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Intraocular cysticercosis: clinical characteristics and visual outcome after vitreoretinal surgery
Intraocular Cysticercosis: Clinical Characteristics and Visual Outcome after Vitreoretinal Surgery Tarun Sharma, MD, Sourav Sinha, MD, Nitant Shah, MD, Lingam Gopal, MD, Mahesh P. Shanmugam, MD, Pramod Bhende, MD, Muna Bhende, MD, Nitin S. Shetty, MD, Rajat Agrawal, MD, Dhanashree Deshpande, MD, Jyotirmay Biswas, MD, B. Sukumar, MPhil Purpose: To report the clinical characteristics of, discuss the surgical options for, and analyze the factors affecting the anatomic and visual outcome of intraocular cysticercosis. Design: Retrospective, noncomparative, interventional case series. Participants: Forty-five eyes of 44 Indian patients with posterior segment intraocular cysticercosis. Methods: The charts of 45 eyes, in which intraocular cysticercosis was removed by vitreoretinal surgery (either transscleral or transvitreal), were reviewed. Main Outcome Measures: These included the postoperative retinal status and the best-corrected Snellen visual acuity. Results: Intraocular cysticercosis was present in the vitreous cavity of 27 eyes (60%) and in the subretinal space of 18 eyes (40%). Anterior segment inflammation was seen in 13 eyes (28.8%) and vitreous inflammation in 38 eyes (84.4%). Retinal detachment was observed in 22 eyes (48.8%), with proliferative vitreoretinopathy in 13 eyes (59.09%). Subretinal cysts anterior to the equator (4 eyes) were removed transsclerally, whereas subretinal cysts posterior to the equator and intravitreal cysts (41 eyes) were removed transvitreally. The mean follow-up was 10.5 months. At the last follow-up, the retina was attached in 39 eyes (86.6%); visual acuity of ⱖ5/200 was achieved in 67.5%. Conclusions: Current vitreoretinal surgical techniques enable removal of intraocular cysticercosis in all cases, with reattachment of the retina in 86.6% and recovery of ambulatory vision in approximately 67% of cases. Ophthalmology 2003;110:996 –1004 © 2003 by the American Academy of Ophthalmology.
Cysticercosis, the most common ocular platyhelminth infestation in humans, is caused by encystment of the larvae of the tapeworm Taenia solium.1 Humans are the definitive hosts and pigs the intermediate hosts for T. solium. In cysticercosis, humans become the intermediate host by ingesting eggs of T. solium from contaminated food or water. After penetrating the intestinal wall, the embryo invades the bloodstream and can lodge in various organs, such as brain, skeletal muscles, eye, and subcutaneous tissue. The ocular manifestations can be devastating as the cysticercus increases in size, leading to blindness in 3 to 5 years; death of the parasite causes marked release of toxic products, leading to a profound inflammatory reaction and destruction of the eye.2 Originally received: February 8, 2002. Accepted: October 31, 2002. Manuscript no. 220092. Vitreoretinal Service, Sankara Nethralaya, Vision Research Foundation, Chennai, India. Presented as a scientific poster at the annual meeting of the American Academy of Ophthalmology, 2001 (poster P 333), New Orleans. Supported by the Vision Research Foundation, Chennai, India. The authors have no proprietary interest in the publication of this article. Reprint requests to Tarun Sharma, MD, Sankara Nethralaya, 18 College Road, Chennai 600 017, India. E-mail: [email protected]
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© 2003 by the American Academy of Ophthalmology Published by Elsevier Science Inc.
Medical treatment of ocular cysticercosis with antihelminthic drugs such as praziquantel is not known to be curative.3,4 Although destruction of the larvae in situ by photocoagulation,5,6 cryotherapy,7 and diathermy8 has been attempted with some success, early surgical removal of the parasite is the treatment of choice. We reviewed the charts of 45 cases of intraocular cysticercosis treated by different vitreoretinal surgical techniques. The purpose of the study was to describe the clinical characteristics of, discuss the surgical options for, and analyze the factors affecting the anatomic and visual outcome of intraocular cysticercosis.
Material and Methods The records of 45 eyes of 44 Indian patients with intraocular cysticercosis treated with vitreoretinal surgery in a single tertiary eye care center from 1987 to 2001 were reviewed retrospectively. All patients had posterior segment intraocular cysticercosis, diagnosed either by the characteristic fundus picture showing a cyst with scolex or by ultrasonography in patients with hazy media. On presentation, the parameters noted were age, sex, right or left eye, and vegetarian or nonvegetarian food habits. The pretreatment clinical data included the type and duration of presenting symptoms and associated systemic features, such as seizures and subcutaneous nodules. ISSN 0161-6420/03/$–see front matter doi:10.1016/S0161-6420(03)00096-4
Sharma et al 䡠 Intraocular Cysticercosis and Vitreoretinal Surgery Table 1. Clinical Profile and Surgical
Sex
Preoperative VA
Duration of Symptoms (days)
Vitreous Inflammation
RD
31 10 27 18 12 40 27 18 36 25 30 33 22 9 28 40 40 50 42 37 28 9 25 23 21 39 26 39 38 13 29 40
M M M F F M M M M M M F F M M M M M M M M F M M M M M M M M M M
PL PL 20/20 20/20 PL 20/200 PL 20/600 20/200 PL 20/40 PL PL PL HM PL 20/600 PL 5/200 20/80 20/200 PL CF 1 m 20/40 HM 20/80 20/40 20/200 20/600 20/40 20/600 20/30
10 16 90 150 7 180 30 18 45 7 60 120 15 10 60 90 90 150 12 240 60 90 30 30 90 180 20 17 120 60 60 8
Y Y Y N Y Y Y Y Y Y Y N Y Y Y Y Y Y N Y N Y Y Y Y Y Y N Y Y Y Y
4Q 3Q X X 4Q X 4Q 1Q 2Q 4Q 1Q 4Q X 4Q 4Q 4Q X 4Q X X X X X X 2Q X X X 3Q X 3Q X
46 5 37 23 35 27 32 6 22 13 12 15 8
M M M F M M M M F F F F F
20/60 PL HM 20/200 5/200 CF 1 m 20/400 HM HM HM HM 20/120 CF 1 m
365 4 120 1080 60 15 900 30 3 90 120 30 10
Y Y Y Y Y Y ⫹ VH N Y Y Y Y N Y
X 4Q 1Q X 2Q X X 1Q 1Q X 4Q X X
Patient No.
Age (yrs)
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45
A ⫽ anterior; AR ⫽ attached retina; CF ⫽ counting fingers; DR ⫽ detached retina; ERM ⫽ epiretinal membrane; F ⫽ female; HM ⫽ hand movements; quadrant; RD ⫽ retinal detachment; SOR ⫽ silicone oil removal; SR ⫽ Subretinal; SRG ⫽ subretinal gliosis; SR-M ⫽ sub macular; SR-P ⫽ subretinal
The best-corrected Snellen visual acuity was recorded. All patients had a detailed ophthalmic evaluation, including slit-lamp biomicroscopy, to note inflammatory changes in the anterior and posterior segments and cataractous changes. The intraocular pressure was recorded with applanation tonometry. Indirect ophthalmoscopy was performed to note the size and location of the cyst with regard to intravitreal or subretinal location, involvement of the macula, and region of the fundus involved. In eyes with clear media, a detailed fundus drawing was done; associated retinal detachment and its extent and proliferative vitreoretinopathy (PVR), if any, were also noted. Ultrasound B-scan with vector A-scan (Alcon Ultrascan Analyzer, Irvine, CA) was done in the vitreous setting in 25 eyes. Plain and contrast-enhanced computed tomographic scan of the brain was performed in 11 patients with suspected cerebral cysticercosis. Magnetic
resonance imaging of the brain was performed on two patients. All available surgical specimens (37 eyes) were subjected to histopathologic study and microscopic examination. All patients underwent surgery under general anesthesia. The intraoperative parameters noted were the type of surgical technique used, complications observed during the procedure, and whether the cyst was removed in toto or piecemeal. The intraocular cysticerci were removed either through an external sclerotomy with choroidal incision or via pars plana vitrectomy.
Transscleral Approach Transscleral approach was used for subretinal cysts located anterior to the equator. A 360° limbal peritomy was performed, and all
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Ophthalmology Volume 110, Number 5, May 2003 Outcome in Intraocular Cysticercosis
PVR
Cyst Location
Surgery
Anatomic Outcome
Postoperative VA
Follow-up (mos)
P A, P, SR X X A, P, SR X X X P X X P, SR X X A, P A, P X P X X X X X X X X X X X X P
V V SR-P V V SR-M V V V V SR-P V SR-M SR-P V V SR-P V SR-M V V V V V SR-P SR-P SR-P SR-M V V SR-P
TV TV TS TV TV TV TV TV TV TV TV TV TV TS TV TV TV TV TV TV TV TV TV TV TV TV TS TV TV TV TV
AR DR AR AR DR AR AR AR AR DR AR AR AR DR DR AR AR AR AR AR AR AR AR AR AR AR AR AR AR AR AR
5/200 PL CF 1 m 20/20 HM 20/120 NA 20/20 NA PL 20/40 20/120 5/200 PL HM HM 20/200 CF 1 m CF 1 m 20/20 20/200 CF 1 m 20/30 20/20 20/600 20/120 20/30 CF 1 m 20/120 20/20 HM
34 2 3 2 4 4 0.5 10 0.7 2 7 17 4 8 6 15 15 4 2 2 72 76 7 3 2 17 19 2 11 2 24
X X X A, P SRG X X X P P X A, P X X
V V SR-P V V SR-P SR-M SR-P V SR-P SR-P V V V
TV TV TV TV TV TV TV TV TV TV TS TV TV TV
AR AR DR AR AR AR AR AR AR AR AR AR AR AR
20/20 20/60 NA NA NA 20/120 CF 1 m 20/60 20/200 20/200 5/200 20/80 20/60 20/20
3 4 2 2 1 13 11 2 20 15 2 4 2 11
Remarks SOR ⫹ ERM removal Abandoned during surgery Developed ERM, advised surgery Cyst rupture, abandoned during surgery
Abandoned during surgery SOR SOR ⫹ cataract, dry macular fold SRG Redetached after second surgery Redetached Cataract Cyst cut with Microvit Laser barrage after surgery Cyst cut with Microvit Dry retinal fold superiorly 2 resurgeries, SOR and cataract Preoperative laser around cyst Developed ERM, advised surgery Preoperative laser around cyst, SOR, cataract, trabeculectomy Abandoned during surgery Cyst cut with Microvit Cyst cut with Microvit Cataract surgery Cyst rupture, PO SRG at macula Cyst rupture, PO subretinal scar Inferior dry retinal fold Cyst rupture, PO inferior retinal fold Cyst rupture Scar—superiorly dragged fovea
M ⫽ male; N ⫽ no; NA ⫽ not applicable; P ⫽ posterior; PL ⫽ light perception; PO ⫽ postoperative; PVR ⫽ proliferative vitreoretinopathy; Q ⫽ peripheral; TS ⫽ transscleral; TV ⫽ transvitreal; V ⫽ intravitreal cyst; VA ⫽ visual acuity; X ⫽ absent; Y ⫽ yes.
four recti were tagged with 4-O silk. The cyst was localized with indirect ophthalmoscopy, and the exact site was marked with diathermy. A radial sclerotomy of adequate size was made at this site, and preplaced sutures were taken with 6-O polyglactin. The choroid was exposed after the scleral fibers were separated with a scarifier, and obvious blood vessels were cauterized. Just before the choroid was incised, indirect ophthalmoscopy was repeated to confirm that the parasite had not moved. The cyst was removed through the choroidal incision with gentle pressure on the globe. The preplaced sutures were used to close the sclerotomy. After the sclerotomy was supported with an adequately sized silicone tire (MIRA, Inc., Waltham, MA) or No. 240 encircling band, the conjunctiva was closed with 6-O polyglactin.
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Transvitreal Approach Transvitreal approach was used for intravitreal cysts and subretinal cysts located posterior to the equator. A limited or a 360° limbal peritomy was done. An encircling 2.5-mm band (No. 240; MIRA) was positioned to support the posterior vitreous base in eyes with peripheral vitreous traction. Sclerotomies for the vitreous cutter, endoilluminator, and infusion cannula were made 3 to 3.5 mm from the limbus, depending on the age of the patient and the lens status. A standard three-port vitrectomy was performed in all cases. For a intravitreal cyst, after it was freed from vitreous attachments, the cyst was either sucked into a flute needle or the vitreous
Sharma et al 䡠 Intraocular Cysticercosis and Vitreoretinal Surgery
Figure 1. Intravitreal cysticercus. Note the invaginated scolex, seen as a white structure inside the cyst cavity.
Figure 3. Subretinal cysticercus in the macular region.
cutter or removed with a 20-gauge cryoprobe with a silicone sleeve and delivered through the sclerotomy, which was enlarged if necessary. In some cases, the cyst was cut and removed. For a subretinal cyst, a retinotomy was made close to the cyst, avoiding the large retinal blood vessels. For submacular cysts, retinotomy was made preferentially along the horizontal raphe. A siliconetipped extrusion cannula was used to deliver the cyst into the vitreous cavity and remove it, as mentioned previously. Fluid– gas exchange was performed, and the retinotomy was sealed with an endolaser. Associated retinal detachment and PVR were managed by standard techniques to settle the retina. Silicone oil or intraocular gases were used as tamponading agents, depending on the indication and surgeon preference. After surgery, the parameters studied were the best-corrected Snellen visual acuity, the retinal status, reoperations, and their outcome. Anatomic success was defined as an attached retina and functional success as a visual acuity of ⱖ5/200 at the last followup. The mean follow-up was 10.5 months (range, 2 weeks to 76 months) with a median of 5.2 months. Twenty eyes had a follow-up of longer than 6 months. Fisher’s exact and Pearson’s chi-square test tests were used to analyze the significance of various factors to the anatomic and visual outcome, with a significance level at P ⱕ 0.05.
Results Demographic Data and Anterior Segment Findings Forty-five eyes of 44 patients (1 bilateral) with intraocular cysticercosis underwent vitreoretinal surgery. The clinical profiles of included patients are summarized in Table 1. Of the patients examined, 33 (75%) were male and 11 (25%) female. The right eye was involved in 28 (62.2%) cases and the left eye in 17 (37.8%). At the time of diagnosis, age ranged from 5 to 50 years (mean, 26.35 years). Six patients were younger than 10 years and 7 between 10 and 20 years. The maximum number of cases, i.e., 29 (64.4%), was seen in the age group between 20 and 40 years, whereas only 3 patients were older than 40 years. Thirty-four (77.3%) patients were found to be taking a nonvegetarian diet. The most common presenting symptom was decreased vision, seen in 42 eyes (93.3%). Other symptoms were floaters in 12 (26.6%), pain in 8 (17.7%), and redness in 6 (13.3%) eyes. One patient had strabismus and one had diplopia on presentation. The duration of symptoms varied from ⬍1 month for 21 eyes (46.7%), 1 to 3 months for 13 (28.9%), 3 to 6 months for 8 (17.7%), and ⬎ 6 months for 3 (6.6%). Seven patients gave a history of seizures. One patient had subcutaneous cysticercosis.
Figure 2. Subretinal cysticercus at different times. Note the scolex showing movement.
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Ophthalmology Volume 110, Number 5, May 2003 of the live cyst could be observed on B-scan, with the probe held steady and the ultrasound beam passing through the cyst. Computed tomographic scan showed evidence of cerebral cysticercosis in 11 (24.4%) cases, out of which 7 patients had histories of seizures. All had hyperdense lesions in the brain. Two patients showed ring-enhancing lesions on intravenous contrast. Histopathologic examination was performed in 37 eyes. The cysts were transported to the laboratory in 10% formalin. On microscopic examination, a trilaminated corrugated cell wall could be seen. Some specimens showed multiple calcareous corpuscles under the cyst wall. Evidence of suckers and hooklets and a branched tract in the protoscolex constituted other diagnostic features (Fig 5A, B).
Surgical Procedures and Their Outcome
Figure 4. Ultrasound B-scan showing a curvilinear echo corresponding to the cyst wall of a subretinal cyst associated with detachment of the overlying retina. The scolex (arrow) is seen as a high-density shadow inside the cyst. Note the high-amplitude spikes on the A-scan that correspond to the detached retina, the anterior cyst wall, and the scolex.
The initial visual acuity was 20/20 to 20/40 in 7 eyes (15.5%), 20/60 to 20/200 in 9 (20%), 20/200 to 5/200 in 7 (15.5%), and ⬍5/200 in 22 (48.8%), out of which 12 eyes had only light perception. The anterior segment was normal in 25 eyes (55.6%), whereas signs of anterior uveitis could be seen in 13 eyes (28.8%). A relative afferent pupillary defect was noted in seven eyes (15.6%). The intraocular pressure was 10 to 18 mmHg in 32 eyes (71.1%), ⬍8 mmHg in 7 eyes (15.6%), and digitally normal in 6 eyes (13.3%). Cataractous changes were seen in six eyes (13.3%).
Posterior Segment Findings Examination of the posterior segment showed signs of inflammation in the vitreous cavity in 38 (84.4%) eyes. One case had vitreous hemorrhage. The retina was found to be attached in 23 (51.2%) eyes. Of the 22 (48.8%) eyes with retinal detachment, the extent was noted to be 1 quadrant in 5 eyes, 2 quadrants in 3 eyes, 3 quadrants in 3 eyes, and total detachment in 11 eyes. In the eyes with retinal detachment, 13 (59.09%) showed PVR on preoperative examination. Clinically, the cyst was seen in the vitreous cavity (Fig 1) in 27 eyes (60%) and was subretinal (Fig 2) in 18 eyes (40%); one patient showed a subretinal cyst that had partially come into the vitreous cavity. Of the subretinal cysts, five were in the macular area (Fig 3), four were equatorial or anterior to the equator, and nine were posterior to the equator. The most common location of the cyst in 17 (37.8%) eyes was the inferotemporal quadrant, whereas in 12 (26.6%) eyes, it was in the upper temporal quadrant. Five (11.1%) cysts were in the upper nasal and six (13.3%) in the lower nasal quadrant; five (11.1%) cysts were located in the macular area.
Ancillary Investigations A cyst could be demonstrated in all 25 eyes in which ultrasound examination was performed. On B-scan, a circular curvilinear echo corresponding to the cyst wall was seen, and the scolex was seen as a round, high-density echo connected to this curvilinear echo. A-scan demonstrated two high-amplitude echoes corresponding to the cyst walls; a 100% high reflective echo was seen when the beam passed through the scolex (Fig 4). Spontaneous movements
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Three patients underwent scleral buckling and removal of the cyst transsclerally without vitrectomy, whereas one patient underwent transscleral cyst removal with vitrectomy (Table 2). All had subretinal peripheral cysts located equatorially or anterior to the equator. Before surgery, two patients had attached retinas, and one had a total retinal detachment without PVR. In the eyes that underwent transscleral cyst removal, the retina was attached in three eyes (75%) after the first operation, whereas functional success (visual acuity, ⬎5/200) was achieved in two eyes (50%). One patient required reoperation, but the retina remained detached after surgery and was deemed inoperable. In all remaining 41 eyes, the cyst could be successfully removed by an internal approach with three-port pars plana vitrectomy (Table 3). However, in four eyes, after removal of the cyst and clearing the media opacity, the underlying retinal detachment was found to be inoperable. Of the remaining 37 eyes, the retina was attached before surgery in 20 eyes and detached in 17 (Table 2). After the first surgery, anatomic success was achieved in 35 (94.6%) of the 37 eyes. Of the remaining two eyes with detached retinas, one patient underwent successful reoperation, whereas the other did not follow up for the surgery. Thus, for the transvitreal group, retinal attachment was seen in 36 eyes (97.2%) and functional success in 25 (67.5%) of 37 eyes (Figs 6A, B and 7A, B). Irrespective of whether the cyst was removed transsclerally or transvitreally, the overall anatomic success rate was 86.6% (39 of 45 eyes), and the functional success was 67.5% (27 of 40 eyes); in 5 eyes (cases 7, 9, 34, 35, and 36), postoperative vision was not recorded in the charts.
Intraoperative Complications and Additional Procedures In the eyes that underwent transscleral cyst removal, minimal hemorrhage was noted during surgery at the site of cyst removal in two eyes. This resolved in the postoperative period and did not affect the surgical outcome. In the eyes with transvitreal cyst removal, the complications encountered during surgery were iatrogenic breaks in 11 (26.8%) eyes and instrument touch without breaks in 2 (4.8%) eyes. The cyst got stuck during removal in the sclerotomy site in one eye (which was removed with the 20-gauge endocryoprobe) and in the vitreous cutter in one eye (which was cut by the vitrectomy probe). The cyst could be removed in toto in 35 eyes (77.7%) but got ruptured during removal in 6 eyes (13.3%); 1 rupture occurred outside the globe. In four (8.9%) cases, the cyst was cut and removed inside the vitreous cavity with the vitreous cutter. After surgery, three eyes showed an epiretinal membrane, out of which two were operated for removal of the same, one along with silicone oil removal. One case required silicone oil removal, two required cataract extraction, two underwent cataract plus sil-
Sharma et al 䡠 Intraocular Cysticercosis and Vitreoretinal Surgery Table 2. Surgical Management and Anatomic Outcome in Intraocular Cysticercosis
RD ⫽ retinal detachment; FU ⫽ follow-up.
icone oil removal, and one underwent trabeculectomy with mitomycin C in addition to cataract and silicone oil removal.
Prognostic Predictors of Surgical Outcome The influence of various preoperative and intraoperative variables on the anatomic and functional success was analyzed with SPSS software (SPSS Inc., Chicago, IL). It was found that the anatomic success was significantly better in the age group ⬎30 years (P ⫽ 0.049), in eyes without preoperative retinal detachment (P ⫽ 0.009), with retinal detachment less than two quadrants (P ⫽ 0.051), and with preoperative visual acuity of ⬎5/200 (P ⫽ 0.014). The functional outcome was better in eyes with retinal detachment less than two quadrants (P ⫽ 0.013) and preoperative vision of ⬎5/200 (P ⫽ 0.032). The presence of anterior segment inflammation significantly affected the anatomic outcome (P ⫽ 0.003), but not the functional success (P ⫽ 0.091). Other factors, such as the gender of the patient, food habits, duration of symptoms, location of the cyst, vitreous inflammation, and PVR, did not affect the anatomic or functional outcome.
Discussion Although extraocular cysticercosis is troublesome because of associated pain, proptosis, and restricted ocular move-
ments, invasion of intraocular tissues by the parasite is more devastating on account of the inflammatory destruction it causes. Our study showed that intraocular cysticercosis predominantly affected males in their third and fourth decades of life. Other studies have also shown preponderance in young males.9,10 The exact reason for this is unknown, but the ratio of the working female population’s being low (and so less exposed to unhygienic food and water) may be the contributing factor. Most of the patients had a nonvegetarian diet, with less than one fourth being vegetarians. Consumption of ill-cooked pork has been cited as a major cause of taeniasis. However, fecal contamination of food and water, as well as autoinfection, plays a very important role in Table 3. Transvitreal Approach Surgery
No. Eyes (%)
Vitrectomy ⫹ cyst removal Vitrectomy ⫹ cyst removal ⫹ gas Vitrectomy ⫹ cyst removal ⫹ SOI Lensectomy ⫹ vitrectomy ⫹ cyst removal Lensectomy ⫹ vitrectomy ⫹ cyst removal ⫹ SOI
16 (39.02) 9 (21.95) 7 (17.07) 5 (12.19) 4 (09.75)
SOI ⫽ silicone oil injection.
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Figure 5. A, Gross photograph of a live cysticercus removed from the vitreous cavity. Note the evaginated scolex. B, Microphotograph showing the scolex and the branched tract (arrow) in the intestine of a cysticercus (stain, hematoxylin– eosin; magnification, ⫻100).
Figure 6. Preoperative and postoperative photographs of a patient operated on for intravitreal cysticercosis. A, An 18-year-old male patient with intravitreal cysticercus in the superotemporal quadrant; visual acuity was 20/600. B, Ten months after surgery, the cyst entry site shows a chorioretinal scar; visual acuity had improved to 20/20.
Figure 7. Preoperative and postoperative photographs of a 40-year-old male patient with subretinal cysticercosis. A, Cyst seen in the subretinal space along the inferotemporal arcade; visual acuity was 20/200. B, Four months after surgery, a chorioretinal scar is seen at the site occupied by the cyst; visual acuity was 20/120.
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Sharma et al 䡠 Intraocular Cysticercosis and Vitreoretinal Surgery Table 4. Comparison of Anatomic and Functional Successes with Those in Previous Reports Study
No. Eyes
Postoperative VA
Anatomic Outcome
Follow-up
Transvitreal approach Natarajan26 5 ⬎20/40 (100%) 100% 6 mos Hutton22 1 20/20 AR 2 wks Messner19 1 20/70 AR 2 wks Zinn24 1 20/50 AR 1 yr 25 Steinmetz 1 20/25 AR 3 mos Kruger-Leite15 1 CF 1 m AR 4 mos Luger27 1 25/20 AR 2 wks Transscleral approach 20 1 CF NA Bartholomew * Aracena21† 1 Transvitreal ⫹ transscleral Cardenas16 30 ⬎20/200 (19%) 33.3% Not given This study 45 ⬎5/200 (67.5%) AR (86.6%) 10.5 mos *Visual loss due to massive intraoperative hemorrhage. Successful transscleral removal; details not mentioned. AR ⫽ attached retina; CF ⫽ counting fingers; NA ⫽ not applicable; VA ⫽ visual acuity.
†
causing cysticercosis. Atul et al,9 who studied the sociodemographic trends in ocular cysticercosis in India, showed a male preponderance of 2:1, with the maximum number of patients seen in the fourth decade; 30% of them were vegetarians. The right eye was more commonly involved than the left. Other studies,9 –12 which document left eye predilection, explained it on the basis of a more direct course of the left carotid from the aorta. Bilateralism has rarely been reported.13,14 In our study, only one patient had bilateral involvement. Several important characteristics of intraocular cysticercosis can be highlighted. We observed the cyst to be more commonly located in the vitreous cavity (27 eyes [60%]) as compared with its location in the subretinal space (40%). Other authors, too, make similar observations.15,16 The cysticercosis most probably enters the eye via the choroidal circulation; the large choroidal vessels have a larger flow rate. From the choroid, it migrates into the subretinal space and then into the vitreous cavity through a hole in the retina. This passage incites inflammation and results in the formation of a chorioretinal scar. In the 27 eyes with intravitreal cysts, we noted the presence of such a scar in 23 eyes either before or during surgery after clearing the inflammatory material. However, in 4 eyes (cases 20, 21, 23, and 33), we did not detect entry site chorioretinal scars. We therefore hypothesize that in these cases, the cyst might have entered the vitreous cavity from the retinal arteries, optic nerve head, or ciliary body, an area located very anteriorly and hence difficult to view during vitreous surgery. One eye (case 23) showed isolated segmental sheathing of the inferotemporal arcade; the vasculitis could have been caused either by passage of the parasite through the retinal artery or associated immunologic reactions. Approximately 85% cases showed vitreous inflammation; one fourth of them had spillover anterior uveitis. It was seen that even a live cyst could induce inflammation, as
stated by Cardenas et al.16 Inflammation could worsen the prognosis by causing a traction or combined traction–rhegmatogenous retinal detachment. Therefore, we used oral prednisolone (1 mg/kg body weight, with a maximum dose of 60 mg) in all patients with evidence of intraocular inflammation; however, the treatment was tapered according to the clinical response in the postoperative period. Most cases required a 2-week course. We did not use antihelminthic drugs for posterior segment intraocular cysticercosis, but they are known to be helpful in neurocysticercosis and orbital cysticercosis, which affect the extraocular muscles.17,18 Retinal detachment was seen in approximately half the cases. Preoperative localization of the break may prove to be difficult on account of poor visualization. Traction induced by inflammatory membranes played an important role in many cases. PVR also registered a higher incidence (60%). This could be explained by the inflammatory component. Cardenas et al16 have documented retinal detachment in 63% in their series, although the incidence of PVR was not mentioned. Most authors agree that early surgical removal is the treatment of choice in intraocular cysticercosis. Messner and Kammerer19 showed in their case report that even a delay of up to 9 months in surgery did not affect the visual outcome and that conservative treatment with steroids was feasible. It has also been suggested that attempts to remove a cyst before it detaches from the subretinal space and becomes free-floating in the vitreous might cause loss of the eye by hemorrhage or cyst rupture.19 In our study, too, a patient (case 21) with a delay of ⬎4 years in surgery did not have an untoward surgical outcome. However, we opted for immediate surgical removal in all cases where this was feasible, because removal of even subretinal cysticercosis with modern vitreoretinal techniques is safe. Transscleral cyst removal was performed in four eyes with the parasite located anterior to the equator. The problem with this approach is the movement of a live cyst to another location, especially after exposure to strong illumination of the indirect ophthalmoscope, leading to either retinal incarceration or vitreous loss. Vitreous hemorrhage (despite choroidal diathermy), partial cyst removal, and cyst rupture are other complications encountered. Transscleral removal thus becomes a hazardous procedure, and accurate localization becomes the most important step. A dead parasite would be easier to remove because no movement would be expected. We could achieve an anatomic success rate of 75% and a functional success rate of 50% with this approach. Other authors have used this approach, although with poorer results20,21 (Table 4). The transvitreal approach was used for intravitreal cysts and subretinal cysts posterior to the equator. This approach is preferable to more difficult procedures22 in which exposure posteriorly is made possible by performing a canthotomy, disinserting the recti, and performing a lateral orbitotomy and Kronlein procedure, followed by transscleral removal of the cyst, as advocated by some authors.20,23 Complete separation of all vitreous attachments from the cyst and intact removal by using only aspiration, without cutting, are the essential steps of pars plana vitrectomy.24 –26
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Ophthalmology Volume 110, Number 5, May 2003 It is important to remove the posterior hyaloid in all cases to prevent postoperative contraction of the vitreous cortex, which can induce a tractional retinal detachment. It has been stated that cutting the cyst in situ with the vitreous cutter may release the toxic contents, inducing more postoperative inflammation.27 However, in the nine eyes in which the cyst was either cut or ruptured inside the vitreous cavity in our study, the outcome was not compromised. Of the four cases in which the cyst was cut with the vitreous cutter (cases 17, 21, 35, and 36), one maintained vision, one showed visual improvement, and two did not come for a follow-up. In the five eyes in which the cyst ruptured inside the vitreous cavity (cases 10, 38, 40, 42, and 44), three showed visual improvement, one maintained vision, and one case was abandoned during surgery. There was no statistically significant difference in the anatomic (P ⫽ 0.65) or functional (P ⫽ 0.592) outcome between the cases in which the cyst was removed in toto and the cases in which it was not. We believe that an adequate vitrectomy with infusion of balanced salt solution can wash out all the toxic products. Table 4 compares the anatomic and visual results of this study with those of published case series and isolated case reports. The results of our study suggest that posterior segment intraocular cysticercosis could be successfully removed in all cases, either by a transscleral or transvitreal route, depending on location. Both approaches provided good results; however, the two could not be compared, because their indications were different. Precise localization is crucial in the first approach, whereas a good vitrectomy with removal of the posterior hyaloid is important in the second. Cutting the cyst in situ or inadvertent cyst rupture did not compromise the outcome. Early surgery is advocated in all cases, because use of retinotomies and an endolaser makes removal of subretinal cysticerci safe. It is not necessary to increase the size of the sclerotomy to equal the cyst diameter, because the cyst molds itself and can be extracted through much smaller openings.
6. 7. 8. 9. 10. 11. 12. 13. 14. 15. 16. 17. 18. 19. 20. 21. 22. 23.
References 24. 1. Duke-Elders S, Perkins ES. System of Ophthalmology. Inflammations of the Uveal Tract: Uveitis. St. Louis: Mosby, 1966;chap. 3, v. 9, 478 – 87. 2. Junior L. Ocular cysticercosis. Am J Ophthalmol 1949;32: 523– 48. 3. Santos R, Chavarria M, Aguirre AE. Failure of medical treatment in two cases of intraocular cysticercosis. Am J Ophthalmol 1984;97:249 –50. 4. Kestelyn P, Taelman H. Effect of praziquantel on intraocular cysticercosis: a case report. Br J Ophthalmol 1985;69:788 –90. 5. Santos R, Dalma A, Ortiz E, Sanchez-Bulnes L. Management
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25. 26. 27.
of subretinal and vitreous cysticercosis: role of photocoagulation and surgery. Ophthalmology 1979;86:1501–7. George AE, Biswas J, Agarwal R, et al. Subretinal cysticercosis in a patient with AIDS: treatment with xenon arc photocoagulation. Retina 1999;19:467– 8. Mais FA. [Cryosurgery in ocular cysticercosis]. Rev Bras Oftalmol 1969;28:99 –103. Gemolotto G. A contribution to the surgical treatment of intraocular cysticercosis. Arch Ottalmol 1955;59:365– 8. Atul K, Kumar TH, Mallika G, Sandip M. Socio-demographic trends in ocular cysticercosis. Acta Ophthalmol Scand 1995; 73:438 – 41. Reddy PS, Satyendran OM. Ocular cysticercosis. Am J Ophthalmol 1964;57:664 – 6. Malik SRK, Gupta AK, Choudhry S. Ocular cysticercosis. Am J Ophthalmol 1968;66:1168 –71. Sen DK, Thomas A. Cysticercosis cellulosae causing subconjunctival abscess. Am J Ophthalmol 1969;68:714 –5. Topilow HW, Yimoyines DJ, Freeman HM, et al. Bilateral multifocal intraocular cysticercosis. Ophthalmology 1981;88: 1166 –72. Balakrishnan E. Bilateral intraocular cysticerci. Br J Ophthalmol 1961;45:150 –1. Kruger-Leite E, Jalkh AE, Quiroz H, Schepens CL. Intraocular cysticercosis. Am J Ophthalmol 1985;99:252–7. Cardenas F, Quiroz H, Plancarte A, et al. Taenia solium ocular cysticercosis: findings in 30 cases. Ann Ophthalmol 1992;24: 25– 8. Del Brutto OH, Sotelo J, Roman GC. Therapy for neurocysticercosis: a reappraisal. Clin Infect Dis 1993;17:730 –5. Sekhar GC, Lemke BN. Orbital cysticercosis. Ophthalmology 1997;104:1599 – 604. Messner KH, Kammerer WS. Intraocular cysticercosis. Arch Ophthalmol 1979;97:1103–5. Bartholomew RS. Subretinal cysticercosis. Am J Ophthalmol 1975;79:670 –3. Aracena T, Roca FP. Macular and peripheral subretinal cysticercosis. Ann Ophthalmol 1981;13:1265–7. Hutton WL, Vaiser A, Snyder WB. Pars plana vitrectomy for removal of intravitreous cysticercus. Am J Ophthalmol 1976; 81:571–3. Segal P, Mrzyglod S, Smolarz-Dudarewicz J. Subretinal cysticercosis in the macular region. Am J Ophthalmol 1964;57: 655– 64. Zinn KM, Guillory SL, Friedman AH. Removal of intravitreous cysticerci from the surface of the optic nervehead. A pars plana approach. Arch Ophthalmol 1980;98:714 – 6. Steinmetz RL, Masket S, Sidikaro Y. The successful removal of a subretinal cysticercus by pars plana vitrectomy. Retina 1989;9:276 – 80. Natarajan S, Malpani A, Kumar Nirmalan P, Dutta B. Management of intraocular cysticercosis. Graefes Arch Clin Exp Ophthalmol 1999;237:812– 4. Luger MH, Stilma JS, Ringens PJ, van Baarlen J. In-toto removal of subretinal Cysticercus cellulosae by pars plana vitrectomy. Br J Ophthalmol 1991;75:561–3.
Cysticercosis, the most common ocular platyhelminth infestation in humans, is caused by encystment of the larvae of the tapeworm Taenia solium.1 Humans are the definitive hosts and pigs the intermediate hosts for T. solium. In cysticercosis, humans become the intermediate host by ingesting eggs of T. solium from contaminated food or water. After penetrating the intestinal wall, the embryo invades the bloodstream and can lodge in various organs, such as brain, skeletal muscles, eye, and subcutaneous tissue. The ocular manifestations can be devastating as the cysticercus increases in size, leading to blindness in 3 to 5 years; death of the parasite causes marked release of toxic products, leading to a profound inflammatory reaction and destruction of the eye.2 Originally received: February 8, 2002. Accepted: October 31, 2002. Manuscript no. 220092. Vitreoretinal Service, Sankara Nethralaya, Vision Research Foundation, Chennai, India. Presented as a scientific poster at the annual meeting of the American Academy of Ophthalmology, 2001 (poster P 333), New Orleans. Supported by the Vision Research Foundation, Chennai, India. The authors have no proprietary interest in the publication of this article. Reprint requests to Tarun Sharma, MD, Sankara Nethralaya, 18 College Road, Chennai 600 017, India. E-mail: [email protected]
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© 2003 by the American Academy of Ophthalmology Published by Elsevier Science Inc.
Medical treatment of ocular cysticercosis with antihelminthic drugs such as praziquantel is not known to be curative.3,4 Although destruction of the larvae in situ by photocoagulation,5,6 cryotherapy,7 and diathermy8 has been attempted with some success, early surgical removal of the parasite is the treatment of choice. We reviewed the charts of 45 cases of intraocular cysticercosis treated by different vitreoretinal surgical techniques. The purpose of the study was to describe the clinical characteristics of, discuss the surgical options for, and analyze the factors affecting the anatomic and visual outcome of intraocular cysticercosis.
Material and Methods The records of 45 eyes of 44 Indian patients with intraocular cysticercosis treated with vitreoretinal surgery in a single tertiary eye care center from 1987 to 2001 were reviewed retrospectively. All patients had posterior segment intraocular cysticercosis, diagnosed either by the characteristic fundus picture showing a cyst with scolex or by ultrasonography in patients with hazy media. On presentation, the parameters noted were age, sex, right or left eye, and vegetarian or nonvegetarian food habits. The pretreatment clinical data included the type and duration of presenting symptoms and associated systemic features, such as seizures and subcutaneous nodules. ISSN 0161-6420/03/$–see front matter doi:10.1016/S0161-6420(03)00096-4
Sharma et al 䡠 Intraocular Cysticercosis and Vitreoretinal Surgery Table 1. Clinical Profile and Surgical
Sex
Preoperative VA
Duration of Symptoms (days)
Vitreous Inflammation
RD
31 10 27 18 12 40 27 18 36 25 30 33 22 9 28 40 40 50 42 37 28 9 25 23 21 39 26 39 38 13 29 40
M M M F F M M M M M M F F M M M M M M M M F M M M M M M M M M M
PL PL 20/20 20/20 PL 20/200 PL 20/600 20/200 PL 20/40 PL PL PL HM PL 20/600 PL 5/200 20/80 20/200 PL CF 1 m 20/40 HM 20/80 20/40 20/200 20/600 20/40 20/600 20/30
10 16 90 150 7 180 30 18 45 7 60 120 15 10 60 90 90 150 12 240 60 90 30 30 90 180 20 17 120 60 60 8
Y Y Y N Y Y Y Y Y Y Y N Y Y Y Y Y Y N Y N Y Y Y Y Y Y N Y Y Y Y
4Q 3Q X X 4Q X 4Q 1Q 2Q 4Q 1Q 4Q X 4Q 4Q 4Q X 4Q X X X X X X 2Q X X X 3Q X 3Q X
46 5 37 23 35 27 32 6 22 13 12 15 8
M M M F M M M M F F F F F
20/60 PL HM 20/200 5/200 CF 1 m 20/400 HM HM HM HM 20/120 CF 1 m
365 4 120 1080 60 15 900 30 3 90 120 30 10
Y Y Y Y Y Y ⫹ VH N Y Y Y Y N Y
X 4Q 1Q X 2Q X X 1Q 1Q X 4Q X X
Patient No.
Age (yrs)
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45
A ⫽ anterior; AR ⫽ attached retina; CF ⫽ counting fingers; DR ⫽ detached retina; ERM ⫽ epiretinal membrane; F ⫽ female; HM ⫽ hand movements; quadrant; RD ⫽ retinal detachment; SOR ⫽ silicone oil removal; SR ⫽ Subretinal; SRG ⫽ subretinal gliosis; SR-M ⫽ sub macular; SR-P ⫽ subretinal
The best-corrected Snellen visual acuity was recorded. All patients had a detailed ophthalmic evaluation, including slit-lamp biomicroscopy, to note inflammatory changes in the anterior and posterior segments and cataractous changes. The intraocular pressure was recorded with applanation tonometry. Indirect ophthalmoscopy was performed to note the size and location of the cyst with regard to intravitreal or subretinal location, involvement of the macula, and region of the fundus involved. In eyes with clear media, a detailed fundus drawing was done; associated retinal detachment and its extent and proliferative vitreoretinopathy (PVR), if any, were also noted. Ultrasound B-scan with vector A-scan (Alcon Ultrascan Analyzer, Irvine, CA) was done in the vitreous setting in 25 eyes. Plain and contrast-enhanced computed tomographic scan of the brain was performed in 11 patients with suspected cerebral cysticercosis. Magnetic
resonance imaging of the brain was performed on two patients. All available surgical specimens (37 eyes) were subjected to histopathologic study and microscopic examination. All patients underwent surgery under general anesthesia. The intraoperative parameters noted were the type of surgical technique used, complications observed during the procedure, and whether the cyst was removed in toto or piecemeal. The intraocular cysticerci were removed either through an external sclerotomy with choroidal incision or via pars plana vitrectomy.
Transscleral Approach Transscleral approach was used for subretinal cysts located anterior to the equator. A 360° limbal peritomy was performed, and all
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Ophthalmology Volume 110, Number 5, May 2003 Outcome in Intraocular Cysticercosis
PVR
Cyst Location
Surgery
Anatomic Outcome
Postoperative VA
Follow-up (mos)
P A, P, SR X X A, P, SR X X X P X X P, SR X X A, P A, P X P X X X X X X X X X X X X P
V V SR-P V V SR-M V V V V SR-P V SR-M SR-P V V SR-P V SR-M V V V V V SR-P SR-P SR-P SR-M V V SR-P
TV TV TS TV TV TV TV TV TV TV TV TV TV TS TV TV TV TV TV TV TV TV TV TV TV TV TS TV TV TV TV
AR DR AR AR DR AR AR AR AR DR AR AR AR DR DR AR AR AR AR AR AR AR AR AR AR AR AR AR AR AR AR
5/200 PL CF 1 m 20/20 HM 20/120 NA 20/20 NA PL 20/40 20/120 5/200 PL HM HM 20/200 CF 1 m CF 1 m 20/20 20/200 CF 1 m 20/30 20/20 20/600 20/120 20/30 CF 1 m 20/120 20/20 HM
34 2 3 2 4 4 0.5 10 0.7 2 7 17 4 8 6 15 15 4 2 2 72 76 7 3 2 17 19 2 11 2 24
X X X A, P SRG X X X P P X A, P X X
V V SR-P V V SR-P SR-M SR-P V SR-P SR-P V V V
TV TV TV TV TV TV TV TV TV TV TS TV TV TV
AR AR DR AR AR AR AR AR AR AR AR AR AR AR
20/20 20/60 NA NA NA 20/120 CF 1 m 20/60 20/200 20/200 5/200 20/80 20/60 20/20
3 4 2 2 1 13 11 2 20 15 2 4 2 11
Remarks SOR ⫹ ERM removal Abandoned during surgery Developed ERM, advised surgery Cyst rupture, abandoned during surgery
Abandoned during surgery SOR SOR ⫹ cataract, dry macular fold SRG Redetached after second surgery Redetached Cataract Cyst cut with Microvit Laser barrage after surgery Cyst cut with Microvit Dry retinal fold superiorly 2 resurgeries, SOR and cataract Preoperative laser around cyst Developed ERM, advised surgery Preoperative laser around cyst, SOR, cataract, trabeculectomy Abandoned during surgery Cyst cut with Microvit Cyst cut with Microvit Cataract surgery Cyst rupture, PO SRG at macula Cyst rupture, PO subretinal scar Inferior dry retinal fold Cyst rupture, PO inferior retinal fold Cyst rupture Scar—superiorly dragged fovea
M ⫽ male; N ⫽ no; NA ⫽ not applicable; P ⫽ posterior; PL ⫽ light perception; PO ⫽ postoperative; PVR ⫽ proliferative vitreoretinopathy; Q ⫽ peripheral; TS ⫽ transscleral; TV ⫽ transvitreal; V ⫽ intravitreal cyst; VA ⫽ visual acuity; X ⫽ absent; Y ⫽ yes.
four recti were tagged with 4-O silk. The cyst was localized with indirect ophthalmoscopy, and the exact site was marked with diathermy. A radial sclerotomy of adequate size was made at this site, and preplaced sutures were taken with 6-O polyglactin. The choroid was exposed after the scleral fibers were separated with a scarifier, and obvious blood vessels were cauterized. Just before the choroid was incised, indirect ophthalmoscopy was repeated to confirm that the parasite had not moved. The cyst was removed through the choroidal incision with gentle pressure on the globe. The preplaced sutures were used to close the sclerotomy. After the sclerotomy was supported with an adequately sized silicone tire (MIRA, Inc., Waltham, MA) or No. 240 encircling band, the conjunctiva was closed with 6-O polyglactin.
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Transvitreal Approach Transvitreal approach was used for intravitreal cysts and subretinal cysts located posterior to the equator. A limited or a 360° limbal peritomy was done. An encircling 2.5-mm band (No. 240; MIRA) was positioned to support the posterior vitreous base in eyes with peripheral vitreous traction. Sclerotomies for the vitreous cutter, endoilluminator, and infusion cannula were made 3 to 3.5 mm from the limbus, depending on the age of the patient and the lens status. A standard three-port vitrectomy was performed in all cases. For a intravitreal cyst, after it was freed from vitreous attachments, the cyst was either sucked into a flute needle or the vitreous
Sharma et al 䡠 Intraocular Cysticercosis and Vitreoretinal Surgery
Figure 1. Intravitreal cysticercus. Note the invaginated scolex, seen as a white structure inside the cyst cavity.
Figure 3. Subretinal cysticercus in the macular region.
cutter or removed with a 20-gauge cryoprobe with a silicone sleeve and delivered through the sclerotomy, which was enlarged if necessary. In some cases, the cyst was cut and removed. For a subretinal cyst, a retinotomy was made close to the cyst, avoiding the large retinal blood vessels. For submacular cysts, retinotomy was made preferentially along the horizontal raphe. A siliconetipped extrusion cannula was used to deliver the cyst into the vitreous cavity and remove it, as mentioned previously. Fluid– gas exchange was performed, and the retinotomy was sealed with an endolaser. Associated retinal detachment and PVR were managed by standard techniques to settle the retina. Silicone oil or intraocular gases were used as tamponading agents, depending on the indication and surgeon preference. After surgery, the parameters studied were the best-corrected Snellen visual acuity, the retinal status, reoperations, and their outcome. Anatomic success was defined as an attached retina and functional success as a visual acuity of ⱖ5/200 at the last followup. The mean follow-up was 10.5 months (range, 2 weeks to 76 months) with a median of 5.2 months. Twenty eyes had a follow-up of longer than 6 months. Fisher’s exact and Pearson’s chi-square test tests were used to analyze the significance of various factors to the anatomic and visual outcome, with a significance level at P ⱕ 0.05.
Results Demographic Data and Anterior Segment Findings Forty-five eyes of 44 patients (1 bilateral) with intraocular cysticercosis underwent vitreoretinal surgery. The clinical profiles of included patients are summarized in Table 1. Of the patients examined, 33 (75%) were male and 11 (25%) female. The right eye was involved in 28 (62.2%) cases and the left eye in 17 (37.8%). At the time of diagnosis, age ranged from 5 to 50 years (mean, 26.35 years). Six patients were younger than 10 years and 7 between 10 and 20 years. The maximum number of cases, i.e., 29 (64.4%), was seen in the age group between 20 and 40 years, whereas only 3 patients were older than 40 years. Thirty-four (77.3%) patients were found to be taking a nonvegetarian diet. The most common presenting symptom was decreased vision, seen in 42 eyes (93.3%). Other symptoms were floaters in 12 (26.6%), pain in 8 (17.7%), and redness in 6 (13.3%) eyes. One patient had strabismus and one had diplopia on presentation. The duration of symptoms varied from ⬍1 month for 21 eyes (46.7%), 1 to 3 months for 13 (28.9%), 3 to 6 months for 8 (17.7%), and ⬎ 6 months for 3 (6.6%). Seven patients gave a history of seizures. One patient had subcutaneous cysticercosis.
Figure 2. Subretinal cysticercus at different times. Note the scolex showing movement.
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Ophthalmology Volume 110, Number 5, May 2003 of the live cyst could be observed on B-scan, with the probe held steady and the ultrasound beam passing through the cyst. Computed tomographic scan showed evidence of cerebral cysticercosis in 11 (24.4%) cases, out of which 7 patients had histories of seizures. All had hyperdense lesions in the brain. Two patients showed ring-enhancing lesions on intravenous contrast. Histopathologic examination was performed in 37 eyes. The cysts were transported to the laboratory in 10% formalin. On microscopic examination, a trilaminated corrugated cell wall could be seen. Some specimens showed multiple calcareous corpuscles under the cyst wall. Evidence of suckers and hooklets and a branched tract in the protoscolex constituted other diagnostic features (Fig 5A, B).
Surgical Procedures and Their Outcome
Figure 4. Ultrasound B-scan showing a curvilinear echo corresponding to the cyst wall of a subretinal cyst associated with detachment of the overlying retina. The scolex (arrow) is seen as a high-density shadow inside the cyst. Note the high-amplitude spikes on the A-scan that correspond to the detached retina, the anterior cyst wall, and the scolex.
The initial visual acuity was 20/20 to 20/40 in 7 eyes (15.5%), 20/60 to 20/200 in 9 (20%), 20/200 to 5/200 in 7 (15.5%), and ⬍5/200 in 22 (48.8%), out of which 12 eyes had only light perception. The anterior segment was normal in 25 eyes (55.6%), whereas signs of anterior uveitis could be seen in 13 eyes (28.8%). A relative afferent pupillary defect was noted in seven eyes (15.6%). The intraocular pressure was 10 to 18 mmHg in 32 eyes (71.1%), ⬍8 mmHg in 7 eyes (15.6%), and digitally normal in 6 eyes (13.3%). Cataractous changes were seen in six eyes (13.3%).
Posterior Segment Findings Examination of the posterior segment showed signs of inflammation in the vitreous cavity in 38 (84.4%) eyes. One case had vitreous hemorrhage. The retina was found to be attached in 23 (51.2%) eyes. Of the 22 (48.8%) eyes with retinal detachment, the extent was noted to be 1 quadrant in 5 eyes, 2 quadrants in 3 eyes, 3 quadrants in 3 eyes, and total detachment in 11 eyes. In the eyes with retinal detachment, 13 (59.09%) showed PVR on preoperative examination. Clinically, the cyst was seen in the vitreous cavity (Fig 1) in 27 eyes (60%) and was subretinal (Fig 2) in 18 eyes (40%); one patient showed a subretinal cyst that had partially come into the vitreous cavity. Of the subretinal cysts, five were in the macular area (Fig 3), four were equatorial or anterior to the equator, and nine were posterior to the equator. The most common location of the cyst in 17 (37.8%) eyes was the inferotemporal quadrant, whereas in 12 (26.6%) eyes, it was in the upper temporal quadrant. Five (11.1%) cysts were in the upper nasal and six (13.3%) in the lower nasal quadrant; five (11.1%) cysts were located in the macular area.
Ancillary Investigations A cyst could be demonstrated in all 25 eyes in which ultrasound examination was performed. On B-scan, a circular curvilinear echo corresponding to the cyst wall was seen, and the scolex was seen as a round, high-density echo connected to this curvilinear echo. A-scan demonstrated two high-amplitude echoes corresponding to the cyst walls; a 100% high reflective echo was seen when the beam passed through the scolex (Fig 4). Spontaneous movements
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Three patients underwent scleral buckling and removal of the cyst transsclerally without vitrectomy, whereas one patient underwent transscleral cyst removal with vitrectomy (Table 2). All had subretinal peripheral cysts located equatorially or anterior to the equator. Before surgery, two patients had attached retinas, and one had a total retinal detachment without PVR. In the eyes that underwent transscleral cyst removal, the retina was attached in three eyes (75%) after the first operation, whereas functional success (visual acuity, ⬎5/200) was achieved in two eyes (50%). One patient required reoperation, but the retina remained detached after surgery and was deemed inoperable. In all remaining 41 eyes, the cyst could be successfully removed by an internal approach with three-port pars plana vitrectomy (Table 3). However, in four eyes, after removal of the cyst and clearing the media opacity, the underlying retinal detachment was found to be inoperable. Of the remaining 37 eyes, the retina was attached before surgery in 20 eyes and detached in 17 (Table 2). After the first surgery, anatomic success was achieved in 35 (94.6%) of the 37 eyes. Of the remaining two eyes with detached retinas, one patient underwent successful reoperation, whereas the other did not follow up for the surgery. Thus, for the transvitreal group, retinal attachment was seen in 36 eyes (97.2%) and functional success in 25 (67.5%) of 37 eyes (Figs 6A, B and 7A, B). Irrespective of whether the cyst was removed transsclerally or transvitreally, the overall anatomic success rate was 86.6% (39 of 45 eyes), and the functional success was 67.5% (27 of 40 eyes); in 5 eyes (cases 7, 9, 34, 35, and 36), postoperative vision was not recorded in the charts.
Intraoperative Complications and Additional Procedures In the eyes that underwent transscleral cyst removal, minimal hemorrhage was noted during surgery at the site of cyst removal in two eyes. This resolved in the postoperative period and did not affect the surgical outcome. In the eyes with transvitreal cyst removal, the complications encountered during surgery were iatrogenic breaks in 11 (26.8%) eyes and instrument touch without breaks in 2 (4.8%) eyes. The cyst got stuck during removal in the sclerotomy site in one eye (which was removed with the 20-gauge endocryoprobe) and in the vitreous cutter in one eye (which was cut by the vitrectomy probe). The cyst could be removed in toto in 35 eyes (77.7%) but got ruptured during removal in 6 eyes (13.3%); 1 rupture occurred outside the globe. In four (8.9%) cases, the cyst was cut and removed inside the vitreous cavity with the vitreous cutter. After surgery, three eyes showed an epiretinal membrane, out of which two were operated for removal of the same, one along with silicone oil removal. One case required silicone oil removal, two required cataract extraction, two underwent cataract plus sil-
Sharma et al 䡠 Intraocular Cysticercosis and Vitreoretinal Surgery Table 2. Surgical Management and Anatomic Outcome in Intraocular Cysticercosis
RD ⫽ retinal detachment; FU ⫽ follow-up.
icone oil removal, and one underwent trabeculectomy with mitomycin C in addition to cataract and silicone oil removal.
Prognostic Predictors of Surgical Outcome The influence of various preoperative and intraoperative variables on the anatomic and functional success was analyzed with SPSS software (SPSS Inc., Chicago, IL). It was found that the anatomic success was significantly better in the age group ⬎30 years (P ⫽ 0.049), in eyes without preoperative retinal detachment (P ⫽ 0.009), with retinal detachment less than two quadrants (P ⫽ 0.051), and with preoperative visual acuity of ⬎5/200 (P ⫽ 0.014). The functional outcome was better in eyes with retinal detachment less than two quadrants (P ⫽ 0.013) and preoperative vision of ⬎5/200 (P ⫽ 0.032). The presence of anterior segment inflammation significantly affected the anatomic outcome (P ⫽ 0.003), but not the functional success (P ⫽ 0.091). Other factors, such as the gender of the patient, food habits, duration of symptoms, location of the cyst, vitreous inflammation, and PVR, did not affect the anatomic or functional outcome.
Discussion Although extraocular cysticercosis is troublesome because of associated pain, proptosis, and restricted ocular move-
ments, invasion of intraocular tissues by the parasite is more devastating on account of the inflammatory destruction it causes. Our study showed that intraocular cysticercosis predominantly affected males in their third and fourth decades of life. Other studies have also shown preponderance in young males.9,10 The exact reason for this is unknown, but the ratio of the working female population’s being low (and so less exposed to unhygienic food and water) may be the contributing factor. Most of the patients had a nonvegetarian diet, with less than one fourth being vegetarians. Consumption of ill-cooked pork has been cited as a major cause of taeniasis. However, fecal contamination of food and water, as well as autoinfection, plays a very important role in Table 3. Transvitreal Approach Surgery
No. Eyes (%)
Vitrectomy ⫹ cyst removal Vitrectomy ⫹ cyst removal ⫹ gas Vitrectomy ⫹ cyst removal ⫹ SOI Lensectomy ⫹ vitrectomy ⫹ cyst removal Lensectomy ⫹ vitrectomy ⫹ cyst removal ⫹ SOI
16 (39.02) 9 (21.95) 7 (17.07) 5 (12.19) 4 (09.75)
SOI ⫽ silicone oil injection.
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Ophthalmology Volume 110, Number 5, May 2003
Figure 5. A, Gross photograph of a live cysticercus removed from the vitreous cavity. Note the evaginated scolex. B, Microphotograph showing the scolex and the branched tract (arrow) in the intestine of a cysticercus (stain, hematoxylin– eosin; magnification, ⫻100).
Figure 6. Preoperative and postoperative photographs of a patient operated on for intravitreal cysticercosis. A, An 18-year-old male patient with intravitreal cysticercus in the superotemporal quadrant; visual acuity was 20/600. B, Ten months after surgery, the cyst entry site shows a chorioretinal scar; visual acuity had improved to 20/20.
Figure 7. Preoperative and postoperative photographs of a 40-year-old male patient with subretinal cysticercosis. A, Cyst seen in the subretinal space along the inferotemporal arcade; visual acuity was 20/200. B, Four months after surgery, a chorioretinal scar is seen at the site occupied by the cyst; visual acuity was 20/120.
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Sharma et al 䡠 Intraocular Cysticercosis and Vitreoretinal Surgery Table 4. Comparison of Anatomic and Functional Successes with Those in Previous Reports Study
No. Eyes
Postoperative VA
Anatomic Outcome
Follow-up
Transvitreal approach Natarajan26 5 ⬎20/40 (100%) 100% 6 mos Hutton22 1 20/20 AR 2 wks Messner19 1 20/70 AR 2 wks Zinn24 1 20/50 AR 1 yr 25 Steinmetz 1 20/25 AR 3 mos Kruger-Leite15 1 CF 1 m AR 4 mos Luger27 1 25/20 AR 2 wks Transscleral approach 20 1 CF NA Bartholomew * Aracena21† 1 Transvitreal ⫹ transscleral Cardenas16 30 ⬎20/200 (19%) 33.3% Not given This study 45 ⬎5/200 (67.5%) AR (86.6%) 10.5 mos *Visual loss due to massive intraoperative hemorrhage. Successful transscleral removal; details not mentioned. AR ⫽ attached retina; CF ⫽ counting fingers; NA ⫽ not applicable; VA ⫽ visual acuity.
†
causing cysticercosis. Atul et al,9 who studied the sociodemographic trends in ocular cysticercosis in India, showed a male preponderance of 2:1, with the maximum number of patients seen in the fourth decade; 30% of them were vegetarians. The right eye was more commonly involved than the left. Other studies,9 –12 which document left eye predilection, explained it on the basis of a more direct course of the left carotid from the aorta. Bilateralism has rarely been reported.13,14 In our study, only one patient had bilateral involvement. Several important characteristics of intraocular cysticercosis can be highlighted. We observed the cyst to be more commonly located in the vitreous cavity (27 eyes [60%]) as compared with its location in the subretinal space (40%). Other authors, too, make similar observations.15,16 The cysticercosis most probably enters the eye via the choroidal circulation; the large choroidal vessels have a larger flow rate. From the choroid, it migrates into the subretinal space and then into the vitreous cavity through a hole in the retina. This passage incites inflammation and results in the formation of a chorioretinal scar. In the 27 eyes with intravitreal cysts, we noted the presence of such a scar in 23 eyes either before or during surgery after clearing the inflammatory material. However, in 4 eyes (cases 20, 21, 23, and 33), we did not detect entry site chorioretinal scars. We therefore hypothesize that in these cases, the cyst might have entered the vitreous cavity from the retinal arteries, optic nerve head, or ciliary body, an area located very anteriorly and hence difficult to view during vitreous surgery. One eye (case 23) showed isolated segmental sheathing of the inferotemporal arcade; the vasculitis could have been caused either by passage of the parasite through the retinal artery or associated immunologic reactions. Approximately 85% cases showed vitreous inflammation; one fourth of them had spillover anterior uveitis. It was seen that even a live cyst could induce inflammation, as
stated by Cardenas et al.16 Inflammation could worsen the prognosis by causing a traction or combined traction–rhegmatogenous retinal detachment. Therefore, we used oral prednisolone (1 mg/kg body weight, with a maximum dose of 60 mg) in all patients with evidence of intraocular inflammation; however, the treatment was tapered according to the clinical response in the postoperative period. Most cases required a 2-week course. We did not use antihelminthic drugs for posterior segment intraocular cysticercosis, but they are known to be helpful in neurocysticercosis and orbital cysticercosis, which affect the extraocular muscles.17,18 Retinal detachment was seen in approximately half the cases. Preoperative localization of the break may prove to be difficult on account of poor visualization. Traction induced by inflammatory membranes played an important role in many cases. PVR also registered a higher incidence (60%). This could be explained by the inflammatory component. Cardenas et al16 have documented retinal detachment in 63% in their series, although the incidence of PVR was not mentioned. Most authors agree that early surgical removal is the treatment of choice in intraocular cysticercosis. Messner and Kammerer19 showed in their case report that even a delay of up to 9 months in surgery did not affect the visual outcome and that conservative treatment with steroids was feasible. It has also been suggested that attempts to remove a cyst before it detaches from the subretinal space and becomes free-floating in the vitreous might cause loss of the eye by hemorrhage or cyst rupture.19 In our study, too, a patient (case 21) with a delay of ⬎4 years in surgery did not have an untoward surgical outcome. However, we opted for immediate surgical removal in all cases where this was feasible, because removal of even subretinal cysticercosis with modern vitreoretinal techniques is safe. Transscleral cyst removal was performed in four eyes with the parasite located anterior to the equator. The problem with this approach is the movement of a live cyst to another location, especially after exposure to strong illumination of the indirect ophthalmoscope, leading to either retinal incarceration or vitreous loss. Vitreous hemorrhage (despite choroidal diathermy), partial cyst removal, and cyst rupture are other complications encountered. Transscleral removal thus becomes a hazardous procedure, and accurate localization becomes the most important step. A dead parasite would be easier to remove because no movement would be expected. We could achieve an anatomic success rate of 75% and a functional success rate of 50% with this approach. Other authors have used this approach, although with poorer results20,21 (Table 4). The transvitreal approach was used for intravitreal cysts and subretinal cysts posterior to the equator. This approach is preferable to more difficult procedures22 in which exposure posteriorly is made possible by performing a canthotomy, disinserting the recti, and performing a lateral orbitotomy and Kronlein procedure, followed by transscleral removal of the cyst, as advocated by some authors.20,23 Complete separation of all vitreous attachments from the cyst and intact removal by using only aspiration, without cutting, are the essential steps of pars plana vitrectomy.24 –26
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Ophthalmology Volume 110, Number 5, May 2003 It is important to remove the posterior hyaloid in all cases to prevent postoperative contraction of the vitreous cortex, which can induce a tractional retinal detachment. It has been stated that cutting the cyst in situ with the vitreous cutter may release the toxic contents, inducing more postoperative inflammation.27 However, in the nine eyes in which the cyst was either cut or ruptured inside the vitreous cavity in our study, the outcome was not compromised. Of the four cases in which the cyst was cut with the vitreous cutter (cases 17, 21, 35, and 36), one maintained vision, one showed visual improvement, and two did not come for a follow-up. In the five eyes in which the cyst ruptured inside the vitreous cavity (cases 10, 38, 40, 42, and 44), three showed visual improvement, one maintained vision, and one case was abandoned during surgery. There was no statistically significant difference in the anatomic (P ⫽ 0.65) or functional (P ⫽ 0.592) outcome between the cases in which the cyst was removed in toto and the cases in which it was not. We believe that an adequate vitrectomy with infusion of balanced salt solution can wash out all the toxic products. Table 4 compares the anatomic and visual results of this study with those of published case series and isolated case reports. The results of our study suggest that posterior segment intraocular cysticercosis could be successfully removed in all cases, either by a transscleral or transvitreal route, depending on location. Both approaches provided good results; however, the two could not be compared, because their indications were different. Precise localization is crucial in the first approach, whereas a good vitrectomy with removal of the posterior hyaloid is important in the second. Cutting the cyst in situ or inadvertent cyst rupture did not compromise the outcome. Early surgery is advocated in all cases, because use of retinotomies and an endolaser makes removal of subretinal cysticerci safe. It is not necessary to increase the size of the sclerotomy to equal the cyst diameter, because the cyst molds itself and can be extracted through much smaller openings.
6. 7. 8. 9. 10. 11. 12. 13. 14. 15. 16. 17. 18. 19. 20. 21. 22. 23.
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