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Prophylaxis of Acute Posttraumatic Bacterial EndophthalmitisA Multicenter, Randomized Clinical Trial of Intraocular Antibiotic Injection, Report 2
Masoud Soheilian, MD;
Nasrin Rafati, MD;
Mohammad-Reza Mohebbi, PhD;
Shahin Yazdani, MD;
Houshang Faghihi Habibabadi, MD;
Mostafa Feghhi, MD;
Hossein A. Shahriary, MD;
Jamil Eslamipour, MD;
Niloofar Piri, MD;
Gholam A. Peyman, MD; for the Traumatic Endophthalmitis Trial (TET) Research Group
Arch Ophthalmol. 2007;125(4):460-465.
ABSTRACT
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Objective To evaluate the efficacy of intraocular gentamicin sulfate and clindamycin in the prevention of acute posttraumatic bacterial endophthalmitis following penetrating eye injuries.
Method We conducted a multicenter, randomized, double-masked controlled trial of 346 eyes with penetrating eye injury. Following primary repair, eyes were randomized to intracameral or intravitreal injection of 40 µg of gentamicin sulfate and 45 µg of clindamycin (cases) vs balanced salt solution (controls).
Main Outcome Measure Occurrence of endophthalmitis within 2 weeks.
Results Endophthalmitis occurred in 8 (2.3%) of 167 eyes in the control group and only in 1 (0.3%) of 179 eyes in the case group (P = .04; odds ratio, 8.93 [95% confidence interval, 1.11-71.43]). In eyes with an intraocular foreign body, endophthalmitis developed in 7 of 25 control eyes and in none of 27 eyes receiving antibiotics. However, in eyes without an intraocular foreign body, endophthalmitis developed in 1 of 142 eyes and 1 of 152 eyes in the 2 groups, respectively (P value for interaction = .04). Intravitreal injection was superior to intracameral injection in preventing endophthalmitis (P value for interaction = .01). Vitreous culture results were positive in 6 (67%) of 9 eyes with endophthalmitis.
Conclusion Intraocular gentamicin and clindamycin are effective in the prevention of acute posttraumatic bacterial endophthalmitis in eyes with retained intraocular foreign body.
Application to Clinical Practice Prophylaxis of traumatic endophthalmitis.
Trial Registration clinicaltrials.gov Identifier: NCT00398658
INTRODUCTION
One of the most important and devastating complications following penetrating eye injuries is the development of endophthalmitis. The incidence has been reported from 3.3% to 30% in different series and is highly dependent on the setting and circumstances of trauma.1-4 Both gram-positive and gram-negative organisms can be causative agents, although mixed infection may also occur.1-2 Bacillus cereus has recently been recognized as a virulent organism in posttraumatic endophthalmitis. This ubiquitous organism has a predilection for soil; therefore, it is a common assumption that dirty lacerations are more likely to become infected with this organism, especially when a retained intraocular foreign body (IOFB) exists.2-3,5-7 The visual prognosis of treated eyes with acute posttraumatic bacterial endophthalmitis is generally poor; only a small percentage of salvaged eyes regain ambulatory vision.6-9 By the time infection is clinically evident, initiation of antibiotic therapy may be too late to reverse the severe inflammatory response. These facts underscore the importance of preventive strategies in penetrating eye injuries.
Traditionally, prophylactic intravenous, subconjunctival, and topical antibiotics have been recommended for most cases of penetrating eye injuries, although strong evidence for their use is lacking. Our clinical trial was preceded by a pilot study conducted to refine the design and methods of the trial.1 The current multicenter randomized clinical trial compares the development of acute posttraumatic bacterial endophthalmitis in patients assigned to 2 treatment arms: intraocular antibiotic injection or intraocular balanced salt solution (BSS) injection in a randomized manner. To our knowledge, this is the first randomized study evaluating the effectiveness of intraocular antibiotic injection (gentamicin sulfate and clindamycin) combined with other prophylactic methods, including systemic, topical, and subconjunctival routes of antibiotic administration, for prevention of acute posttraumatic bacterial endophthalmitis following penetrating eye injuries.
METHODS
A multicenter, group-sequential, randomized, double-masked clinical trial was conducted at 4 university-based hospitals in 3 cities in Iran. The research followed the guidelines of the Declaration of Helsinki.10 All patients consented to participation in this study and the ethics committees of the involved institutes and the Iranian National Research Center of Medical Sciences approved the study.
PARTICIPANTS
All patients with penetrating eye injuries referred to collaborating institutes for primary repair were enrolled considering the following exclusion criteria: absence of light perception, presence of endophthalmitis at the time of initial evaluation, total corneal opacity, age younger than 3 years, severe intracameral hemorrhage, history of intraocular surgery, and presence of a corneal ulcer. Monocular patients and the better eye in simultaneous bilateral injuries were also excluded.
INTERVENTION
Complete ocular examination was performed for every patient. Media clarity was also classified according to red reflex: poor (< 20/200), fair (20/200-20/60), or good (> 20/50). The degree of cell and flare in the anterior chamber and vitreous were determined according to Hogan and Kimura scores on a scale from 0 to 4.11 An orbital x-ray was taken for all patients as well as a high-resolution orbital computed tomographic scan for those with retained IOFBs. All patients were admitted, and administration of intravenous gentamicin sulfate (3-5 mg/kg) every 8 hours along with cefazolin sodium (50 mg/kg) every 6 hours was initiated and continued for 5 days following primary repair.
Enrolled eyes were randomized to injection of 0.1 mL of BSS or a combination of 40 µg of gentamicin sulfate and 45 µg of clindamycin (0.1 mL) following primary repair of globe laceration. Eyes with lacerations anterior to rectus muscle insertions with an intact lens capsule received intracameral injection. However, eyes with lacerations limited to or extending posterior to rectus muscle insertions and eyes with a ruptured lens capsule received intravitreal injection.
SURGICAL TECHNIQUE
All patients underwent surgery under general anesthesia. Corneal and scleral lacerations were repaired in the usual manner. At the conclusion of primary repair, eyes were randomly assigned to antibiotic or BSS injection as described earlier. Intracameral injection was performed through the limbus with a 27 needle. For better and more secure intravitreal injection, a microvitreoretinal blade was used through the sclera 4 mm behind the limbus in phakic eyes (3.5 mm in aphakic eyes). First, 0.2 mL of vitreous was aspirated with a 23 needle on a tuberculin syringe with the needle pointing toward the midvitreous.12 After changing needles, antibiotic or BSS was injected slowly into the anterior vitreous using a 27 needle with the bevel facing up. Finally, the sclerotomy site was closed. At the conclusion, 20 mg of gentamicin sulfate and 4 mg of betamethasone were injected subconjunctivally.
POSTOPERATIVE MEDICATIONS AND FOLLOW-UP
The postoperative regimen included gentamicin sulfate drops 4 times daily and atropine drops 3 times daily for 1 week. Topical betamethasone was also administered 4 times daily for 6 weeks. Oral prednisolone (1 mg/kg per day) was initiated 24 hours postoperatively and tapered after 1 week depending on the severity of inflammation.
All patients were hospitalized for 15 days during which they underwent routine daily examinations. One masked observer independently examined the patients on days 1, 2, 3, 5, 7, and 14. A complete ophthalmic examination was performed during each visit to determine the amount of anterior chamber and vitreous reaction and haziness. Echography was performed in cases with poor visibility of the posterior segment 24 hours after repair to detect posterior segment complications.
MAIN OUTCOME MEASURES
The primary outcome measure in this study was development of endophthalmitis. Endophthalmitis was diagnosed in the setting of pain, lid swelling, decreased visual acuity, and 3+ cells in the anterior chamber together with any of the following: vitritis with loss of red reflex, vitreous involvement detected by echography in cases with media opacity, or positive culture results of harvested intraocular fluids. The diagnosis of endophthalmitis was confirmed by 2 other masked, independent observers. The secondary outcome measures were rate and type of additional procedures required during hospitalization.
SAMPLE SIZE
Sample size was estimated based on published data from other studies with an estimated incidence of 8% for posttraumatic endophthalmitis.13 The aim of this study was to reduce this incidence to 4% (effect size = 4%). With power set at the 80% level and a type I error of 5%, a row sample size of 450 patients was required for each arm of the study. We planned to perform 3 interim analyses during the trial; therefore, the overall sample size was increased to 1035 according to Pocock stopping boundaries. Our pilot study, in which patients were followed up for a longer period, revealed a high rate of case loss; therefore, we decided to perform this study on an inpatient basis.
RANDOMIZATION
Randomization was performed using the random block permutation method according to a computer-generated randomization list. The block lengths varied randomly (8, 10, and 12). Random allocation sequence was performed by a biostatistician at the study coordination center (Ophthalmic Research Center, Labbafinejad Medical Center). Details of the series were unknown to any of the investigators and were contained in a set of sealed envelopes each labeled with the name of the collaborating institute and a number. These envelopes were sent to study centers to principal investigators. A research coordinator at each center allocated patients to the antibiotic or BSS injection groups based on randomization sequences inside the envelopes.
MASKING PROCEDURE
The study was designed as a double-masked clinical trial. At the time of primary repair, an unmasked coordinator determined assignment of patients to the antibiotic or BSS groups. At each follow-up, a masked ophthalmologist completed the physical examination and consulted a masked retina specialist (principal investigator at each center) for measuring the main outcomes of treatment, specifically development of endophthalmitis. Two other independent, masked ophthalmologists confirmed the diagnosis of endophthalmitis. Only the study biostatistician and the head principal investigator had access to raw data, but none had any contact with the study participants.
STATISTICAL METHODS
The Pocock approach to group sequential testing with 3 interim analyses was used to compare the main outcome in case and control groups. Recruited patients were divided into 3 sequences; each sequence contained 346 patients (173 cases and 173 controls). After completion of follow-up for each sequence, interim analysis was performed to detect any statistically significant difference. Odds ratios and 95% confidence intervals were used to assess the magnitude of intergroup differences in the main outcome. The Mantel-Haenszel test was used to determine the homogeneity of collaborating institutes in terms of study outcomes. The likelihood ratio test was used to compare prognostic factors and also for subgroup analysis. Logistic regression analysis and the Mantel-Haenszel test were used to identify risk factors and potential confounders. The Breslow-Day test was used to evaluate the interaction of confounders on the main outcome of the study. Our study was terminated after the first interim analysis, 5 years after initiation of the trial.
RESULTS
This study includes 346 eyes of 346 patients enrolled in a multicenter randomized clinical trial from July 1999 until accrual ended in September 2004. Eyes were randomly assigned to BSS injection (167 eyes) or antibiotic injection (179 eyes). Distribution of patients in different collaborating institutes was as follows: 110 cases from Labbafinejad Medical Center, Tehran, Iran; 177 cases from Farabi Eye Hospital, Tehran; 30 cases from Sina Hospital, Ahwaz, Iran; and 29 from Alzahra Hospital, Zahedan, Iran. Enrolled patients were hospitalized for 15 days, all interventions and evaluations were performed during this period, and case loss was nil (available in an eFigure). Treatment arms were balanced regarding patient and eye characteristics at the time of enrollment. General characteristics of patients are summarized in Table 1.
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eFigure. Flow of participants through each stage of randomization. BSS indicates balanced salt solution.
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Table 1. General Characteristics of 346 Patients Randomized to Antibiotic or BSS Injection
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Overall, acute posttraumatic bacterial endophthalmitis developed in 9 eyes (2.6%), including 8 eyes (2.3%) in the BSS injection group (controls) and only 1 eye in the antibiotic injection group (0.3%) (P = .04 likelihood ratio test; odds ratio, 8.93 [95% confidence interval (CI), 1.11-71.43]), indicating a meaningful difference between treatment arms in favor of antibiotic injection. There was a significant association between IOFB and endophthalmitis (P = .04, Mantel-Haenszel test). The odds ratio was adjusted controlling for IOFB using the Mantel-Haenszel method, which showed no meaningful change on the treatment group comparison (adjusted odds ratio, 8.6 [95% CI, 1.2-62.5]).
The benefit of treatment was seen only among eyes with an IOFB. In eyes with an IOFB, endophthalmitis developed in 7 of 25 control eyes and in none of 27 eyes receiving antibiotics, whereas in eyes without an IOFB, endophthalmitis developed in 1 of 142 eyes and 1 of 152 eyes in the 2 groups, respectively (P value for interaction = .04) (Table 2).
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Table 2. Development of Endophthalmitis in Cases vs Controls Stratified According to Presence of IOFB and Site of Injection
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The association between injection site (intracameral vs intravitreal) and development of endophthalmitis was significant (P = .05, Mantel-Haenszel test). However, the adjusted odds ratio for intergroup comparison showed no meaningful change after controlling for injection site using the Mantel-Haenszel method (adjusted odds ratio, 9.2 [95% CI, 1.3-90.9]). In eyes receiving intracameral injection, endophthalmitis developed in none of 49 control eyes and in 1 of 77 eyes receiving antibiotics. In eyes with intravitreal injection, endophthalmitis developed in 8 of 118 control eyes and none of 102 eyes receiving antibiotics (P value for interaction = .01). These findings indicate that intravitreal injection may be superior to intracameral injection in preventing acute posttraumatic bacterial endophthalmitis (Table 2). No significant difference was observed between collaborating institutes in terms of the development of endophthalmitis (P = .33, Mantel-Haenszel test).
Logistic regression analysis was performed to identify risk factors for endophthalmitis in the control group; only 3 factors, including retained IOFB, presence of afferent pupillary defect, and vitreous prolapse, were significantly associated with the development of acute posttraumatic bacterial endophthalmitis. There was no correlation between size of IOFB and development of endophthalmitis (P = .82) (Table 1).
Intraocular specimens obtained during pars plana vitrectomy in eyes with endophthalmitis yielded positive culture results in 6, including Staphylococcus epidermidis in 3 eyes and Pseudomonas aeruginosa, gram-negative coccobacilli, and nonfermentive gram-negative bacilli each in 1 eye.
Secondary procedures (lensectomy, vitreoretinal operations for IOFB removal, or retinal detachment and enucleation) had to be performed in 63 (51%) and 61 eyes (49%) in the case and control groups, respectively (P = .80). Three eyes had to be enucleated and all were in the control group. Histopathologic examination of ocular contents failed to reveal any microorganism. No corneal or retinal toxic reaction related to use of antibiotics (gentamicin and clindamycin) was observed in this study.
COMMENT
This randomized multicenter trial evaluated the effectiveness of adding an intraocular injection of 40 µg of gentamicin sulfate and 45 µg of clindamycin to other methods of prophylaxis against acute posttraumatic bacterial endophthalmitis. Our study was terminated after the first interim analysis (5 years after launch of the study, during which 346 eyes were enrolled) disclosed a significant difference in favor of antibiotic injection. The odds ratio of developing posttraumatic endophthalmitis in the control group was 8.93 (95% CI, 1.11-71.93) times higher than treated eyes. There was significant association between presence of an IOFB and development of endophthalmitis such that the benefit of treatment was observed only in eyes with an IOFB. However, in eyes without an IOFB, the rate of endophthalmitis was similar in cases and controls.
Intraocular injection bypasses the blood-ocular barrier and appears to be the most effective method of achieving high intraocular antibiotic concentrations. Theoretically, the selected prophylactic antibiotic regimen should provide adequate coverage against both gram-positive and gram-negative organisms. Clindamycin has a mode of action similar to vancomycin hydrochloride and a good spectrum of activity against gram-positive bacteria.2, 14-15 Gentamicin has a broad-spectrum bactericidal activity, which is effective against Staphylococcus aureus and aerobic gram-negative bacilli. Its bactericidal ability against gram-positive pathogens in higher concentrations is advantageous. In an animal study, 10 µg/mL of clindamycin and 8 µg/mL of gentamicin sulfate in the infusion fluid was shown to be nontoxic in rabbit eyes and significantly reduced colony-forming units of S aureus after vitrectomy.16 We used 40 µg and 45 µg of clindamycin because the vitreous volume in average human eyes is almost 5 times that of rabbit eyes. Furthermore, both gentamicin and clindamycin have shown a postantibiotic effect on S aureus (inhibition of bacterial regrowth after decline of antibiotic concentration below minimum inhibitory concentration levels).17
In addition to antibiotic concentration, time-dependent bactericidal activity is also another important factor to be considered in the selection of intraocular antibiotics. The half-life of clindamycin is 3 hours in noninflamed phakic eyes.18 The half-life of gentamicin is 14 hours in aphakic, infected, nonvitrectomized rabbit eyes.19 Therefore, one may assume that after intravitreal injection of these antibiotics, exposure time to bacteria is longer than the required duration shown in an in vitro study.20
Because of the high reported incidence of Bacillus endophthalmitis following penetrating trauma, a broad-spectrum antibiotic regimen covering this species should be used.2, 13 This fact, together with the earlier-mentioned reasons, led us to select a combination of gentamicin and clindamycin. These agents display a synergistic effect against both B cereus and S aureus.2, 13, 15 By adding 5 µg/mL of gentamicin sulfate, a 4-fold decrease in the minimum inhibitory concentration of clindamycin has been reported in 35 isolates of S aureus.21
Independent risk factors associated with acute posttraumatic bacterial endophthalmitis in our study were retained IOFB, presence of afferent pupillary defect, and vitreous prolapse. Factors reported to be associated with endophthalmitis in previous reports include a dirty wound, breach of the lens capsule, presence of an IOFB, delay in primary repair, and trauma in a rural setting.11, 14, 22-26 However, one report did not find the presence of an IOFB to be a risk factor for development of endophthalmitis.13
In this study, we did not culture intraocular fluids at the time of primary wound repair because our previous pilot study,1 as well as the experience of others, showed that positive culture results do not necessarily correlate with subsequent infection.22, 27 One study reported that 33% of aqueous culture samples in open-globe injuries were positive for microorganisms; however, none of the patients developed endophthalmitis.28 Another study reported that 26% of eyes with an IOFB had positive culture results with no evidence of endophthalmitis.29 Therefore, obtaining routine culture specimens in all cases of open-globe injuries does not seem to be necessary. We obtained intraocular specimens for microbiological study in all eyes with endophthalmitis. The rate of culture-positive endophthalmitis was 67% in our series and the most common isolated microorganisms were S epidermidis; however, Bacillus species were not isolated in our series. The rate of culture-negative posttraumatic endophthalmitis in the current study was 34%, which is within the 17% to 42% range reported by others.23, 26-27,30-32 These figures underscore the importance of the clinical diagnosis of endophthalmitis based on a high index of suspicion. Although this approach may increase the chance of including eyes with traumatic uveitis, it decreases the chance of missing some truly infected cases that are culture negative.
Published literature on posttraumatic endophthalmitis mostly contains case series, and in the absence of a large randomized clinical trial, the preferred method of prophylaxis remains unanswered. Animal models have demonstrated the efficacy of intravitreal antibiotics for prophylaxis of posttraumatic endophthalmitis.33-34 The results of our previously reported pilot study also revealed that all cases of acute posttraumatic bacterial endophthalmitis occurred in controls; however, the observed difference failed to reach statistical significance.1 A small, randomized trial using therapeutic (not prophylactic) doses of vancomycin and ceftazidime also reported the efficacy of such treatment in the prevention of posttraumatic endophthalmitis.35 To the best of our knowledge, the present study is the first large randomized clinical trial evaluating the effect of prophylactic intraocular antibiotic injection against posttraumatic endophthalmitis. Limitations to this study include the short follow-up period of 2 weeks, which limits the ability to detect any possible instances of late-onset and chronic endophthalmitis.
In summary, the results of this multicenter study provide strong evidence supporting the role of adjunct intraocular antibiotic injection at the time of primary repair in reducing the rate of acute posttraumatic bacterial endophthalmitis in open-globe injuries with retained IOFB. We did not observe any case of B cereus endophthalmitis; therefore, a broad-spectrum antibiotic regimen like that used in this study may not be necessary. Future studies should evaluate the role of safer new-generation intraocular antibiotics alone and as an adjunct to other methods of prophylaxis. Studies with longer follow-up are required to determine whether prophylactic intraocular antibiotic injection at the time of primary repair significantly reduces late-onset endophthalmitis following penetrating ocular injures.
AUTHOR INFORMATION
Correspondence: Masoud Soheilian, MD, Ophthalmology Department, Labbafinejad Medical Center, Boostan 9 Street, Pasdaran Avenue, Tehran 16666, Iran (masoud_soheilian{at}yahoo.com).
Submitted for Publication: February 12, 2006; final revision received July 4, 2006; accepted July 8, 2006.
Financial Disclosure: None reported.
Funding/Support: This study was supported by the Iranian National Research Center for Medical Sciences and the Ophthalmic Research Center, Shaheed Beheshti University of Medical Sciences, Tehran.
Previous Presentations: This study was presented in part at the American Academy of Ophthalmology Annual Meeting; October 17, 2005; Chicago, Ill, and at the Cannes Retina Festival; September 13, 2006; Cannes, France.
Additional Information: The eFigure is available.
Acknowledgment: We thank the enrolled patients who agreed to be hospitalized for 15 days and randomly assigned to treatment for the benefit of future patients. We would also like to thank colleagues who supported this study by referring patients.
| Members of the Traumatic Endophthalmitis Trial (TET) Research Group, July 1999 to December 2004
Clinical centers and personnel who contributed data for TET patients.
Clinical Centers. Number of enrolled patients is given in parentheses after the center location. Personnel listed are principal investigators and other personnel who performed examinations or procedures for patients in this trial by the end of December 30, 2004.
Labbafinejad Medical Center, Tehran, Iran (110): principal investigators, Masoud Soheilian, MD, Nasrin Rafati, MD; coinvestigators, Shahin Yazdani, MD, Jamil Eslamipour, MD, Hamid Ahmadieh, MD, Mohsen Azarmina, MD, Mohammad H. Dehghan, MD, Siamak Moradian, MD, Maryam Aletaha, MD, Arash Anisian, MD, Bahram Rahmani, MD; Farabi Eye Hospital, Tehran (177): principal investigator, Houshang Faghihi Habibabady, MD; coinvestigators, Niloofar Piri, MD, Mehdi Nili, MD, Morteza Movasat, MD; Sina General Hospital, Ahwaz, Iran (30): principal investigator, Mostafa Feghhi, MD; coinvestigators, Hassan Akbari, MD, Fereydoun Farrahi, MD, Foad Haghi, MD, Ali Kasiri, MD; Alzahra Hospital, Zahedan, Iran (29): principal investigator, Hossein A. Shahriary, MD, coinvestigators, Alireza Khataeei, MD, Alireza Maleki, MD.
Consultant for the TET. Gholam A. Peyman, MD
Coordinating Center and Writing Committee. Ophthalmic Research Center, Labbafinejad Medical Center, Shaheed Beheshti University of Medical Sciences: Masoud Soheilian, MD, Nasrin Rafati, MD, Mohammad R. Mohebbi, PhD, Shahin Yazdani, MD.
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Author Affiliations: Department of Ophthalmology and Ophthalmic Research Center, Labbafinejad Medical Center, Shaheed Beheshti University of Medical Sciences (Drs Soheilian, Rafati, Mohebbi, Yazdani, and Eslamipour), Negah Eye Hospital (Drs Soheilian, Rafati, and Yazdani), and Department of Ophthalmology, Farabi Eye Hospital, Tehran University of Medical Sciences (Drs Faghihi Habibabadi and Piri), Tehran, Iran; Department of Ophthalmology, Sina General Hospital, Ahwaz University of Medical Sciences, Ahwaz, Iran (Dr Feghhi); Department of Ophthalmology, Alzahra Hospital, Zahedan University of Medical Sciences, Zahedan, Iran (Dr Shahriary); and Department of Ophthalmology, Tulane Health Science Center, New Orleans, La (Dr Peyman).
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