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Curcumin alleviates eosinophilic meningitis through reduction of eosinophil count following albendazole treatment against Angiostrongylus cantonensis in mice

  • LING-YUH SHYU (a1) (a2), HAN-HSIN CHANG (a3), JENG-DONG HSU (a4), DAVID PEI-CHENG LIN (a5), YING-HOCK TENG (a1) (a6) and HSIU-HSIUNG LEE (a1) (a2)...
Summary

Angiostrongylus cantonensis (A. cantonensis) is the most common cause of parasitic eosinophilic meningitis worldwide. By using an animal model of BALB/c mice infected with A. cantonensis, previous studies indicated that the anthelmintic drug, albendazole, could kill A. cantonensis larvae and prevent further infection. However, the dead larvae will induce severe immune responses targeting at brain tissues. To alleviate the detrimental effects caused by the dead larvae, we administered curcumin, a traditional anti-inflammatory agent, as a complementary treatment in addition to albendazole therapy, to determine whether curcumin could be beneficial for treatment. The results showed that although curcumin treatment alone did not reduce worm number, combined treatment by albendazole and curcumin helped to reduce eosinophil count in the cerebrospinal fluid, better than using albendazole alone. This alleviating effect did not affect albendazole treatment alone, since histological analysis showed similar worm eradication with or without addition of curcumin. Nevertheless, curcumin treatment alone and combined albendazole-curcumin treatment did not inhibit MMP-9 expression in the brain tissue. In conclusion, curcumin, when used as a complementary treatment to albendazole, could help to alleviate eosinophilic meningitis through suppression of eosinophil count in the cerebrospinal fluid.

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Corresponding author
*Corresponding author: Chung Shan Medical University, Department of Parasitology, Taiwan, ROC, 110, Sec. 1, Jianguo N. Road., Taichung City 402, Taiwan. Tel: +886 4 24730022 ext 11642. Fax: 886-4-24714143. E-mail: sly@csmu.edu.tw
References
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Alicata, J. E. (1988). Angiostrongylus cantonensis (eosinophilic meningitis): Historical events in it's recognition as a new parasitic disease of man. Journal of the Washington Academy of Sciences 78, 3846.
Boonrao, M., Yodkeeree, S., Ampasavate, C., Anuchapreeda, S. and Limtrakul, P. (2010). The inhibitory effect of turmeric curcuminoids on matrix metalloproteinase-3 secretion in human invasive breast carcinoma cells. Archives of Pharmacal Research 33, 989998.
Bradford, M. M. (1976). Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248254.
Caldeira, R. L., Mendonça, C. L., Goveia, C. O., Lenzi, H. L., Graeff-Teixeira, C., Lima, W. S., Mota, E. M., Pecora, I. L., Medeiros, A. M. and Carvalho, O. S. (2007). First record of molluscs naturally infected with Angiostrongylus cantonensis (Chen, 1935) (Nematoda: Metastrongylidae) in Brazil. Memórias do Instituto Oswaldo Cruz 102, 887889.
Chen, H. T. (1935). Un nouveau nematode pulmonaire: Pulmonema cantonensis, n.g.m. sp. Des rats de canton. Annals of Parasitology 13, 312317.
Chen, K. M. and Lai, S. C. (2007). Biochemical and pathological evaluation of albendazole/thalidomide co-therapy against eosinophilic meningitis or meningoencephalitis induced by Angiostrongylus cantonensis. Journal of Antimicrobial Chemotherapy 59, 264276.
Chotmongkol, V., Kittimongkolma, S., Niwattayakul, K., Intapan, P. M. and Thavornpitak, Y. (2009). Comparison of prednisolone plus albendazole with prednisolone alone for treatment of patients with eosinophilic meningitis. The American Journal of Tropical Medicine and Hygiene 81, 443445.
Diao, Z., Chen, X., Yin, C., Wang, J., Qi, H. and Ji, A. (2009). Angiostrongylus cantonensis: effect of combination therapy with albendazole and dexamethasone on Th cytokine gene expression in PBMC from patients with eosinophilic meningitis. Experimental Parasitology 123, 15.
Epstein, J., Sanderson, I. R. and Macdonald, T. T. (2010). Curcumin as a therapeutic agent: the evidence from in vitro, animal and human studies. British Journal of Nutrition 103, 15451557.
Gasche, Y., Fujimura, M., Morita-Fujimura, Y., Copin, J. C., Kawase, M., Massengale, J. and Chan, P. H. (1999). Early appearance of activated matrix metalloproteinase-9 after focal cerebral ischemia in mice: a possible role in blood-brain barrier dysfunction. Journal of Cerebral Blood Flow & Metabolism 19, 10201028.
He, H. J., Lv, Z. Y., Li, Z. Y., Zhang, L. Y., Liao, Q., Zheng, H. Q., Su, W. Y., Rao, S. Q., Yu, X. B. and Wu, Z. D. (2011). Efficacy of combined treatment with albendazole and baicalein against eosinophilic meningitis induced by Angiostrongylus cantonensis in mice. Journal of Helminthology 85, 9299.
Lai, S. C. (2006). Chinese herbal medicine Yin-Chen-Extract as an adjunct to anthelmintic albendazole used against Angiostrongylus cantonensis-induced eosinophilic meningitis or meningoencephalitis. The American Journal of Tropical Medicine and Hygiene 75, 556562.
Lai, S. C., Chen, K. M., Chang, Y. H. and Lee, H. H. (2008). Comparative efficacies of albendazole and the Chinese herbal medicine long-dan-xie-gan-tan, used alone or in combination, in the treatment of experimental eosinophilic meningitis induced by Angiostrongylus cantonensis. Annals of Tropical Medicine and Parasitology 102, 143150.
Lai, S. C., Twu, J. J., Jiang, S. T., Hsu, J. D., Chen, K. M., Chiaing, H. C., Wang, C. J., Tseng, C. K., Shyu, L. Y. and Lee, H. H. (2004). Induction of matrix metalloproteinase-9 in murine eosinophilic meningitis caused by Angiostrongylus cantonensis. Annals of Tropical and Medicine and Parasitology 98, 715724.
Lan, K. P., Wang, C. J., Lai, S. C., Chen, K. M., Lee, S. S., Hsu, J. D. and Lee, H. H. (2004). The efficacy of therapy with albendazole in mice with parasitic meningitis caused by Angiostrongylus cantonensis. Parasitology Research 93, 311317.
Lee, H. H., Chou, H. L., Chen, K. M. and Lai, S. C. (2004). Association of matrix- metalloproteinase-9 in eosinophilic meningitis of BALB/c mice caused by Angiostrongylus cantonensis. Parasitology Research 94, 321328.
Leone, S., De Marco, M., Ghirga, P., Nicastri, E., Esposito, M. and Narciso, P. (2007). Eosinophilic meningitis in a returned traveler from Santo Domingo: case report and review. Journal of Travel Medicine 14, 407410.
Leppert, D., Leib, S. L., Grygar, C., Miller, K. M., Schaad, U. B. and Holländer, G. A. (2000). Matrix metalloproteinase (MMP)-8 and MMP-9 in cerebrospinal fluid during bacterial meningitis: association with blood-brain barrier damage and neurological sequelae. Clinical Infectious Diseases 31, 8084.
Luessi, F., Sollors, J., Torzewski, M., Müller, H. D., Siegel, E., Blum, J., Sommer, C., Vogt, T. and Thömke, F. (2009). Eosinophilic meningitis due to Angiostrongylus cantonensis in Germany. Journal of Travel Medicine 16, 292294.
Maldonado, A., Simões, R. O., Oliveira, A. P., Motta, E. M., Fernandez, M. A., Pereira, Z. M., Monteiro, S. S., Torres, E. J. and Thiengo, S. C. (2010). First report of Angiostrongylus cantonensis (Nematoda: Metastrongylidae) in Achatina fulica (Mollusca: Gastropoda) from Southeast and South Brazil. Memórias do Instituto Oswaldo Cruz 105, 938941.
Malvy, D., Ezzedine, K., Receveur, M. C., Pistone, T., Crevon, L., Lemardeley, P. and Josse, R. (2008). Cluster of eosinophilic meningitis attributable to Angiostrongylus cantonensis infection in French policemen troop returning from the Pacific Islands. Travel Medicine and Infectious Disease 6, 301304.
Marathe, S. A., Ray, S. and Chakravortty, D. (2010). Curcumin increases the pathogenicity of Salmonella enterica serovar Typhimurium in murine model. PLoS One 5, e11511.
Mehra, D., Sternberg, D. I., Jia, Y., Canfield, S., Lemaitre, V., Nkyimbeng, T., Wilder, J., Sonett, J. and D'Armiento, J. (2010). Altered lymphocyte trafficking and diminished airway reactivity in transgenic mice expressing human MMP-9 in a mouse model of asthma. The American Journal of Physiology-Lung Cellular and Molecular Physiology 298, 189–96.
Mishra, K., Dash, A. P., Swain, B. K. and Dey, N. (2009). Anti-malarial activities of Andrographis paniculata and Hedyotis corymbosa extracts and their combination with curcumin. Malaria Journal 8, 2634.
Nomura, S. and Lin, P. H. (1945). First case report of human infection with Hamostrongylus ratti Yokogawa. Formosan Medical World 3, 589592.
Perez, O., Capron, M., Lastre, M., Venge, P., Khalife, J. and Capron, A. (1989). Angiostrongylus cantonensis: role of eosinophils in the neurotoxic syndrome (Gordon-like phenomenon). Experimental Parasitology 68, 403413.
Perry, M. C., Demeule, M., Régina, A., Moumdjian, R. and Béliveau, R. (2010). Curcumin inhibits tumor growth and angiogenesis in glioblastoma xenografts. Molecular Nutrition & Food Research 54, 11921201.
Punyagupta, S., Juttijudata, P. and Bunnag, T. (1975). Eosinophilic meningitis in Thailand. Clinical studies of 484 typical cases probably caused by Angiostrongylus cantonensis. The American Journal of Tropical Medicine and Hygiene 24, 921931.
Reddy, R. C., Vatsala, P. G., Keshamouni, V. G., Padmanaban, G. and Rangarajan, P. N. (2005). Curcumin for malaria therapy. Biochemical Biophysical Research Communications 326, 472474.
Rosenberg, G. A., Kornfeld, M., Estrada, E., Kelley, R. O., Liotta, L. A. and Stetler- Stevenson, W. G. (1992). TIMP-2 reduces proteolytic opening of blood-brain barrier by type IV collagenase. Brain Research 576, 203207.
Sawanyawisuth, K. and Sawanyawisuth, K. (2010). Drug target in eosinophilic meningitis caused by Angiostrongylus cantonensis. Infectious Disords- Drug Targets 10, 322328.
Sharma, R. A., Gescher, A. J. and Steward, W. P. (2005). Curcumin: the story so far. European Journal of Cancer 41, 19551968.
Shih, P. C., Lee, H. H., Lai, S. C., Chen, K. M., Jiang, S. T., Chen, Y. F. and Shiow, S. J. (2007). Efficacy of curcumin therapy against Angiostrongylus cantonensis-induced eosinophilic meningitis. Journal of Helminthology 81, 15.
Slom, T. J., Cortese, M. M., Gerber, S. I., Jones, R. C., Holtz, T. H., Lopez, A. S., Zambrano, C. H., Sufit, R. L., Sakolvaree, Y., Chaicumpa, W., Herwaldt, B. L. and Johnson, S. (2002). An outbreak of eosinophilic meningitis caused by Angiostrongylus cantonensis in travelers returning from the Caribbean. New England Journal of Medicine 346, 668675.
Thiengo, S. C., Maldonado, A., Mota, E. M., Torres, E. J., Caldeira, R., Carvalho, O. S., Oliveira, A. P., Simões, R. O., Fernandez, M. A. and Lanfredi, R. M. (2010). The giant African snail Achatina fulica as natural intermediate host of Angiostrongylus cantonensis in Pernambuco northeast Brazil. Acta Tropica 115, 194199.
Tsai, H. C., Chung, L. Y., Chen, E. R., Liu, Y. C., Lee, S. S., Chen, Y. S., Sy, C. L., Wann, S. R. and Yen, C. M. (2008). Association of matrix metalloproteinase-9 and tissue inhibitors of metalloproteinase-4 in cerebrospinal fluid with blood-brain barrier dysfunction in patients with eosinophilic meningitis caused by Angiostrongylus cantonensis. The American Journal of Tropical Medicine and Hygiene 78, 2027.
Tsai, H. C., Lee, S. S., Huang, C. K., Yen, C. M., Chen, E. R. and Liu, Y. C. (2004). Outbreak of eosinophilic meningitis associated with drinking raw vegetable juice in southern Taiwan. The American Journal of Tropical Medicine and Hygiene 71, 222226.
Tsai, H. C., Liu, Y. C., Kunin, C. M., Lai, P. H., Lee, S. S., Chen, Y. S., Wann, S. R., Lin, W. R., Huang, C. K., Ger, L. P., Lin, H. H. and Yen, M. Y. (2003). Eosinophilic meningitis caused by Angiostrongylus cantonensis associated with eating raw snails: correlation of brain magnetic resonance imaging scans with clinical findings. The American Journal of Tropical Medicine and Hygiene 68, 281285.
Tsai, T. H., Liu, Y. C., Wann, S. R., Lin, W. R., Lee, S. J., Lin, H. H., Chen, Y. S., Yen, M. Y. and Yen, C. M. (2001). An outbreak of meningitis caused by Angiostrongylus cantonensis in Kaohsiung. Journal of Microbiology, Immunology and Infection 34, 5056.
Tu, W. C. and Lai, S. C. (2006). Angiostrongylus cantonensis: efficacy of albendazole -dexamethasone co-therapy against infection-induced plasminogen activators and eosinophilic meningitis. Experimental Parasitology 113, 815.
Venkatesan, P. (1998). Albendazole. Journal of Antimicrobial Chemotherapy 41, 145147.
Wang, L. C., Jung, S. M., Chen, C. C., Wong, H. F., Wan, D. P. and Wan, Y. L. (2006). Pathological changes in the brains of rabbits experimentally infected with Angiostongylus cantonesis after albendazole treatment: histopathological and magnetic resonance imaging studies. Journal of Antimicrobial Chemotherapy 57, 294300.
Yoshimura, K. and Soulsby, E. J. L. (1976). Angiostrongylus cantonensis: Lymphoid cell responsiveness and antibody production in rats. The American Journal of Tropical Medicine and Hygiene. 25, 99107.
Yoshimura, K., Sugaya, H., Kawamura, K. and Kumagai, M. (1988). Ultrastructural and morphometric analyses of eosinophils from the cerebrospinal fluid of the mouse and guinea-pig infected with Angiostrongylus cantonensis. Parasite Immunology 10, 411423.
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