Hostname: page-component-586b7cd67f-dlnhk Total loading time: 0 Render date: 2024-12-02T23:24:41.142Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  07 November 2011

LING-YUH SHYU ,
HAN-HSIN CHANG ,
JENG-DONG HSU ,
DAVID PEI-CHENG LIN ,
YING-HOCK TENG  and
HSIU-HSIUNG LEE
LING-YUH SHYU*
Affiliation:
Institute of Medicine, Chung Shan Medical University, Taiwan, ROC Department of Parasitology, Chung Shan Medical University, Taiwan, ROC
HAN-HSIN CHANG
Affiliation:
School of Nutrition, Chung Shan Medical University, Taiwan, ROC
JENG-DONG HSU
Affiliation:
Department of Pathology, Chung Shan Medical University, Taiwan, ROC
DAVID PEI-CHENG LIN
Affiliation:
School of Medical Laboratory and Biotechnology, Chung Shan Medical University, Taiwan, ROC
YING-HOCK TENG
Affiliation:
Institute of Medicine, Chung Shan Medical University, Taiwan, ROC Chung Shan Medical University, Department of Emergency Medicine, Taiwan, ROC
HSIU-HSIUNG LEE
Affiliation:
Institute of Medicine, Chung Shan Medical University, Taiwan, ROC Department of Parasitology, Chung Shan Medical University, Taiwan, ROC
*
*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: [email protected]
Get access Rights & Permissions [Opens in a new window]

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.

Keywords

Angiostrongylus cantonensiseosinophilic meningitiscurcumincomplementary medication
Type
Research Article
Information
Parasitology , Volume 139 , Issue 3 , March 2012 , pp. 358 - 365
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

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, 38–46.Google Scholar
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, 989–998.CrossRefGoogle ScholarPubMed
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, 248–254.CrossRefGoogle ScholarPubMed
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, 887–889.CrossRefGoogle ScholarPubMed
Chen, H. T. (1935). Un nouveau nematode pulmonaire: Pulmonema cantonensis, n.g.m. sp. Des rats de canton. Annals of Parasitology 13, 312–317.Google Scholar
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, 264–276.CrossRefGoogle ScholarPubMed
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, 443–445.CrossRefGoogle ScholarPubMed
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, 1–5.CrossRefGoogle ScholarPubMed
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, 1545–1557.CrossRefGoogle ScholarPubMed
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, 1020–1028.CrossRefGoogle ScholarPubMed
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, 92–99.CrossRefGoogle ScholarPubMed
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, 556–562.CrossRefGoogle ScholarPubMed
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, 143–150.Google Scholar
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, 715–724.Google Scholar
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, 311–317.CrossRefGoogle ScholarPubMed
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, 321–328.CrossRefGoogle ScholarPubMed
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, 407–410.Google Scholar
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, 80–84.CrossRefGoogle ScholarPubMed
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, 292–294.CrossRefGoogle ScholarPubMed
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, 938–941.CrossRefGoogle ScholarPubMed
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, 301–304.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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, 26–34.CrossRefGoogle ScholarPubMed
Nomura, S. and Lin, P. H. (1945). First case report of human infection with Hamostrongylus ratti Yokogawa. Formosan Medical World 3, 589–592.Google Scholar
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, 403–413.CrossRefGoogle ScholarPubMed
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, 1192–1201.Google Scholar
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, 921–931.Google Scholar
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, 472–474.CrossRefGoogle ScholarPubMed
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, 203–207.Google Scholar
Sawanyawisuth, K. and Sawanyawisuth, K. (2010). Drug target in eosinophilic meningitis caused by Angiostrongylus cantonensis. Infectious Disords- Drug Targets 10, 322–328.Google Scholar
Sharma, R. A., Gescher, A. J. and Steward, W. P. (2005). Curcumin: the story so far. European Journal of Cancer 41, 1955–1968.Google Scholar
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, 1–5.CrossRefGoogle ScholarPubMed
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, 668–675.CrossRefGoogle ScholarPubMed
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, 194–199.Google Scholar
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, 20–27.Google Scholar
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, 222–226.Google Scholar
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, 281–285.Google Scholar
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, 50–56.Google Scholar
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, 8–15.CrossRefGoogle ScholarPubMed
Venkatesan, P. (1998). Albendazole. Journal of Antimicrobial Chemotherapy 41, 145–147.Google Scholar
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, 294–300.CrossRefGoogle Scholar
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, 99–107.CrossRefGoogle ScholarPubMed
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, 411–423.CrossRefGoogle ScholarPubMed