Basic Study
Copyright ©The Author(s) 2015. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastroenterol. Apr 28, 2015; 21(16): 4829-4839
Published online Apr 28, 2015. doi: 10.3748/wjg.v21.i16.4829
Toxoplasma gondii causes death and plastic alteration in the jejunal myenteric plexus
Eduardo José de Almeida Araújo, Larissa Marchi Zaniolo, Suellen Laís Vicentino, Marcelo Biondaro Góis, Jacqueline Nelisis Zanoni, Aristeu Vieira da Silva, Débora de Mello Gonçales Sant’Ana
Eduardo José de Almeida Araújo, Departamento de Histologia, Centro de Ciências Biológicas, Universidade Estadual de Londrina, 86057-970 Paraná, Brazil
Larissa Marchi Zaniolo, Programa de Pós-graduação em Ciência Animal, Universidade Paranaense, 87502-210 Paraná, Brazil
Suellen Laís Vicentino, Marcelo Biondaro Góis, Débora de Mello Gonçales Sant’Ana, Jaqueline Nelisis Zanoni, Departamento de Ciências Morfológicas. Universidade Estadual de Maringa, 87020-900 Paraná, Brazil
Aristeu Vieira da Silva, Departamento de Biologia, Universidade Estadual de Feira de Santana, 44036-900 Bahia, Brazil
Author contributions: Araújo EJA, Zaniolo LM, Vicentino SL, Góis MB, Zanoni JN, da Silva AV and Sant’Ana DMG contributed equally to this work; Araújo EJA, Zanoni JN, da Silva AV and Sant’Ana DMG designed the research; Zaniolo LM, Vicentino SL and Góis MB performed the research and analyzed the data; Araújo EJA, Sant’Ana DMG and Góis MB wrote and reviewed the paper.
Ethics approval: All procedures involving animals were reviewed and approved by the Ethics Committee in Research Involving Animal Experimentation of the Paranaense University (Universidade Paranaense), Brazil (Protocol 12361/2008).
Institutional animal care and use committee: All procedures involving animals were reviewed and approved by the Ethics Committee in Research Involving Animal Experimentation of the Paranaense University (Universidade Paranaense), Brazil (Protocol 12361/2008).
Conflict-of-interest: Eduardo José de Almeida Araújo is an employee of State University of Londrina, Brazil. Jacqueline Nelisis Zanoni and Débora de Mello Gonçales Sant’Ana are an employee of State University of Maringá, Brazil. Aristeu Vieira da Silva is an employee of State University of Feira de Santana, Brazil. Eduardo José de Almeida Araújo has received research funding from Conselho Nacional de Desenvolvimento Científico e Tecnológico, Brazil; Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Brazil; Fundação Araucária de Apoio ao Desenvolvimento Científico e Tecnológico do Estado do Paraná, Brazil. Jacqueline Nelisis Zanoni has received research funding from Conselho Nacional de Desenvolvimento Científico e Tecnológico, Brazil; Fundação Araucária de Apoio ao Desenvolvimento Científico e Tecnológico do Estado do Paraná, Brazil. Aristeu Vieira da Silva has received research funding from Conselho Nacional de Desenvolvimento Científico e Tecnológico, Brazil; Fundação de Amparo à Pesquisa do Estado da Bahia. Débora de Mello Gonçales Sant’Ana has received research funding from Conselho Nacional de Desenvolvimento Científico e Tecnológico, Brazil; Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Brazil; Fundação Araucária de Apoio ao Desenvolvimento Científico e Tecnológico do Estado do Paraná, Brazil.
Data sharing: No additional data are available.
Open-Access: This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Correspondence to: Dr. Eduardo José de Almeida Araújo, Departamento de Histologia, Centro de Ciências Biológicas, Universidade Estadual de Londrina, PO 10.011, 86057-970 Paraná, Brazil. eduardoaraujo@uel.br
Telephone: +55-433-3714327 Fax: +55-433-3715828
Received: November 7, 2014
Peer-review started: November 8, 2014
First decision: December 11, 2014
Revised: January 1, 2015
Accepted: January 30, 2015
Article in press: January 30, 2015
Published online: April 28, 2015
Processing time: 171 Days and 12.6 Hours
Abstract

AIM: To assess the effects of ME-49 Toxoplasma gondii (T. gondii) strain infection on the myenteric plexus and external muscle of the jejunum in rats.

METHODS: Thirty rats were distributed into two groups: the control group (CG) (n = 15) received 1 mL of saline solution orally, and the infected group (IG) (n = 15) inoculated with 1 mL of saline solution containing 500 oocysts of M-49 T. gondii strain orally. After 36 d of infection, the rats were euthanized. Infection with T. gondii was confirmed by blood samples collected from all rats at the beginning and end of the experiment. The jejunum of five animals was removed and submitted to routine histological processing (paraffin) for analysis of external muscle thickness. The remaining jejunum from the others animals was used to analyze the general population and the NADH-diaphorase, VIPergic and nitrergic subpopulations of myenteric neurons; and the enteric glial cells (S100-IR).

RESULTS: Serological analysis showed that animals from the IG were infected with the parasite. Hypertrophy affecting jejunal muscle thickness was observed in the IG rats (77.02 ± 42.71) in relation to the CG (51.40 ± 12.34), P < 0.05. In addition, 31.2% of the total number of myenteric neurons died (CG: 39839.3 ± 5362.3; IG: 26766.6 ± 2177.6; P < 0.05); hyperplasia of nitrergic myenteric neurons was observed (CG: 7959.0 ± 1290.4; IG: 10893.0 ± 1156.3; P < 0.05); general hypertrophy of the cell body in the remaining myenteric neurons was noted [CG: 232.5 (187.2-286.0); IG: 248.2 (204.4-293.0); P < 0.05]; hypertrophy of the smallest varicosities containing VIP neurotransmitter was seen (CG: 0.46 ± 0.10; IG: 0.80 ± 0.16; P < 0.05) and a reduction of 25.3% in enteric glia cells (CG: 12.64 ± 1.27; IG: 10.09 ± 2.10; P < 0.05) was observed in the infected rats.

CONCLUSION: It was concluded that infection with oocysts of ME-49 T. gondii strain caused quantitative and plastic alterations in the myenteric plexus of the jejunum in rats.

Keywords: Enteric nervous system; Infectious diseases; Glial cells; Nitric oxide; Neuronal plasticity; Small intestine; Toxoplasmosis; Vasoactive intestinal peptide

Core tip: The authors assessed the effects of ME-49 Toxoplasma gondii (T. gondii) strain infection on the myenteric plexus and external muscle of the jejunum in rats. They found an uncommon result when T. gondii infection was evaluated in rats: death of myenteric neurons and enteric glial cells. In addition, the remaining neurons showed hypertrophy and the number of nitrergic neurons increased. These alterations were possibly responsible for hypertrophy of the external muscle observed in the jejunal wall. The strain (ME-49) and the life form (oocysts) of T. gondii used here were the determinants of all these findings.