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Serum IgG-ELISA for Diagnosis and Treatment Follow-up of Ophthalmic Cysticercosis


AUTHORS:
Priyadarshi Soumyaranjan Sahu 1,3
Pramod Kumar Sahu 2,4
Subhash Chandra Parija 1

1 Department of Microbiology and 2 Department of Ohthalmology, Jawaharlal Institute of Postgraduate Medical Education and Research, Pondicherry-605006, India.
3Division of Pathology, School of Medicine, International Medical University, 57000 Kuala Lumpur, Malaysia.
4Department of Ophthalmology, UCMS and Guru Teg Bahadur Hospital, Shahdara, New Delhi-110095, India

ADDRESS OF THE CORRESPONDING AUTHOR:
Dr Priyadarshi Soumyaranjan Sahu 
Division of Pathology, School of Medicine, 
International Medical University, 
57000 Kuala Lumpur, Malaysia 
Corresponding author e-mail ID: priyadarshi_sahu@yahoo.co.in; Priyadarshi@imu.edu.my

RUNNING TITLE	:	Serodiagnosis of ophthalmic cisticercosis

KEY WORDS: Cysticercus cellulosae, Taenia solium, Ophthalmic cysticercosis, ELISA. 



Abstract
Ophthalmic cysticercosis (OCC) caused by Taenia solium larval infection in eye, is emerging as a far commoner disease in the tropics. There is a scarcity in serodiagnostics to aid its laboratory diagnosis; thereby management still continues to pose a serious challenge. Presently serum IgG-ELISAs were performed on 40 consecutive clinically diagnosed OCC cases. Extra-ocular muscle was found to be the predominant site of infection where ocular motility disorder was the major clinical presentation. ELISA using larval somatic and excretory secretory (ES) antigens was positive in 32.5% and 45% cases respectively. Anti-ES antibodies were detected more frequently in cases having extraocular cysts compared to intraocular location. Differential levels of antibodies specific to above two antigens were estimated during the course of parasite degeneration as evident from findings following treatment. These indigenous tests might be used as an adjunct to existing tools for diagnosis as well treatment follow up. 













 
Introduction
Human cysticercosis is a parasitic infection caused by Cysticercus cellulosae, the larval form of the cestode, Taenia solium. Cysticercosis in humans is acquired by ingestion of faecally contaminated food, water or vegetables containing ova of T.solium. Human cysticercosis affecting the eye is called as ophthalmic cysticercosis (OCC) [1]. Cysticercosis of eye is initially asymptomatic but in the later stage, symptoms develop due to increase in cyst size or destruction of eyeball by the chronic inflammatory reaction. The clinical picture of a living intravitreous or subretinal Cysticercus is practically pathognomonic. Symptoms usually manifest in a later stage of the infection and the eye may be destroyed by the chronic inflammatory reaction [2]. The inflammatory reaction is possibly mediated by the toxins or degenerated products from the parasite and is usually accentuated on its death. Intravitreous or subretinal cysts usually lead to blindness within three years to five years unless the parasite is surgically removed from the eye [3]. The clinical manifestations of orbital or adnexal cysticercosis are entirely different and depend on the location, size, relation to adjacent structures and stage of evolution of the cyst. Extra ocular form of cysticercosis may also frequently manifest as subconjunctival abscess [4].

Diagnosis of OCC, either intraocular or extra ocular, usually depends on the history of tapeworm infection, ophthalmoscopy, ultrasonography (USG), computed tomography (CT), and biopsy.3 The reports are very few on serological study of OCC [5]. Also there is a scarcity in putting effort to develop serodiagnostics to aid its laboratory diagnosis. Thereby, management of both intraocular and extra ocular forms still continues to pose a serious challenge to clinicians.

In our laboratory we have standardized ELISA-based diagnosis of cysticercosis in eye where both tear fluid and serum were analyzed for presence of specific IgG or IgA antibodies employing T. solium metacestode somatic and ES antigens [6]. Although the serum IgG-ELISA showed a lower sensitivity against somatic antigens compared to that using ES antigens, however the specificitis of these two assays were high (92.3% and 94.87% using somatic and ES antigens respectively). The output of serum IgG �ELISA was better than other investigators findings on serum studies especially when ES antigen was employed.[5] This may be due to the living stage of the parasite in eye as we have got this correlation in our latest study on neurocysticercosis [7]. In the present study, an attempt is made to employ the previously standardized ELISA in clinically suspected OCC cases for laboratory diagnosis and treatment follow-up based on peripheral IgG antibody response in order to verify  the sequential release of antibodies specific to either somatic or ES antigens during the parasite degeneration  following albendazole therapy.

Material and Methods
All applicable institutional and governmental regulations concerning the ethical use of human volunteers were followed during this research.

Patients: This study was conducted in a tertiary care Hospital located in Pondicherry (India) after obtaining institutional ethical approval. Samples were collected from 40 clinically suspected cases of cysticercosis in eye. These suspected cases were with subconjunctival cysts, the orbital cystic mass with echogenic spot on USG suggestive of fluid filled parasitic cyst. In these cases scolex was not clearly visualized by USG. There were 4 cases subconjunctival with protruding cysts visible directly. The informed consent was obtained from each subject. A detail history was taken and a thorough clinical examination was done in each case and the clinical presentation noted. Information about the complications in eye and other symptoms like seizure, were collected from the patient as well from close relatives. A presumptive diagnosis of cysticercosis of eye and adnexa was made based on observation of a cystic lesion in the orbit or adnexa by ophthalmoscopy, further substantiated by USG of eye. Either CT scan or magnetic resonance imaging (MRI) was performed to check for involvement in brain and spinal cord. Five milliliters of venous blood was collected from each of the cases of OCC under aseptic precautions and was allowed to clot. The serum was separated and stored in pair at -200C till use.

Serum IgG -ELISA: The C. cellulosae somatic antigen was prepared from naturally infected porcine cysts following the procedure described by Sreenivasamurthy et al [8]. The excretory secretory (ES) antigen was prepared by in vitro culture of C. cellulosae (obtained from naturally infected pigs) in RPMI-1640 medium (HiMedia, Mumbai, India) following the procedure described by D�Souza et al [9].

The ELISA using T. solium metacestode somatic antigen and ES antigen was carried out separately for detection of IgG antibodies in serum samples from cases of OCC and controls. All the test sera were analyzed at the dilution of 1:200 in phosphate buffered saline (PBS) pH 7.2 following the protocol as described in our previous study [6].

Medical management: Albendazole was given to each patient diagnosed to have an extra ocular cyst. The albendazole was given in a dosage of 15mg/kg body weight/day divided in three doses for a period of ten days. Prednisolone (1 mg/kg per day) over 4 to 6 weeks was given in addition to albendazole in the treatment of orbital cysticercosis [10]. There were 7 patients who underwent primary surgical excision.

Post treatment follow-up of patients: The response to therapy and the presence of residual deficit at the final follow-up visit were documented. A total of 18 extra ocular cysticercosis cases were examined clinically following treatment up to 3 months. Post surgery cases (7 intra ocular cysticercosis) were also follwed up upto 3 months.  The serum samples collected at the intervals of 1 week, 1 month and 3 months were tested for the presence of anti-Cysticercus IgG antibody. Later we analyzed the follow-up data for estimating the degree of clinical resolution and residual deficit in our patients. Clinical resolution was considered based on complete resolution of clinical signs, spontaneous extrusion of the cyst, or imaging showing resolution of the cyst in cases where residual deficits persisted. Residual deficit was based on the criteria as described by Rath et al [11].

Results
In the present series, extra ocular muscle was found to be the predominant site (32.5% cases) of Cysticercus infection, followed by conjunctiva (25% cases) including 2 case each in lacrymal fossa, upper formix, bellow canthus, eyelid and optic nerve. Intra ocular sites included 7.5% cases in vitreous chamber; 2 cases each in macular (subretinal), and uvea. The major clinical signs and symptoms of OCC in the present series were summarized in Table-1. Ocular discomfort was the major complain in 52.5% cases. Other symptoms included blurring of vision in 27.5% patients, proptosis in 30% patients, and restriction in extraocular movement in 20% patients. Other less frequent presentations included binocular diplopia in 7.5% cases, ptosis in 5% cases, optic neuritis in 5% cases, preretinal fibrosis in 2.5% cases, necrotizing chorioretinitis in 2.5% cases, swelling in 15% cases, headache in 20% cases, and loss of vision in 1 case. Computed tomography scan was performed in all patients. The results demonstrated NCC in 2 patients.

Results of the serum IgG-ELISA in patients with intraocular and extraocular cyst in eye are presented in Table-2. The overall results on 40 clinically suspected cases showed the serum assay demonstrating a diagnostic level of antibodies in only 45% sera from clinically diagnosed cases where the parasite ES antigen was used and it was 32.5% using somatic antigen. When we saggregated the results based on location of the parasite cyst in eye, the ELISA using ES antigen was positive in 17 of 33 (51.5%) cases with extraocular location and only in 1 case with intraocular location. Using ES and somatic antigen, it was positive in 12 of 33 (36.3%) extraocular cases and 1 of 7 (14.2%) intraocular cases respectively. 

Collapse of the cyst cavity and obscuration of the scolex, were progressively seen as the cyst reduced in size by USG, on treatment with albendazole orally in patients with orbital cysticercosis. Complete resolution of the cyst was seen in all cases after 4 months to 5 months. The results of ELISA for detection of Cysticercus antibodies in serum during the follow up period are summarized in Table-3. ELISA using C. cellulosae somatic antigen demonstrated a diagnostic level of IgG antibodies in serum in 6 of 18 cases included in the followed-up study. The IgG-ELISA using somatic antigen demonstrated antibodies in sera from 6, 8 and 9 cases at 1 week, 1 month and 3 months respectively after treatment. ELISA using C. cellulosae ES antigen demonstrated a diagnostic level of IgG antibodies in serum from 8 of 18 cases at the time of diagnosis before treatment. The IgG-ELISA using ES antigen demonstrated antibodies in sera from 9, 8 and 8 cases at 1 week, 1 month and 3 months respectively following treatment. No change in positivity was observed in serum IgG-ELISAs among the cases after surgical excision of the cyst (data not presented).

Discussion
OCC has been reported from different parts of India with variable frequency.  Here we report a large series of patients of OCC seen over 3 years at a tertiary care center in Pondicherry (a southern province in India). The last report from our centre was 11 cases [12]. A few recently reported series of cases from India include 25 cases from Vellore [13], 44 from Chennai [14], 35 cases in a more recent report from Chennai [15], 18 from New Delhi [16], and 43 from Chandigarh [17]. A case of AIDS patient with subretinal cysticercosis has also been reported from Chennai [18]. Some earlier studies also described many more cases of ocular cysticercosis from South India [19]. Intraocular and extraocular cysticercosis has also been reported from North India during last many decades including recent reports from New Delhi and Uttar Pradesh [14,20,21,22]. Cases of intraocular and orbital cysticercosis have also been reported from Bombay [23,24]. All these studies show an increased reporting of OCC from different parts of India including South India, which indicates that OCC, is emerging as a far commoner disease than previously considered. 

In the present series the cysticerci are found in the extraocular muscle in one-third of cases (13 out of 40 cases). The conjunctiva and sub conjunctiva are the other major sites (25% cases). The site of infection differs in different geographical locations; most common site of localization being the posterior segment of the eye in most Western reports [3] where as the ocular adnexa is the common site of localization in most Indian studies. Ocular cysticercosis involving both the anterior and posterior segments of the eye is more frequent but anterior chamber cysticercosis is considered rare in India [25]. No case of anterior chamber cysticercosis is recorded in the present series. Ocular motility disorder is observed to be the major clinical presentation (20% cases) in the present series. This may be due to relatively more number of the cases of extraocular muscle cysticercosis (32.5% cases) documented in the present study. 

Though only few cases of optic nerve infection had been reported in the world literature, the majority are from India [20,26,27].  However, the present study documented for the first time two cases of optic nerve cysticercosis from Pondicherry. Both the patients presented with pain, diminution of vision and proptosis. One of the two cases is diagnosed as optic nerve cysticercosis based on ultrasonography and radioimaging. Both the cases were positive for Cysticercus antibody in serum by the ELISA test.

The ELISA using T. solium metacestode somatic and ES antigens is evaluated for the first time for diagnosis and treatment follow-up of OCC. Overall in our study, serum IgG-ELISA using somatic and ES antigens detected antibodies in 32.5% and 45% respectively among clinically suspected cases. Though several serological assays have been developed and evaluated for detection of Cysticercus antigen and antibody in serum for diagnosis of NCC in human with varying degree of sensitivity and specificity; reports on serodiagnosis of OCC were only few and restricted to detection of antibody in serum [4,5,26,27]. Also the nature of antigens used for detection of antibodies are not clear in those repots. Seropositivity was found to correlate with clinical profile of OCC in few studies while other studies did not find so. However, in our study the IgG-ELISA particularly using ES antigens, showed a higher sensitivity during diagnosis. The lower sensitivity of the ELISA using somatic antigens can be justified because the parasite usually remains viable in eye when cases attend the clinic and is it postulated that the living parasite escapes for the immunity by masking its somatic antigenic epitopes. Also it has been reported earlier that there is a correlation of viablility with serum IgG antibodies specific to the parasite ES antigens as seen in NCC [7].  In our previous study on OCC, the anti-Cysticercus IgG antibodies could be demonstrated in serum with a moderate sensitivity and high specificity. However, IgA-antibody assay showed 100 sensitivity and absolute specificity in tear fluid [6]. But this assay has its limitations that there is chance of dilution of the antibodies in tear results from any irritation to the eye while collecting the specimen and also there may be need of an immediate processing due the minute quantity of the specimen being unsuitable for storage. When we compare between two clinical forms of cysicercosis, serum IgG-ELISA shows comparatively lower sensitivities in diagnosis of OCC than NCC [7]. 

Sensitivity of the serum IgG-ELISA in patients with intraocular and extraocular cyst differered. The ELISA using ES antigen was positive in more frequently (51.5%) with extraocular location compared to the cases with intraocular location (14.2%). Using somatic antigen in the assay also it was positive in 36.3% extraocular cases and the same 14.2% intraocular cases. This poor sensitivity of the antibody tests in intraocular cases than extraocular cases may be due to the privileged situation of eye with regard to immunology; more precisely due to avascularity of the cornea and lens and the physiological selectivity of blood-aqueous barrier as well as absence of lymphatic channels within the globe itself as mentioned earlier [5].

Medical therapy is the recommended mode of treatment for the cases of extraocular and retro-orbital cysticercosis [28]. In the present study, the albendazole therapy in cases with orbital cysticercosis is found to be extremely effective and achieves clinical resolution in most patients. Despite clinical resolution, only a few numbers of patients have residual deficits. Reports of earlier Indian studies have also shown the promising results in treatment of extraocular cysticercosis with oral albendazole [14]. The post treatment follow up of OCC is usually done by monitoring the cases clinically based on physical examination, ophthalmoscopy or imaging [17,29]. There was no information available on serological monitoring of the cases of OCC following therapy. Nevertheless, serological monitoring has been found to be useful in monitoring cases of NCC following treatment, by detection of both antigen as well as antibodies. In the present study, the serological tests for the treatment follow up were found very useful. We observed a correlation between the progressive degenerarion of the parasite (in orbit) and the titre of the antibodies in serum specific to the somatic antigens of the parasite. The IgG-ELISA using somatic antigen demonstrated antibodies in sera from 6, 8 and 9 cases at 1 week, 1 month and 3 months respectively after treatment. This increase in number of patients for the anti-somatic antibodies shows that in due course of degeneration of the parasite, appearance of somatic antigens (parasite degenerated peptides) elevate an antibody response in the host. 

USG alone is not useful to confirm the diagnosis in presence of a cysticercus cyst in eye. It may suggest a probable cystic mass; it always does not provide a confirmed diagnosis in case of orbital cysts unlike the floating intraocular cysts. Also ophthalmoscopy may not be helpful in diagnosis of peripherally located parasite and also in cases of severe inflammation [30]. Moreover, in the cases of sub conjunctival cysts sometimes, parasitic cysts appear like dermolipoma [3].  Hence, there is need of an alternative and suitable laboratory based diagnosis to confirm the clinical diagnosis based on imaging.  The serum IgG-ELISA using the parasite somatic as well ES antigens evaluated in our laboratory for diagnosis as well follow up of the medically treated cases of OCC might be benificial and used as an adjunct to existing tools.



Conclusion
This was the first study evaluating an antibody ELISA based diagnosis and treatment follow-up of clinically suspected cases of OCC. A sequential release of antibodies specific to either somatic or ES antigens during the parasite degeneration was observed as evident from the treatment follow up study. It might be possible that when the parasite is alive, the somatic antigens are masked due to parasitic adaptation. However, upon death the parasite somatic antigens start degenerating activating immune system to develop anti-somatic antibodies in peripheral blood. Hence, the serum IgG-ELISA evaluated in our laboratory for diagnosis as well follow up of the medically treated cases might be benificial and used as an adjunct to existing tools. 

Acknowledgement
The authors acknowledge the timely help of Prof D�Souza, Head, Department of Parasitology, Veterinary College, Bangalore (India), for providing the laboratory facility for culturing Cysticercus cellulosae for collection of excretory secretory antigens.


References
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Table 1	Summary of the clinical signs and symptoms with respect to clinical diagnosis for ophthalmic cysticercosis
Signs and symptoms Frequency (%) of total cases (N=40)Signs and symptoms Frequency (%) of total cases (N=40)Ocular discomfort21 (52.5)Necrotizing chorioretinitis01 (2.5)Blurring of vision11 (27.5)Proptosis12 (30)Loss of vision01 (2.5)Ptosis02 (5)Preretinal fibrosis01 2.5)Swelling06 (15)Binocular diplopia03 (7.5)Headache08 (20)Optic neuritis02 (5)Exotropia01 (2.5)Restriction of extraocular movement08 (20)Extrusions from sub conjunctiva02 (5)*N: number of subjects.









Table 2	Results of the serum IgG-ELISA in patients with intraocular and extraocular cyst in eye
Location of the cyst in eyeNumber of cases each categoryN (%) cases positive for serum IgG-ELISA usingSomatic antigenES antigenIntra ocular location71 (14.2)1 (14.2)Extraocular location3312 (36.3)17 (51.5)Total4013 (32.5)18 (45)









Table 3	ELISA for detection of Cysticercus antigens and IgG antibodies in serum from cases of extraocular cysticercosis following treatment
Duration of follow up cases (N=18)Number (%) of sera from follow-up cases of extraocular cysticercosis positive for ELISA for detection of IgG antibody usingSomatic antigenES antigenBefore treatment6 (33.33)8 (44.44)After 1 week6 (33.33)9 (50)After 1 month8 (44.44)8 (44.44)After 3 months9 (50)8 (44.44)*N: number of subjects. 









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