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Leukogram and cortisol parameters in Swiss mice experimentally infected with Angiostrongylus costaricensis

Published online by Cambridge University Press:  06 August 2021

E. Benvegnú
Affiliation:
Postgraduate Program on Bioexperimentation, University of Passo Fundo (UPF), Campus I, BR 285, Bairro São José, Passo Fundo, Rio Grande do Sul99052-900, Brazil
C.C. Hermes
Affiliation:
Postgraduate Program on Bioexperimentation, University of Passo Fundo (UPF), Campus I, BR 285, Bairro São José, Passo Fundo, Rio Grande do Sul99052-900, Brazil
J.A. Guizzo
Affiliation:
Postgraduate Program on Veterinary Medicine, Federal University of Santa Maria, Santa Maria97105-900, Brazil
S.M. Soares
Affiliation:
Postgraduate Program on Pharmacology, Federal University of Santa Maria, Santa Maria97105-900, Brazil
M.M. Costa
Affiliation:
Postgraduate Program on Bioexperimentation, University of Passo Fundo (UPF), Campus I, BR 285, Bairro São José, Passo Fundo, Rio Grande do Sul99052-900, Brazil
R. Rodriguez
Affiliation:
Pathology Institute of Passo Fundo, Rua Teixeira Soares 885, Centro, 99010-08Passo Fundo, Brazil
R. Frandoloso
Affiliation:
Postgraduate Program on Bioexperimentation, University of Passo Fundo (UPF), Campus I, BR 285, Bairro São José, Passo Fundo, Rio Grande do Sul99052-900, Brazil
M.I.B. Vieira*
Affiliation:
Postgraduate Program on Bioexperimentation, University of Passo Fundo (UPF), Campus I, BR 285, Bairro São José, Passo Fundo, Rio Grande do Sul99052-900, Brazil
*
Author for correspondence: M.I.B. Vieira, E-mail: [email protected]

Abstract

This study describes changes in haematological parameters, cytokine profile, histopathology and cortisol levels in Swiss mice experimentally infected with Angiostrongylus costaricensis. Twenty-eight Swiss mice were divided into two groups (G1 and G2) of 14 animals each. In each group, eight animals were infected orally with ten third-stage larvae of A. costaricensis and six were used as a control group. The mice of groups G1 and G2 were sacrificed 14 and 24 days after infection, respectively. Samples were collected for histopathological and haematological analyses and determination of the cytokine profile and cortisol levels. Granulomatous reaction, eosinophilic infiltrate and vasculitis in the intestinal tract, pancreas, liver and spleen were observed with varying intensity in infected animals. Our results showed that the mice developed normocytic and hypochromic anaemia, and that the histopathological lesions caused by the experimental infection influenced increases in cortisol, neutrophil and monocyte levels. In addition to this, we detected increased interleukin-6 and tumour necrosis factor alpha levels in the infected animals.

Type
Research Paper
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Alfaro-Alarcón, A, Veneziano, V, Galiero, G, et al. (2015) First report of a naturally patent infection of Angiostrongylus costaricensis in a dog. Veterinary Parasitology 212, 431434.CrossRefGoogle Scholar
Anthony, RM, Rutitzky, LI, Urban, JF, Stadecker, MJ and Gause, WC (2007) Protective immune mechanisms in helminth infection. Nature Reviews Immunology 7, 975987.CrossRefGoogle ScholarPubMed
Bender, AL, Maurer, RL, da Silva, MCF, Bem, R, Terraciano, PB, da Silva, ACA and Graeff-Teixeira, C (2003) Ovos e órgãos reprodutores de fêmeas de Angiostrongylus costaricensis sao reconhecidos mais intensamente por soros humanos de fase aguda na angiostrongilíase abdominal. Revista da Sociedade Brasileira de Medicina Tropical 36, 449454.CrossRefGoogle Scholar
Burkhard, MJ, Brown, DE, McGrath, JP, et al. (2001) Evaluation of the erythroid regenerative response in two different models of experimentally induced iron deficiency anemia. Veterinary Clinical Pathology 30, 7685.CrossRefGoogle ScholarPubMed
Burnham, KP, Anderson, DR and Huyvaert, KP (2011) AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behavioral Ecology and Sociobiology 65, 2335.CrossRefGoogle Scholar
Calcagni, E (2006) Stress system activity, innate and T helper cytokines, and susceptibility to immune-related diseases. Annals of the New York Academy of Sciences 1069, 6276. Doi: 10.1196/annals.1351.006.CrossRefGoogle Scholar
Castro, R, Zou, J, Secombes, CJ and Martin, SAM (2011) Cortisol modulates the induction of inflammatory gene expression in a rainbow trout macrophage cell line. Fish Shellfish Immunology 30, 215223.CrossRefGoogle Scholar
Chulilla, JAM, Colás, MSR and Martín, MG (2009) Classification of anemia for gastroenterologists. World Journal of Gastroenterology 15, 46274637.CrossRefGoogle Scholar
Cortes, A, Sotillo, J, Muñoz-Antoli, C, Fried, B, Esteban, JG and Toledo, R (2014) Intestinal IFN-γ production is associated with protection from clinical signs, but not with elimination of worms, in Echinostoma caproni infected-mice. Parasitology Research 113, 20372045.CrossRefGoogle Scholar
de Vasconcelos, DIB, Mota, EM and Pelajo-Machado, M (2017) Characterisation of the vascular pathology in Sigmodon hispidus (Rodentia: Cricetidae) following experimental infection with Angiostrongylus costaricensis (Nematoda: Metastrongylidae). Memórias do Instituto Oswaldo Cruz 112, 328338.CrossRefGoogle Scholar
Economou, M and Zissis, M (2000) Infectious cases of acute pancreatitis. Annals of Gastroenterology 13, 98101.Google Scholar
Escobedo, G, Roberts, CW, Carrero, JC and Morales-Montor, J (2005) Parasite regulation by host hormones: an old mechanism of host exploitation? Trends Parasitology 21, 588593.CrossRefGoogle ScholarPubMed
Fan, CK, Lin, YH, Du, WY and Su, KE (2003) Infectivity and pathogenicity of 14-month-cultured embryonated eggs of Toxocara canis in mice. Veterinary Parasitology 113(2), 145155.CrossRefGoogle ScholarPubMed
Fernando, MR, Reyes, JL, Iannuzzi, J, Leung, G and McKay, DM (2014) The pro-inflammatory cytokine, interleukin-6, enhances the polarization of alternatively activated macrophages. PLoS One 9, 112.CrossRefGoogle ScholarPubMed
Geiger, SM, Abrahams-Sandi, E, Soboslay, PT, Hoffmann, WH, Pfaff, AW, Graeff-Teixeira, C and Schulz-Key, H (2001) Cellular immune responses and cytokine production in BALB/c and C57BL/6 mice during the acute phase of Angiostrongylus costaricensis infection. Acta Tropica 80, 5968.CrossRefGoogle ScholarPubMed
Geiger, SM, Hoffmann, WH, Soboslay, PT, Pfaff, AW, Graeff-Teixeira, C and Schulz-Key, H (2003) Angiostrongylus costaricensis infection in C57BL/6 mice: MHC-II deficiency results in increased larval elimination but unaltered mortality. Parasitology Research 90, 415420.CrossRefGoogle ScholarPubMed
Graeff-Teixeira, C, Camillo-Coura, L and Lenzi, HL (1991) Histopathological criteria for the diagnosis of abdominal angiostrongyliasis. Parasitology Research 77, 606611.CrossRefGoogle Scholar
Green, AM, DiFazio, R and Flynn, JL (2013) IFN-γ from CD4 t cells is essential for host survival and enhances CD8 t cell function during Mycobacterium tuberculosis infection. The Journal of Immunology 190, 270277.CrossRefGoogle ScholarPubMed
Gülen, B, Dur, A, Serinken, M, Karcioğlu, Ö and Sönmez, E (2016) Pain treatment in patients with acute pancreatitis: a randomized controlled trial. Turkish Journal of Gastroenterology 27, 192196.CrossRefGoogle ScholarPubMed
Hermes, CC, Benvegnú, E, Costa, MM, Rodriguez, R and Vieira, MIB (2020) Abdominal angiostrongyliasis: pathologic findings in Swiss mice infected with different doses of Angiostrongylus costaricensis. Journal of Helminthology 94, 169, 1–7.CrossRefGoogle ScholarPubMed
Hu, X and Ivashkiv, LB (2009) Cross-regulation of signaling pathways by interferon-γ: implications for immune responses and autoimmune diseases. Immunity 31, 539550.CrossRefGoogle ScholarPubMed
Hurvich, CM and Tsai, CL (1989) Regression and time series model selection in small samples. Biometrika 76, 297307.CrossRefGoogle Scholar
Incani, RN, Caleiras, E, Martín, M and González, C (2007) Human infection by Angiostrongylus costaricensis in Venezuela: first report of a confirmed case. Revista do Instituto de Medicina Tropical de São Paulo 49, 197200.CrossRefGoogle ScholarPubMed
Inoue, SI, Niikura, M, Mineo, S and Kobayashi, F (2013) Roles of IFN-γ and γδ T cells in protective immunity against blood-stage malaria. Frontiers in Immunology 4, 19.CrossRefGoogle ScholarPubMed
Ishih, A and Nishimura, M (1997) Differential responses of SM/j and A/J mice to experimental Angiostrongylus costaricensis infection. International Journal for Parasitology 27, 14111414.CrossRefGoogle Scholar
Jain, NC (1986) Weiss, Douglas J., Wardrop, K. Jane (Eds) Schalm's veterinary hematology, Wiley-Blackwell.Google Scholar
Junqueira, LC and Carneiro, J (1995) Histologia Básica. 8th edn. Rio de Janeiro, Guanabara Koogan.Google Scholar
Khuroo, MS, Zargar, SA, Yattoo, GN, Koul, P, Khan, BA, Dar, MY and Alai, MS (1992) Ascaris-induced acute pancreatitis. British Journal of Surgery 79(12), 13351338.CrossRefGoogle ScholarPubMed
Körner, H, McMorran, B, Schlüter, D and Fromm, P (2010) The role of TNF in parasitic diseases: still more questions than answers. International Journal for Parasitology 40, 879888.CrossRefGoogle ScholarPubMed
Kramer, MK, Greer, GJ, Quinonez, JF, et al. (1998) First reported outbreak of abdominal angiostrongyliasis. Clinical Infectious Diseases 26, 365372.CrossRefGoogle ScholarPubMed
Liu, YM, Bair, MJ, Chang, WH, Lin, SC and Chan, YJ (2005) Acute pancreatitis caused by tapeworm in the biliary tract. The American Journal of Tropical Medicine and Hygiene 73(2), 377380.CrossRefGoogle ScholarPubMed
María, GA, Villarroel, M, Chacón, G and Gebresenbet, G (2004) Scoring system for evaluating the stress to cattle of commercial loading and unloading. Veterinary Record 154, 818821.CrossRefGoogle ScholarPubMed
Maswoswe, SM, Peters, W and Warhurst, DC (1985) Corticosteroid stimulation of the growth of Plasmodium falciparum gametocytes in vitro. Annals Tropical Medicine Parasitology 79, 607616.CrossRefGoogle ScholarPubMed
Moreau, E and Chauvin, A (2010) Immunity against helminths: interactions with the host and the intercurrent infections. Journal of Biomedicine and Biotechnology 10, 19.CrossRefGoogle Scholar
Morera, P and Céspedes, R (1971) Angiostrongylus costaricensis n. sp. (Nematoda: Metastrongyloidea), a new lungworm occurring in man in Costa Rica. Revista de Biologia Tropical 18, 173185.Google Scholar
Morera, P, Lazo, R, Urquizo, J and Llaguno, M (1983) First record of Angiostrongylus costaricensis Morera and Cespedes, 1971 in Ecuador. The American Journal of Tropical Medicine and Hygiene 32, 4601461.CrossRefGoogle ScholarPubMed
Mota, EM and Lenzi, HL (2005) Angiostrongylus costaricensis: complete redescription of the migratory pathways based on experimental Sigmodon hispidus infection. Memórias do Instituto Oswaldo Cruz 100, 407420.CrossRefGoogle ScholarPubMed
Paim, FC, Duarte, MMMF, Costa, MM, et al. (2011) Cytokines in rats experimentally infected with Trypanosoma evansi. Experimental Parasitology 128, 365370.CrossRefGoogle ScholarPubMed
Rambo, PR, Agostini, AA and Graeff-Teixeira, C (1997) Abdominal angiostrongylosis in Southern Brazil – prevalence and parasitic burden in mollusc intermediate hosts from eighteen endemic foci. Memórias do Instituto Oswaldo Cruz 92, 914.CrossRefGoogle ScholarPubMed
R Core Team, . (2014). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.Google Scholar
Rebello, KM, Barros, JSL, Mota, EM, Carvalho, PC, Perales, J, Lenzi, HL and Neves-Ferreira, AGC (2011) Comprehensive proteomic profiling of adult Angiostrongylus costaricensis, a human parasitic nematode. Journal of Proteomics 74, 15451559.CrossRefGoogle ScholarPubMed
Rodriguez, R, Dequi, RM, Peruzzo, L, Mesquita, PM, Garcia, E and Fornari, F (2008) Abdominal angiostrongyliasis: report of two cases with different clinical presentations. Revista do Instituto de Medicina Tropical de São Paulo 50, 339341.CrossRefGoogle ScholarPubMed
Romero-Alegría, A, Belhassen-García, M, Velasco-Tirado, V, Garcia-Mingo, A, Alvela-Suárez, L, Pardo-Lledias, J and Sánchez, MC (2014) Angiostrongylus costaricensis: systematic review of case reports. Advances in Infectious Diseases 04, 3641.CrossRefGoogle Scholar
Schnyder, M, Fahrion, A, Riond, B, Ossent, P, Webster, P, Kranjc, A, Glaus, T and Deplazes, P (2010) Clinical, laboratory and pathological findings in dogs experimentally infected with Angiostrongylus vasorum. Parasitology Research 107, 14711480.CrossRefGoogle ScholarPubMed
Singh, H, Jain, D and Kiran, B (2016) Acute pancreatitis complicating hepatitis A virus infection: a case report. Eastern Journal of Medicine 1(2), 7172.Google Scholar
Spratt, DM (2015) Species of Angiostrongylus (Nematoda: Metastrongyloidea) in wildlife: a review. International Journal for Parasitology Parasites and Wildlife 4, 178189.CrossRefGoogle ScholarPubMed
Symonds, MR and Moussalli, A (2011) A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike's information criterion. Behavioral Ecology and Sociobiology 65, 1321.CrossRefGoogle Scholar
Törnhage, CJ and Alfvén, G (2015) Children with recurrent psychosomatic abdominal pain display increased morning salivary cortisol and high serum cortisol concentrations. Acta Paediatrica 104, 577580.CrossRefGoogle ScholarPubMed
Vignali, D and Kuchroo, V (2012) IL-12 family cytokines: immunological playmakers. Nature Immunology 13(8), 722728.CrossRefGoogle ScholarPubMed
Zelová, H and Hošek, J (2013) TNF-α signalling and inflammation: interactions between old acquaintances. Inflammation Research 62, 641651.CrossRefGoogle ScholarPubMed