Parasites, Hosts and Diseases

The Korea Society for Parasitology and Tropical Medicine (대한기생충학·열대의학회)
권호 표지
DOI QR코드

DOI QR Code

Comprehensive Review of Ocular Angiostrongyliasis with Special Reference to Optic Neuritis

  • Feng, Ying (Department of Histology, Zhongshan School of Medicine, Sun Yat-sen University) ;
  • Nawa, Yukifumi (Research Affairs, Faculty of Medicine, Khon Kaen University) ;
  • Sawanyavisuth, Kittisak (Department of Internal Medicine, Faculty of Medicine, Khon Kaen University) ;
  • Lv, Zhiyue (Key Laboratory of Tropical Disease Control (Sun Yat-Sen University), Ministry of Education) ;
  • Wu, Zhong-Dao (Key Laboratory of Tropical Disease Control (Sun Yat-Sen University), Ministry of Education)
  • Received : 2013.05.31
  • Accepted : 2013.10.11
  • Published : 2013.12.31
Download PDF
⟨ Previous Next ⟩

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.

Keywords

References

  1. Wang QP, Lai DH, Zhu XQ, Chen XG, Lun ZR. Human angiostrongyliasis. Lancet Infect Dis 2008; 8: 621-630. https://doi.org/10.1016/S1473-3099(08)70229-9
  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.
  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. https://doi.org/10.1258/td.2010.100294
  4. Prommindaroj K, Leelawongs N, Pradatsundarasar A. Human angiostrongyliasis of the eye in Bangkok. Am J Trop Med Hyg 1962; 1: 759-761.
  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.
  7. Kanchanaranya C, Punyagupta S. Case of ocular angiostrongyliasis associated with enosinophilic meningitis. Am J Ophthalmol 1971; 71: 931-934. https://doi.org/10.1016/0002-9394(71)90268-6
  8. Kanchanaranya C, Prechanond A, Punyagupta S. Removal of living worm in retinal Angiostrongylus catonensis. Am J Ophthalmol 1972; 74: 456-458. https://doi.org/10.1016/0002-9394(72)90908-7
  9. Singalavanija A, Wangspa S, Techareon S. Intravitreal angiostrongiliasis. Aust N Z J Ophthalmol 1986; 14: 381-384. https://doi.org/10.1111/j.1442-9071.1986.tb00476.x
  10. Patikulsila D, Ittipunkul N, Theerakittikul B. Intravitreal angiostrongyliasis: report of two cases. J Med Assoc Thai 2003; 86: 981-985.
  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. https://doi.org/10.1016/j.trstmh.2006.07.010
  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. https://doi.org/10.1038/eye.2008.135
  13. Sinawat S, Yospaiboon Y, Sinawat S. Subretinal angiostrongyliasis- induced optic neuritis. Clin Ophthalmol 2013; 7: 977-979.
  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. https://doi.org/10.1017/S0022149X00012876
  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.
  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.
  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. https://doi.org/10.1016/S0035-9203(98)90956-7
  18. Ihalamulla RL, Fernando SD, Weerasena KH, Cross JH, Dissannike AS, C. 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. https://doi.org/10.1136/jnnp.2007.122093
  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.
  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. Chin J Ophthalmol 1999; 35: 470-471 (in Chinese).
  22. Li Q-F. A case of ocular angiostrongyliasis confirmed by a removal of a living worm from the anterior chamber of the eye. Chin J Ophthalmol 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.
  25. Wang LC, Wang IH, Jou JR. Optic neuritis secondary to Angiostrongylus cantonensis infection. Ocul Immunol Inflamm 2006; 14: 189-191. https://doi.org/10.1080/09273940600657702
  26. Liu IH, Chung YM, Chen SJ, Cho WL. Necrotizing retinitis induced by Angiostrongylus cantonensis. Am J Ophthalmol 2006; 141: 577-579. https://doi.org/10.1016/j.ajo.2005.09.033
  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.
  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. https://doi.org/10.1645/0022-3395(2002)088[0211:OAWMSI]2.0.CO;2
  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 Monatsbl Augenheilkd 2002; 219: 892-895. https://doi.org/10.1055/s-2002-36945
  31. Widagdo, Sunardi, Lokollo DM, Margono SS. Ocular angiostrongyliasis in Semarang, Central Java. Am J Trop Med Hyg 1977; 26: 72-74.
  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. https://doi.org/10.1016/0035-9203(82)90158-4
  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. https://doi.org/10.1038/sj.eye.6701442
  35. Paul A, Pammal AT. Ocular parasitosis: A rare cause of hypertensive uveitis. Indian J Ophthalmol 2008; 56: 501-502. https://doi.org/10.4103/0301-4738.43369
  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.
  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. https://doi.org/10.1016/j.parint.2012.02.005
  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.
  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 2002; 115: 1312-1315.
  42. Lin Y, Wang XT. Discussion on the clinical manifestations of angiostrongyliasis in China. Chin J Trop Med 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. https://doi.org/10.1371/journal.pntd.0000520
  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. https://doi.org/10.1645/GE-2214.1
  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. https://doi.org/10.1001/archopht.1982.01030040581004
  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.
  47. Fadil H, Kelley RE, Gonzalez-Toledo E. Differential diagnosis of multiple sclerosis. Int Rev Neurobiol 2007; 79: 393-422. https://doi.org/10.1016/S0074-7742(07)79018-9
  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. https://doi.org/10.1034/j.1600-0420.1998.760623.x
  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.
  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. https://doi.org/10.1007/s00436-012-2995-6
  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. https://doi.org/10.1016/j.exer.2008.05.017
  52. Zh RW, Zh ZK, Yu HM, et al. The effect on the optic neuritis of EAE mice treated by $\beta$-element. Chin J Immunol 2011; 27: 342-346.

Cited by

  1. The pathogenesis of optic neuritis caused by Angiostrongylus cantonensis in BALB/c mice vol.7, pp.1, 2014, https://doi.org/10.1186/1756-3305-7-339
  2. Animal model of human disease with optic neuritis: neuropapillitis in a rat model infected with Angiostrongylus cantonensis vol.113, pp.11, 2014, https://doi.org/10.1007/s00436-014-4067-6
  3. Emergence of Neural Angiostrongyliasis in Eastern Australia vol.15, pp.3, 2013, https://doi.org/10.1089/vbz.2014.1622
  4. Effects of albendazole combined with TSII-A (a Chinese herb compound) on optic neuritis caused by Angiostrongylus cantonensis in BALB/c mice vol.8, pp.1, 2013, https://doi.org/10.1186/s13071-015-1214-6
  5. Infectious optic neuropathies: a clinical update vol.7, pp.None, 2015, https://doi.org/10.2147/eb.s69173
  6. A Case of Ocular Angiostrongyliasis with Molecular Identification of the Species in Vietnam vol.53, pp.6, 2013, https://doi.org/10.3347/kjp.2015.53.6.713
  7. Angiostrongylus cantonensis: a review of its distribution, molecular biology and clinical significance as a human pathogen vol.143, pp.9, 2016, https://doi.org/10.1017/s0031182016000652
  8. Angiostrongylus cantonensis in anterior chamber vol.67, pp.1, 2013, https://doi.org/10.4103/ijo.ijo_843_18
  9. Genetic characterization of Angiostrongylus larvae and their intermediate host, Achatina fulica, in Thailand vol.14, pp.9, 2013, https://doi.org/10.1371/journal.pone.0223257
  10. Eosinophilic meningitis due to Angiostrongylus cantonensis in Europe vol.93, pp.None, 2013, https://doi.org/10.1016/j.ijid.2020.01.012
  11. Two Ocular Angiostrongyliasis Cases in Thailand with Molecular Identification of Causative Parasite Species vol.102, pp.6, 2013, https://doi.org/10.4269/ajtmh.19-0701
  12. Practical Guidance for Clinical Microbiology Laboratories: Diagnosis of Ocular Infections vol.34, pp.3, 2013, https://doi.org/10.1128/cmr.00070-19
  13. An unusual cause of visual loss: Subfoveal, motile angiostrongyliasis vol.51, pp.3, 2021, https://doi.org/10.1177/0049475520986392
  14. Cluster of Angiostrongyliasis Cases Following Consumption of Raw Monitor Lizard in the Lao People’s Democratic Republic and Review of the Literature vol.6, pp.3, 2013, https://doi.org/10.3390/tropicalmed6030107