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Risk Factors for Recurrence of Postoperative Trichiasis
Implications for Trachoma Blindness Prevention
Hui Zhang, MS;
Ram P. Kandel, MPH;
Bassant Sharma, MD;
Deborah Dean, MD, MPH
Arch Ophthalmol. 2004;122:511-516.
ABSTRACT
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Background Trachoma is the leading worldwide cause of preventable blindness. Surgery can alleviate trachomatous trichiasis (TT), the blinding sequelae of trachoma, but recurrence rates are high.
Objective To investigate risk factors for TT recurrence.
Methods We conducted a prospective case-control cohort study in Nepal that included patients with TT who were undergoing bilamellar tarsal-rotation surgery and control subjects who have scarring but no TT. Conjunctivae were graded for trachoma and swabbed to detect Chlamydia trachomatis by in-house and commercial (Roche Amplicor; Roche Diagnostics Corp, Indianapolis, Ind)–polymerase chain reaction. Univariate and multivariate analyses were performed for associations with chlamydiae and other risk factors.
Results Postoperative TT recurrence rates were 11.1% (4 cases) at 6 months and 25.0% (11 cases) at 12 months while no controls developed TT. Significantly, 5 (45.5%) of 11 patients with TT recurrences at 12 months had chlamydial infection at baseline (odds ratio, 6.0; 95% confidence interval, 1.5-24.3; P = .01), 8 (72.7%) at 6 months (odds ratio, 28; 95% confidence interval, 4.3-181.0; P <.001), and 9 (81.8%) at 12 months (odds ratio, 48; 95% confidence interval, 7.5-302.6; P = .00). No controls were infected during this time. Active trachoma and the baseline number of eyelashes touching the globe were also risk factors for TT recurrence.
Main Outcome Measures The outcome variable was TT recurrence at 6 and 12 months.
Conclusion To our knowledge, this is the first study to demonstrate that chlamydial infection at the time of surgery and at follow-up is a significant risk factor for postoperative TT recurrence.
INTRODUCTION
Of the 38 million individuals who are blind in the world today, an estimated 7 to 9 million (approximately 18%-24%) are blind because of trachoma,1-2 a leading cause of preventable blindness. An additional 11 million have a complication of trachoma referred to as trachomatous trichiasis (TT), that is, 1 or more eyelashes touching the globe or evidence of epilation.1, 3 Trachomatous trichiasis presents an immediate risk of blindness due to abrasion of the cornea, which frequently results in bacterial superinfection and healing by scar formation with the inevitable consequence of corneal opacification.4-5 While the prevalence of trachoma has decreased in most of the developed world, the burden of blindness falls disproportionately in the developing world, where poverty, poor hygiene, and poor sanitation remain problematic.
Trachoma is a chronic ocular disease caused by the obligate intracellular bacterium Chlamydia trachomatis.6 Persistent or repeated childhood infection can lead to conjunctival scarring that occurs as early as 5 years of age and can progress to more severe scarring and TT within 10 to 40 years.7 In hyperendemic areas where clinical disease and infection rates are high (30%-50%), 8% to 17.5% of the population may have TT.8-11 The World Health Organization (WHO) has initiated the Global Elimination of Blinding Trachoma by 2020, which calls for implementation of the SAFE strategy.12 The SAFE strategy encompasses 4 different arms of treatment and prevention of disease: (1) Surgery to prevent blindness in those who have trichiasis and/or entropion. (2) Antibiotics (tetracycline ointment or azithromycin for active trachoma) to combat active chlamydial infection. (3) Facial cleanliness. (4) Environmental improvement.
Surgery is the most effective and direct means of treating TT. Many surgical techniques have been used including cryoablation, electroepilation, eversion splinting, tarsal advance, tarsal grooving, tarsal advance and rotation, and bilamellar tarsal rotation.13-14 A randomized control trial in 1990 showed that the bilamellar tarsal-rotation procedure was superior to other treatment methods because it had the lowest recurrence rate regardless of coexisting eyelid closure defect, previous surgery, severity of trichiasis preoperatively, and the skill of the surgeon.13 It was also technically simpler and quicker than the tarsal advance and rotation method.13 Hence, the bilamellar tarsal-rotation procedure was recommended by WHO for TT surgery.15 However, TT recurrence has been reported with all surgical techniques and has been observed from as early as 1 year to as late as 11 years following the initial surgery.8, 14, 16-18
The high rates of TT recurrence, up to 75%16 in many trachoma-endemic countries worldwide, suggest that underlying environmental risk factors might contribute to disease progression. Patients with TT reside in communities where reinfection is possible from household contacts or contact with infected children. To our knowledge, the association between chlamydial infection at the time of surgery and TT recurrence has not been studied. A significant correlation between infection and recurrence would support the need for antibiotic therapy at the time of surgery to reduce and possibly to prevent TT recurrence. Our study sought to evaluate whether infection with C trachomatis and other clinical factors at the time of surgery and at 6- and 12-month follow-ups would predict TT recurrence.
METHODS
STUDY POPULATION AND SELECTION OF CASES AND CONTROLS
This was a prospective case-control cohort study designed to evaluate risk factors for postoperative TT recurrence. The study was approved by the Nepal Netra Jhoti Sangh (Nepali government prevention of blindness program), Kathmandu, and the institutional review board of Children's Hospital Oakland Research Institute, Oakland, Calif.
A survey was conducted in the trachoma-endemic Kapilvastu District of the Lumbini Zone in Nepal to grade trachoma and identify cases of TT. After obtaining informed consent, research staff enumerated and clinically examined all household members. Trachoma was graded using the modified grading scale according to WHO guidelines19 by the same ophthalmologist at all time points as follows: follicular trachomatous inflammation (TF) (ie, the presence of  5 follicles 0.5 mm in diameter on the central upper tarsal conjunctiva); intense trachomatous inflammation (TI) (inflammatory thickening of upper tarsal conjunctiva with obstruction of >50% of the vessels); trachomatous conjunctival scarring (TS) (ie, the presence of easily visible scarring in upper tarsus); TT (the presence of 1 eyelash touching the globe or evidence of epilation); and corneal opacity (the presence of visible central corneal opacity sufficiently dense to obscure the papillary margin). To classify the degree of TS, individuals were graded as having C1 for mild scarring, C2 for moderate scarring, or C3 for severe scarring.2 Patients were considered to have active trachoma if there was evidence of TF and/or intense TI.
Cases were defined as patients with individual eyelids having a trachoma grade of TT. Cases were matched by age and sex to controls, defined as those with conjunctival scarring without evidence of TT who resided in the same village. Visual acuity was assessed using a standard Snellen "E" chart measured at 6 m and categorized using WHO definitions of visual impairment and blindness. Cases and controls were examined at baseline and again at 6- and 12-month follow-ups for TT recurrence in the operated on eye or for development of TT in an unoperated on eye, respectively. Patients with TT were offered free corrective eyelid surgery, which occurred at baseline.
CONJUNCTIVAL SAMPLE COLLECTION
To determine C trachomatis infection rates for both cases and controls, upper tarsal conjunctival swabs were collected at baseline and at 6 and 12 months. Swabs were placed in collection media (M4-RT; Micro-Test, Lilburn, Ga) and labeled with a date and a unique identification number. Specimens were maintained at –20°C before transport to the laboratory where they were stored at –80°C until processed. Cases and controls with evidence of active trachoma were treated with topical tetracycline according to WHO recommendations2 after obtaining the swab, although treatment was not observed. Sterile technique, including the use of a new set of surgical gloves for each case of TT, was performed to prevent cross-contamination of C trachomatis infection among patients. For controls, hands were washed with soap and water in between each examination.
TRICHIASIS SURGERY
The bilamellar tarsal-rotation procedure was performed on all case of minor ( 5 eyelashes touching the globe) and major (>5 eyelashes touching the globe) TT at baseline as recommended by WHO,15 including patients with TT with evidence of self-epilation. Each patient was reexamined postoperatively and at 6 and 12 months. Any surgical complications were noted.
DETECTION OF C trachomatis INFECTION
All samples were processed according to the commercial (Roche Amplicor)–polymerase chain reaction (PCR) kit instructions (Roche Diagnostics Corp, Indianapolis, Ind) to detect C trachomatis in a masked fashion. The colorimetric assay contained positive and negative controls for each 96-well plate; a 96-well internal control plate was processed in parallel with patient and control samples. The internal control plate served to identify inhibitors for PCR. When inhibitors were present, DNA was extracted from the original sample and amplified using an in-house PCR protocol as described previously.20 The final determination of a positive or negative Roche Amplicor-PCR result was based on the results of the computerized plate reader in comparison with positive and negative control readings as well as with the respective internal control plate according to the package insert. To validate Roche Amplicor–PCR results, all equivocal and positive samples were subjected to in-house PCR testing. Samples were considered positive by the in-house PCR when the product was the correct molecular weight in comparison with positive controls (and where negative control samples were negative) as determined by electrophoresis on a 2% agarose gel stained with ethidium bromide.20 Reinfection was defined as confirmed infection at 2 different time points where an intervening sample was negative. Persistent infection was defined as positive infections at 2 or more consecutive time points.
DATA ANALYSIS
The outcome variable was the TT recurrence rate at 6 and 12 months as measured by 1 or more eyelashes touching the globe after surgery. The explanatory variable was C trachomatis infection status at each time point as measured by Roche Amplicor–PCR and in-house PCR results. Univariate and multivariate analyses were performed using Stata software (version 7.0; Stata Corp, College Station, Tex). To maintain patient confidentiality, only the patient's individual identification number was used in the analyses. Contingency table analysis was performed to examine crude associations and  2 test or the Fisher exact test was used to determine significance. Multiple regressions were performed where the change in the  coefficient exceeded 10%. Patients with TT who were operated on and who had or did not experience a recurrence for chlamydial infection were compared, and the association of TT recurrence with the number of eyelashes touching the globe at the time of surgery, the degree of TS, and the presence of active trachoma at the time of surgery were analyzed. Cluster analysis was performed to compare exposure to infected household members for TT cases and controls as previously described.21-22
RESULTS
DEMOGRAPHICS OF THE COHORT
Seventy-nine subjects were enrolled in the study; 53 (67.1%) had TT with 1 eyelid operated on at baseline except for 1 patient who had bilateral surgery. One patient with TT could not be operated on owing to alcohol intoxication at the scheduled time of surgery. The sample size for analysis, therefore, consisted of 78 subjects with 79 eyelids (Table 1). All subjects from the community who had TT were enrolled in the study, and only 26 controls in the same community were available for age- and sex-matching with the cases. Of the patients with TT, 20 eyelids (25.3%) had minor TT and 23 eyelids (29.1%) had major TT at the time of surgery. Only 2 of the patients in the control group had active trachoma, both were graded as having TF.
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Table 1. Characteristics of the Study Cohort at Baseline*
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CHLAMYDIAL INFECTION AND TT RECURRENCE
Of the samples that were positive by the Roche Amplicor–PCR test and by in-house PCR testing, all were of the correct molecular weight compared with positive control samples on agarose gels. One sample contained an inhibitor and tested negative by in-house PCR. The baseline infection rate of the patients with TT was 24.5% (13/53); at 6 and 12 months the rates of TT were 27.8% (10/36) and 27.3% (12/44), respectively (Table 2); all controls tested negative for chlamydial infection at baseline and at 6 and 12 months. Cluster analysis of 171 (99.4%) of 172 household members of the cases and controls demonstrated no difference for exposure to infected household individuals for those patients with TT who were operated on compared with controls. The average household size was 5 for cases and 5 for controls with similar numbers of infected individuals among the households. There was no household with only 1 individual. No statistical difference was noted in the number of preschool children for households with cases compared with households for controls. Infection for household members was assayed exactly as described earlier; 26% were infected; there were no inhibitors detected for these samples.
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Table 2. Infection Status and Trachomatous Trichiasis (TT) Recurrence and Occurrence
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There were no surgical complications. All cases of TT recurrence were minor (5 eyelashes touching the globe); none of the controls developed TT during the 12-month period. At the 6-month follow-up, there were 4 cases of TT recurrence, constituting an incidence rate of 11.1%. Three of the 4 cases had moderate scarring (TS C2) and 1 had mild scarring (TS C1) at baseline. At the 12-month follow-up, there were 11 cases of TT recurrence with a cumulative incidence rate of 25.0%. Seven (63.6%) of these 11 were new cases, giving an incidence rate of 15.9%. While most controls had mild to moderate scarring (TS C1–TT C2) at baseline, 7 of the 11 recurrent cases had moderate to severe scarring (TS C2–TT C3) at 12 months.
Controlling for age and sex, univariate and multiple regression analysis showed that infection with C trachomatis was associated with TT recurrence at 6 and 12 months (Table 3). Of the 4 cases of TT recurrence at the 6-month follow-up, 2 patients (50%) were infected with C trachomatis at baseline (P = .15), but all 4 patients (100%) were infected at 6 months (P = .001). Of the 11 cases of TT recurrence at the 12-month follow-up, 6 patients (54.5%) were infected with C trachomatis at baseline (P = .02), 8 patients (72.7%) were infected at 6 months (P <.001), and 9 patients (81.8%) were infected at 12 months (P <.001). An additional 2 test was performed to verify that those without follow-up resembled those at follow-up by sex, age, and infection status at baseline. We found that there were no significant statistical differences between the 2 groups.
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Table 3. Association of Infection With Postoperative Recurrence of Trachomatous Trichiasis (TT)*
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Persistent infection was also significantly associated with TT recurrence at 12 months (Table 3). Six of the 9 cases of TT recurrence who were positive for infection at 12 months were also previously infected at 6 months, and 4 of these 6 patients had infection at all 3 time points (P = .03 and P <.001, Fisher exact test, respectively). While we did not sample for infection in between the follow-up time points of 6 and 12 months and, thus, cannot rule out reinfection, it is possible that these cases represent persistent infection. Odds ratio for association of TT recurrence with infection was statistically significant at 6 and 12 months (Table 4).
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Table 4. Odds Ratio (OR) for the Association of Infection With Postoperative Recurrence of Trachomatous Trichiasis (TT)
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CLINICAL RISK FACTORS FOR RECURRENCE OF TT
Multiple regression showed that the number of eyelashes touching the globe at the time of surgery and the presence of an active trachoma infection at 6 months were also risk factors of TT recurrence (Table 5). While active trachoma (TF/TI) at the time of surgery (baseline) was not predictive of TT recurrence, TF at 6 months was predictive of recurrence at 12 months (P = .011) and intense trachomatous inflammation was predictive of recurrence at 6 and 12 months (P = .011 and P = .004, respectively). Visual impairment, TS, and corneal opacity were not predictive of TT recurrence at 6 or 12 months.
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Table 5. Clinical Risk Factors for Postoperative Recurrence of Trachomatous Trichiasis (TT)*
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COMMENT
We know of no previous studies on the association of C trachomatis infection with TT recurrence following surgery. Our study found infection was a significant risk factor for postoperative TT recurrence. Recurrence has been well documented following surgery, but the rates tend to vary depending on the type of surgery, duration of follow-up, and country where the surgery was performed. The bilamellar tarsal-rotation technique is considered to be the most effective operative procedure with the lowest recurrence rates compared with tarsal advance, electrolysis, and cryoablation.14 In Oman, TT recurrence rates were reported to be 20% to 23% for the tarsal rotation technique compared with 71% for electrolysis and 82% for cryoablation at 2 years.14 In Gambia, 63 operated on eyes (55%) had recurrence at 10 years after tarsal rotation surgery.23 Similarly, Mali reported TT recurrence in 50 cases (75%) after 11 years.16 Recently, a study in Oman reported TT recurrence in 181 cases (61.8%) and 157 cases (50.6%) following tarsal rotation and electroepilation, respectively, over a follow-up period ranging from 1 to 4 years.8 Our study, reports a TT recurrence rate of 11.1% at 6 months and a cumulative rate of 25.0% at 12 months. Our finding of a significant association of C trachomatis infection with increasing rates of TT recurrence over time provides one explanation for the observed recurrence rates noted in this and the aforementioned studies.
We found excellent correlation between infection and active trachoma, which is consistent with the theory that active trachoma may be a marker for chlamydial infection.11 Munoz et al11 found that while one third of the women with TF and 37% to 44% of those with intense trachomatous inflammation had evidence for chlamydial infection, the rate of infection in women without active trachoma was low—4% to 5%. Another study found that 52.9% of those with TF and 77.0% of those with intense trachomatous inflammation were positive for infection by direct fluorescent antibody cytology.24
Active trachoma at baseline and at 6 months correlated with the incidence of TT at each time point in our study, but only active trachoma at 6 months was predictive of TT recurrence at 12 months. These findings are supported by a study in Tanzania where, after controlling for age, the presence of active trachoma among a cohort of women with TS was a significant predictor of the 7-year incidence of TT.11 In contrast, a study in Gambia found that active trachoma was not associated with TT recurrence at a median of 10 years after tarsal rotation surgery.23 It is possible that while active trachoma correlates with the prevalence and incidence of TT, once TT develops, 1 episode of active trachoma becomes less important in recurrence. However, with ongoing or repeated episodes, which could indicate reinfection or persistence of infection, active trachoma might become an important component of TT recurrence. Additionally, topical treatment may not be sufficient to interrupt this cycle. We found cases of reinfection and persistence despite topical tetracycline treatment of active trachoma, which is consistent with previous studies where reemergence of infection was noted within 4 weeks of completion of topical treatment.25-26 Thus, it will be valuable to conduct prospective studies that address the issue of whether specific prevalence rates of active trachoma correlate with both infection and higher rates of TT recurrence.
Herein, the significant association between infection and TT at baseline suggests that infection is important for development of TT. We have also demonstrated that reinfection or persistent infection is a risk factor for TT recurrence after surgery. Repeated infection has been shown to be important in the development of trachomatous scarring27 and, therefore, the development of TT. Infection has also been shown to be significantly associated with the incidence of TT among women with scarring.11 The concurrent presence of TS and exposure to chlamydiae may predispose patients to reinfection and, therefore, progressive scarring.
Although none of the controls in this study had infection during the 12 months of the study, they did have considerable TS, which reflects prior infection. Only 2 of the controls had active trachoma, which is consistent with a lack of active infection in this group as demonstrated by our PCR test results. Based on cluster analysis, both TT cases and controls had equal exposure to infected household members, which strongly suggests that reinfection or persistent infection in our population is linked with the pathogenesis of disease progression.
Loss to follow-up is a limitation of prospective cohort studies and we encountered the same dilemma, especially at the 6-month follow-up. Presumably, patients who were doing well and free of postoperative TT recurrence were more likely not to return for follow-up evaluation. However, 8 of those lost to follow-up at 6 months were seen again at 12 months, providing data at both baseline and 12 months. Our follow-up data at 12 months was 83% for TT cases and 100% for controls. Since we had sufficient numbers and statistical significance at 12 months and since the association between infection and TT recurrence was consistent at 6 and 12 months, this likely indicates that our findings are valid for both time points.
The TT recurrence in our study was in the minor category, and likely due to the short follow-up of 6 and 12 months. Other studies have found that the development of major TT after surgery increases with the time to follow-up.8, 14, 18 For example, for cases who underwent tarsal-rotation surgery in Oman, the rate of major recurrence increased from 15.4% at 1 to 2 years to 25.5% at 4 years.8 In Tanzania, the recurrence rate increased from 19% at 24 months to 21% at 36 months after tarsal-rotation surgery.18 We would, therefore, expect major TT recurrence to develop with time along with an increase in the overall rate of minor and major recurrence.
The number of eyelashes touching the globe at baseline was a risk factor for recurrence at 12 months but not at 6. This may be due to the short duration of follow-up at 6 months. With shorter follow-ups, patients have less opportunity to become reinfected or to have progressive scarring that could result in recurrence. Further, those with major TT at the time of surgery would be more likely to have recurrence than those with minor TT as the underlying fibrosis may be more advanced. Since most of our TT cases at baseline had moderate to severe TS (TS C2-C3), it is not surprising that the number of eyelashes at baseline predicted recurrence at 12 months. Further, since there was no TT recurrence among those patients who had evidence of epilation at baseline, it is likely that there were even more cases of recurrence than what was observed because patients who had epilated in the past may also have been more likely to epilate after surgery if they developed recurrence.
Although we had sufficient sample size for analyses in this study, larger prospective studies are required in other trachoma-endemic countries to substantiate our findings. Our results are important within the context of the SAFE strategy as they suggest the need for integration of surgery and antibiotic use to potentially prevent postoperative TT recurrence. Research on azithromycin or other treatment modalities at the time of surgery and at other postoperative time points should be conducted to determine the most effective regimen for reducing TT recurrence.
AUTHOR INFORMATION
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Corresponding author and reprints: Deborah Dean, MD, MPH, University of California at San Francisco School of Medicine, Children's Hospital Oakland Research Institute, 5700 Martin Luther King Jr Way, Oakland, CA 94609 (e-mail: ddean{at}chori.org).
Submitted for publication May 13, 2003; final revision received November 19, 2003; accepted November 19, 2003.
This study was supported by a fellowship from Fight for Sight, New York, NY (Ms Zhang); grant ITI 01-040 from the International Trachoma Initiative, New York, NY (Dr Dean); and Public Health Service grant EY/AI12219 from the National Eye Institute, National Institutes of Health, Bethesda, Md (Dr Dean).
We extend our deepest gratitude to the people of the Kapilvastu District of the Lumbini Zone, without whom this research would not be possible. We also thank the Director of Lumbini Rana-Ambika Eye Hospital, Amar Deuja, MD, for his tremendous assistance and support in conducting the fieldwork.
From the Children's Hospital Oakland Research Institute, Oakland, Calif (Ms Zhang and Dr Dean); Lumbini Rana-Ambika Eye Hospital, Bhairahawa, Nepal (Mr Kandel and Dr Sharma); and the Department of Medicine, University of California at San Francisco School of Medicine (Dr Dean). The authors have no relevant financial interest in this article.
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