Epidemic keratoconjunctivitis outbreak at a tertiary referral eye care clinic

Epidemic keratoconjunctivitis outbreak at a tertiary referral eye care clinic V. Montessori, MD, FRCPCa S. Scharf, RN, CICa S. Holland, MD, FRCSCb D. H. Werker, MD, FRCPCc,d F. J. Roberts, MD, FRCPCa E. Bryce, MD, FRCPCa Vancouver, British Columbia, Canada An outbreak of epidemic keratoconjunctivitis (EKC) occurred at a tertiary referral eye care clinic between late September and mid-November 1995. Before the outbreak, instruments were cleaned with 70% isopropyl alcohol and handwashing between patients was not routine. Infection control measures were implemented when the outbreak was recognized in mid-October. Control measures included triaging suspected cases to a separate waiting area, cohorting cases to a specific examining room, endorsing the use of gloves and handwashing during examinations of patients, and cleaning instruments with a buffered bleach solution. Thirty-six cases were diagnosed before the infection control measures were taken, and 3 cases were seen after the control measures were taken. Also, numerous secondary cases occurred in the community. No additional cases were diagnosed from December to February 25, 1996. Acquisition of the infection was linked to visits to 4 of 20 physicians in the eye clinic with 61% of cases associated with visits to 1 of those 4 physicians. The use of diagnostic lenses applied directly to the eye was associated with infection (odds ratio = 2.83, 95% confidence interval = 0.79 to 10.4), although this did not reach statistical significance. The use of tonometers, ophthalmic solutions, or laser therapy was not associated with infection, and all environmental cultures were negative. This outbreak emphasizes the need for implementation of routine infection control guidelines to prevent nosocomial transmission of epidemic keratoconjunctivitis and stresses the need for appropriate disinfection of instruments. (AJIC Am J Infect Control 1998;26:399-405)

Epidemic keratoconjunctivitis (EKC) is an acute adenovirus infective conjunctivitis characterized by symptoms of photophobia, watery ocular discharge, pain, and conjunctival injection. Risks for infection identified in previous outbreaks have included contaminated ophthalmo-

From the Division of Medical Microbiology and Infection Control,a Department of Ophthalmology,b Vancouver Hospital and Health Sciences Center, Communicable Disease Epidemiology Services, BC Center for Disease Control,c Vancouver, British Columbia, and the Federal Field Epidemiology Training Program, Health Canada.d Presented in part at the 34th Annual Infectious Disease Society of America (IDSA) Meeting, New Orleans, La, September 18-20, 1996. Reprint requests: E. Bryce, MD, FRCPC, Division of Medical Microbiology, Vancouver Hospital and Health Sciences Center, LSP—1—855 W. 12th Ave., Vancouver, BC, Canada V5Z 1M9. Copyright © 1998 by the Association for Professionals in Infection Control and Epidemiology, Inc. 0196-6553/98 $5.00 + 0

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logic solutions, ocular instruments, and inconsistent handwashing between patients.1-3 A nosocomial outbreak of EKC occurred between late September and mid-November 1995 at a tertiary referral eye care clinic. The objectives of this article are to describe the outbreak, the infection control measures implemented, and the results of a case-control study aimed at identifying risk factors for acquiring the infection. MATERIALS AND METHODS Outbreak

The eye care clinic provides primary ophthalmologic care to patients in the Vancouver area and is the tertiary care referral center for the province of British Columbia. Each day, approximately 400 patients visit the clinic, which is staffed by 20 physicians and 120 office assistants. An operating suite, laser equipment, diagnostic ultrasound, and an optician provide additional patient care. On October 13, 1995, the infection control team at 399

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Table 1. Infection control protocol Routine prevention of nosocomial EKC

A. Triage (performed by receptionist) Before examination, inquire, re: exposure to someone with red eyes or fever in the last 10 days Note any eye discharge or redness B. Segregate Any patient with a positive exposure history, red eyes, or discharge: Segregate in a separate examination room Wear gloves during examination and be scrupulous about washing hands (this includes the receptionist if administering eye drops) Be meticulous with administration of drops to avoid cross-contamination Avoid procedures such as tonometry and use of lens if at all possible Consider delaying any surgical procedures At the end of the examination, disinfect the room with a bleach solution (1000 ppm) Clean the tonometer and lens (if used) by immersion in bleach solution for 10 minutes and rinse well in cold water Educate patients about the disease and its communicability if EKC is diagnosed or suspected Culture any suspected case Maintain a central log of EKC cases C. Routine All areas should: Wipe down the examination room at the end of the day with a dilute buffered bleach solution (1000 ppm) Between patients, wipe the lenses and tonometers with dilute bleach and rinse thoroughly Wipe down the examination and waiting room with dilute bleach once per week Remove reading material from waiting room area weekly Wash hands after every patient contact Receive regular in-service education about body substance precautions and EKC protocols Control during outbreak of EKC

A. Triage (performed by receptionist) Before examination, inquire re: exposure to someone with red eyes or fever in the last 10 days, presence of eye discharge Note any eye discharge or redness B. Segregate Any patient with a positive exposure history, red eyes, or discharge: Segregate in a separate examination and waiting room C. Routine Wear gloves during the examination of all patients with vigorous hand washing afterward (this includes receptionist if administering eye drops) Be meticulous with administration of drops to avoid cross-contamination Avoid procedures such as tonometry and use of lens if at all possible Consider delaying any surgical procedures At the end of the examination of all patients, disinfect the room with a bleach solution Clean all instruments that contact the conjunctiva of all patients by immersion in bleach solution for 10 minutes and then rinse well in cold water All areas should: Wipe down the examination room at the end of the day with a dilute buffered bleach solution (1000 ppm) Wipe down the examination and waiting rooms with dilute bleach once per day until the outbreak is controlled Remove reading material from waiting room area Receive regular in-service education about body substance precautions and EKC protocols

Vancouver Hospital and Health Sciences Center was alerted to 19 cases of EKC seen during an 18day period. An investigation was begun, and infection control measures were implemented. Virology

Whenever possible, viral swabs were obtained from the conjunctivae of patients with symptoms compatible with EKC. Environmental viral swabs

also were collected on October 13, 1995, the first day the outbreak was identified. Sterile swabs were applied to surfaces in the offices and common areas of the clinic. Specimens were taken from several different sites, including tonometer heads, headrests from slit lamp microscopes, diagnostic lenses, countertops from examining rooms, and ocular solutions. The swabs were placed in a sterile vial with viral transport medium (Minimal Essential Medium with bovine serum albumin,

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Epidemic keratoconjunctivitis (EKC) is an infection of the eye caused by a virus. It can cause painful inflammation (redness) of the eye and may cause blurring of vision. It usually improves over a period of a few weeks. It is very contagious and easy to spread to other members of your family and friends. The following are suggestions to help avoid spread of infection. 1. Avoid touching your eyes whenever possible. If you do touch your eyes, wash your hands well with soap and warm water as soon as possible. 2. Do not share items such as towels, pillowcases, sunglasses, or any other item that comes into contract with your eyes or hands. 3. Please inform your eye doctor (ophthalmologist) and family doctor that you have EKC. 4. Please advise the receptionist at the eye care center that you have EKC when you return for your next appointment. Fig 1. EKC-patient information pamphlet.

Table 2. Patient demographics and clinical characteristics Case (N = 28)

Sex Female Male Median age (yr)(range) Primary ocular diagnosis Diabetic retinopathy Diminished visual acuity Glaucoma Iritis Corneal disease Other Previous ocular surgery Ocular medications β-blocker Corticosteroid Cholinergic Antibiotic Medical illnesses Systemic corticosteroids Diabetes mellitus Neutropenia Contact lens Eyeglasses

Control (N = 25)

P value

16 12 65(20-88)

13 12 64(27-84)

NS NS NS

8 7 5 1 2 5 14

2 4 5 1 6 7 14

NS NS NS NS NS NS NS

4 6 2 3

4 6 3 2

NS NS NS NS

2 8 0 2 24

4 2 1 2 18

NS NS NS NS NS

NS, Not significant.

Case-control study

penicillin, streptomycin, l-glutamine, hydroxyethyl piperazine ethanesulfonic acid buffer, amphotericin B, gentamicin, and sodium bicarbonate) and sent to the University of British Columbia Virology Laboratory for culture. Adenovirus isolates were sent to the Provincial Laboratory for typing by restriction fragment length polymorphism (RFLP).4

A case-control study was performed to explore what risks may have been associated with acquiring EKC. A confirmed case was defined as a patient who visited the clinic on or after September 14 (the visit date of the first patient with EKC) who had subsequent development of symptoms compatible with EKC

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Fig 2. Epidemic curve (visit date) of EKC cases, September through November, 1995.

Infection control measures

within 3 to 30 days, and a clinical diagnosis of EKC by an ophthalmologist, and/or an ocular culture that grew adenovirus. A suspect case was defined as a patient who visited the eye care center on or after September 14 who presented acutely with at least 3 of the following symptoms compatible with EKC: ocular redness, swelling, tearing or discharge, photophobia, ocular pain or discomfort, or foreign body sensation, within 3 to 30 days of the visit, but was not examined or cultured. Control patients were recruited by sending a memorandum to all physicians at the eye clinic requesting names of 2 patients who visited their offices on September 21, 1995 (1 week after the index patient’s visit) or October 10, 1995 (midway through the outbreak). A questionnaire was designed to collect information about patient demographics, clinical characteristics of the illness, and possible risks for acquiring infection. Data from the cases and controls were obtained by phone interviews and chart reviews by the investigators (V.M., S.S.). Data analysis was performed using EpiInfo 6 (Version 6.02, October 1994, Centers for Disease Control and Prevention, and World Health Organization, Geneva, Switzerland.) Categorical variables were analyzed by means of the χ2 test or Fisher’s exact test. Continuous variables were analyzed with the t test. A P value of < .05 was considered significant on 2-tailed testing.

Infection control measures are summarized in Table 1. Instruments were cleaned with a buffered bleach solution (1400 to 1500 ppm) for 10 to 15 minutes as recommended by the Association for Professionals in Infection Control and Epidemiology, Inc. (APIC) guidelines.5 Other important infection control measures that were implemented included the triaging of suspected clinical cases to a separate waiting area and cohorting these cases to a specific examining room. Because previous work has demonstrated that adenovirus can be cultured from the hands of health care workers despite handwashing, gloves were provided for use while examining patients in addition to reinforcing the importance of handwashing.2 The buffered bleach solution that was used to clean instruments also was used to clean all office surfaces and common areas in the clinic at the end of each day. Surfaces that were touched by patients were wiped between patient visits with a clean towel moistened with buffered bleach. Additional measures included holding educational sessions for staff and providing educational material to patients (Fig 1). Also, a 10-day leave of absence was advocated for any health care worker with EKC. RESULTS

A total of 39 confirmed and suspected cases of EKC were diagnosed from September 25 to

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Fig 3. Epidemic curve (onset of symptoms) of EKC cases, September through November, 1995.

November 14, 1995. (Fig 2). Thirty-six of the 39 patients visited the clinic and acquired their infections before the implementation of infection control measures. No additional cases in the initial outbreak were seen after November 14, 1995. (A second outbreak occurred in July and August 1996; however, a case-control study was not performed.) Twenty-eight of the 39 patients and 25 of the 34 control patients were interviewed by telephone. Attempts to contact the other 11 patients and 9 control patients by telephone were not successful, and their physicians denied the investigators access to their office charts. Although the request for control patients that was given to the other physicians in the eye clinic should have provided names of approximately 70 patients, only 34 names were obtained from 6 physicians. Fourteen of 20 physicians did not provide names of potential control patients from their practices. Viral cultures were done for 21 patients, and culture results for 12 patients were positive for adenovirus type 8, subgroup D. All environmental cultures (23) were negative. Demographics and clinical characteristics (Table 2) were similar for cases and controls. Fig 3 demonstrates the epidemic curve generated from the dates of the onset of patients’ symptoms. The illness was similar to that described in the literature with an incubation period of approximately 7 days.2 Mean duration of the symptoms was 24 days, whereas 8 patients (28%) reported

ongoing symptoms at the time of the interview (up to 64 days). Eight patients reported that family members were secondarily infected. Acquisition of the infection was related to visits to 4 of 20 physicians; 61% of the clinical cases were associated with visits to 1 particular physician. Fundoscopy was a risk factor by univariate analysis with an odds ratio (OR) of 3.38 (95% confidence interval (CI): 1.0 to 11.7, P = .04), but was no longer significant when exposure to this 1 physician was controlled for. There was no increased risk associated with having been seen by receptionists, nurses or residents. An association with the disease was seen in patients who had diagnostic lenses applied directly to the eye (OR: 2.83, 95% CI: 0.79 to 10.4, P = .07), but this did not achieve statistical significance. In this outbreak no risk was associated with routine ophthalmologic assessment, including the administration of ocular solutions, slit lamp examination, tonometry, or laser treatment. The administration of ocular solutions by physicians rather than medical office assistants was negatively associated with illness (OR: 0.23, 95% CI: 0.06 to 0.83, P = .01). DISCUSSION

Community-based outbreaks of EKC have been reported since the 1950s; however, over the past few decades the epidemiology of the outbreaks

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has changed and nosocomial spread is now the most common factor.6 EKC usually is self-limiting, with patients recovering over a 4-week period. However, complications such as subepithelial corneal infiltration may impair vision for up to a year or more. A proportion of patients in this study (28%) reported symptoms persisting at the time of their interviews. Thus, it could be anticipated that the true mean duration of symptoms is longer than the 24 days reported for this outbreak. In addition, the potentially significant effect on visual acuity caused by EKC infection and its propensity for secondary transmission underline the importance of avoiding nosocomial outbreaks. Diagnosis of EKC relies on both clinical and laboratory parameters. In this study, ocular culture was positive for adenovirus in 12 of 21 (57%) clinically suspected cases, and in 0 of 23 environmental cultures. Similarly, Jernigan et al2 were unable to culture virus from 17 environmental sites and had a sensitivity of 18 of 26 (69%) from ocular cultures. Whereas previous studies have found increased risk associated with the use of certain ocular instruments, such as pneumotonometry, this study did not identify any increased risk associated with routine ophthalmologic assessment.1 It may be that the study lacked the power to detect statistically significant risks associated with specific procedures or instruments. It also should be noted that 18 of the 39 cases had been seen in a single physician’s practice (the “primary practice”). This physician cooperated fully with infection control measures and his patients with EKC were interviewed for the case-control study, but the names of control patients were not provided. It also is possible that not all clinical cases were reported to infection control as other eye care clinic physicians did not want their patients to be contacted. Thus, the study may be biased as a result of the absence of control patients from the practice predominantly involved in the outbreak and the incomplete case finding. A negative association between illness and administration of ocular solutions by a physician rather than a medical office assistant was noted. Again, this finding may be biased as a result of the lack of control patients from the primary practice in the outbreak and the small number of control patients overall. In addition, 70% of the patients in the primary practice had ocular solutions administered by nonphysicians. Still, it is possible that the infection control techniques practiced by

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the medical office assistants were less effective than those practiced by physicians. Similar to the work by Koo et al1 and Jernigan et al,2 this study suggested that contact with a particular health care worker was associated with transmission of EKC. Interestingly, unlike other outbreaks, the health care worker was not infected, suggesting that he or his instruments may have acted as a vector for infection between patients. This possibility underlines the importance of handwashing between patients. An association with acquiring infection also was noted in patients who had a diagnostic lens applied directly to the eye. As direct eye inoculation is thought to be the most efficient means of transmission, it is important to stress the adequate disinfection of these instruments.6 Physicians reported damage to their specialized lenses after several days of soaking in bleach between patient contacts. Damage most frequently occurred on sealed 2-piece lenses and often was associated with soaking past the recommended time or soaking the entire lens in the bleach rather than just the areas that contacted the eye. Damage to these expensive lenses made compliance variable. Problems in using the buffered bleach to clean other instruments also were noted. Soaking tonometer heads for the suggested 10 to 15 minutes between patients was impractical during busy office hours. Care had to be taken to rinse the tonometer heads well after the bleach to avoid any contact of bleach to the patients’ eyes. If the tips were rinsed in warm water rather than cool, they could swell, making them difficult to fit back into the tonometer. A literature review for alternative practical and effective disinfection methods was not successful. Past studies have documented the ability of adenovirus to persist for months in a dried state on work surfaces and instruments and the resistance of adenovirus to common disinfecting agents such as isopropyl alcohol.7,8 Difficulties with disinfection of ophthalmologic medical instruments previously have been documented in the literature, yet design of these instruments and manufacturers’ recommendations for disinfection have not changed significantly.9 Several months after this nosocomial outbreak of EKC occurred, a second cluster of cases was identified at the same clinic. Twenty cases diagnosed over a 2-week period, in addition to 2 secondary cases, largely were associated with a particular physician. Strict adherence to infection control measures controlled this outbreak. This second cluster of cases demonstrated that the risk for nosocomial acquisi-

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tion was recurrent and suggested that either infection control guidelines distributed after the first outbreak were insufficient or compliance was poor. The purchase of infection control materials, such as gloves and bottles of bleach, did not mirror the reported adherence to infection control measures, suggesting that compliance was indeed the problem. Efforts were renewed to encourage adoption of the recommendations. Education of physicians and support staff proved to be paramount to the ultimate improvement in compliance. A revised infection control protocol for both routine and outbreak situations was adopted (Table 1). This report emphasizes the importance of routine infection control protocols in eye care centers to provide optimum care in a safe environment. Equipment disinfection was important in halting the outbreak, but alternatives to bleach immersion are needed. Ongoing research in this field is warranted. Most important, ongoing education and emphasis on infection control remain, as always, the keys to preventing nosocomial acquisition of EKC. We thank Dr. C. Sherlock of the Virology Laboratory, University of British Columbia, and Dr. S. Byrne of the Provincial Laboratory for their assistance in the isolation and typing of the adenovirus isolates.

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References 1. Koo D, Bouvier B, Wesley M, Courtright P, Reingold A. Epidemic keratoconjunctivitis in a university medical center ophthalmology clinic; need for re-evaluation of the design and disinfection of instruments. Infect Control Hosp Epidemiol 1989;10:547-52. 2. Jernigan JA, Lowry BA, Hayden FG, Kyger SA, Conway BP, Groschel DHM, et al. Adenovirus type 8 epidemic keratoconjunctivitis in an eye clinic: risk factors and control. J Infect Dis 1993;167:1307-13. 3. Axar MJ, Dhaliwal DK, Bower KS, Kowalski RP, Gordon YJ. Possible consequences of shaking hands with your patients with epidemic keratoconjunctivitis. Am J Ophthalmol 1996;121:711-2. 4. Singh-Naz N, Brown M, Ganeshananthan M. Nosocomial Adenovirus infection: molecular epidemiology of an outbreak. Pediatr Infect Dis J 1993;12(11):922-5. 5. Landry ML. Epidemic keratoconjunctivitis. In: Olmstead RN, editor. Infection control and applied epidemiology. St. Louis: Mosby; 1996. p. 42-1—42-2. 6. Ford E, Nelson K, Warren D. Epidemiology of epidemic keratoconjunctivitis. Epidemiol Rev 1987;9:244-61. 7. Jawetz E. The story of shipyard eye. Br Med J 1959:873-6. 8. Gordon YJ, Gordon RY, Romanowski E, Aruallo-Cruz TP. Prolonged recovery of desiccated Adenoviral serotypes 5, 8, and 19 from plastic and metal surfaces in vitro. Ophthalmology 1993;100(12):1835-9. 9. Centers for Disease Control. Epidemic keratoconjunctivitis in an ophthalmology clinic—California. MMWR Morb Mortal Wkly Rep 1990;39:598-601.

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