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Korean J Parasitol > Volume 51(6):2013 > Article
Feng, Nawa, Sawanyavisuth, Lv, and Wu: Comprehensive Review of Ocular Angiostrongyliasis with Special Reference to Optic Neuritis

Abstract

Angiostrongyliasis, caused by Angiostrongylus cantonensis infection, is a food-borne parasitic disease. Its larvae evoke eosinophilic inflammation in the central nervous system, but can also cause pathological changes in the eyes. Among ocular angiostrongyliasis cases, the incidence of optic neuritis is low and only few sporadic reports exist. Some patients with optic neuritis developed obvious hypopsia or even vision loss, which would seriously influence the quality of life of patients. Prompt treatment of optic neuritis caused by A. cantonensis is the key factor for minimizing the incidence of serious complications of this disease. In this review, we first provide a comprehensive overview of ocular angiostrongyliasis, and then focus on the clinical features of optic neuritis caused by A. cantonensis.

INTRODUCTION

Angiostrongyliasis caused by infection with Angiostrongylus cantonensis is primarily characterized by eosinophilic meningitis, meningoencephalitis, or myelitis [1]. Ingestion of raw or half-cooked apple snails containing third stage larvae (L3) of A. cantonensis is the commonest route of infection. After ingestion by humans, the L3 migrate to the central nervous system (CNS) via blood stream and cause eosinophilic meningitis, often associated with encephalitis and myelitis (meningo-encephalo-myelitis) [2]. At the same time, the larvae also can invade the eyes and cause various ocular symptoms including optic neuritis [3]. Ocular angiostrongyliasis, however, has been neglected due to its low incidence.

CURRENT STATUS OF OCULAR ANGIOSTRONGYLIASIS

Recently Diao et al. [3] summarized a total of 35 cases of ocular angiostrongyliasis. We also made an extensive literature survey on ocular angiostrongyliasis and found 42 cases including the cases reviewed by Diao et al. [3]. Of these, nearly a half (19 cases) were from Thailand [4-13], including the first case report from that country in 1962 [4] and the most recent case reported in 2013 [13]. There are a few sporadic reports of ocular angiostrongyliasis from other countries, mostly from Asia. We have found 5 cases from Sri Lanka [14-18], 2 [14,15] of which were cited by Diao et al. [3]. Two cases were reported from India [19,20]. Although Diao et al. [3] noted 3 cases from India, they mistakenly included 1 case from Taiwan (their reference #17, in our reference #25) as an Indian case. Four cases have been reported from mainland China [21-24] and 2 cases from Taiwan [25,26]. Among them, 1 case from Taiwan [25] was not cited in the review of Diao et al. [3]. Two cases from Japan [27,28] were both found in Okinawa Prefecture. One case from Vietnam [29] was not included in the list of Diao's cases [3]. One case each was reported from Indonesia [31], Papua New Guinea [32], Malaysia [33], South Africa [34], Nepal [35], and Jamaica [36], in the order of the reported year. The cases from Malaysia and Jamaica were not mentioned in the review of Diao et al. [3]. The case from Malaysia [33] was reported as an ocular gnathostomiasis. However, the picture provided in the publication [33] shows that the worm is definitely not a Gnathostoma larva: the body is filariform without an apparent head bulb, indicating that this worm is highly likely to be the larva of A. cantonensis.
All 42 cases of ocular angiostrongyliasis are listed in Table 1. Among them, the oldest records were reported by Joseph [37] and Nicholls [38] in Sri Lanka in 1925 (redescribed by Dissanike and Cross in 2004 [15]). The most recent one was the optic neuritis case reported from Khon Kaen, Thailand, by Sinawat et al. [13] in 2013. Except for the case from Jamaica [36], 41 out of 42 were recorded in Asia, corresponding to the geographical distribution of this parasite. Among 42 ocular angiostrongyliasis cases, 19 were from Thailand, 5 from Sri Lanka and only 1 or 2 cases from other countries. Since 47% of all angiostrongyliasis cases in general are from Thailand and 27% from China [1], a high prevalence of ocular cases in Thailand is to be expected. However, the low number of ocular cases reported from other countries in the region is unexpected. Given the low frequency of the condition even in Thailand, cases elsewhere might not be diagnosed correctly. Alternatively, there might be an intra-species variation in the pathogenicity and behavior of the L3 in the host. Related to this, genetic variation in relation to the geographic location of A. cantonensis has been reported [39].
In addition to the sporadic cases listed in Table 1, Punyagupta et al. [40] analyzed clinical features of 484 cases of typical eosinophilic meningitis and found that 16% of patients had visual impairment, while 12% had an optic disc abnormality such as papilledema or atrophy. In China, clinical features of angiostrongyliasis cases of an outbreak in Wenzhou were analyzed [41] and the ocular manifestation was listed as one of the major features [42]. Ocular angiostrongyliasis cases were described also in recent reports of angiostrongyliasis outbreaks in China. Lv et al. [43] reported 2 ocular cases among 33 angiostrongyliasis cases in an outbreak in Dali. Wang et al. [44] reported 16 cases of visual disorders with different degrees of severity, such as photophobia, blurred vision, diplopia, defect in the field vision and eye floaters out of 81 cases in an outbreak of angiostrongyliasis in Beijing. In this outbreak, 25 patients showed severe symptoms and all ocular cases were found in this group. These reports indicate that the actual incidence of ocular angiostrongyliasis is likely much higher than commonly appreciated.

CLINICAL FEATURES OF OCULAR ANGIOSTRONGYLIASIS

The average age of the patients in 39 cases was 34 years (3-72 years), and unknown in the remaining 3 cases. There was an obvious sex difference (28 males, 12 females, and 2 unknown). Except for 1 case from Taiwan [26], all patients were affected only in 1 eye with no significant difference for the frequency of the affected sides (22 left and 19 right, including a case of bilateral necrotizing retinitis, data not available for 2 cases). In most instances, worms were found and surgically removed from the anterior chamber (14 cases) or from vitreous fluid (15 cases). In 10 cases, worms were found either on the retina or sub-retina. Even in such retinal involvement cases, worms were successfully removed surgically. In 4 retinal involvement cases in Thailand, laser ablation with or without oral steroids was successfully performed [11]. Among 30 cases of successful surgical removal, only 1 recorded the presence of 2 worms. In all other cases, ocular lesions seemed to be caused by a single worm. These ranged in length from 5 to 28 mm, but the majority was juveniles (young adults) around 10 mm long. The majority of ocular cases was not associated with CNS symptoms. Among the 42 ocular cases, only 12 patients were also suffering from eosinophilic meningitis. Peripheral blood eosinophilia was noted in 11 cases and 6 of them were among the cases with CNS symptoms.

OPTIC NEURITIS AND OTHER OCULAR ABNORMALITIES

Among 42 cases of ocular angiostrongyliasis, 6 were diagnosed as optic neuritis. The very first report of optic neuritis due to A. cantonensis infection described a case from China [22]. Subsequently, 4 cases have been reported from Thailand [12,13] and 1 case from Taiwan [25].
The diagnosis of optic neuritis can be made clinically by visual symptoms, positive rapid relative afferent pupillary defect (RAPD), and prolongation of visual evoked potentials (VEP) [45,46]. In the first A. cantonensis infection-associated optic neuritis case from China [22], the patient complained of mild headache, a low-grade fever, and slight ataxia. At the beginning, this patient was treated as a case of influenza because of non-specific symptoms, but A. cantonensis infection was suspected after the sudden onset of retinal detachment. The definite diagnosis was made by surgical removal of the worm.
The first angiostrongyliasis-associated optic neuritis case in Thailand [11] was a 21-year-old man suffering from progressive headache for 2 weeks. Repeated lumbar puncture could not relieve his headache and a week later he developed blurred vision in his left eye. The RAPD of his left eye was positive and VEP showed prolonged latency for this eye. Angiostrongylus worm was found in the vitreous space and treated with the argon laser.
In 2008, Sinawat et al. [12] studied 3 cases of optic neuritis caused by A. cantonensis. In all 3 cases, the fundus examination revealed generalized retinal pigment epithelial alteration, subretinal tracks, retinal edema, macular edema. and a pale disc, suggesting optic neuritis. In the first case, the patient, a 47-year-old man, complained of blurred vision in the left eye but denied headache. The latent phase of VEP was prolonged but the amplitude was normal. The RAPD of the left eye was positive and visual acuity was 1/60. Antibodies against the 29 KD antigen of A. cantonensis were detected in the serum. An immature male worm in the anterior chamber was aspirated by simcoe cannula after laser photocoagulation. The second case was a 27-year-old man presented with progressive visual loss in the left eye for 3 weeks. He presented with a 2-month history of eosinophilic meningitis before the onset of blurred vision. A moving larva was found in the superotemporal area of the vitreous humor. Diode laser was directly applied to the parasite and the dead worm was surgically removed. The third case was a 36-year-old man who developed visual loss in his right eye for 1 week without any history of headache. In this case, the intraocular inflammation was not detected and the RAPD was negative. The electroretinogram and VEP were normal. A subretinal living parasite was treated with a diode laser. His visual acuity was not much improved because of the retinal pigment degeneration.
Sinawat et al. [13] reported an additional ocular angiostrongyliasis case with retrobulbar optic neuritis. The patient was a 27-year-old Thai male presenting with progressive visual loss and a membrane-like floater in the right eye that had persisted for 1 month. The patient had a positive RAPD and delayed VEP in his right eye. The parasite found in the subretinal space was treated with a diode laser and surgically removed.
A case of optic neuritis reported from Taiwan was a 38-year-old man who suffered from headache and neck stiffness with blurred vision and color blindness in the left eye associated with binocular horizontal diplopia. The optic neuritis was confirmed by having a positive RAPD and delayed VEP in his left eye. The patient received larvicidal drugs and steroid treatment for 2 weeks, and his visual accuracy and color sense in the left eye were improved. As an overview (Table 2), all optic neuritis patients were males. Two cases in Thailand were affected in the right eye and the other 4 in the left eye. Unlike other infectious causes of optic neuritis [47,48], optic neuritis associated with ocular angiostrongyliasis is almost always unilateral. It may occur with or without eosinophilic meningitis or blood eosinophilia. Two of 6 cases had preceding meningitis. If both conditions coexist, eosinophilic meningitis will occur prior to optic neuritis or ocular involvement based on its life cycle. The larvae migrate to the meninges prior to randomly migrating to other tissues [1]. The postulated mechanism for optic neuritis is an increased intracranial pressure [25] or direct invasion [49]. In 2008, Jin et al. [49] performed MRI examinations for 74 angiostrongyliasis patients and found 33 with abnormal MRI including 1 optic neuritis case. In this optic neuritis case, a nodular lesion was observed on the optic nerve by the brain MRI. Related to this, optic nerve compression due to A. cantonensis was also reported from China [24].
Ocular involvement other than optic neuritis in angiostrongyliasis included blepharospasm, uveitis, macular edema, retinal edema, necrotic retinitis, panophthalmitis, papilledema, and optic nerve compression. In the case of necrotic retinitis reported from Taiwan [25], the patient had sudden loss of vision in both eyes and yellow transudate of retina accompanied by bulla formed by bilateral retinal detachment. Both serum and cerebrospinal fluid were antibody-positive against A. cantonensis by ELISA, and serum and subretinal fluid were positive for A. cantonensis by western blotting [25].

DIAGNOSIS, TREATMENT, AND PROGNOSIS OF OPTIC NEURITIS CAUSED BY A. CANTONENSIS

The most common diagnostic method for optic neuritis caused by A. cantonensis infection is ophthalmological examination (ophthalmoscope, ERG, and VEP). Furthermore, inquiry of history of eating intermediate hosts of A. cantonensis is also a key for diagnosis. Immunodiagnosis, including ELISA, western blotting, and use of specific monoclonal antibodies, provide strong supportive evidence. Peripheral blood eosinophilia is also indicative. The most reliable diagnostic method so far is to find put larvae or juveniles of A. cantonensis by ophthalmoscopy.
The usual method of treatment of optic neuritis caused by A. cantonensis is surgical removal of the parasites. If the parasites have not yet caused tissues damage, laser-mediated killing of living worms is a recommended therapeutic measure, which is better than surgical removal. In addition, oral administration of steroids may improve visual acuity by reducing intraocular inflammation. Anthelmintics, such as albendazole, are not recommended because dead parasites may cause serious intraocular inflammation [11].
In spite of these therapeutic measures, the prognosis for optic neuritis caused by A. cantonensis is not favorable. As shown in Table 2, only slight improvement of visual acuity occurred after treatment in most cases. For both optic and general ocular angiostrongyliasis, the outcome of therapy depends on the duration of infection and the initial visual acuity at the first visit of patients to doctors [3].

PERSPECTIVES OF OPTIC NEURITIS CAUSED BY A. CANTONENSIS

Although the incidence of optic neuritis in A. cantonensis infection is far lower than that of eosinophilic meningitis, its poor prognosis in terms of vision loss seriously affects the quality of the life of patients. At present, we do not fully know the answers to the following questions:
  1. How do larvae migrate into the eyes? Via blood flow or by other routes?

  2. What is the relationship between optic neuritis and eosinophilic meningitis?

  3. What is the relationship among clinical symptoms, pathological changes, and the prognosis? What causes those pathological changes?

  4. How can we treat cases of optic neuritis due to A. cantonensis infection?

Because only a limited number of optic neuritis cases have been reported, development of an animal model for A. cantonensis-associated optic neuritis is necessary.

ANIMAL EXPERIMENTS FOR OPTIC NEURITIS CAUSED BY A. CANTONENSIS

In the past 20 years, many animal experiments have been carried out using rodent models of A. cantonensis infection [50]. Among them, mice have been studied most extensively because of their susceptibility to the parasite. Until now, however, there are no animal models for optic neuritis caused by A. cantonensis. Rats and mice have provided research models for optic neuritis caused by other conditions, such as multiple sclerosis. In these models, histopathological changes of the retina and optic nerve were observed by H-E staining, and demyelination of the optic nerve was observed by electron microscopy. Similarly, fundoscopy has been used to observe the damage to the optic papilla and ERG/VEP used to examine changes in vision and visual acuity. Ganglion cells of the retina were also the focal point of the study of optic neuritis [51,52]. Similar methodology should be adopted for the study of optic neuritis caused by A. cantonensis.
In our preliminary animal study using mice infected with A. cantonensis, we found the infected animals manifested obvious inflammatory infiltration in the retina and optic nerve, and demyelination was found in the optic nerve. Meanwhile, VEP and ERG were very different compared with normal control animals (unpublished results). These results indicate A. cantonensis can cause pathological and clinical changes of eyes in experimental animals.
In conclusion, ocular angiostrongyliasis was comprehensively reviewed with special focus on optic neuritis caused by A. cantonensis, and we put forward questions about the urgent problems which need to be solved. This study provides a baseline for future research on optic neuritis caused by A. cantonensis.
National Basic Research Program2010CB530004
National Nature Science Foundation81271855
National Nature Science Foundation81261160324
Natural Science Foundation of Guangdong Province4203021

ACKNOWLEDGMENTS

This work was supported by a grant from the National Basic Research Program of China (2010CB530004), the National Natural Science Foundation of China (grant no. 81271855, 81261160324) and The PhD Start-up Fund of Natural Science Foundation of Guangdong Province of China (4203021) grant.

REFERENCES

1. Wang QP, Lai DH, Zhu XQ, Chen XG, Lun ZR. Human angiostrongyliasis. Lancet Infect Dis 2008;8: 621-630. PMID: 18922484.
crossref pmid
2. Cross JH. Clinical manifestations and laboratory diagnosis of eosinophilic meningitis syndrome associated with angiostrongyliasis. Southeast Asian J Trop Med Public Health 1978;9: 161-170. PMID: 725650.
pmid
3. Diao Z, Wang J, Qi H, Li X, Zheng X, Yin C. Human ocular angiostrongyliasis: a literature review. Trop Doct 2011;41: 76-78. PMID: 21296846.
crossref pmid
4. Prommindaroj K, Leelawongs N, Pradatsundarasar A. Human angiostrongyliasis of the eye in Bangkok. Am J Trop Med Hyg 1962;1: 759-761. PMID: 13986349.

5. Ketsuwan P, Pradatsundarasaar A. Third case of ocular angiostrongyliasis in Thailand. J Med Assoc Thai 1965;48: 799-805.

6. Ketsuwan P, Pradatsundarasar A. Second case of ocular angiostrongyliasis in Thailand. Am J Trop Med Hyg 1966;15: 50-51. PMID: 5901630.
pmid
7. Kanchanaranya C, Punyagupta S. Case of ocular angiostrongyliasis associated with enosinophilic meningitis. Am J Ophthalmol 1971;71: 931-934. PMID: 5102754.
crossref pmid
8. Kanchanaranya C, Prechanond A, Punyagupta S. Removal of living worm in retinal Angiostrongylus catonensis. Am J Ophthalmol 1972;74: 456-458. PMID: 5053690.
crossref pmid
9. Singalavanija A, Wangspa S, Techareon S. Intravitreal angiostrongiliasis. Aust N Z J Ophthalmol 1986;14: 381-384. PMID: 3814428.
crossref pmid
10. Patikulsila D, Ittipunkul N, Theerakittikul B. Intravitreal angiostrongyliasis: report of two cases. J Med Assoc Thai 2003;86: 981-985. PMID: 14650712.
pmid
11. Sawanyawisuth K, Kitthaweesin K, Limpawattana P, Intapan PM, Tiamkao S, Jitpimolmard S, Chotmongkol V. Intraocular angiostrongyliasis: clinical findings, treatments and outcomes. Trans R Soc Trop Med Hyg 2007;101: 497-501. PMID: 17064748.
crossref pmid
12. Sinawat S, Sanguansak T, Angkawinijwong T, Ratanapakorn T, Intapan PM, Sinawat S, Yospaiboon Y. Ocular angiostrongyliasis: clinical study of three cases. Eye (Lond) 2008;22: 1446-1448. PMID: 18535614.
crossref pmid
13. Sinawat S, Yospaiboon Y, Sinawat S. Subretinal angiostrongyliasis-induced optic neuritis. Clin Ophthalmol 2013;7: 977-979. PMID: 23818750.
crossref pmid pmc
14. Durette-Desset MC, Chabaud AG, Cassim MH, Ismail MM, Premaratne UN, Abeyewickreme W, Dissanaike AS. On an infection of a human eye with Parastrongylus (=Angiostrongylus) sp. in Sri Lanka. J Helminthol 1993;67: 69-72. PMID: 8509620.
crossref pmid
15. Dissanaike AS, Cross JH. Ocular parastrongyliasis (=angiostrongyliasis): probable first report of human infection from a patient in Ceylon (Sri Lanka). Parassitologia 2004;46: 315-316. PMID: 15828436.
pmid
16. Dissanaike AS, Ihalamulla RL, Naotunne TS, Senarathna T, Withana DS. Third report of ocular parastrongyliasis (angiostrongyliasis) from Sri Lanka. Parassitologia 2001;43: 95-97. PMID: 11921545.
pmid
17. Wariyapola D, Goonesinghe N, Priyamanna TH, Fonseka C, Ismail MM, Abeyewickreme W, Dissanaike AS. Second case of ocular parastrongyliasis from Sri Lanka. Trans R Soc Trop Med Hyg 1998;92: 64-65. PMID: 9692155.
crossref
18. Ihalamulla RL, Fernando SD, Weerasena KH, Cross JH, Dissannike AS, Fonseka C. A further case of Parastrongtjliasis (=Angiostrongyliasis) from the eye of a patient in Sri Lanka. Ceylon J Medical Sci 2007;50: 15-17.

19. Baheti NN, Sreedharan M, Krishnamoorthy T, Nair MD, Radhakrishnan K. Neurological picture. Eosinophilic meningitis and an ocular worm in a patient from Kerala, south India. J Neurol Neurosurg Psychiatry 2008;79: 271. PMID: 18281446.
crossref pmid
20. Malhotra S, Mehta DK, Arora R, Chauhan D, Ray S, Jain M. Ocular angiostrongyliasis in a child--first case report from India. J Trop Pediatr 2006;52: 223-225. PMID: 16186138.
crossref pmid
21. Wang WJ, Li JH, He YL. A case of ocular angiostrongyliasis confirmed by surgical removal of a worm under retina by vitreous body operation. Zhonghua Yan Ke Za Zhi 1999;35: 470-471 (in Chinese).

22. Li QF. A case of ocular angiostrongyliasis confirmed by a removal of a living worm from the anterior chamber of the eye. Zhonghua Yan Ke Za Zhi 2000;36: 216 (in Chinese).

23. Xiang DM, Zhang MD, Li DN, Mao YN. A report about angiostrongyliasis cantonensis in anterior chamber of a child's eye. Chin J Strabismus Pediatr Ophthalmol 2001;9: 91.

24. Qi H, Diao Z, Yin C. A case of optic nerve compression caused by Angiostrongylus cantonensis. Am J Trop Med Hyg 2009;81: 4. PMID: 19556557.
pmid
25. Wang LC, Wang IH, Jou JR. Optic neuritis secondary to Angiostrongylus cantonensis infection. Ocul Immunol Inflamm 2006;14: 189-191. PMID: 16766404.
crossref pmid
26. Liu IH, Chung YM, Chen SJ, Cho WL. Necrotizing retinitis induced by Angiostrongylus cantonensis. Am J Ophthalmol 2006;141: 577-579. PMID: 16490516.
crossref pmid
27. Nelson RG, Warren RC, Scotti FA, Call TG, Kim BS. Ocular angiostrongyliasis in Japan: a case report. Am J Trop Med Hyg 1988;38: 130-132. PMID: 3341516.
pmid
28. Toma H, Matsumura S, Oshiro C, Hidaka T, Sato Y. Ocular angiostrongyliasis without meningitis symptoms in Okinawa, Japan. J Parasitol 2002;88: 211-213. PMID: 12053973.
crossref pmid
29. Hoa LV, Tn HV, Phuong HN. L'angiostrongybose oculaire chez l'homme au Sud Viet-Nam. Bull Soc Pathol Exot 1973;66: 743-746.

30. Thu TP, Nguyen NX, Lan le T, Küchle M. Ocular angiostrongylus cantonensis in a female Vietnamese patient: case report. Klin Monbl Augenheilkd 2002;219: 892-895. PMID: 12548476.
crossref pmid
31. Widagdo , Sunardi , Lokollo DM, Margono SS. Ocular angiostrongyliasis in Semarang, Central Java. Am J Trop Med Hyg 1977;26: 72-74. PMID: 842785.
pmid
32. Scrimgeour EM, Chambers BR, Kaven J. A probable case of ocular angiostrongyliasis in New Britain, Papua New Guinea. Trans R Soc Trop Med Hyg 1982;76: 538-540. PMID: 6926775.
crossref pmid
33. Mokhtar E, Alias A, Abd Ghani Z, Azlan NZ. A live intraocular Gnathostoma spp. with diffuse unilateral subacute Neuroretinitis. Int Med J 2003;2.

34. Kumar V, Kyprianou I, Keenan JM. Ocular angiostrongyliasis: removal of a live nematode from the anterior chamber. Eye (Lond) 2005;19: 229-230. PMID: 15232595.
crossref pmid
35. Paul A, Pammal AT. Ocular parasitosis: A rare cause of hypertensive uveitis. Indian J Ophthalmol 2008;56: 501-502. PMID: 18974522.

36. Mattis A, Mowatt L, Lue A, Lindo J, Vaughan H. Ocular angiostrongyliasis-first case report from Jamaica. West Indian Med J 2009;58: 383-385. PMID: 20099782.
pmid
37. Joseph HP. Clinical notes on the effects of a nematode larva in the eye. Ceylon J Sci (Sect D) 1925;1: 143.

38. Nicholls L. Note on nematode larva removed from the eye of man. Ceylon J Sci (Sect D) 1925;1: 145.

39. Tokiwa T, Harunari T, Tanikawa T, Komatsu N, Koizumi N, Tung KC, Suzuki J, Kadosaka T, Takada N, Kumagai T, Akao N, Ohta N. Phylogenetic relationships of rat lungworm, Angiostrongylus cantonensis, isolated from different geographical regions revealed widespread multiple lineages. Parasitol Int 2012;61: 431-436. PMID: 22387862.
crossref pmid
40. Punyagupta S, Juttijudata P, Bunnag T. Eosinophilic meningitis in Thailand. Clinical studies of 484 typical cases probably caused by Angiostrongylus cantonensis. Am J Trop Med Hyg 1975;24: 921-931. PMID: 1200257.
pmid
41. Wang X, Huang H, Dong Q, Lin Y, Wang Z, Li F, Nawa Y, Yoshimura K. A clinical study of eosinophilic meningoencephalitis caused by angiostrongyliasis. Chin Med J (Engl) 2002;115: 1312-1315. PMID: 12411101.
pmid
42. Lin W, Wang XT. Discussion on the clinical manifestations of angiostrongyliasis. Re Dai Yi Xue Za Zhi 2005;5: 1345-1346 (in Chinese).

43. Lv S, Zhang Y, Chen SR, Wang LB, Fang W, Chen F, Jiang JY, Li YL, Du ZW, Zhou XN. Human angiostrongyliasis outbreak in Dali, China. PLoS Negl Trop Dis 2009;3: e520. PMID: 19771154.
crossref pmid pmc
44. Wang J, Qi H, Diao Z, Zheng X, Li X, Ma S, Ji A, Yin C. An outbreak of angiostrongyliasis cantonensis in Beijing. J Parasitol 2010;96: 377-381. PMID: 19874073.
crossref pmid
45. Cox TA, Thompson HS, Hayreh SS, Snyder JE. Visual evoked potential and pupillary signs. A comparison in optic nerve disease. Arch Ophthalmol 1982;100: 1603-1607. PMID: 7138329.
crossref pmid
46. Tabatabaei SA, Soleimani M, Alizadeh M, Movasat M, Mansoori MR, Alami Z, Foroutan A, Joshaghani M, Safari S, Goldiz A. Predictive value of visual evoked potentials, relative afferent pupillary defect, and orbital fractures in patients with traumatic optic neuropathy. Clin Ophthalmol 2011;5: 1021-1026. PMID: 21845028.
crossref pmid pmc
47. Fadil H, Kelley RE, Gonzalez-Toledo E. Differential diagnosis of multiple sclerosis. Int Rev Neurobiol 2007;79: 393-422. PMID: 17531852.
crossref pmid
48. Larsen M, Toft PB, Bernhard P, Herning M. Bilateral optic neuritis in acute human immunodeficiency virus infection. Acta Ophthalmol Scand 1998;76: 737-738. PMID: 9881565.
crossref pmid
49. Jin EH, Ma Q, Ma DQ, He W, Ji AP, Yin CH. Magnetic resonance imaging of eosinophilic meningoencephalitis caused by Angiostrongylus cantonensis following eating freshwater snails. Chin Med J (Engl) 2008;121: 67-72. PMID: 18208669.
pmid
50. OuYang L, Wei J, Wu Z, Zeng X, Li Y, Jia Y, Ma Y, Zhan M, Lei W. Differences of larval development and pathological changes in permissive and nonpermissive rodent hosts for Angiostrongylus cantonensis infection. Parasitol Res 2012;111: 1547-1557. PMID: 22777701.
crossref pmid
51. Shindler KS, Ventura E, Dutt M, Rostami A. Inflammatory demyelination induces axonal injury and retinal ganglion cell apoptosis in experimental optic neuritis. Exp Eye Res 2008;87: 208-213. PMID: 18653182.
crossref pmid pmc
52. Zh RW, Zh ZK, Yu HM, et al. The effect on the optic neuritis of EAE mice treated by β-element. Chin J Immunol 2011;27: 342-346.

Table 1.
Comprehensive review of the clinical features of ocular angiostrongyliasis cases in the world.
Age Sex Affected side VA Rt VA Lt duration Worm in Size of worm Ocular disease Meningitis eosinophilia treatment outcome Year Reference
1 Thai 34 M R LP 20/20 6 weeks AC 13 mm N N surgival removal count finger: slightly improved 1962 4
2 Thai 22 M L 6/6 LP 2 months AC 18.86 mm N N surgival removal not improved 1966 5
3 Thai 21 M L 6/6 2/60 1 day AC 8.55 mm chronic retinitis and vitreous opacity N N paracentesis improved, 6/24 1965 6
4 Thai 34 M L 6/6 CF 10 days VF 11.7 mm panophthalmitis Y Y surgival removal not improved 1971 7
5 Thai 36 M L 20/20 CF 2 feet 9 days retina 12.5 mm retinal and macular edema Y NA surgival removal not improved 1974 8
6 Thai 72 F R CF 1 month VF 9.22 mm N N surgival removal not improved 1986 9
7 Thai 28 M R CF 1 foot 20/20 14 days VF < 10 mm N N aspirator and vitrectomy improved, 20/200 2003 10
8 Thai 44 M L NA NA NA VF 12 mm + 1dead worm N N aspirator and vitrectomy improved, 6/200 10
9 Thai 21 M L 6/9 2/60 14 days VF NA optic neuritis Y Y laser, oral steroid not improved 2007 11
10 Thai 36 F L 6/6 CF NA VF 9.8 mm papilledema Y NA surgival removal slightly improved 11
11 Thai 22 F R 1/60 6/6 2 months VF 10.9 mm N N surgival removal NA 11
12 Thai 39 M R 6/6 6/6 10 days VF NA N NA laser normal VA 11
13 Thai 33 F L 6/6 1/60 7 days subretinal NA N N laer, steroid slightly improved, 5/60 11
14 Thai 28 M R 6/24 6/6 4 days subretinal NA N NA laser, oral steroid not improved 11
15 Thai 48 M R CF 6/6 21 days VF 11.4 mm N N laser, surgical removal not improved 11
16 Thai 47 M L 6/6 CF 2 feet 21 days AC ND optic neuritis N NA laser, aspirator IV methylprednisolone improved, 2/60 2008 12
17 Thai 27 M L 6/6 1/60 21 days VF ND optic neuritis?? Y NA laser, surgical removal slightly improved, 6/60 12
18 Thai 36 M R 2/60 6/6 7 days subretinal ND optic neuritis?? N NA laser slightly improved, 6/60 12
19 Thai 27 M R CF 1 feet 1 month subretinal 15 mm optic neuritis N N albendazole, steroid laser slightly improved 2/60 2013 13
20 Sri Lanka 30 M R No LP NA 1 month AC 11.6 mm N NA forceps extraction NA 1993 14
21 Sri Lanka 30 M R 6/60 6/6 2 days subretina to VF 6.3 mm retinal edema Y Y forceps extraction not improved 1998 15
22 Sri Lanka 20 M L 6/6 6/9 3 days AC 6.5 mm N N needle aspiration improved 2001 16
23 Sri Lanka M R LP 6/6 days AC 11.4 mm N NA surgival removal improved, 6/60 2004 17
24 Sri Lanka 25 F R 6/60 6/6 14 days retina 8.5 mm N NA surgival removal NA 2007 18
25 India 12 M L 6/6 6/60 14 days AC 28 mm optic neuritis?? N Y surgival removal improved, 6/6 2006 19
26 India 40 F L NA NA NA VF 13 mm Y Y surgival removal NA 2008 20
27 Mainland China 34 M L retina 12 mm N 1999 21
28 Mainland China 35 M L AC 12.3 mm optic neuritis N 2000 22
29 Mainland China AC 2001 23
30 Mainland China 47 M R blurred NA NA optic nerve optic nerve compression Y NA surgival removal not improved 2009 24
31 Taiwan 52 F R/L CF LP 7 days (-) bilateral necrotizing retinitis Y NA IV methylprednisolone not improved 2006 25
32 Taiwan 38 M L 20/20 20/50 2 days not identified (-) optic neuritis Y Y mebendazole, IV methylprednisolone slightly improved, 20/25 2006 26
33 Japan 62 F L 20/25 2/200 1 day VF 12 mm optic neuritis?? N Y surgival removal not improved 2002 27
34 Japan 24 M L 6/6 6/9 to 6/100 1 day VF 5 mm Y Y oral steroid, LP improved, normal VA6/6 1988 28
35 Vietnam 12 mm N 1974 29
36 Vietnam 3 F R 3 days AC 15 mm Y surgival removal VA0.6 2002 30
37 Indonesia 23 F L 5/5 3/60 14 days AC 11.1 mm N N paracentesis not improved 1977 31
38 Papua New Guinea 45 F R 6/36 6/6 3 months VF <1 cm acute ciliary injection with blepharospasm N Y topical steroid, topical antibiotics not improved 1982 32
39 Malaysia 57 M L 6/6 6/36 3 days retina ND N Y surgival removal improved, 6/24 2003 33
40 Soouth Africa (UK) 33 M R 6/9 6/5 2 days AC 22 mm anterior uveitis N NA needle aspiration improved, normal VA6/6 2005 34
41 Nepal M R 20/80 20/20 VF 15 mm uveitis N 2008 35
42 Jamica 30 F L 6/5 CF 1 month AC 19.9 mm N N surgival removal improved, 6/36 2009 36

M: male, F: female, R: right, L: left, CF: count finger LP: light perception, AC: anterior chamber, VF: vitreous fluid, Y: Yes, N: No, ND: not determined, NA: not available

Table 2.
Reported cases of optic neuritis due to A. cantonensis infection
Country or area Age Sex Affected side of eye Meningitis RAPD VEP Outcome (improvement) Ref.
Mainland China 35 M left no + prolonged NA [22]
Taiwan 38 M left yes + prolonged slightly [25]
Thailand 47 M left no + prolonged improved [12]
Thailand 27 M left yes NA NA slightly [12]
Thailand 36 M right no - normal slightly [12]
Thailand 27 M right no + prolonged slightly [13]

M, male; NA, not available; RAPD, relative afferent pupillary defect; VEP, visual evoked potentials.

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