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CLINICAL SCIENCE
Direct fluorescent antibody assay and polymerase chain reaction for the detection of Chlamydia trachomatis in patients with vernal keratoconjunctivitis
Maria Cristina Nishiwaki-DantasI, Mariza Toledo de AbreuII, Cynthia Mendonça de MeloI, Ivana Lopes RomeroI, Rubens Belfort Matos NetoII, Paulo Elias Correa DantasI,III,
Corresponding author
pauloecdantas@uol.com.br

Tel.: 55 11 21767225
I Department of Ophthalmology, Corneal and External Disease Service, Santa Casa of São Paulo, Brazil.
II Department of Ophthalmology, Federal University of São Paulo, Brazil.
III Sorocaba Eye Hospital.
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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="cesec10" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle60">INTRODUCTION</span><p id="para10" class="elsevierStylePara elsevierViewall">Vernal keratoconjunctivitis &#40;VKC&#41; is a chronic ocular allergy characterized by itching and conjunctival hyperemia with papillary hypertrophy of the upper palpebral or tarsal conjunctiva and&#47;or limbus&#46; It is frequently associated with corneal involvement&#46;<a class="elsevierStyleCrossRefs" href="#bib1">1&#8211;3</a></p><p id="para20" class="elsevierStylePara elsevierViewall">Trachoma is a chronic follicular keratoconjunctivitis characterized by the presence of follicles in the upper palpebral conjunctiva and limbus&#46; Mucous discharge may be present&#44; along with itching&#44; which is less intense than that experienced in VKC&#46; Follicular necrosis and subconjunctival inflammation may lead to conjunctival scars&#44; Arlt&#39;s lines and Herbert&#39;s pits&#44; which are pathognomonic features of trachoma&#46; Palpebral and secondary corneal involvement may also be present&#46;</p><p id="para30" class="elsevierStylePara elsevierViewall">Transmission occurs by direct eye-to-eye and hand-to-eye contact&#44; usually by contaminated ocular discharge&#44; clothes&#44; bed sheets&#44; towels and the proliferation of flies in homes and schools&#46;<a class="elsevierStyleCrossRefs" href="#bib4">4&#44;5</a></p><p id="para40" class="elsevierStylePara elsevierViewall">The diagnosis of both VKC and trachoma is essentially clinical&#46; With trachoma&#44; especially in endemic areas and in chronic and cicatricial trachoma&#44; clinical diagnosis is straightforward&#46; However&#44; in the early stages of the infection&#44; due to its relatively benign and asymptomatic course&#44; it may not be easily differentiated from viral&#44; bacterial&#44; or allergic conjunctivitis&#46; In these cases&#44; laboratory tests become essential&#44; especially direct fluorescent antibody assays &#40;DFAs&#41;&#46;<a class="elsevierStyleCrossRefs" href="#bib6">6&#44;7</a></p><p id="para50" class="elsevierStylePara elsevierViewall">DFAs are easily performed but require adequate transportation and storage of the samples in a refrigerator&#44; a fluorescent microscope&#44; and well-trained personnel&#46;</p><p id="para60" class="elsevierStylePara elsevierViewall">Polymerase chain reaction &#40;PCR&#41; has been suggested to test for <span class="elsevierStyleItalic">Chlamydia trachomatis</span> that has both the specificity of cell culture and a level of sensitivity similar to that of DFA&#46; PCR is an in vitro method for detecting DNA sequences by enzymatic amplification of a specific fragment that can synthesize more than one million copies of one DNA sequence in a short period of time&#46;</p><p id="para70" class="elsevierStylePara elsevierViewall">VKC and trachoma share many features&#46; They both affect school-age children and young adults in hot&#44; dry climate areas&#46; They are characterized by chronic keratoconjunctivitis&#44; usually bilateral&#44; that waxes and wanes throughout the year&#46;<a class="elsevierStyleCrossRefs" href="#bib8">8&#44;9</a> One key difference is that whereas VKC stimulates a papillary reaction of the conjunctiva&#44; trachoma stimulates a follicular response&#46; However&#44; following the early follicular hypertrophy of trachoma &#40;phase TF&#41;&#44; a papillary reaction &#40;phase TI&#41; may cover the follicles&#46; Also&#44; follicles and papillae may coexist&#46; In these cases&#44; giant papillae would be dominant and would obscure the follicles&#46; Limbal follicles may also be obscured by the characteristic papillae and edema of limbal VKC&#46; In this phase&#44; we believe that many cases of trachoma may not be getting clinically diagnosed&#44; especially in the presence of a common comorbid papillary disease such as VKC&#46;</p><p id="para80" class="elsevierStylePara elsevierViewall">V&#233;rin et al&#46; first described a possible association between VKC and trachoma in 1980&#46;<a class="elsevierStyleCrossRef" href="#bib8">8</a> Later&#44; in 1988&#44; Friedlaender &#38; Cameron presented four cases of possible association&#46;<a class="elsevierStyleCrossRef" href="#bib3">3</a> One year later&#44; V&#233;rin et al&#46; &#40;1989&#41; described 8 &#40;23&#46;5&#37;&#41; cases of <span class="elsevierStyleItalic">Chlamydia trachomatis</span> infection confirmed the Wang and Grayston technique in 34 patients with VKC&#46;<a class="elsevierStyleCrossRef" href="#bib9">9</a></p><p id="para90" class="elsevierStylePara elsevierViewall">The possible association between VKC and trachoma was not addressed again until 2000&#44; when Melo et al&#46; studied 72 patients with allergic conjunctivitis&#44; 38 &#40;52&#46;8&#37;&#41; of whom had a positive DFA for <span class="elsevierStyleItalic">Chlamydia trachomatis</span>&#46;<a class="elsevierStyleCrossRef" href="#bib10">10</a> In that study&#44; the control group &#40;60 patients&#41; did not have any positive DFAs&#46; Statistical analysis identified a significant association between the diseases&#46;</p><p id="para100" class="elsevierStylePara elsevierViewall">The purpose of this study was to use PCR and DFA to detect the presence of <span class="elsevierStyleItalic">Chlamydia trachomatis</span> in patients with VKC compared with a control group and also to compare the efficacies of both tests for detecting <span class="elsevierStyleItalic">Chlamydia trachomatis</span> in patients with VKC&#46;</p></span><span id="cesec20" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle70">MATERIALS AND METHODS</span><p id="para110" class="elsevierStylePara elsevierViewall">One hundred seventy-seven patients were divided into two groups&#46;</p><p id="para120" class="elsevierStylePara elsevierViewall">Group A consisted of 87 patients with VKC from the Ocular Allergy Service of the Department of Ophthalmology&#46; Patients using topical or systemic antibiotics were excluded&#46; Patients were diagnosed with VKC using the following criteria&#58; a clinical history of chronic bilateral conjunctivitis &#40;at least one year&#41; with seasonal exacerbations &#40;i&#46;e&#46;&#44; itching&#44; photophobia&#44; and foreign body sensation&#41;&#59; hypertrophic papillae at the superior palpebral conjunctiva and&#47;or limbus&#59; and&#44; eventually&#44; Horner-Trantas dots&#44; superficial punctate keratitis and shield ulcers or corneal scars from shield ulcers&#46;</p><p id="para130" class="elsevierStylePara elsevierViewall">Group B &#40;the control group&#41; consisted of 90 patients who presented for regular eye examinations &#40;refractometry&#41; and were neither complaining of allergic conjunctivitis nor taking topical or systemic antibiotics&#46;</p><p id="para140" class="elsevierStylePara elsevierViewall">All patients in groups A and B were informed of the purpose of the study&#44; and all patients signed an informed consent&#46; The institutional review ethical committee approved this study&#46;</p><p id="para150" class="elsevierStylePara elsevierViewall">Patients were asked about their disease length&#44; symptoms&#44; and familial and personal histories of atopy and other ocular diseases&#46;</p><p id="para160" class="elsevierStylePara elsevierViewall">The symptoms assessed included itching&#44; tearing&#44; photophobia&#44; discharge&#44; and reduced visual acuity&#46;</p><p id="para170" class="elsevierStylePara elsevierViewall">The following components were included in the examination&#58; a measurement of visual acuity&#59; slit lamp biomicroscopy to evaluate conjunctival hyperemia&#59; a test for the presence of papillae at the conjunctiva and&#47;or limbus and other conjunctival&#44; limbal&#44; and corneal alterations &#40;follicles and scars&#41;&#59; tonometry&#59; and a fundus examination&#46; All patients were examined by the same doctor&#46;</p><p id="para180" class="elsevierStylePara elsevierViewall">All patients underwent tissue sampling for the detection of <span class="elsevierStyleItalic">Chlamydia trachomatis</span> by DFA&#46; The superior palpebral conjunctiva of the right eye was scraped five times with a Kimura spatula&#46; The sample was then placed in a demarcated circle on the appropriate slide&#44; dried for 5 minutes&#44; fixed with absolute methanol and stained with the fluorescent monoclonal antibody &#40;Microtrak-SyvaTM&#41;&#46; After 30 minutes of incubation in a moist chamber at room temperature&#44; the slides were washed with distilled water and were left to dry again&#46; The samples were examined by an experienced technician under immersion fluorescent microscopy with epi-illumination at 1000X magnification&#46; The material was considered adequate when it included at least 100 epithelial cells per field&#46; The criterion for a positive diagnosis was the presence of five or more elementary bodies per sample&#46;</p><p id="para190" class="elsevierStylePara elsevierViewall">The PCR was calibrated by obtaining a positive control from a patient who had no allergic conjunctivitis and a clinical diagnosis of trachoma&#44; which was confirmed by a positive DFA for <span class="elsevierStyleItalic">Chlamydia trachomatis&#46;</span> The negative control was obtained from a patient who presented with no signs or symptoms of either trachoma or allergic conjunctivitis and had a negative DFA for <span class="elsevierStyleItalic">Chlamydia trachomatis</span>&#46; The positive and negative controls were obtained to accurately calibrate the PCR for the detection of <span class="elsevierStyleItalic">Chlamydia trachomatis&#46;</span></p><p id="para200" class="elsevierStylePara elsevierViewall">All patients in groups A and B had the superior palpebral conjunctiva of their right eye scraped with a Dacron swab&#46; The part of the swab containing the collected material was placed in a plastic tube with the transportation medium&#46; Samples were taken immediately to a Molecular Biology laboratory within 4 hours after collection&#46; The material was processed according to the technique introduced by Bobo&#46;<a class="elsevierStyleCrossRef" href="#bib11">11</a></p><p id="para210" class="elsevierStylePara elsevierViewall">For each sample&#44; an initial PCR was performed to verify the presence of &#946;-human globin to avoid false negative results&#46; The primers had the following sequences&#58; <span class="elsevierStyleBold"><span class="elsevierStyleItalic">Primer</span> HGH1&#58; 5&#8242; &#8211; TGCCTTCCCAACCATTCCCTTA &#8211; 3&#8242; and <span class="elsevierStyleItalic">Primer</span> HGH2&#58; 5&#8242; &#8211; CCACTCACGGATTTCTGTTGTGTTTC &#8211; 3&#8242;</span>&#46; Detection of the fragment occurred at 420-bp long&#46;</p><p id="para220" class="elsevierStylePara elsevierViewall">In the samples in which &#946;-human globin was detected&#44; a second PCR was performed to detect and amplify a highly conserved region of the specific major outer membrane protein &#40;MOMP&#41; for <span class="elsevierStyleItalic">Chlamydia trachomatis</span>&#46; The sequences of the primers used to detect <span class="elsevierStyleItalic">Chlamydia trachomatis</span> follow&#58; <span class="elsevierStyleBold"><span class="elsevierStyleItalic">Primer</span> 1&#58; 5&#8242; - GAT AGC GAG CAC AAA GAG AGC TAA &#8211; 3&#8242;&#59; <span class="elsevierStyleItalic">Primer</span> 2&#58; 5&#8242; &#8211; TTC ACA TCT GTT TGC AAA ACA CGG TCG AAA ACA AAG &#8211; 3&#8242;&#59; <span class="elsevierStyleItalic">Primer</span> 3&#58; 5&#8242; - TCT GCT TCC TCC TTG CAA GCA AGT CTG CC &#8211; 3&#8242;&#59; and <span class="elsevierStyleItalic">Primer</span> 4&#58; 5&#8242; - CCA TAG TAA CCC ATA CGC ATG CTG &#8211; 3&#8242;&#46;</span></p><p id="para230" class="elsevierStylePara elsevierViewall">The amplified fragment was then examined by electrophoresis in agarose gel that was stained with ethidium bromide&#46; Detection of the fragment occurred at 151-bp long&#46;</p><p id="para240" class="elsevierStylePara elsevierViewall">Calculations of sensitivity and specificity were conducted&#44; and a receiver operating characteristic &#40;ROC&#41; curve was plotted to evaluate and compare the diagnostic capabilities of both laboratory tests&#46; Sensitivity&#44; specificity&#44; ROC curves&#44; and areas under the curve were calculated with the assumption that DFA is the gold standard for <span class="elsevierStyleItalic">Chlamydia</span> spp&#46; diagnosis&#46; ROC curves were plotted using a categorical variable with only two possible outcomes &#40;positive and negative&#41;&#44; which can lead to underestimation of the area under the curve&#46; MedCalc software version 9&#46;3&#46;7&#46;0 was used for all calculations&#46;</p><p id="para250" class="elsevierStylePara elsevierViewall">We certify that all applicable institutional and governmental regulations concerning the ethical use of human volunteers were followed during this research&#46;</p></span><span id="cesec30" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle80">RESULTS</span><span id="cesec40" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle90">Clinical evaluation</span><p id="para260" class="elsevierStylePara elsevierViewall">Group A consisted of 87 patients with VKC&#46; Patient ages in this group ranged from 2 to 23 years &#40;mean age &#61; 9&#46;6&#177;4&#46;8 years&#41;&#59; 74 patients &#40;73&#46;6&#37;&#41; were white&#44; and 23 &#40;26&#46;4&#37;&#41; were black&#59; 27 &#40;31&#46;0&#37;&#41; were female&#44; and 60 &#40;69&#46;0&#37;&#41; were male &#40;<a class="elsevierStyleCrossRef" href="#tbl1">Table 1</a>&#41;&#46;</p><elsevierMultimedia ident="tbl1"></elsevierMultimedia><p id="para270" class="elsevierStylePara elsevierViewall">Group B &#40;control group&#41; consisted of 90 patients&#46; Patient ages ranged from 2 to 23 years &#40;medium age &#61; 9&#46;0&#177;5&#46;0 years&#41;&#59; 45 patients &#40;50&#46;0&#37;&#41; were male&#44; and 45 &#40;50&#46;0&#37;&#41; female&#59; 68 patients &#40;75&#46;6&#37;&#41; were white&#44; and 22 &#40;24&#46;4&#37;&#41; were black &#40;<a class="elsevierStyleCrossRef" href="#tbl1">Table 1</a>&#41;&#46;</p><p id="para280" class="elsevierStylePara elsevierViewall">No statistical differences were identified between groups A and B based on either race &#40;&#967;<span class="elsevierStyleSup">2</span> &#61; 0&#44; <span class="elsevierStyleItalic">p</span> &#61; 1&#46;0&#41; or age &#40;<span class="elsevierStyleItalic">t</span> &#61; -0&#46;862&#59; <span class="elsevierStyleItalic">p</span> &#61; 0&#46;39&#41;&#46; The majority of VKC patients &#40;86&#46;2&#37;&#41; were less than 15 years old&#46; In group B&#44; 88&#46;9&#37; of the patients were under the age of 15&#46; Caucasians were predominant in both groups &#40;73&#46;6&#37; in group A and 75&#46;6&#37; in group B&#41;&#46;</p><p id="para290" class="elsevierStylePara elsevierViewall">In group A&#44; 69&#46;0&#37; of the patients were male&#44; and in group B&#44; 50&#46;0&#37; of the patients were male&#46; This difference between the groups was statistically significant &#40;&#967;<span class="elsevierStyleItalic"><span class="elsevierStyleSup">2</span></span> &#61; 5&#46;831&#44; <span class="elsevierStyleItalic">p</span> &#61; 0&#46;016&#41;&#46;</p><p id="para300" class="elsevierStylePara elsevierViewall">All patients in group A presented with itching and red eyes&#46; Symptoms of corneal involvement &#40;i&#46;e&#46;&#44; punctate keratitis&#44; superficial corneal opacities&#44; shield ulcer&#44; and peripheral neovascularization&#41; were identified in 15 patients &#40;17&#46;2&#37;&#41;&#46; Seventeen patients &#40;19&#46;5&#37;&#41; in group A &#40;i&#46;e&#46;&#44; patients with VKC&#41; had conjunctival and limbal scars &#40;i&#46;e&#46;&#44; scars in the upper tarsal conjunctiva and pits in the superior limbus&#41;&#44; both of which were suggestive of trachoma &#40;TS&#41;&#46; Follicles &#40;more than six&#41;&#44; suggesting follicular trachoma &#40;TF&#41;&#44; were identified in the upper tarsal conjunctiva in two patients &#40;2&#46;3&#37;&#41; from group A&#46; No patients presented with typically trachomatous corneal opacities or palpebral alterations&#46;</p></span><span id="cesec50" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle100">Direct fluorescent antibody test</span><p id="para310" class="elsevierStylePara elsevierViewall">All samples had more than 100 epithelial cells per field and were considered adequate for laboratory analysis&#46;</p><p id="para320" class="elsevierStylePara elsevierViewall">In group A&#44; 44 samples &#40;50&#46;6&#37;&#41; were negative &#40;less than five fluorescent elementary bodies&#41;&#44; and 43 samples &#40;49&#46;4&#37;&#41; were positive &#40;more than five fluorescent elementary bodies&#41;&#46; Positive DFA was identified in all patients with suggestive signs of trachoma &#40;two patients with more than six follicles in the upper tarsal conjunctiva and 13 of 17 patients with conjunctival and limbal scars&#41;&#46; In group B&#44; all samples were negative&#46;</p></span><span id="cesec60" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle110">Polymerase Chain Reaction</span><p id="para330" class="elsevierStylePara elsevierViewall">In group A&#44; human &#946;-globin was detected in 70 samples &#40;80&#46;4&#37;&#41;&#59; 14 &#40;20&#46;0&#37;&#41; were positive for <span class="elsevierStyleItalic">Chlamydia trachomatis</span>&#46; In group B&#44; human &#946; globin was identified in 60 samples &#40;66&#46;7&#37;&#41;&#44; one &#40;1&#46;7&#37;&#41; of which was PCR-positive for <span class="elsevierStyleItalic">Chlamydia trachomatis</span>&#46;</p><p id="para340" class="elsevierStylePara elsevierViewall">Correlating the clinical findings with the results of the PCR&#44; we observed that two patients from group A with suggestive signs of TF had positive PCR results&#46; The PCR results were also positive in eight of the 17 patients with suggestive TS&#46;</p></span><span id="cesec70" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle120">Direct Fluorescent Antibody Assay vs&#46; Polymerase Chain Reaction</span><p id="para350" class="elsevierStylePara elsevierViewall">All patients in group A with positive PCR results also had positive DFAs&#46; Only one patient from group B with a negative DFA had a positive PCR result &#40;<a class="elsevierStyleCrossRefs" href="#fig1">Figures 1 and 2</a>&#41;</p><elsevierMultimedia ident="fig1"></elsevierMultimedia><elsevierMultimedia ident="fig2"></elsevierMultimedia><p id="para360" class="elsevierStylePara elsevierViewall"><a class="elsevierStyleCrossRef" href="#fig3">Figure 3</a> displays ROC curves for DFA and PCR&#46;</p><elsevierMultimedia ident="fig3"></elsevierMultimedia><p id="para370" class="elsevierStylePara elsevierViewall">Areas under the ROC curves were 1&#46;0 &#40;95&#37; CI &#61; 0&#46;958 to 1&#46;000&#41; for the DFA and 0&#46;663 &#40;95&#37; CI &#61; 0&#46;553 to 0&#46;761&#41; for the PCR&#46; A pairwise comparison of ROC curves revealed a difference of 0&#46;337 &#40;95&#37; CI &#61; 0&#46;223 to 0&#46;451&#44; <span class="elsevierStyleItalic">p</span>&#60;0&#46;001&#41;&#46;</p><p id="para380" class="elsevierStylePara elsevierViewall">The sensitivity and specificity of the DFA were 100 &#40;95&#37; CI &#61; 91&#46;7 to 100&#41; and 100 &#40;95&#37; CI &#61; 91&#46;9 to 100&#41;&#44; respectively&#46; The sensitivity of the PCR was 23&#46;56 &#40;95&#37; CI &#61; 19&#46;1 to 48&#46;5&#41;&#44; and the specificity of the PCR was 100 &#40;95&#37; CI &#61; 91&#46;9 to 100&#41;&#46;</p></span></span><span id="cesec80" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle130">DISCUSSION</span><p id="para390" class="elsevierStylePara elsevierViewall">In our study&#44; as in previous publications&#44; VKC occurred more frequently in children less than 15 years old &#40;86&#46;25&#37;&#41; and in males &#40;69&#46;0&#37;&#41;&#46;<a class="elsevierStyleCrossRefs" href="#bib1">1&#44;2</a> A clinical diagnosis of VKC was made in all patients from group A&#44; and they all reported itching&#46;</p><p id="para400" class="elsevierStylePara elsevierViewall">A clinical diagnosis of <span class="elsevierStyleItalic">Chlamydia trachomatis</span> infection could also have been made by the presence of scars&#46; However&#44; in the earlier stages of infection&#44; the relatively benign and asymptomatic course and the preponderance of signs and symptoms of VKC could obfuscate the correct diagnosis&#46; In our study&#44; scars suggestive of trachoma were detected in 17 patients &#40;19&#46;5&#37;&#41; from group A&#46;</p><p id="para410" class="elsevierStylePara elsevierViewall">All the samples that were prepared for DFA were used because all had the minimum of 100 epithelial cells per field&#46; The presence of five or more fluorescent elementary bodies was considered a positive result in the analysis of the samples&#46;<a class="elsevierStyleCrossRef" href="#bib6">6</a></p><p id="para420" class="elsevierStylePara elsevierViewall">In group A&#44; 49&#46;4&#37; of the samples presented positive DFA&#44; and in group B&#44; all 90 samples were negative&#46; Of the 43 patients with positive DFA&#44; 19 had suggestive clinical signs of trachoma&#44; and the majority of the remaining cases could be diagnosed only by laboratory tests&#46;</p><p id="para430" class="elsevierStylePara elsevierViewall">PCR is considered the most sensitive non-culture test for the detection of <span class="elsevierStyleItalic">Chlamydia trachomatis</span> in non-ocular samples&#46; Problems related to contamination and the presence of DNA polymerase inhibitors&#44; such as blood and lysozyme&#44; could result in false-negative and false-positive results&#46; The routine use of a negative control and an internal control &#40;for the detection of human &#946;-globin&#41; would eliminate the risk of misreading for the methodology applied in this study&#46;</p><p id="para440" class="elsevierStylePara elsevierViewall">Human &#946;-globin was detected in 70 of the 87 samples from group A and in 60 of the 90 samples from group B&#46; Therefore&#44; 80&#46;4&#37; and 66&#46;7&#37; of the samples&#44; respectively&#44; were used&#46; Although many studies have used the plasmid for DNA amplification&#44; some Chlamydia <span class="elsevierStyleItalic">trachomatis</span> strains with no plasmid have been described&#46;<a class="elsevierStyleCrossRef" href="#bib7">7</a> Therefore&#44; we opted to amplify a conserved region of nucleotides in the MOMP gene&#46;</p><p id="para450" class="elsevierStylePara elsevierViewall">We obtained fewer positive PCRs than DFAs&#58; 14 samples in group A &#40;corresponding to 20&#46;0&#37;&#41; and 1 sample in group B &#40;corresponding to 1&#46;7&#37;&#41;&#46;</p><p id="para460" class="elsevierStylePara elsevierViewall">Frequent questions raised by practitioners include whether VCK causes trachoma&#44; whether trachoma causes VKC or whether their co-occurrence is merely coincidental&#46; These questions arise because both diseases affect the same group of patients &#40;i&#46;e&#46;&#44; school children in hot and dry areas&#41;&#46;</p><p id="para470" class="elsevierStylePara elsevierViewall">V&#233;rin et al&#46; reported that <span class="elsevierStyleItalic">Chlamydia trachomatis</span> could act as an allergen or as the trigger of an allergic process&#44; suggesting that a chronic chlamydial infection&#44; which alters the immunologic events on the ocular surface&#44; could be associated with the local allergic response&#46;<a class="elsevierStyleCrossRefs" href="#bib8">8&#44;9</a></p><p id="para480" class="elsevierStylePara elsevierViewall">Friedlaender and Cameron observed that the infectious nature of trachoma was not relevant in the pathogenesis of VKC&#46; Atopic patients&#44; such as those with VKC&#44; present with some local or systemic immunological compromise&#44; which could explain the greater incidence of staphylococcal and herpetic infections and possibly chlamydial infections&#46;<a class="elsevierStyleCrossRef" href="#bib3">3</a> In addition&#44; the integrity of the epithelium is considered the first line of defense of the ocular surface in many infectious conditions&#46; VKC patients have conjunctival alterations due to chronic inflammation&#44; vascular hyperpermeability&#44; and excoriation&#44; all of which compromise the integrity of the ocular surface&#44; rendering the patient more susceptible to secondary infections&#44; such as trachoma&#46;<a class="elsevierStyleCrossRef" href="#bib3">3</a></p><p id="para490" class="elsevierStylePara elsevierViewall">Another factor to be considered is that all VKC patients present with itching as their main symptom&#44; and they excessively manipulate their eyes&#44; thus transferring significant numbers of microorganisms&#44; possibly including <span class="elsevierStyleItalic">Chlamydia trachomatis</span>&#44; from their hands to their eyes&#46; <span class="elsevierStyleItalic">Chlamydia trachomatis</span> can also be carried by contaminated secretions&#44; which are commonly found in the eyes of VKC patients&#46;</p><p id="para500" class="elsevierStylePara elsevierViewall">SCARPI et al&#46; observed in their study that itching was the main symptom in trachoma patients &#40;11&#46;47&#37;&#41;&#59; they likely also included some patients with concomitant trachoma and allergic conjunctivitis&#46;<a class="elsevierStyleCrossRef" href="#bib12">12</a></p><p id="para510" class="elsevierStylePara elsevierViewall">Rao et al&#46; investigated the presence of <span class="elsevierStyleItalic">Chlamydia trachomatis</span> in 127 patients with acute&#44; chronic&#44; and recurrent conjunctivitis&#46;<a class="elsevierStyleCrossRef" href="#bib5">5</a> Of the 22 patients with clinically diagnosed allergic conjunctivitis&#44; seven &#40;31&#46;8&#37;&#41; had a positive culture for <span class="elsevierStyleItalic">Chlamydia trachomatis&#46;</span></p><p id="para520" class="elsevierStylePara elsevierViewall">Notably&#44; DFA is still considered the gold standard for <span class="elsevierStyleItalic">Chlamydia trachomatis</span> detection&#46; Without it&#44; clinical diagnoses would have been made in only 19 of 43 patients &#40;44&#46;2&#37;&#41; with positive DFAs&#44; indicating that trachoma would not have been diagnosed in 55&#46;8&#37; of patients&#46; These cases would have been treated as severe and refractory allergic conjunctivitis&#46;</p><p id="para530" class="elsevierStylePara elsevierViewall">Despite its low sensitivity in this study&#44; DNA amplification by PCR is still used for the detection of ocular chlamydial infection&#59; more recently&#44; however&#44; nucleic acid amplification tests &#40;NAATs&#41; based on the amplification of rRNA have been developed&#44; providing a potential advantage because bacterial rRNA is present at up to 10&#44;000 times the copy numbers of genomic DNA and at up to 1&#44;000 times the copy numbers of plasmid DNA&#46; This development opens a field of new opportunities for the detection of chlamydial infections using these techniques&#46;<a class="elsevierStyleCrossRefs" href="#bib13">13&#44;14</a></p><p id="para540" class="elsevierStylePara elsevierViewall">Although both trachoma and VKC have characteristic periods of waxing and waning even without treatment&#44; the chronicity&#44; the recurrent nature and the long duration of the diseases can be highly disabling&#46; Patients are disabled not only by the severe symptoms in the acute phases but also by the more frequent occurrences of complications&#44; such as lid abnormalities and conjunctival and corneal scars&#44; which can cause reduced visual acuity&#44; impairing the acquisition of reading skills in children&#46;<a class="elsevierStyleCrossRefs" href="#bib1">1&#44;3</a></p><p id="para550" class="elsevierStylePara elsevierViewall">Trachoma is a self-limiting disease&#44; resolving in approximately one year even without treatment&#46; However&#44; treatment is essential to avoid recurrences&#44; scars&#44; and other sequelae&#46; Immunological diseases such as VKC are treated with anti-allergic and anti-inflammatory drugs such as corticosteroids that depress cell immunity and are implicated in the control of infections and trachoma&#46; In contrast&#44; trachoma is treated with antibiotics&#46; Therefore&#44; because the treatments differ for VKC and trachoma&#44; it is essential to accurately determine their co-occurrence to initiate the appropriate treatment&#46;</p><p id="para560" class="elsevierStylePara elsevierViewall">Based on the population studied and the applied methodologies&#44; we report several findings&#46; First&#44; there was an association between VKC and <span class="elsevierStyleItalic">Chlamydia trachomatis</span> infection that was confirmed by positive DFAs in 49&#46;4&#37; of VKC patients and by positive PCRs in 20&#46;0&#37; of patients&#46; Second&#44; DFA detected <span class="elsevierStyleItalic">Chlamydia trachomatis</span> in a greater number of patients than did PCR&#44; making it the more sensitive and specific test&#46; Third&#44; although the diagnosis of trachoma is essentially clinical&#44; the disease may not be detected in some VKC patients&#46; In conclusion&#44; we suggest considering laboratory tests to routinely detect <span class="elsevierStyleItalic">Chlamydia trachomatis</span> by DFA in patients with severe and refractory VKC&#46;</p></span></span>"
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        1 => array:2 [
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          "titulo" => "INTRODUCTION"
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          "titulo" => "MATERIALS AND METHODS"
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          "titulo" => "RESULTS"
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            0 => array:2 [
              "identificador" => "cesec40"
              "titulo" => "Clinical evaluation"
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            1 => array:2 [
              "identificador" => "cesec50"
              "titulo" => "Direct fluorescent antibody test"
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            2 => array:2 [
              "identificador" => "cesec60"
              "titulo" => "Polymerase Chain Reaction"
            ]
            3 => array:2 [
              "identificador" => "cesec70"
              "titulo" => "Direct Fluorescent Antibody Assay vs&#46; Polymerase Chain Reaction"
            ]
          ]
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        4 => array:2 [
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          "titulo" => "DISCUSSION"
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        5 => array:2 [
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          "titulo" => "ACKNOWLEDGMENTS"
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        6 => array:1 [
          "titulo" => "REFERENCES"
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    "pdfFichero" => "main.pdf"
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    "fechaRecibido" => "2011-03-23"
    "fechaAceptado" => "2011-08-15"
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          "clase" => "keyword"
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          "palabras" => array:4 [
            0 => "Vernal keratoconjunctivitis"
            1 => "Chlamydia trachomatis"
            2 => "Polymerase chain reaction"
            3 => "Direct fluorescent antibody assay"
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        "resumen" => "<span id="ceabs10" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle10">OBJECTIVES&#58;</span><p id="spara90" class="elsevierStyleSimplePara elsevierViewall">To identify <span class="elsevierStyleItalic">Chlamydia trachomatis</span> via polymerase chain reaction and a direct fluorescent antibody assay in patients with vernal keratoconjunctivitis while comparing the efficacies of both tests for detecting <span class="elsevierStyleItalic">Chlamydia trachomatis</span> in these conditions&#46;</p></span> <span id="ceabs20" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle20">METHODS&#58;</span><p id="spara100" class="elsevierStyleSimplePara elsevierViewall">Conjunctival scraping samples were obtained from 177 patients who were divided into two groups&#58; a vernal keratoconjunctivitis group &#40;group A&#41; and a control group &#40;group B&#41;&#46; The polymerase chain reaction and a direct fluorescent antibody assay were performed&#46; Sensitivity&#44; specificity&#44; receiver operating characteristic curves&#44; and areas under the curve were calculated for both tests in groups A and B&#46; Receiver operating characteristic curves were plotted using a categorical variable with only two possible outcomes &#40;positive and negative&#41;&#46;</p></span> <span id="ceabs30" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle30">RESULTS&#58;</span><p id="spara110" class="elsevierStyleSimplePara elsevierViewall">Statistical analysis revealed a significant association between vernal keratoconjunctivitis and <span class="elsevierStyleItalic">Chlamydia trachomatis</span> infection detected by a direct fluorescent antibody assay with high sensitivity and specificity&#46; All patients in group A with positive polymerase chain reactions also presented with positive direct fluorescent antibody assays&#46;</p></span> <span id="ceabs40" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle40">CONCLUSION&#58;</span><p id="spara120" class="elsevierStyleSimplePara elsevierViewall">The association between vernal keratoconjunctivitis and <span class="elsevierStyleItalic">Chlamydia trachomatis</span> infection was confirmed by positive direct fluorescent antibody assays in 49&#46;4&#37; of vernal keratoconjunctivitis patients and by positive polymerase chain reactions in 20&#37; of these patients&#46; The direct fluorescent antibody assay detected <span class="elsevierStyleItalic">Chlamydia trachomatis</span> in a higher number of patients than did the polymerase chain reaction&#46; Although the diagnosis of trachoma is essentially clinical&#44; the disease may not be detected in vernal keratoconjunctivitis patients&#46; Due to the high frequency of chlamydial infection detected in patients with vernal keratoconjunctivitis&#44; we suggest considering routine laboratory tests to detect <span class="elsevierStyleItalic">Chlamydia trachomatis</span> in patients with severe and refractory allergic disease&#46;</p></span>"
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            "titulo" => "OBJECTIVES&#58;"
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            "titulo" => "METHODS&#58;"
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            "titulo" => "RESULTS&#58;"
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        "nota" => "<p class="elsevierStyleNotepara" id="cenpara10">No potential conflict of interest was reported&#46;</p> <p class="elsevierStyleNotepara" id="cenpara20">Nishiwaki-Dantas MC designed and conducted the study&#59; collected&#44; managed&#44; analyzed&#44; and interpreted the data&#59; prepared&#44; reviewed&#44; and approved the manuscript&#46; Abreu MT designed and conducted the study&#59; managed&#44; analyzed&#44; and interpreted the data&#59; prepared&#44; reviewed&#44; and approved the manuscript&#46; Melo CM designed and conducted the study&#59; collected&#44; managed&#44; analyzed&#44; and interpreted the data&#59; prepared&#44; reviewed&#44; and approved the manuscript&#46; Romero IL designed and conducted the study&#59; collected&#44; managed&#44; analyzed&#44; and interpreted the data&#59; prepared&#44; reviewed&#44; and approved the manuscript&#46; Neto RBM designed and conducted the study&#59; collected the data&#59; prepared&#44; reviewed&#44; and approved the manuscript&#46; Dantas PEC designed and conducted the study&#59; managed&#44; analyzed&#44; and interpreted the data&#59; prepared&#44; reviewed&#44; and approved the manuscript&#46;</p>"
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          "en" => "<p id="spara10" class="elsevierStyleSimplePara elsevierViewall">Venn diagram from group A &#40;43 DFA-positive results&#41;&#46;</p>"
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                  \t\t\t\t  " align="left" valign="top" scope="col">N&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="left" valign="top" scope="col">&#37;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="left" valign="top" scope="col">N&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="left" valign="top" scope="col">&#37;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="left" valign="top">27&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="left" valign="top">31&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="left" valign="top">64&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="left" valign="top">23&nbsp;\t\t\t\t\t\t\n
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                    0 => array:2 [
                      "titulo" => "Vernal Keratoconjunctivitis"
                      "autores" => array:1 [
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                          "etal" => false
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                            0 => """
                              A Leonardi \n
                              \t\t\t\t\t\t\t\t
                              """
                            1 => """
                              LM Smith \n
                              \t\t\t\t\t\t\t\t
                              """
                            2 => """
                              AG Secchi \n
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                    0 => array:1 [
                      "LibroEditado" => array:5 [
                        "editores" => "MBAbelson"
                        "titulo" => "Allergic Diseases of the Eye"
                        "paginaInicial" => "pp179"
                        "paginaFinal" => "pp196"
                        "serieFecha" => "2000"
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                0 => array:2 [
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                    0 => array:2 [
                      "titulo" => "Conjuntivites al&#233;rgicas"
                      "autores" => array:1 [
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                            0 => """
                              MC Nishiwaki-Dantas \n
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                              """
                            1 => """
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                      "LibroEditado" => array:5 [
                        "editores" => "ALHLima, MCNishiwaki-Dantas, MRAlves"
                        "titulo" => "Manual do Conselho Brasileiro de Oftalmologia&#46; Doen&#231;as Externas Oculares e C&#243;rnea"
                        "paginaInicial" => "199"
                        "paginaFinal" => "221"
                        "serieFecha" => "1999"
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                      "titulo" => "Vernal keratoconjunctivitis and trachoma"
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                              MH Friedlaender \n
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                              J Cameron \n
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                        "tituloSerie" => "Int Ophthalmol"
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                        "paginaInicial" => "47"
                        "paginaFinal" => "51"
                        "link" => array:1 [
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                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/3220668"
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                      "titulo" => "The prevention of blindness from trachoma"
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                              BR Jones \n
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                        "tituloSerie" => "Trans Ophthalmol UK"
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                        "volumen" => "95"
                        "paginaInicial" => "16"
                        "paginaFinal" => "32"
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                      "titulo" => "Ocular chlamydial infections"
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                              SK Rao \n
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                              HN Madhavan \n
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                              GS Lakshmi \n
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                      "titulo" => "An&#225;lise de exames de imunofluoresc&#234;ncia direta para o diagn&#243;stico de tracoma"
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                              NH Medina \n
                              \t\t\t\t\t\t\t\t
                              """
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                              RM Gentil \n
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                              M Cara&#231;a \n
                              \t\t\t\t\t\t\t\t
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                              CK Suzuki \n
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                            4 => """
                              HHB Melles \n
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                      "titulo" => "Sensitivity of immunofluorescence with monoclonal antibodies for detection of <span class="elsevierStyleItalic">Chlamydia trachomatis</span> inclusions in cell culture"
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        "titulo" => "ACKNOWLEDGMENTS"
        "texto" => "<p id="para570" class="elsevierStylePara elsevierViewall">The authors wish to acknowledge Niro Kasahara&#44; MD&#44; PhD&#44; from the Statistics and Epidemiology Service of the Department of Ophthalmology of Santa Casa in S&#227;o Paulo&#44; Brazil&#44; for the statistical review and analysis provided&#44; FAPESP &#40;Funda&#231;&#227;o de Amparo &#224; Pesquisa do Estado de S&#227;o Paulo&#41; for financial support and Prof&#46; Dra&#46; Lia Mara Rossi&#44; from Faculdade de Ci&#234;ncias M&#233;dicas da Santa Casa de S&#227;o Paulo&#46;</p><p id="para580" class="elsevierStylePara elsevierViewall">Statement about Conformity with Author Information&#58; This study was reviewed and approved by the Bioethics Committee from Santa Casa in S&#227;o Paulo&#44; Brazil&#46;</p>"
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