the incidence rate of endophthalmitis which relaxed the independence assumption and required only that after extracapsular surgery in Western Australia over the 21- the procedures be independent across patients (the clusters). This year period (Fig. 2), with a five-yearly OR of 0.75 (95% CI produced correct standard errors, probabilities, and confidence inter- 0.57–0.98, P ϭ 0.04) after adjustment for patient characteris- vals, leaving the odds ratios and beta coefficients unchanged.45 tics and hospital of surgery. No decline in the incidence rate was observed during the 12 years of phacoemulsification surgery. RESULTS The incidence of postoperative endophthalmitis decreased by 50% during the transition from intracapsular to extracapsu- There were 117,083 cataract procedures performed in 76,424 lar extraction methods (2.92 vs. 1.46 cases per 1000 proce- patients in Western Australia from 1980 to 2000 inclusive. dures). In contrast, there was no reduction in the incidence of There were 210 cases (occurring in 209 patients) of endoph- postoperative endophthalmitis from the extracapsular to the thalmitis after cataract surgery. The cumulative incidence rate phacoemulsification technique (OR 0.80, 95% CI 0.59–1.09). of postoperative endophthalmitis was 1.79 per 1000 proce- The intracapsular procedure and the combined group of other dures over the 21-year period. Table 2 shows characteristics of cataract extraction and lens-related procedures had a higher the two groups of patients and the results of the multivariate risk for endophthalmitis than did extracapsular and phaco- logistic regression analysis. emulsification surgery, independent of year of surgery, demographic variables, and hospital of surgery. However, after ad- Patient Characteristics justment for all the other risk factors in the model, this association was no longer significant (Table 3). Cataract surgery was more commonly performed among fe- Approximately 10% of patients in endophthalmitis cases male patients and patients with private health insurance. Older and 5% of those in others had undergone both cataract surgery

Downloaded from iovs.arvojournals.org on 10/01/2021 1324 Li et al. IOVS, May 2004, Vol. 45, No. 5

TABLE 2. Characteristics of Cataract Surgery Patients and Multivariate Logistic Regression Analysis of Risk Factors for Postcataract Surgery Endophthalmitis

Incidence of Cases of Others— Endophthalmitis Postoperative Cataract (Per 1,000 Endophthalmitis Procedures Cataract Variable [No. (%)] [No. (%)] Operations) OR 95% CI P

Patient factors Gender Male (reference) 83 (39.5) 49,029 (42.0) 1.69 1.00 Female 127 (60.5) 67,844 (58.0) 1.87 1.12 0.84–1.49 0.44 Age Ͻ80 years (reference) 133 (63.3) 83,978 (71.9) 1.58 1.00 Ն80 years 77 (36.7) 32,895 (28.1) 2.34 1.50 1.13–1.99 0.005 Cancer history No cancer or previous skin cancer (reference) 199 (94.8) 111,985 (95.8) 1.77 1.00 Previous cancer (excluding skin cancer) 11 (5.2) 4,888 (4.2) 2.25 1.23 0.67–2.26 0.50 Charlson comorbidity None (reference) 189 (90.0) 104,254 (89.2) 1.81 1.00 Present 21 (10.0) 12,619† (10.8) 1.66 1.04 0.66–1.65 0.86 Health insurance status Private (reference) 123 (58.6) 64,825 (55.5) 1.89 1.00 Public 84 (40.0) 50,600 (43.3) 1.66 1.47 0.83–2.63 0.19 Other 3 (1.4) 1,448 (1.2) 2.07 0.77 0.24–2.53 0.67 Locality of residence* Metropolitan (reference) 160 (76.2) 95,059 (81.3) 1.68 1.00 Rural 42 (20.0) 17,861 (15.3) 2.35 1.49 0.97–2.28 0.07 Remote 8 (3.8) 3,594 (3.1) 2.22 1.33 0.61–2.90 0.48 Hospital factors Type Public hospital (reference) 87 (41.4) 55,465 (47.5) 1.57 1.00 Private hospital 123 (58.6) 61,408 (52.5) 2.00 2.38 1.32–4.27 0.004 Location Metropolitan hospital (reference) 182 (86.7) 103,383 (88.5) 1.76 1.00 Rural hospital 28 (13.3) 13,490 (11.5) 2.07 0.94 0.56–1.59 0.83 Total volume of cataract operations† The largest (24,301 procedures, n ϭ 1) (reference) 39 (18.6) 24,262 (20.8) 1.60 1.00 Large (2,004–10,017 procedures, n ϭ 16) 133 (63.3) 72,285 (61.8) 1.84 1.37 0.88–2.11 0.16 Medium (1,411–1,907 procedures, n ϭ 7) 17 (8.1) 11,748 (10.1) 1.44 0.93 0.52–1.66 0.80 Small (Ͻ1,000 procedures, n ϭ 28) 21 (10.0) 8,578 (7.3) 2.44 1.40 0.73–2.69 0.31 Length of stay Same day‡ 91 (43.3) 47,198 (40.4) 1.92 1.42 0.95–2.13 0.09 1 day 27 (12.9) 16,516 (14.1) 1.63 1.15 0.72–1.85 0.55 2–5 days (reference) 66 (31.4) 43,123 (36.9) 1.53 1.00 6–7 days 7 (3.3) 4,937 (4.2) 1.42 0.84 0.37–1.92 0.68 8ϩ days 19 (9.1) 5,099 (4.4) 3.71 2.08 1.18–3.67 0.01 Surgical factors Technique Extracapsular/Phacoemulsiﬁcation (reference) 165 (78.6) 100,258 (85.8) 1.64 1.00 Intracapsular 15 (7.1) 5,145 (4.4) 2.91 1.67 0.95–2.95 0.08 Other cataract extraction/Lens-related procedures 30 (14.3) 11,470 (9.8) 2.61 1.52 0.95–2.45 0.08 Other eye procedures during the same admission§ No other eye procedure (reference) 190 (90.5) 111,156 (95.0) 1.71 1.00 Glaucoma/drainage 4 (1.9) 1,913 (1.6) 2.09 1.11 0.42–2.95 0.83 Vitreoretinal procedure࿣ 6 (2.9) 1,190 (1.0) 5.02 2.71 1.18–6.23 0.02 Anterior vitrectomy 2 (0.9) 778 (0.7) 2.56 1.48 0.36–6.15 0.59 Corneal graft 1 (0.5) 393 (0.3) 2.54 1.14 0.16–8.33 0.90 Lacrimal/eyelid procedures 4 (1.9) 90 (0.1) 42.55 23.50 8.50–64.98 Ͻ0.001 Other 3 (1.4) 1,519 (1.3) 1.97 1.05 0.33–3.28 0.94 Environmental factors Year of surgery (1980–2000) 0.98 0.95–1.02 0.27 Season of surgery Spring (reference) 42 (20.0) 30,238 (25.9) 1.39 1.00 Summer 44 (21.0) 25,086 (21.4) 1.75 1.27 0.83–1.93 0.27 Autumn 61 (29.0) 30,941 (26.5) 1.97 1.41 0.95–2.08 0.08 Winter 63 (30.0) 30,608 (26.2) 2.05 1.48 1.00–2.18 0.05

Cases ϭ 210, Others ϭ 116,873, Overall Incidence ϭ 1.79 per 1,000. Standard errors were adjusted for clustering of procedures on individual patients. * There were 359 (0.3% of 117,083) procedures missing a locality but none were cases. † n denotes the number of hospital. ‡ Due to the virtual nonexistence of same-day surgery before 1990, additional analysis restricted to procedures performed in 1990–2000 revealed that compared with inpatient admission for 2–5 days, the odds ratio for endophthalmitis after same-day surgery was 1.62 (95% CI 1.01–2.61, P ϭ 0.047). § Some of the other eye procedures overlap, with some patients having more than one other eye procedure during the same admission. ࿣ Data include procedures to treat endophthalmitis during the same admission as the cataract procedure.

Downloaded from iovs.arvojournals.org on 10/01/2021 IOVS, May 2004, Vol. 45, No. 5 Risk Factors for Endophthalmitis after Cataract Surgery 1325

FIGURE 1. (A) Average length of stay and percentage of same-day cataract procedures in Western Australia. (B) Changing patterns of length of stay after cataract surgery pre- and post-1990 in Western Australia.

and another eye procedure during the same admission. Patients DISCUSSION who had lacrimal or eyelid procedures during the same hospital admission were at a significantly higher risk of development These data confirm our previous finding that a “center effect” of endophthalmitis than those who had cataract surgery only has a significant bearing on the incidence of endophthalmitis (OR 23.50, 95% CI 8.50–64.98). Although patients undergoing after cataract surgery.29 There was also a large difference in the a vitreoretinal procedure during the same admission appear to risk between public and private hospitals, independent of the be at risk, review of those medical records revealed that many other factors. Differences in the systems of patient care may be of the vitreoretinal procedures were undertaken as treatment the underlying issue, particularly as we also found a lower risk for endophthalmitis that developed during the same admission for inpatients in the 1990 to 2000 period. This suggests that the as that for cataract surgery. perioperative and early postoperative care of patients may be an important factor in the risk of endophthalmitis, and this may be related to the reliability of administration of prophylactic Environmental Factors antibiotics. Cataract procedures were fairly evenly distributed across sea- It is not feasible to control all the identified significant risk sons, with summer being the least likely season for patients to factors; however, some of those described are manageable. It is undergo cataract extraction. However, more endophthalmitis ill advised to perform lacrimal or eyelid procedures at the time cases resulted from surgery performed in winter and autumn of cataract surgery, but it may be useful to increase the length than from those performed in spring and summer. Cataract of hospital stay from same day to at least 2 days, and to surgeries performed during winter had a higher risk of endoph- optimize perioperative clinical protocols, especially in private thalmitis than those performed during spring (OR 1.48, 95% CI hospitals. An important finding was that patients aged 80 years 1.00–2.18). or more were more likely to develop postoperative endophthalmitis, independent of comorbidity, and other factors. This suggests that additional measures could be beneficially di- rected toward this age group. Our findings suggest that to minimize the risk of endophthalmitis, the over 80-year age group would benefit from avoid- ing winter surgery and being admitted to hospital for a few days for cataract surgery. The model allows us to estimate risks under various scenarios for this age group, as demonstrated in Table 4. Estimates from the model suggest a possible reduction in the endophthalmitis incidence rate of 23% to 78% for the 80-year or older age group, or 68% to 78% overall. In 2000 the 80-year or older group had 26.5% of the 11,439 cataract operations, of which 24.5% were inpatients (33% of the private patients, 14% of the public patients). If the remaining 75.5% elderly patients were also operated on as inpatients, an additional 2300 inpatients would double the number of inpatient admissions overall, adding approximately AUD$2 million to the health expenditure in Western Australia each year. Alterna- tively, elderly patients may benefit from more specific additional chemoprophylactic measures before, during, and after cataract surgery. Our findings also suggest that there is FIGURE 2. Trends in endophthalmitis following extracapsular and potential to greatly reduce the risk of postoperative endoph- phacoemulsification procedures in Western Australia. thalmitis by reducing the differences in the hospital systems

Downloaded from iovs.arvojournals.org on 10/01/2021 1326 Li et al. IOVS, May 2004, Vol. 45, No. 5

TABLE 3. Logistic Regression Analysis of the Inﬂuence of Surgical Type on the Risk of Postoperative Endophthalmitis

Association Adjusted for Association Adjusted for Demographic Variables all Variables in the Univariate Association* and Hospital† Multivariate Model‡ (Model 1) (Model 2) (Model 3)

Variable OR 95% CI P OR 95% CI P OR 95% CI P

Extracapsular/phacoemulsiﬁcation (reference) 1.00 ——1.00 ——1.00 —— Intracapsular 1.81 1.06, 3.10 0.03 1.80 1.06, 3.09 0.03 1.67 0.95, 2.95 0.08 Other cataract and lens-related procedures 1.64 1.06, 2.54 0.03 1.62 1.04, 2.54 0.03 1.52 0.95, 2.45 0.08 Year of surgery 1.01 0.98, 1.03 0.70 1.00 0.97, 1.03 0.99 0.98 0.95, 1.02 0.27

Cases ϭ 210 and Others ϭ 116,873. Standard errors were adjusted for clustering of procedures on individual patients. * Model 1: Surgical technique only. † Model 2: Model 1 plus age, gender, locality of patient residence, and hospital type (public or private). ‡ Model 3: All variables in the multivariate logistic regression model (Table 2).

between the public and private sectors. Our case– control than the actual type of cataract surgery. These findings empha- study and ongoing research should enhance our understand- size the importance of adjustment for other risk factors when ing of some of the factors responsible for the hospital system examining the impact of changing surgical practice on out- effect. come. Consistent with previous findings, our study has shown that The finding that season was a risk factor is consistent with the incidence of postoperative endophthalmitis decreased by existing literature on seasonal patterns of morbidity and mor- half during the transition from intracapsular to extracapsular tality. Hippocrates observed over 2000 years ago that “spring is 3,9,11,29 extraction methods. However, no further reduction in the most healthy, and least mortal.” Research has shown sea- incidence from extracapsular to phacoemulsification extrac- sonal variation in the occurrence of infectious diseases, with tion was observed (Fig. 2). The significant decrease in endoph- the highest incidence during winter.46 These patterns may thalmitis after extracapsular extraction occurred over a long reflect greater exposure to infectious diseases in winter and period, suggesting that a refinement of systems and surgical human responsiveness to changes in photoperiod, tempera- technique have occurred gradually over time. Given that the ture, and rainfall.46 Although the seasons were a significant risk reduction in the incidence of endophthalmitis after extracap- factor, they did not account for the temporal fluctuation in sular surgery took 21 years (with no significant reduction endophthalmitis we have described elsewhere.29 Season may during the first 10 years), the 12 years in which phacoemulsification was performed may be too short for any evident be a de facto marker of other environmental indices, and reduction in endophthalmitis incidence to be observed. therefore further study is required to clarify this association The overall risk of postoperative endophthalmitis was between endophthalmitis and weather. higher after intracapsular extraction, as well as other cataract Our findings suggest that simultaneous cataract and lacrimal and lens-related procedures, compared with extracapsular and or eyelid surgery is ill advised. They also suggest that the phacoemulsification procedures. However, other factors such incidence of postoperative endophthalmitis may be reduced as the hospital of surgery, the length of stay, and undergoing with a systematic approach to elderly patients, the length of other eye procedures appear to be more predominant risks hospital stay, and relevant clinical protocols.

TABLE 4. Endophthalmitis Risk Scenarios Based on Actual Data and the Multivariate Logistic Regression Model

Difference in Estimated Number Estimated Incidence Rate§ Actual Data* Scenario† of Cases Incidence Rate‡ (%)

Age Ͻ 80 Cataract procedures 84,111 Same-day surgery in a private hospital in winter 144 1.73 ϩ8 Endophthalmitis cases 133 Inpatient 2–5 days in a private hospital in winter 101 1.20 Ϫ24 Incidence rate 1.58‡ Inpatient 2–5 days in a public hospital in winter 43 0.51 Ϫ68 Inpatient 2–5 days in a public hospital in spring 29 0.34 Ϫ78 Age Ն 80 Cataract procedures 32,972 Same-day surgery in a private hospital in winter 84 2.56 ϩ10 Endophthalmitis cases 77 Inpatient 2–5 days in a private hospital in winter 59 1.80 Ϫ23 Incidence rate 2.34‡ Inpatient 2–5 days in a public hospital in winter 25 0.76 Ϫ67 Inpatient 2–5 days in a public hospital in spring 17 0.51 Ϫ78 All patients Cataract procedures 117,083 Inpatient 2–5 days in a public hospital during: Endophthalmitis cases 210 Winter 68 0.58 Ϫ68 Incidence rate 1.79‡ Spring 46 0.39 Ϫ78

* Actual number of procedures performed and cases occurring in Western Australia in 1980–2000 for each respective group. † Calculated assuming that all other risk factors in Table 2 are at the reference level. ‡ Number of cases per 1,000 procedures. § Percentage differences between actual and estimated incidence rates.

Downloaded from iovs.arvojournals.org on 10/01/2021 IOVS, May 2004, Vol. 45, No. 5 Risk Factors for Endophthalmitis after Cataract Surgery 1327

References 24. de Gottrau P, Leuenberger PM. Postoperative endophthalmitis in the Geneva Ophthalmologic Clinic [in French]. Klin Monatsbl 1. Kresloff, MS, Castellarin AA, Zarbin MA. Endophthalmitis. Surv Augenheilkd. 1994;204:265–267. Ophthalmol. 1998;43:193–224. 25. Kattan HM, Flynn HW, Pflugfelder SC, Robertson C, Forster RK. 2. Aaberg TM, Flynn HW, Schiffman J, Newton J. Nosocomial acute- Nosocomial endophthalmitis survey: current incidence of infec- onset postoperative endophthalmitis survey: a 10-year review of tion after intraocular surgery. Ophthalmology. 1991;98:227–238. incidence and outcomes. Ophthalmology. 1998;105:1004–1010. 26. Fahmy JA. Endophthalmitis following cataract extraction: a study 3. Semmens JB, Li J, Morlet N, Ng J. Trends in cataract surgery and of 24 cases in 4,498 operations. Acta Ophthalmol Scand. 1975; post-operative endophthalmitis in Western Australia (1980–1998): 53:522–536. The Endophthalmitis Population Study of Western Australia. Clin 27. Allen HF, Mangiaracine AB. Bacterial endophthalmitis after cata- Exp Ophthalmol. 2003;31:213–219. ract extraction II. Incidence in 36,000 consecutive operations with 4. Eifrig CW, Flynn HW, Scott IU, et al. Acute-onset postoperative special reference to preoperative topical antibiotics. Arch Oph- endophthalmitis: review of incidence and visual outcomes (1995– thalmol. 1974;91:3–7. 2001). Ophthalmic Surg Lasers. 2002;33:373–378. 28. Christy NE, Lall P. Postoperative endophthalmitis following cata- 5. Somani S, Grinbaum A, Slomovic AR, et al. Postoperative ract surgery. Arch Ophthalmol. 1973;90:361–366. endophthalmitis: incidence, predisposing surgery, clinical course 29. Morlet N, Li J, Semmens JB, Ng J. The Endophthalmitis Population and outcome. Can J Ophthalmol. 1997;32:303–310. Study of Western Australia (EPSWA): first report. Br J Ophthalmol. 6. Montan P, Lundstrom M, Stenevi U, Thorburn W. Endophthalmitis 2003;87:574–576. following cataract surgery in Sweden: the 1998 national prospec- 30. Menikoff JA, Speaker MG, Marmor M, Raskin EM. A case-control tive study. Acta Ophthalmol Scand. 2002;80:258–261. study of risk factors for postoperative endophthalmitis. Ophthal- 7. Versteegh MF, Van Rij G. Incidence of endophthalmitis after cata- mology. 1991;98:1761–1768. ract surgery in the Netherlands: several surgical techniques com- 31. Lehmann OJ, Roberts CJ, Ikram K, Campbell MJ, McGill JI. Asso- pared. Doc Ophthalmol. 2000;100:1–6. ciation between nonadministration of subconjunctival cefuroxime 8. Wegener M, Alsbirk PH, Hojgaard-Olsen K. Outcome of 1,000 and postoperative endophthalmitis. J Cataract Refract Surg. 1997; consecutive clinic and hospital-based cataract surgeries in a Danish 23:889–893. county. J Cataract Refract Surg. 1998;24:1152–1160. 32. Montan PG, Koranyi G, Setterquist HE, Stridh A, Philipson BT, 9. Norregaard JC, Thoning H, Bernth-Petersen P, Andersen TF, Javitt Wiklund K. Endophthalmitis after cataract surgery: risk factors JC, Anderson GF. Risk of endophthalmitis after cataract extraction: relating to technique and events of the operation and patient results from the International Cataract Surgery Outcomes study. history. Ophthalmology. 1998;105:2171–2177. Br J Ophthalmol. 1997;81:102–106. 33. Lertsumitkul S, Myers PC, O’Rourke MT, Chandra J. Endophthalmi- 10. Javitt JC, Street DA, Tielsch JM, et al. National outcomes of cataract tis in the western Sydney region: a case-control study. Clin Exp extraction: retinal detachment and endophthalmitis after outpa- Ophthalmol. 2001;29:400–405. tient cataract surgery. Cataract Patient Outcomes Research Team. 34. Holman CD, Bass AJ, Rouse IL, Hobbs MS. Population-based link- Ophthalmology. 1994;101:100–105. age of health records in Western Australia: development of a 11. Javitt JC, Vitale S, Canner JK, et al. National outcomes of cataract health services research linked database. Aust NZ J Public Health. extraction: endophthalmitis following inpatient surgery. Arch 1999;23:453–459. Ophthalmol. 1991;109:1085–1089. 35. Semmens JB, Lawrence-Brown MMD, Fletcher DR, Rouse IL, Hol- 12. Schmitz S, Dick HB, Krummenauer F, Pfeiffer N. Endophthalmitis man CDJ. The Quality of Surgical Care Project: a model to evaluate in cataract surgery: results of a German survey. Ophthalmology. surgical outcomes in Western Australia using population-based 1999;106:1869–1877. record linkage. Aust NZ J Surg. 1998;68:397–403. 13. Desai P, Minassian DC, Reidy A. National cataract surgery survey 36. World Health Organisation. International Classification of Dis- 1997–8: a report of the results of the clinical outcomes. Br J eases. Manual of the International Statistical Classification Of Ophthalmol. 1999;83:1336–1340. Diseases, Injuries, and Causes Of Death. Geneva, Switzerland: 14. Desai P. The national cataract surgery survey: II. Clinical out- World Health Organisation; 1977. comes. Eye. 1993;7:489–494. 37. World Health Organisation. International Classification of Proce- 15. Fisch A, Salvanet A, Prazuck T, et al. Epidemiology of infective dures in Medicine. Geneva, Switzerland: World Health endophthalmitis in France: the French Collaborative Study Group Organisation; 1978. on Endophthalmitis. Lancet. 1991;338:1373–1376. 38. The Official NCC Australian Version of ICD-9-CM. Tabular List of 16. Mayer E, Cadman D, Ewings P, et al. A 10 year retrospective survey Diseases. Sydney, Australia: National Coding Centre, Faculty of of cataract surgery and endophthalmitis in a single eye unit: inject- Health Sciences, University of Sydney; 1995. able lenses lower the incidence of endophthalmitis. Br J Ophthal- 39. The Official NCC Australian Version of ICD-9-CM. Tabular List mol. 2003;87:867–869. (Annotated) and Index of Procedures. Sydney, Australia: National 17. Riley AF, Malik TY, Grupcheva CN, Fisk MJ, Craig JP, McGhee CN. Coding Centre, Faculty of Health Sciences, University of Sydney; The Auckland cataract study: co-morbidity, surgical techniques, 1995. and clinical outcomes in a public hospital service. Br J Ophthal- 40. The International Statistical Classification of Disease and Re- mol. 2002;86:185–190. lated Health Problems, 10th Revision, Australian Modification 18. Yorston D, Gichuhi S, Wood M, Foster A. Does prospective mon- (ICD-10-AM). Tabular List of Procedures ICD-10-AM: MBS-Ex- itoring improve cataract surgery outcomes in Africa? Br J Ophthal- tended. 2nd ed. Sydney, Australia: National Centre for Classifica- mol. 2002;86:543–547. tion in Health, Faculty of Health Sciences, University of Sydney; 19. Ernest J, Rejmont L, Pasta J, Nemec P. Endophthalmitis after 2000. cataract surgery [in Czech]. Cesk Slov Oftalmol. 2000;56:351–356. 41. Li J, Morlet N, Semmens JB, Gavin A, Ng J. Coding accuracy for 20. Colleaux KM, Hamilton WK. Effect of prophylactic antibiotics and endophthalmitis diagnosis and cataract procedures in Western incision type on the incidence of endophthalmitis after cataract Australia. Ophthalmic Epidemiol. 2003;10:133–145. surgery. Can J Ophthalmol. 2000;35:373–378. 42. Romano PS, Ross LL, Jollis JG. Adapting a clinical comorbidity 21. Bohigian GM. A study of the incidence of culture-positive endoph- index for use with ICD-9-CM administrative data: differing perspec- thalmitis after cataract surgery in an ambulatory care centre. Oph- tives. J Clin Epidemiol. 1993;46:1075–1079. thalmic Surg Lasers. 1999;30:295–298. 43. Norusis MJ. SPSS for Windows. Base System User’s Guide: Release 22. Chitkara DK, Smerdon DL. Risk factors, complications, and results 5.0. Chicago: SPSS Inc.; 1992. in extracapsular cataract extraction. J Cataract Refract Surg. 44. StataCorp. Stata Statistical Software: Release 7.0. College Station, 1997;23:570–574. TX: Stata Corp.; 2001. 23. Stanila A. Extracapsular extraction of the crystalline lens [in Ro- 45. Zeger SL, Liang KY. Longitudinal data analysis for discrete and manian]. Oftalmologia. 1996;40:264–273. continuous outcomes. Biometrics. 1986;42:121–130.

Downloaded from iovs.arvojournals.org on 10/01/2021 1328 Li et al. IOVS, May 2004, Vol. 45, No. 5

46. Nelson RJ, Demas GE, Klein SL, Kriegsfeld LJ. Seasonal Patterns of diabetes with chronic complications; hemiplegia or paraplegia; Stress, Immune Function, and Disease. Cambridge, UK: Cam- renal disease; any malignancy, including lymphoma and leuke- bridge University Press; 2002: 58–70. mia; moderate or severe liver disease; metastatic solid tumor; and acquired immunodeficiency syndrome. APPENDIX A APPENDIX B Cataract procedures included intracapsular extraction of lens (ICD-9 codes: 5-144; ICD-9-CM codes: 13.11, 13.19; ICD-10-AM Team EPSWA: Other Members codes: 42698-00, 42702-00, 42702-01); extracapsular extraction (linear/aspiration/other) (ICD-9 codes: 5-142, 5-145; ICD- Ian Constable (Sir Charles Gairdner Hospital; St. John of God 9-CM codes: 13.2, 13.3, 13.51, 13.59; ICD-10-AM codes: 42698- Hospital, Subiaco; Lions Eye Institute; The University of West- 01, 42702-02, 42702-03, 42698-04, 42702-08, 42702-09); ern Australia), Ian McAllister (Royal Perth Hospital; St. John of phacoemulsification (ICD-9-CM codes: 13.41-13.43; ICD-10-AM God Hospital, Subiaco; Lions Eye Institute; The University of codes: 42698-02, 42702-04, 42702-05, 42698-03, 42702-06, Western Australia), Chris Kennedy (Fremantle Hospital; St. 42702-07); other cataract extraction (ICD-9 codes: 5-146; ICD- John of God Hospital, Subiaco), Tim Isaacs (Royal Perth Hos- 9-CM codes: 13.64, 13.65, 13.66, 13.69; ICD-10-AM codes: pital; St. John of God Hospital, Subiaco; Lions Eye Institute; The 42731-01, 42698-05, 42702-01, 4270210, 42702-11); and lens- University of Western Australia), John Pearman (Royal Perth related operations (ICD-9 codes: 5-147, 5-149; ICD-9-CM codes: Hospital), D’Arcy Holman (School of Population Health; The 13.70-13.72, 13.9; ICD-10-AM codes under categories of 193, University of Western Australia). 194, 201-203). Endophthalmitis cases were identified using ICD-9 diagnosis codes: 360.0, 360.1; ICD-9-CM codes: 360.00- Other Contributors to the Study 360.04, 360.11-360.19; and ICD-10-AM codes: H44.0, H44.1. Bridget Mullholland (Royal Perth Hospital), Max Bulsara The 17 categories of diseases included in the Charlson (School of Population Health; The University of Western Aus- Index are: myocardial infarction; congestive cardiac failure; tralia), Arem Gavin (School of Population Health; The Univer- peripheral vascular disease; cerebrovascular disease; dementia; sity of Western Australia), Ferenz Kosaras (Royal Perth Hospi- chronic pulmonary disease; rheumatological disease; peptic tal), and The Health Information Centre of the Western ulcer disease; mild liver disease; diabetes (mild to moderate); Australian Department of Health.

Downloaded from iovs.arvojournals.org on 10/01/2021