High frequency of latent Chlamydia trachomatis
infection in patients with rhegmatogenous retinal detachment
Ernest V. Boiko1,2, Alexei L. Pozniak1,
Dmitrii S. Maltsev1, Alexei A. Suetov1, Irina V. Nuralova1
1St. Petersburg Branch
of the Academician S. Fyodorov IRTC “Eye Microsurgery”, St. Petersburg 192283, Russia
2Department of
Ophthalmology, Military Medical Academy, St. Petersburg 194044, Russia
Correspondence to: Ernest V. Boiko.
St. Petersburg Branch of the Academician S. Fyodorov IRTC “Eye Microsurgery”,
21, Yaroslav Gashek St., St. Petersburg 192283, Russia. boiko111@list.ru
Received: 2015-03-08
Accepted: 2015-08-18
Abstract
AIM: To determine the frequency of detection of
ocular and extraocular Chlamydia trachomatis (CT) infection in non-high myopes
with rhegmatogenous retinal detachment (RRD).
METHODS: This was a single-center, nonrandomized,
prospective, case-control study. One hundred and four patients were divided
into a study group with RRD (n=63)
and a control group with traumatic retinal detachment (n=41). Samples of subretinal fluid (SFR), conjunctival,
urethral/cervical swabs, and blood were collected. The frequency of detection
of CT infection in SRF samples was determined by polymerase chain reaction
(PCR), direct fluorescence assay (DFA) and cell culture, whereas that in
conjunctival swabs was determined by PCR and DFA, and those in
urethral/cervical swabs and blood were determined by DFA. Yates Chi-square test
(with Bonferroni correction) and two-tailed Student’s t-test were used for statistical analysis.
RESULTS: SRF CT infection was detected more frequently
in the study group (50.8%-71.4%) than in the control group
(9.8%-12.2%) by all the methods used (P<0.01).
The frequency of detection of conjunctival CT infection by DFA was higher in
the RRD patients compared with the controls (81.0% vs 24.4%, P=0.004). The
PCR detected conjunctival CT infection more often in the study group than in
the controls (46.0% vs 9.8%, P=0.007). The DFA detected CT in blood
specimens almost as frequently as in urogenital specimens, for the RRD patients
(61.2% vs 63.5%) and the controls
(7.3% vs 9.8%).
CONCLUSION: CT infection is
detected with high frequency in non-high myopes with RRD.
KEYWORDS: rhegmatogenous retinal detachment;
Chlamydia trachomatis; myopia;
latent infection
DOI:10.18240/ijo.2016.06.13
Citation: Boiko
EV, Pozniak AL, Maltsev DS, Suetov AA, Nuralova IV. High frequency of latent chlamydia trachomatis
infection in patients with rhegmatogenous retinal detachment. Int
J Ophthalmol 2016;9(6):863-868
INTRODUCTION
Rhegmatogenous
retinal detachment (RRD) is a vision-threatening disease characterized by
the separation of the inner neurosensory retina and the retinal pigment
epithelium[1]. According
to various sources[2-4],
its annual incidence is estimated to be 6.9 to 18.2 per 100 000.
Retinal tear is the most important risk factor and a cause of
RRD. Additionally, retinal thinning, posterior vitreous detachment (PVD), and vitreous tractions are widely considered to be essential
for the formation of a retinal tear. Although the clinical picture of
RRD is well known, the most fundamental causes of the development both of
retinal tears and the preceding retinal and vitreous alterations remain poorly
understood.
Retinal thinning,
PVD and vitreous tractions may develop in the presence of a posterior-segment clinical inflammatory
disease such as infectious uveitis resulting
in retinal tears and RRD[5].
Moreover, it is known that inflammation in general is critical in the pathogenesis
of different vitreoretinal diseases[6].
We theorized that chronic low-grade inflammation directly or indirectly
caused by latent infection may have similar mechanism related to the
development of retinal thinning, PVD and vitreous tractions resulting in
retinal tears and detachment.
One of the most
well-known causes of chronic low-grade inflammation is persistent Chlamydia
trachomatis (CT) infection which can
result in asymptomatic damage to the urogenital tract[7]. Furthermore, CT is a
causative agent of trachoma, which is manifested by chronic conjunctival
inflammation[8]. In
recent years, evidence has accumulated regarding the ability of various CT serovars to induce damage not only to
epithelial, but also to other structures and tissues of the body [9], including those of the
ocular posterior segment[10].
In our previous
work [11], CT elementary bodies were identified
in 74% of the subretinal fluid (SRF) specimens of 50 patients with RRD. Ocular
CT infection in such cases may be explained by evidence of the high incidence
of bacteremia in urogenital CT infection [12].
Therefore, the purpose of this study was to determine the frequency of
detection of both ocular (namely, SRF-related and conjunctival) and extraocular
(namely, urogenital tract and blood) CT infection in non-high myopes with RRD.
SUBJECTS AND METHODS
Subjects This single-center,
nonrandomized, prospective, case-control study was conducted at our
Ophthalmology Clinic in 2010-2012, and involved 104 patients divided into a
study group and a control group. The study group included 63 patients with
clinical signs of typical RRD evaluated by experts in retinal detachment
surgery. These patients had confirmed idiopathic retinal tears, i.e. they had no known ocular diseases
other than RRD. The control group included 41 patients with traumatic retinal
detachment (TRD) resulting usually from a documented episode of open- or
closed-globe injury with retinal involvement (direct retinal damage, tear or
dialysis). Exclusion criteria for both groups included current and/or recent (within
a year) history of uveitis, manifested
or acute urogenital tract diseases, any other systemic or organ specific
signs/symptoms of CT infection. Moreover, they included diabetes,
hypermetropia of more than 2.0 D, and high myopia (more than 6.0 D). Additional
exclusion criterion for the control group alone was the absence of reliable
signs of direct traumatic damage to the retina. All the patients had retinal
re-attachment surgery including extrascleral buckling or pars plana vitrectomy,
either alone or in combination, depending on indications. They were informed
about the purpose of the study and signed an informed written consent. The
study was approved by local Research Ethics Committee and was consistent with
the tenets of Declaration of Helsinki.
Samples Collection and Identification of Chlamydia
Trachomatis Conjunctival, urethral (for
men) and cervical (for women) swabs, and blood were collected preoperatively;
additionally, samples of SRF were collected intraoperatively. All of them were
investigated for the presence of CT infection.
At the time of
retinal re-attachment surgery, SRF was aspirated with a 27-gauge cannula
attached to
a sterilized syringe and inserted either through a scleral puncture for SRF
drainage in extrascleral buckling (n=65),
or through a retinal tear (retinotomy hole) for transretinal drainage in
vitrectomy (n=39). Sample
contamination with blood was occasional; heavily contaminated samples were
discarded. Each sample was centrifuged for 20min at 2000 rpm, and a portion of
the centrifuged deposit was placed into transport medium for culture and polymerase chain reaction
(PCR) testing. Another portion was used to prepare a smear that was air dried
and fixed 10min in 70% cold methanol before being subjected to direct
fluorescence assay (DFA).
After
anesthetization of the conjunctiva with proxymetacaine 0.5% eye drops (Alcaine,
Alcon-Couvreur, Belgium), conjunctival swabs were taken in a standardized
manner (passed firmly four times
across the conjunctiva with a quarter turn between
each pass). Conjunctival smears were prepared by rolling half the swab on a
glass slide. Immediately after smearing, the swab was placed into
transport medium for PCR and stored at
+4℃ up to 3d before
being used in the study. Smears were fixed as described above.
Samples of
conjunctival smears and SRF were placed into 3 mL of modified viral
transport medium with Charcoal (HiMedia Laboratories Pvt. Ltd., Mumbai, India) before
being subjected to PCR and cell culture.
Totally 5 mL venous blood samples were collected from all patients. After clotting,
the sample was centrifuged at 2000 g for 15min at 4℃, and the serum was separated. Serum
smears were prepared and subjected to DFA.
Urethral (for men)
and cervical (for women) specimens were collected with a unisex swab (HiMedia
Laboratories Pvt. Ltd). The swab was rolled on a slide and fixed as described above.
A 0.2-mL portion of each transport medium specimen or each serum sample
was used to detect the pathogen by culture. The portions were placed into
individual wells of 24-well cell culture plates containing McCoy cells grown to
confluence in 10% fetal bovine serum-supplemented Eagle’s Minimum Essential
Medium (MEM) (Biolot, Moscow, Russia) and 1 mg/L cycloheximide (Acros Organics,
Geel, Belgium). The plates were then centrifuged at 2400 rpm for 60min and
incubated at 37℃ in 5% CO2.
After 48h incubation, the culture media was removed from the wells, and the
plates were twice washed with phosphate-buffered
saline (PBS, pH 7.2) and fixed in 96% ethanol for 5min.
Slide smears and
cell cultures were incubated in the presence of ChlamyScan enzyme immunoassay
system (LABDiagnostica, Moscow, Russia) fluorescein-conjugated monoclonal
antibodies to a CT-specific trisaccharide epitope
αKdo(2→8)αKdo(2→4)αKdo for 20min at 37℃ in a moisture chamber. The slides were then
incubated in PBS for 10min, washed twice in PBS and mounted in 90% PBS/ 10%
glycerol.
Microscopic
examination was performed with a Leica DM2500 fluorescence microscope (Leica
Microsystems, Wetzlar, Germany). A sample was
considered positive for CT if at least 10 loci of specific
fluorescence (elementary bodies) were detected.
Real-time PCR was performed using the Rotor-Gene 6000 (Corbett Research,
Sydney, Australia). Extraction of total nucleic acids was conducted with DNA-sorb-B kit
(AmpliSens, Moscow, Russia). Specimens
were tested for the presence of DNA from CT using CT-screen-titer-FRT
(AmpliSens), according to the manufacturer's instructions.
Statistical Analysis Yates Chi-square test (with Bonferroni correction) and two-tailed
Student’s t-test were used to evaluate the significance of
differences between the RRD and control groups in the amount of positive
results and average patient age, respectively. Bonferroni correction for
multiple comparisons was applied where multiple tests were performed, thereby
reducing the nominal P value for statistical significance to 0.016. Otherwise, the nominal P value for statistical significance was 0.05.
RESULTS
The frequency of
detection of CT was significantly higher in the patients with RRD than in the controls,
whereas no statistically significant differences were found in the average
patient age and sex distribution between the groups. The percentage of patients
with myopia was not statistically significantly higher in the RRD group than in
the control group (55.6% vs 26.8%, P=0.07) (Table 1).
In the RRD group,
43 (68.3%) SRF specimens were positive by DFA, and 32 (50.8%) were positive by
PCR; additionally, PCR provided the least number of positive results, whereas
the numbers provided by DFA and culture were comparable.
In the control
group, no
statistically significant differences were revealed between the methods (Table
2). The frequency of detection of CT conjunctival infection was higher in the RRD patients
than in the controls. In the RRD group, 51 (81.0%)
conjunctival swab specimens were positive by DFA, and 29 (46.0%) were positive
by PCR (Table
2). Within each group, the PCR detected the pathogen in subretinal fluids as
frequently as in conjunctival swab specimens (P>0.05). The frequency of detection of the pathogen in all
types of specimens (SRF, conjunctival swab, urogenital swab or blood) by DFA
was the same. Blood
and urogenital-swab specimens yielded a statistically significantly greater
percentage of positive results in the RRD group vs the control group. Within each group, the frequency of detection of the
pathogen in these two types of specimens was approximately the same (P>0.05). In 90.5% of the RRD group patients, at least one of the four (i.e. SRF, conjunctival swab, urogenital swab or blood) specimens was found to be DFA positive for CT. Moreover, within any type
of specimens, the percentage of culture-positive specimens was close to that of
DFA-positive and PCR-positive specimens (P=0.016) (Table 3).
Table 1 Demographic and refraction data
n
(%)
Characteristic |
1RRD (n=63) |
1TRD (n=41) |
P |
Age (a), |
47.2±17.2 |
45.4±16.6 |
20.64 |
Sex |
|
|
|
M |
41 (65.1) |
29 (70.7) |
30.7 |
F |
22 (34.9) |
12 (29.3) |
30.55 |
Refraction data |
|
|
|
Myopia up to 6 D |
35 (55.6) |
11 (26.8) |
30.1 |
Emmetropia and hypermetropia
up to 2 D |
28 (44.4) |
30 (73.2) |
30.18 |
RRD: Rhegmatogenous retinal detachment; TRD: Traumatic retinal
detachment. 1Unless otherwise
indicated, data are expressed as number (percentage) of patients; 2Determined
by use of the two-tailed Student’s
t-test;
3Determined
by use of the Chi-square
test.
Table 2 Rates of positivity for CT among different types of specimens in cases (RRD
group) and controls (TRD group) n (%)
Type of specimen/method |
1RRD group |
1TRD group |
2P |
Subretinal fluid |
|
|
|
DFA |
43 (68.3) |
5 (12.2) |
0.006 |
PCR |
32 (50.8) |
4 (9.8) |
0.003 |
Culture |
45 (71.4) |
5 (12.2) |
<0.001 |
Conjunctival swab |
|
|
|
DFA |
51 (81.0) |
10 (24.4) |
0.004 |
PCR |
29 (46.0) |
4 (9.8) |
0.007 |
Blood |
|
|
|
DFA |
40 (63.5) |
4 (9.8) |
<0.001 |
Urogenital swab |
|
|
|
DFA |
39 (61.9) |
3 (7.3) |
<0.001 |
DFA: Direct
fluorescent assay; PCR: Polymerase chain reaction;
RRD: Rhegmatogenous retinal detachment; TRD: Traumatic
retinal detachment. 1Data
are expressed as number (percentage) of the samples found positive by the
method specified; 2Determined by use of the Chi-square test.
Table 3 Comparison of DFA, PCR and culture results in
SRF specimens n (%)
Group/method |
1Negative |
2Positive |
3P |
RRD |
|
|
|
DFA |
20
(31.7) |
43
(68.3) |
40.07 |
PCR |
31
(49.2) |
32
(50.8) |
50.03 |
Culture |
18
(28.6) |
45
(71.4) |
60.85 |
TRD |
|
|
|
DFA |
36
(87.8) |
5
(12.2) |
4>0.99 |
PCR |
37
(90.2) |
4
(9.8) |
5>0.99 |
Culture |
36
(87.8) |
5 (12.2) |
60.74 |
DFA: Direct
fluorescent assay; PCR: Polymerase chain reaction;
SRF: Subretinal fluid; RRD: Rhegmatogenous retinal
detachment; TRD: Traumatic retinal detachment. 1Data are expressed as number
(percentage) of the SRF specimens found negative by the method specified; 2Data
are expressed as number (percentage) of the SRF specimens found positive by the
method specified; 3Determined by use of the Chi-square test; 4P value for comparison of DFA vs PCR; 5P value for comparison of PCR vs
culture; 6P value for
comparison of DFA vs culture.
DISCUSSION
The association of CT infection with RRD has been postulated by us[11]. This was supported in a single-case study by
Ghaffariyeh et al[13]. In the present work, we confirmed this
association and also found that of RRD with extraocular infection, in
particular, the presence of the pathogen in the urogenital tract and blood. Demonstration of the presence of CT in
SRF specimens of a significant percentage of patients with RRD (50.8%-71.4%)
vs controls (9.8%-12.2%)
makes us suggest that the pathogen may play a role of in the etiology and
pathogenesis of this vision-threatening disease. However, this issue requires further investigation.
It has been generally accepted that CT infection most commonly
affects the urogenital tract[7]
and conjunctiva[8]. However, recently, evidence has
accumulated that, in a high percent of patients with urogenital CT infection,
the latter is accompanied by bacteremia[12],
and if so, the pathogen can get to other organs and tissues. Our results confirm that, in RRD, CT
tends not only to induce local damage to the urogenital tissues (61.9%), but
also to cause bacteremia and infect the eye (63.5% and 46.0%-81.0%,
respectively). Furthermore, we do not
exclude that dissemination of the agent to the posterior segment or extraocular
sites might take place after primary infection of the conjunctiva, since, previously, we have detected intraocular CT
infection following a subconjunctival inoculation with CT in rabbits[10]. CT can infect different types of
cells, including macrophages[14],
neuroglial[15], and
synovial[9] cells. The
pathogen initiates the inflammatory process, triggering the cytokine production
by CT-infected and adjacent cells both through direct damage and antigenic
stimulation[16]. Here the
profile of the cytokines produced is pro-inflammatory and includes IL-10, TNF,
IFN [7], IL-6 [9], IL-12, and IL-8[16], resulting in
generation and maintenance of inflammation. Regarding the posterior segment,
this explanation is supported by findings from other investigators that the
immunoglobulin composition[17]
and pH level[18] of SRF
are close to those of inflammatory exudates (in particular, infectious
exudates). Moreover, the inflammatory nature of the process in RRD is
underscored by the SRF interleukin (IL-10 and IL-12) levels[19]. The pathogen is characterized by a long-term
inflammatory process that involves dystrophic and proliferative histological
changes similar to those observed in trachoma and urogenital chlamydial
infection. By analogy, intraocular infection with CT and the ensuing chronic
inflammatory process produce dystrophic and proliferative vitreoretinal
changes, aggravate them, and, therefore, represent risk factors for the
development of RRD.
Because high myopia
has been found to be associated with significant alterations in the vitreous
and retina, and to increase the risk for RRD forty-fold[20], it is an important risk factor for the disease.
Only non-highly myopic patients were included in the study; in such patients,
unlike highly myopic patients, the significant alterations mentioned above (as
well as the development of RRD) have not been clearly explained so far.
However, because
posterior vitreous detachment occurs significantly more often in individuals
(including young people) with a history of uveitis[21], it might be caused by intraocular inflammation.
Atrophic retinal changes may be also caused by inflammation, which is observed
in herpetic infection (e.g.
Cytomegalovirus retinitis)[22].
In these diseases, in the course of acute high-grade inflammation, atrophic
retinal changes contribute to the development of tears and detachment (another
contributor are post-inflammatory changes in the vitreous). We theorize, that
similar, but in some other way manifested changes might develop in the course
of intraocular low-grade inflammation induced by CT. Because the pathogenesis
of RRD is closely associated with inflammatory process, we find it reasonable to
believe that infectious agents might generate and maintain this disease through
chronic low-grade inflammation. Therefore, we do not exclude that other
bacterial or viral agents of so-called latent infections also may have
association with RRD. Since the involvement of several organs in the course of
chlamydial infection occurs rather often, the association of CT with RRD may be
considered not only in terms of direct infection of intraocular tissues, but
also in terms of the production of proinflammatory mediators at the extraocular
sites of infection. The prevalence of urogenital CT infection in different
populations (3%-12% in different foreign countries[23-25] and 4.9%-14%
in the
Russian Federation[24-25]) is higher than that of
retinal detachment (0.01%-0.02%)[3]; hence, infection of urogenital tract with CT is not
always associated with the development of RRD, and this can be explained by the
following reasons.
First, the
development of RRD requires bacteremia, which is not always observed in
urogenital chlamydial infection (61% of patients with chronic pelvic
inflammatory diseases and a history of chlamydial infection have been found
positive for the presence of CT DNA in the serum[8]). On the other hand, chronic chlamydial infection in
genetically predisposed individuals may result in the development of some
specific damage to the eye, which is observed, e.g. in Reiter’s disease[26].
It is still poorly understood why this chronic infection manifests itself as an
ocular complication (namely, as a retinal detachment), and not as a clinically
apparent conjunctivitis, urogenital or articular pathology. This is a promising
area for investigation of association of chlamydial infection with RRD.
Second, the absence
of RRD in most of the cases of chlamydial infection may be connected with the genetic variability in the pathogen. The
CT
species is divided into a number of serovars, A to K, and
serovar-specific infections differ in prognosis and pathologic consequences[27-28]. However, investigation of
this important issue requires serotyping, and was not the aim of the present
study. Because, in prenatal infection, disseminated damage to the organs is
observed, one cannot also exclude the inherent nature of chlamydial infection
in some patients[29].
In the present work,
to increase reliability of the results, we confirmed the presence of CT
infection in patients with RRD by different methods.
There are no
reasons to consider clinical urogenital
CT infection as a risk factor for RRD, because our study, and, to the best of
our knowledge, other studies provide no basis for such conclusions. Although we
may hypothesize that CT infection in any part of the body (including urogenital
tract) which is usually chronic and asymptomatic may be a risk factor for RRD,
additional studies are needed to establish whether this hypothesis is true.
In the present
study, the reference method (cell culture) demonstrated the percentage of
positive specimens similar to those of DFA and PCR. This corresponds to the
report of others that the sensitivity of PCR is usually considered close to
that of cell culture[30].
Moreover, the association of CT infection with RRD was found to be significant,
even when based on the lowest estimates of the percentage of positive specimens
(46% and 51% of conjunctival swabs and SRF specimens, respectively, by PCR).
Blood and urogenital-swab specimens
were not subjected to PCR, and this is a limitation of the study. Since it is well
known that latent chlamydial infection provides weak stimuli for immune
response[31] and is
accompanied by a low level of antibodies, we did not determine the antibody
levels in sera.
Additionally,
because, in our study, vitrectomy for RRD was performed only in a small
percentage of patients, the data related to the vitreous could not be used in
full-fledged statistical analysis. The lack of this data is another limitation
of the study.
We speculate that,
apart from dystrophic intraocular changes and the development of RRD, the
presence of CT in intraocular structures may result in aggravation of the
course of RRD (potentiation of the development of PVR, in particular) due to
chronic inflammation. This hypothesis does not contradict an important role for
inflammation processes in the pathogenesis of vitreoretinal pathology (in
particular, PVR)[32-33].
In conclusion, we demonstrated the high frequency of detection of CT
in non-high myopes with RRD (which may be associated with the potential
involvement of CT in the pathogenesis of RRD), with a step-by-step development
of typical changes in the vitreous due to a chronic low-grade inflammation.
Further investigation of the role of CT and other infections in the development
of RRD may be aimed at 1) clarification of the role of the pathogen in the
pathogenesis of RRD and 2) reasoning related to the use of systemic and local
antimicrobial therapies in RRD.
ACKNOWLEDGEMENTS
Conflicts of Interest: Boiko EV, None; Pozniak AL,
None; Maltsev DS, None; Suetov AA, None; Nuralova IV, None.
REFERENCES
1
Kuhn F, Aylward B. Rhegmatogenous retinal detachment: a reappraisal of its
pathophysiology and treatment. Ophthalmic
Res 2014;51(1):15-31. [CrossRef] [PubMed]
2 Laatikainen L, Tolppanen EM, Harju H. Epidemiology of rhegmatogenous
retinal detachment in a Finnish population. Acta
Ophthalmol (Copenh) 1985;63(1):59-64. [CrossRef]
3 Van de Put MA, Hooymans JM, Los LI. Dutch Rhegmatogenous Retinal
Detachment Study Group. The incidence of rhegmatogenous retinal detachment in
The Netherlands. Ophthalmology 2013;120(3):616-622. [CrossRef] [PubMed]
4 Mitry D, Chalmers J, Anderson K, Williams L, Fleck BW, Wright A,
Campbell H. Temporal trends in retinal detachment incidence in Scotland between
1987 and 2006. Br J Ophthalmol 2011;95(3):365-369.
[CrossRef] [PubMed]
5 Kerkhoff FT, Lamberts QJ, van den Biesen PR, Rothova A. Rhegmatogenous
retinal detachment and uveitis. Ophthalmology
2003;110(2):427-431. [CrossRef]
6 Yoshimura T, Sonoda KH, Sugahara M, Mochizuki Y, Enaida H, Oshima Y,
Ueno A, Hata Y, Yoshida H, Ishibashi T. Comprehensive analysis of inflammatory
immune mediators in vitreoretinal diseases. PLoS
One 2009;4(12):e8158. [CrossRef] [PubMed] [PMC free article]
7 Mascellino MT, Boccia P,
Oliva A. Immunopathogenesis in chlamydia trachomatis infected women. SRN Obstet Gynecol 2011;2011:436936.
8 Mariotti SP, Pascolini D, Rose-Nussbaumer J. Trachoma: global
magnitude of a preventable cause of blindness. Br J Ophthalmol 2009;93(5):563-568. [CrossRef] [PubMed]
9 Hanada H, Ikeda-Dantsuji Y, Naito M, Nagayama A. Infection of human
fibroblast-like synovial cells with Chlamydia trachomatis results in persistent
infection and interleukin-6 production. Microb
Pathog 2003;34(2):57-63. [CrossRef]
10 Boiko EV, Pozniak AL, Maltsev DS, Suetov AA, Nuralova IV. Chronic
ocular chlamydia trachomatis infection in rabbits: clinical and
histopathological findings in the posterior segment. Invest Ophthalmol Vis Sci 2014;55(2):1176-1183. [CrossRef] [PubMed]
11 Boiko EV, Pozniak AL, Ageev VS. To the detection rate of Chlamydia
infection in regmatogenous retinal detachment. Vestn Oftalmol 2008;124(5):52-55. [PubMed]
12 Zigangirova NA, Rumyantseva YP, Morgunova EY, Kapotina LN, Didenko
LV, Kost EA, Koroleva EA, Bashmakov YK, Petyaev IM. Detection of C. trachomatis
in the serum of the patients with urogenital chlamydiosis. Biomed Res Int 2013;2013:489489. [CrossRef] [PubMed] [PMC free article]
13 Ghaffariyeh A, Honarpisheh N, Lari AR. Detection of Chlamydia
trachomatis in the subretinal fluid of a patient with rhegmatogenous retinal
detachment. Clin Exp Optom
2011;94(5):488-489. [CrossRef]
[PubMed]
14 Jendro MC, Fingerle F, Deutsch T, Liese A, Köhler L, Kuipers JG, Raum
E, Martin M, Zeidler H. Chlamydia trachomatis-infected macrophages induce
apoptosis of activated T cells by secretion of tumor necrosis factor-alpha in
vitro. Med Microbiol Immunol
2004;193(1):45-52. [CrossRef]
[PubMed]
15 Levitt D, Danen R, Levitt P. Selective infection of astrocytes by
Chlamydia trachomatis in primary mixed neuron-glial cell cultures. Infect Immun 1986;54(3):913-916. [PMC free article]
[PubMed]
16 Srivastava P, Jha R, Bas S, Salhan S, Mittal A. In infertile women,
cells from Chlamydia trachomatis infected sites release higher levels of
interferon-gamma, interleukin-10 and tumor necrosis factor-alpha upon
heat-shock-protein stimulation than fertile women. Reprod Biol Endocrinol 2008;6:20. [CrossRef] [PubMed] [PMC free article]
17 Rose GE, Billington BM, Chignell AH. Immunoglobulins in paired
specimens of vitreous and subretinal fluids from patients with rhegmatogenous
retinal detachment. Br J Ophthalmol 1990;74(3):160-162.
[CrossRef]
18 Sergienko SN,
Leus EA, Chichur DA. Acid-Base Balance of Eye Posterior Segment in Retinal
Detachement with PVR. Paper presented at: Third EVRS Congress; September 14,
2003; Sopron, Hungary. Available at http://www.evrs.eu/acid-base-balance-of-eye-posterior-segment-in-retinal-detachement-with-pvr/
Accessed Jan.10, 2015.
19 Lewandowska-Furmanik M, Pozarowska D, Pozarowski P, Matysik A.
TH1/TH2 balance in the subretinal fluid of patients with rhegmatogenous retinal
detachment. Med Sci Monit 2002;8(7):CR526-528.
[PubMed]
20 Colin J, Robinet A. Clear lensectomy and implantation of a low-power
posterior chamber intraocular lens for correction of high myopia: a four-year
follow-up. Ophthalmology
1997;104(1):73-77; discussion 77-78. [CrossRef]
21 Hirokawa H, Takahashi M, Trempe CL. Vitreous changes in peripheral
uveitis. Arch Ophthalmol 1985;103(11):1704-1707.
[CrossRef]
22 Au Eong KG, Beatty S, Charles SJ. Cytomegalovirus retinitis in
patients with acquired immune deficiency syndrome. Postgrad Med J 1999;75(888):585-590. [CrossRef]
23 World Health Organization.
Global prevalence and incidence of selected curable sexually transmitted
infections: overview and estimates. Geneva, Switzerland: World Health
Organization; 2001. Available at
http://www.who.int/hiv/pub/sti/who_hiv_aids_2001.02.pdf Accessed Jan.14, 2015.
24 Detels R, Green AM, Klausner JD, Katzenstein D, Gaydos C, Handsfield
H, Pequegnat W, Mayer K, Hartwell TD, Quinn TC. The incidence and correlates of
symptomatic and asymptomatic Chlamydia trachomatis and Neisseria gonorrhoeae
infections in selected populations in five countries. Sex Transm Dis 2011;38(6):503-509. [CrossRef]
25 Domeika M, Hallén A, Karabanov L, Chudomirova K, Gruber F, Unzeitig
V, Pöder A, Deak J, Jakobsone I, Lapinskaite G, Dajek Z, Akovbian V, Gomberg M,
Khryanin A, Savitcheva A, Takac I, Glazkova L, Vinograd N, Nedeljkovic M.
Chlamydia trachomatis infections in eastern Europe: legal aspects,
epidemiology, diagnosis, and treatment. Sex
Transm Infect 2002;78(2):115-119. [CrossRef]
26 Haller-Schober EM, El-Shabrawi Y. Chlamydial conjunctivitis (in
adults), uveitis, and reactive arthritis, including SARA. Sexually acquired
reactive arthritis. Best Pract Res Clin
Obstet Gynaecol 2002;16(6):815-828. [CrossRef] [PubMed]
27 Mabey D, Peeling RW. Lymphogranuloma venereum. Sex Transm Infect 2002;78(2):90-92. [CrossRef] [PubMed] [PMC free article]
28 Hu VH, Holland MJ, Burton MJ. Trachoma: Protective and Pathogenic
Ocular Immune Responses to Chlamydia trachomatis. PLoS Negl Trop Dis 2013;7(2):e2020. [CrossRef] [PubMed] [PMC free article]
29 Gorbunov EF, Tsinzerling VA, Semenov NV. Characteristics of perinatal
visceral lesions caused by chlamydia trachomatis. Arkh Patol 2007;69(3):33-36. [PubMed]
30 Chernesky MA. The
laboratory diagnosis of Chlamydia trachomatis infections. Infect Dis Med Microbiol 2005;16(1):39-44.
31 Treharne JD. Chlamydia trachomatis: serological diagnosis. Infection 1982;10 (Suppl 1):25-31. [CrossRef]
32 Moysidis SN, Thanos A, Vavvas DG. Mechanisms of inflammation in
proliferative vitreoretinopathy: from bench to bedside. Mediators Inflamm 2012;2012:815937. [CrossRef] [PubMed] [PMC free article]
33 Bastiaans J, van Meurs JC, Mulder VC, Nagtzaam NM, Smits-te Nijenhuis
M, Dufour-van den Goorbergh DC, van Hagen PM, Hooijkaas H, Dik WA. The role of
thrombin in proliferative vitreoretinopathy. Invest Ophthalmol Vis Sci 2014;55(7):4659-4666. [CrossRef] [PubMed]
[Top]