Hostname: page-component-848d4c4894-m9kch Total loading time: 0 Render date: 2024-05-09T17:57:27.728Z Has data issue: false hasContentIssue false
  • English
  • Français

Immune responses induced by co-infection with Capillaria hepatica in Clonorchis sinensis-infected rats

Published online by Cambridge University Press:  08 August 2017

E.-K. Moon ,
S.-H. Lee ,
T.W. Goo  and
F.-S. Quan
E.-K. Moon
Affiliation:
Department of Medical Zoology, Kyung Hee University School of Medicine, Seoul, Korea
S.-H. Lee
Affiliation:
Department of Biomedical Science, Graduate School, Kyung Hee University, Seoul, Korea
T.W. Goo
Affiliation:
Department of Biochemistry, College of Medicine, Dongguk University, Gyeongju, Republic of Korea
F.-S. Quan*
Affiliation:
Department of Medical Zoology, Kyung Hee University School of Medicine, Seoul, Korea
*
*E-mail: fsquan@khu.ac.kr
Get access Rights & Permissions [Opens in a new window]

Abstract

Clonorchis sinensis and Capillaria hepatica are zoonotic parasites that mainly infect the liver and cause serious liver disorders. However, immunological parameters induced by co-infection with these parasites remain unknown. In this study, for the first time, we investigated immunological profiles induced by co-infection with C. hepatica (CH) in C. sinensis (CS)-infected rats (Sprague–Dawley). Rats were infected primarily with 50 metacercariae of C. sinensis; 4 weeks later, they were subsequently infected with 1000 infective C. hepatica eggs. Significantly higher levels of C. sinensis- or C. hepatica-specific IgG antibodies were found in the sera of rats. Interestingly, no cross-reacting antibody was observed between C. sinensis and C. hepatica infections. Significantly raised eosinophil levels were found in the blood of C. sinensis/C. hepatica co-infected rats (CS + CH) compared to the blood of rats infected singly with C. sinensis. Co-infected rats showed significantly higher levels of lymphocyte proliferation and cytokine production compared to a single C. sinensis infection. The worm burden of C. sinensis was significantly reduced in co-infected rats compared to the single C. sinensis infection. These results indicate that the eosinophils, lymphocyte proliferation and cytokine production induced by subsequent infection with C. hepatica in C. sinensis-infected rats might contribute to the observed C. sinensis worm reduction.

Type
Research Paper
Information
Journal of Helminthology , Volume 92 , Issue 4 , July 2018 , pp. 395 - 402
Copyright
Copyright © Cambridge University Press 2017 

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

Bruschi, F., Korenaga, M. & Watanabe, N. (2008) Eosinophils and Trichinella infection: toxic for the parasite and the host? Trends in Parasitology 24, 462–467.Google Scholar
Cadman, E.T. & Lawrence, R.A. (2010) Granulocytes: effector cells or immunomodulators in the immune response to helminth infection? Parasite Immunology 32, 1–19.Google Scholar
Cadman, E.T., Thysse, K.A., Bearder, S., Cheung, A.Y., Johnston, A.C., Lee, J.J. & Lawrence, R.A. (2014) Eosinophils are important for protection, immunoregulation and pathology during infection with nematode microfilariae. PLoS Pathogens 10, e1003988.Google Scholar
Center for Disease Control. (2011) Parasites and health: capillariasis. Available at https://www.cdc.gov/parasites/capillaria/biology_c_hepatica.html (accessed 13 February 2017).Google Scholar
Cheever, A.W., Hoffmann, K.F. & Wynn, T.A. (2000) Immunopathology of schistosomiasis mansoni in mice and men. Immunology Today 21, 465–466.CrossRefGoogle ScholarPubMed
Chen, Y., Huang, B., Huang, S., Yu, X., Li, Y., Song, W., Li, Y. & Lu, F. (2013) Coinfection with Clonorchis sinensis modulates murine host response against Trichinella spiralis infection. Parasitology Research 112, 3167–3179.Google Scholar
Chu, K., Kim, S., Lee, S., Lee, H., Joo, K., Lee, J., Lee, Y., Zheng, S. & Quan, F. (2014) Enhanced protection against Clonorchis sinensis induced by co-infection with Trichinella spiralis in rats. Parasite Immunology 36, 522–530.Google Scholar
Chu, K.B., Kim, S.S., Lee, S.H., Lee, D.H., Kim, A.R. & Quan, F.S. (2016) Immune correlates of resistance to Trichinella spiralis reinfection in mice. Korean Journal of Parasitology 54, 637–643.Google Scholar
El Dib, N.A., Sabry, M.A., Ahmed, J.A., El-Basiouni, S.O. & El-Badry, A.A. (2004) Evaluation of Capillaria philippinensis coproantigen in the diagnosis of infection. Journal of the Egyptian Society of Parasitology 34, 97–106.Google Scholar
Ewing, G.M. & Tilden, I. (1956) Capillaria hepatica: report of fourth case of true human infestation. Journal of Pediatrics 48, 341–348.Google Scholar
Ferreira, L.A. & Andrade, Z.A. (1993) Capillaria hepatica: a cause of septal fibrosis of the liver. Memórias do Instituto Oswaldo Cruz 88, 441–447.Google Scholar
Fuehrer, H. (2014) An overview of the host spectrum and distribution of Calodium hepaticum (syn. Capillaria hepatica): part 2 – Mammalia (excluding Muroidea). Parasitology Research 113, 641–651.CrossRefGoogle ScholarPubMed
Ganley-Leal, L.M., Mwinzi, P.N., Cetre-Sossah, C.B., Andove, J., Hightower, A.W., Karanja, D.M., Colley, D.G. & Secor, W.E. (2006) Correlation between eosinophils and protection against reinfection with Schistosoma mansoni and the effect of human immunodeficiency virus type 1 coinfection in humans. Infection and Immunity 74, 2169–2176.CrossRefGoogle ScholarPubMed
Hamann, K.J., Gleich, G.J., Checkel, J.L., Loegering, D.A., McCall, J.W. & Barker, R.L. (1990) In vitro killing of microfilariae of Brugia pahangi and Brugia malayi by eosinophil granule proteins. Journal of Immunology (Baltimore, Md.: 1950) 144, 3166–3173.Google Scholar
Hesse, M., Cheever, A.W., Jankovic, D. & Wynn, T.A. (2000) NOS-2 mediates the protective anti-inflammatory and antifibrotic effects of the Th1-inducing adjuvant, IL-12, in a Th2 model of granulomatous disease. American Journal of Pathology 157, 945–955.Google Scholar
Hoffmann, K.F., Caspar, P., Cheever, A.W. & Wynn, T.A. (1998) IFN-gamma, IL-12, and TNF-alpha are required to maintain reduced liver pathology in mice vaccinated with Schistosoma mansoni eggs and IL-12. Journal of Immunology (Baltimore, Md.: 1950) 161, 4201–4210.Google Scholar
Hong, S. & Fang, Y. (2012) Clonorchis sinensis and clonorchiasis, an update. Parasitology International 61, 17–24.Google Scholar
Juncker-Voss, M., Prosl, H., Lussy, H., Enzenberg, U., Auer, H. & Nowotny, N. (2000) Serological detection of Capillaria hepatica by indirect immunofluorescence assay. Journal of Clinical Microbiology 38, 431–433.Google Scholar
Kazura, J.W. (1981) Host defense mechanisms against nematode parasites: destruction of newborn Trichinella spiralis larvae by human antibodies and granulocytes. Journal of Infectious Diseases 143, 712–718.Google Scholar
Kim, D., Joo, K. & Chung, M. (2007) Changes of cytokine mRNA expression and IgG responses in rats infected with Capillaria hepatica. Korean Journal of Parasitology 45, 95–102.Google Scholar
Klion, A.D. (2015) How I treat hypereosinophilic syndrome. Blood 126, 1069–1077.Google Scholar
Klion, A.D. & Nutman, T.B. (2004) The role of eosinophils in host defense against helminth parasites. Journal of Allergy and Clinical Immunology 113, 30–37.Google Scholar
Knott, M.L., Matthaei, K.I., Giacomin, P.R., Wang, H., Foster, P.S. & Dent, L.A. (2007) Impaired resistance in early secondary Nippostrongylus brasiliensis infections in mice with defective eosinophilopoeisis. International Journal for Parasitology 37, 1367–1378.Google Scholar
Lee, C.W. (1964) The experimental studies on Capillaria hepatica. Korean Journal of Parasitology 2, 63–77.Google Scholar
Lee, H.K., Jin, S.L., Lee, H.P., Choi, S.J. & Yum, H.K. (2003) Loffler's syndrome associated with Clonorchis sinensis infestation. Korean Journal of Internal Medicine 18, 255–259.Google Scholar
Pit, D., Polderman, A., Baeta, S., Schulz-Key, H. & Soboslay, P. (2001) Parasite-specific antibody and cellular immune responses in humans infected with Necator americanus and Oesophagostomum bifurcum. Parasitology Research 87, 722–729.Google Scholar
Quan, F., Matsumoto, T., Lee, J., Timothy, O., Lee, J., Kim, T.S., Joo, K. & Lee, J. (2004) Immunization with Trichinella spiralis Korean isolate larval excretory–secretory antigen induces protection and lymphocyte subset changes in rats. Immunological Investigations 33, 15–26.Google Scholar
Rim, H. (2005) Clonorchiasis: an update. Journal of Helminthology 79, 269–281.Google Scholar
Sharma, R., Dey, A.K., Mittal, K., Kumar, P. & Hira, P. (2015) Capillaria hepatica infection: a rare differential for peripheral eosinophilia and an imaging dilemma for abdominal lymphadenopathy. Annals of Parasitology 61, 61–64.Google Scholar
Sripa, B., Kaewkes, S., Intapan, P.M., Maleewong, W. & Brindley, P.J. (2010) Food-borne trematodiases in Southeast Asia: epidemiology, pathology, clinical manifestation and control. Advances in Parasitology 72, 305–350.Google Scholar
Vallance, B.A., Matthaei, K., Sanovic, S., Young, I. & Collins, S. (2000) Interleukin-5 deficient mice exhibit impaired host defence against challenge Trichinella spiralis infections. Parasite Immunology 22, 487–492.Google Scholar