Hostname: page-component-5d59c44645-lfgmx Total loading time: 0 Render date: 2024-03-03T23:58:13.266Z Has data issue: false hasContentIssue false

Relationship between histopathological lesions and oxidative stress in mice infected with Angiostrongylus costaricensis

Published online by Cambridge University Press:  13 January 2023

N. R. Zorzi
Affiliation:
Programa de Pós-Graduação em Bioexperimentação, Universidade de Passo Fundo, Bairro São José, Campus I, km 292, BR 285, 99052-900, Passo Fundo, RS, Brazil
E. Benvegnú
Affiliation:
Programa de Pós-Graduação em Bioexperimentação, Universidade de Passo Fundo, Bairro São José, Campus I, km 292, BR 285, 99052-900, Passo Fundo, RS, Brazil Faculdade Especializada na Área de Saúde do Rio Grande do Sul – FASURGS, Passo Fundo, RS, Brazil
C. Hermes
Affiliation:
Programa de Pós-Graduação em Bioexperimentação, Universidade de Passo Fundo, Bairro São José, Campus I, km 292, BR 285, 99052-900, Passo Fundo, RS, Brazil Hospital São Vicente de Paulo (HSVP), Passo Fundo, RS, Brazil
R. Rodriguez
Affiliation:
Instituto de Patologia de Passo Fundo – IPPF, Passo Fundo, RS, Brazil
N. Freddo
Affiliation:
Programa de Pós-Graduação em Bioexperimentação, Universidade de Passo Fundo, Bairro São José, Campus I, km 292, BR 285, 99052-900, Passo Fundo, RS, Brazil
B. Webber
Affiliation:
Programa de Residência Profissional Integrada em Medicina Veterinária, Universidade de Passo Fundo, Passo Fundo, RS, Brazil
F. U. I. do Amaral
Affiliation:
Programa de Pós-Graduação em Bioexperimentação, Universidade de Passo Fundo, Bairro São José, Campus I, km 292, BR 285, 99052-900, Passo Fundo, RS, Brazil
C. A. Scariot
Affiliation:
Programa de Pós-Graduação em Bioexperimentação, Universidade de Passo Fundo, Bairro São José, Campus I, km 292, BR 285, 99052-900, Passo Fundo, RS, Brazil Centro de Ensino Superior Riograndense-CESURG, Sarandi, RS, Brazil
M. Costa
Affiliation:
Programa de Pós-Graduação em Bioexperimentação, Universidade de Passo Fundo, Bairro São José, Campus I, km 292, BR 285, 99052-900, Passo Fundo, RS, Brazil
L. G. Rossato-Grando
Affiliation:
Programa de Pós-Graduação em Bioexperimentação, Universidade de Passo Fundo, Bairro São José, Campus I, km 292, BR 285, 99052-900, Passo Fundo, RS, Brazil
M. I. B. Vieira*
Affiliation:
Programa de Pós-Graduação em Bioexperimentação, Universidade de Passo Fundo, Bairro São José, Campus I, km 292, BR 285, 99052-900, Passo Fundo, RS, Brazil
*
Author for correspondence: M. I. B. Vieira, E-mail: marisabel@upf.br

Abstract

This study describes changes in oxidative stress (OS) parameters in mice experimentally infected with Angiostrongylus costaricensis, which causes abdominal angiostrongyliasis. For this, 28 Swiss mice were used, divided into two groups (G1 and G2), with 14 animals each. Of these, eight were infected with ten infective larvae each, by gavage, and six were used as a control group. Mice from G1 and G2 were euthanized at 14 days and 24 days post-infection, respectively. Tissue samples were used for histopathological analysis and blood (serum) samples were taken to assess the levels of proteins, non-protein thiols (NPTs) and nitric oxide (NO), from centrifugation and subsequent collection of aliquots of the supernatant. Among OS parameters, infected mice in both groups had higher NO levels than the control group, due to the presence of: eosinophil infiltrate in the liver and intestine; pancreatitis; and intestinal granuloma. However, the infected mice of both groups showed a reduction in the levels of NPTs, in relation to the control group, due to the presence of: eosinophilic infiltrate in the liver and intestine; and intestinal granuloma. Our results suggest that A. costaricensis infection has important effects on the intestine, liver and pancreas, and the analyses were performed from the tissue of these organs. The mechanisms for these changes are related to the decrease in the body's main antioxidant defences, as demonstrated by the reduction of NPTs, thus contributing to the development of more severe tissue damage. Thus, the objective of the present study was to evaluate the relationship between histopathological lesions and markers for OS.

Type
Research Paper
Copyright
Copyright © The Author(s), 2023. Published by Cambridge University Press

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

Amer, OSO, Dkhil, MA, Hikal, WM and Al-Quraishy, S (2015) Antioxidant and anti-inflammatory activities of pomegranate (Punica granatum) on Eimeria papillate –induced infection in mice. BioMed Research International 219670.Google Scholar
Andrade, A, Pinto, SC and Oliveira, RS (2002) Animais de Laboratório: criação e experimentação [Laboratory animals: creation and experimentation]. 388 pp. Rio de Janeiro, Editora FIOCRUZ. [In Portuguese.]Google Scholar
Benvegnú, E, Hermes, CC, Guizzo, JA, Soares, SM, Costa, MM, Rodriguez, R, Frandoloso, R and Vieira, MIB (2021) Leukogram and cortisol parameters in Swiss mice experimentally infected with Angiostrongylus costaricensis. Journal of Helminthology, 95(e40), 18.Google ScholarPubMed
Body, SC, Hartigan, PM, Shernan, SK, Formanek, V and Hurford, WE (1995) Nitric oxide: delivery, measurement and clinical application. Journal of Cardiothoracic Vascular Anesthesia 9(6), 748763.CrossRefGoogle ScholarPubMed
Boeckxstaens, GE, Pelckmans, PA, Bult, H, De Man, JG, Herman, AG and Van Maercke, YM (1991) Evidence for nitric oxide as mediator of non-adrenergic, non-cholinergic relaxations induced by ATP and GABA in the canine gut. British Journal of Pharmacology 102(2), 434438.CrossRefGoogle ScholarPubMed
Bracht, A and Ishii- Iwamoto, EL (2003) Métodos de laboratório em Bioquímica [Laboratory methods in biochemistry]. pp. 77101. São Paulo, Manole. [In Portuguese.]Google Scholar
Bradford, MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Analytical Biochemistry 72(1), 248254.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(1), 2335.CrossRefGoogle Scholar
Creagh, EM and O'Neill, LA (2006) TLRs, NLRs and RLRs: a trinity of pathogen sensors that co-operate in innate immunity. Trends in Immunology 27(8), 352357.CrossRefGoogle ScholarPubMed
Di Lorenzo, M, Bass, J and Krantis, A (1995) Use of L-arginine in the treatment of experimental necrotizing enterocolitis. Journal of Pediatric Surgery 30(2), 235241.CrossRefGoogle ScholarPubMed
Docampo, R (1990) Sensitivity of parasites to free radical damage by antiparasitic drugs. Chemico-Biological Interactions 73(1), 127.CrossRefGoogle ScholarPubMed
Ellman, GL (1959) Tissue sulfhydryl groups. Archives of Biochemistry and Biophysics 82(1), 7077.CrossRefGoogle ScholarPubMed
Furukawa, S, Fujita, T, Shimabukuro, M, et al. (2004) Increased oxidative stress in obesity and its impact on metabolic syndrome. The Journal of Clinical Investigation 114(12), 17521761.CrossRefGoogle ScholarPubMed
Gandon, S, Buckling, A, Decaestecker, E and Day, T (2008) Host–parasite coevolution and patterns of adaptation across time and space. Journal of Biology 21(6), 18611866.Google 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(1), 5968.CrossRefGoogle ScholarPubMed
Graeff-Teixeira, C, Camillo-Coura, L and Lenzi, HL (1987) Abdominal angiostrongyliasis an under diagnosed disease. Memórias do Instituto Oswaldo Cruz 82(Suppl 4), 353354.CrossRefGoogle ScholarPubMed
Graeff-Teixeira, C, Avila-Pires, FD, Machado, RCC, Camillo- Coura, L and Lenzi, HL (1990) Identificação de roedores silvestres como hospedeiros do Angiostrongylus costaricensis no sul do Brasil [Identification of wild rodents as hosts of Angiostrongylus costaricensis in southern Brazil]. Rev ista do Instituto de Medicina Tropical de São Paulo 32(3), 147150. [In Portuguese.]CrossRefGoogle Scholar
Graeff-Teixeira, C, Camillo-Coura, L and Lenzi, HL (1991) Histopathological criteria for the diagnosis of abdominal angiostrongyliasis. Parasitology Research 77(7), 606611.CrossRefGoogle ScholarPubMed
Halliwell, B and Whiteman, M (2004) Measuring reactive species and oxidative damage in vivo and in cell culture: how should you do it and what do the results mean? British Journal of Pharmacology 142(2), 231255.CrossRefGoogle Scholar
Han, X, Yao, W, Liu, Z, Li, H, Zhang, ZJ, Hei, Z and Xia, Z (2016) Lipoxin A4 preconditioning attenuates intestinal ischemia reperfusion injury through Keap1/Nrf2 pathway in a lipoxin A4 receptor independent manner. Oxidative Medicine and Cellular Longevity 2016, 9303606.CrossRefGoogle Scholar
Hermes, CC, Benvegnú, E, Costa, MM, Rodriguez, R and Vieira, MIB (2018) Shedding of Angiostrongylus costaricensis larvae in the faeces of Swiss mice experimentally infected with different infective doses. Journal of Helminthology 94(e3).Google Scholar
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(e169).Google Scholar
Hurvich, CM and Tsai, CL (1989) Regression and time series model selection in small samples. Biometrika 76(2), 297307.CrossRefGoogle Scholar
Jones, DP (2006) Redefining oxidative stress. Antioxidantes e Sinalização Redox 8(9–10), 18651879.CrossRefGoogle ScholarPubMed
Lima, ES and Abdalla, DSP (2001) Peroxidação lipídica: mecanismos e avaliação em amostras biológicas [Lipid peroxidation: mechanisms and evaluation in biological samples]. Brazilian Journal of Pharmaceutical Sciences 37(3), 293–303. [In Portuguese.]Google Scholar
Llesuy, SF, Milei, J, Molina, H, Boveris, A and Milei, S (1985) Comparison of lipid peroxidation and myocardial damage induced by adriamycin and 4′-epiadriamycin in mice. Tumori 71(3), 241249.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(4), 407420.CrossRefGoogle ScholarPubMed
Neuschwander-Tetri, BA, Ferrell, LD, Sukhabote, RJ and Grendell, JH (1992) Glutationa monoetil éster melhora a pancreatite induzida por caeruleína no camundongo [Glutathione monoethyl ester ameliorates caerulein-induced pancreatitis in the mouse]. Journal of Clinical Investigation 89(1), 109116. [In Portuguese.]CrossRefGoogle Scholar
Neva, FA and Brown, HW (1994) Basic clinical parasitology, 6th edition, pp. 107–144. Norwalk, CT, Appleton & Lange.Google Scholar
Que, RS, Cao, LP, Ding, GP, Hu, JA, Mao, KJ and Wang, GF (2010) Correlation of nitric oxide and other free radicals with the severity of acute pancreatitis and complicated systemic inflammatory response syndrome. Pancreas 39(4), 536540.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(6), 339341.CrossRefGoogle ScholarPubMed
Rodriguez, R, Sandri, ASS, Porto, SM, et al. (2019) Invasive slug Meghimatium pictum (Stoliczka, 1873) infected by Angiostrongylus costaricensis Morera & Céspedes, 1971, and the possible risk of human infection associated with grape consumption. Journal of Helminthology 93(6), 775777.CrossRefGoogle ScholarPubMed
Sandri, A, Rodriguez, R, Costa, MM, Porto, SM, Schwingel, D and Vieira, MIB (2018) High-dose enoxaparin in the treatment of abdominal angiostrongyliasis in Swiss mice. Journal of Helminthology 92(6), 662667.CrossRefGoogle ScholarPubMed
Schoenberg, MH, Birk, D and Beger, HG (1995) Oxidative stress in acute and chronic pancreatitis. American Journal of Clinical Nutrition 62(Supplement 6), 1306S1314S.CrossRefGoogle ScholarPubMed
Symonds, MRE 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(1), 1321.CrossRefGoogle Scholar
Turrens, JF (2004) Oxidative stress and antioxidant defenses: a target for the treatment of diseases caused by parasitic protozoa. Molecular Aspects of Medicine 25(1–2), 211220.CrossRefGoogle ScholarPubMed
Vieira, PMA (2007) Participação do óxido nítrico na infecção experimental de cães pelo Trypanossoma cruzi [Participation of nitric oxide in experimental infection of dogs by Trypanosoma cruzi]. Dissertação (Mestrado em ciências biológicas), Universidade Federal de Ouro Preto, Ouro Preto, MG. [In Portuguese.]Google Scholar
Viña, J (1990) Glutationa: Metabolismo e Funções Fisiológicas. Boston, CRC Press.Google Scholar
Whittle, BJ, Boughton-Smith, NK and Moncada, S (1992) Biosynthesis and role of the endothelium-derived vasodilator, nitric oxide, in the gastric mucosa. Annals of the New York Academy of Sciences 664(1), 126139.CrossRefGoogle ScholarPubMed
Yang, Y, Zhang, L, Jiang, G, Lei, A, Yu, Q, Xie, J and Chen, Y (2019) Evaluation of the protective effects of Ganoderma atrum polysaccharide on acrylamide-induced injury in small intestine tissue of rats. Food & Function 10(9), 58635872.CrossRefGoogle ScholarPubMed