Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-23T22:31:39.610Z Has data issue: false hasContentIssue false
  • English
  • Français

Saccharomyces boulardii reduces the vertical transmission of Toxocara canis larvae in mice

Published online by Cambridge University Press:  02 March 2021

L.A.X. Cruz Open the ORCID record for L.A.X. Cruz [Opens in a new window] ,
C.D. Hirsch Open the ORCID record for C.D. Hirsch [Opens in a new window] ,
M.Q. de Moura Open the ORCID record for M.Q. de Moura [Opens in a new window] ,
L.F.C. de Avila Open the ORCID record for L.F.C. de Avila [Opens in a new window] ,
L.H.R. Martins Open the ORCID record for L.H.R. Martins [Opens in a new window] ,
G.B. Klafke Open the ORCID record for G.B. Klafke [Opens in a new window] ,
F.R. Conceição Open the ORCID record for F.R. Conceição [Opens in a new window] ,
M.E.A. Berne Open the ORCID record for M.E.A. Berne [Opens in a new window]  and
C.J. Scaini Open the ORCID record for C.J. Scaini [Opens in a new window]
L.A.X. Cruz
Affiliation:
Postgraduate Program in Microbiology and Parasitology, Department of Microbiology and Parasitology, Federal University of Pelotas (UFPel), Pelotas, Rio Grande do Sul, Brazil
C.D. Hirsch
Affiliation:
Postgraduate Program in Health Sciences – Parasitology Laboratory, Federal University of Rio Grande (FURG), Academic Area of the University Hospital,Rio Grande, Rio Grande do Sul, Brazil
M.Q. de Moura
Affiliation:
Postgraduate Program in Health Sciences – Parasitology Laboratory, Federal University of Rio Grande (FURG), Academic Area of the University Hospital,Rio Grande, Rio Grande do Sul, Brazil
L.F.C. de Avila
Affiliation:
Postgraduate Program in Microbiology and Parasitology, Department of Microbiology and Parasitology, Federal University of Pelotas (UFPel), Pelotas, Rio Grande do Sul, Brazil
L.H.R. Martins
Affiliation:
Postgraduate Program in Health Sciences – Parasitology Laboratory, Federal University of Rio Grande (FURG), Academic Area of the University Hospital,Rio Grande, Rio Grande do Sul, Brazil
G.B. Klafke
Affiliation:
Postgraduate Program in Health Sciences – Parasitology Laboratory, Federal University of Rio Grande (FURG), Academic Area of the University Hospital,Rio Grande, Rio Grande do Sul, Brazil
F.R. Conceição
Affiliation:
Department of Biotechnology, Federal University of Pelotas (UFPel), Pelotas, Rio Grande do Sul, Brazil
M.E.A. Berne
Affiliation:
Postgraduate Program in Microbiology and Parasitology, Department of Microbiology and Parasitology, Federal University of Pelotas (UFPel), Pelotas, Rio Grande do Sul, Brazil
C.J. Scaini*
Affiliation:
Postgraduate Program in Health Sciences – Parasitology Laboratory, Federal University of Rio Grande (FURG), Academic Area of the University Hospital,Rio Grande, Rio Grande do Sul, Brazil
*
Author for correspondence: C.J. Scaini, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Probiotics have been shown to reduce the intensity of Toxocara canis infection in mice. However, larval transmission of this nematode also occurs via transplacental and transmammary routes. Thus, the aim of this study was to evaluate the effect of the Saccharomyces boulardii probiotic on the vertical transmission of T. canis in Swiss mice. The mice received 107S. boulardii colony-forming units per gram of food. The supplementation began 15 days before mating and was maintained throughout pregnancy and lactation. The animals were inoculated with 300 T. canis embryonated eggs on the 14th day of pregnancy. The presence of larvae was examined in the organs of the females and their offspring. The examined organs included the following: brain, liver, lungs, heart, kidneys, spleen, eye, skeletal muscle (carcass) and mammary glands of lactating females. There was a 42% (P = 0.041) reduction in the number of larvae transmitted to offspring in the group that received probiotic-supplemented food (GI). Additionally, there was a 50% reduction (P = 0.023) in the number of larvae found in the brains of lactating offspring in the GI group. These results reveal the potential of S. boulardii probiotic use as an auxiliary method of controlling visceral toxocariasis.

Keywords

Toxocariasisvisceral larva migranstransplacental transmissiontransmammary transmissionprobiotic
Type
Research Paper
Information
Journal of Helminthology , Volume 95 , 2021 , e11
Copyright
Copyright © The Author(s), 2021. 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.)

Footnotes

*

Current address: Postgraduate Program in Health Sciences, Federal University of Rio Grande (FURG), Academic Area of the University Hospital – General Osório, s/n, CEP 96200-190, Centro, Rio Grande, Rio Grande do Sul, Brazil.

References

Alijotas-Reig, J, Llurba, E and Gris, JM (2014) Potentiating maternal immune tolerance in pregnancy: a new challenging role for regulatory T cells. Placenta 35(4), 241–248.CrossRefGoogle ScholarPubMed
Amaral, HL, Rassier, GL, Pepe, MS, Gallina, T, Villela, MM, Nobre, MO, Scaini, CJ and Berne, ME (2010) Presence of Toxocara canis eggs on the hair of dogs: a risk factor for visceral larva Migrans. Veterinary Parasitology 174, 115–118.CrossRefGoogle ScholarPubMed
Avila, LF, Conceição, FR, Telmo, PL, Dutra, GF, de Los Santos, DG, Martins, LH, Berne, MEA, da Silva, PE and Scaini, CJ (2012) Saccharomyces boulardii reduces infection intensity of mice with toxocariasis. Veterinary Parasitology 187, 337–340.CrossRefGoogle ScholarPubMed
Avila, LFC, Leon, PMM, Moura, MQ, Berne, MEA, Scaini, CJ and Leivas Leite, FP (2016) Modulation of IL-12 and IFNc by probiotic supplementation promotes protection against Toxocara canis infection in mice. Parasite Immunology 38, 326–330.CrossRefGoogle Scholar
Basualdo, J, Sparo, M, Chiodo, P, Ciarmela, M and Minvielle, M (2007) Oral treatment with a potential probiotic (Enterococcus faecalis CECT 7121) appears to reduce the parasite burden of mice infected with Toxocara canis. Annals of Tropical Medicine and Parasitology 101, 559–562.CrossRefGoogle ScholarPubMed
Bautista-Garfias, CR, Ixta-Rodríguez, O, Martínez-Gómez, F, López, MG and Aguilar-Figureueroa, BR (2001) Effect of viable or dead Lactobacillus casei organisms administered orally to mice on resistance against Trichinella spiralis infection. Parasite 8(2 Suppl), s226–s228.CrossRefGoogle ScholarPubMed
Beaver, PC, Snyder, CH, Carrera, GM, Dent, JH and Lafferty, JW (1952) Chronic eosinophilia due to visceral larva migrans; report of three cases. Pediatrics 9, 7–19.Google ScholarPubMed
Butel, MJ (2014) Probiotics, gut microbiota and health. Médecine et Maladies Infectieuses 44, 1–8.CrossRefGoogle ScholarPubMed
Cardoso, PD, Walcher, DL, da Silva Cadore, P, et al. (2020) Saccharomyces boulardii reduces the mean intensity of infection in mice caused by the consumption of liver contaminated by Toxocara canis. Parasitology Research 119(3), 1161–1165.CrossRefGoogle ScholarPubMed
Chiodo, PG, Sparo, MD, Pezzani, BC, Minvielle, MC and Basualdo, JA (2010) In vitro and in vivo effects of Enterococcus faecalis CECT7121 on Toxocara canis. Memórias do Instituto Oswaldo Cruz 105, 615–620.CrossRefGoogle ScholarPubMed
Clancy, R (2003) Immunobiotics and the probiotic evolution. Immunobiotics and the Probiotic Evolution 38, 9–12.Google ScholarPubMed
De Souza Aguiar, P, Furtado, RD, de Avila, LF, de Lima Telmo, P, Martins, LH, Berne, ME, da Silva, PE and Scaini, CJ (2015) Transmammary infection in BALB/c mice with chronic toxocariasis. Parasitology International 64(2), 145–147.CrossRefGoogle ScholarPubMed
Dunsmore, JD, Thompson, RC and Bates, IA (1983) The accumulation of Toxocara canis larvae in the brains of mice. International Journal for Parasitology 13, 517–521.CrossRefGoogle ScholarPubMed
Dutra, GF, Pinto, NS, da Costa de Avila, LF, de Lima Telmo, P, da Hora, VP, Martins, LH, Berne, ME and Scaini, CJ (2013) Evaluation of the initial and chronic phase of toxocariasis after consumption of liver treated by freezing or cooling. Parasitology Research 112, 2171–2175.CrossRefGoogle ScholarPubMed
Epe, C (2009) Intestinal nematodes: biology and control. The Veterinary Clinics of North America. Small Animal Practice 39, 1091–1107.CrossRefGoogle ScholarPubMed
Glickman, LT and Schantz, PM (1981) Epidemiology and pathogenesis of zoonotic toxocariasis. Epidemiologic Reviews 3, 230–250.CrossRefGoogle ScholarPubMed
Hotez, PJ and Wilkins, PP (2009) Toxocariasis: America's most common neglected infection of poverty and a helminthiasis of global importance? PLoS Neglected Tropical Diseases 3, e400.CrossRefGoogle Scholar
Jin, Z, Akao &, N and Ohta, N (2008) Prolactin evokes lactational transmission of larvae in mice infected with Toxocara canis. Parasitology International 57, 495–498.CrossRefGoogle ScholarPubMed
Jung, C, Hugot, JP and Barreau, F (2010) Peyer's patches: the immune sensors of the intestine. International Journal of Inflammation 2010, 1-12.CrossRefGoogle ScholarPubMed
Lee, KT, Min, HK and Soh, CT (1976) Transplacental migration of Toxocara canis larvae in experimentally infected mice. The Journal of Parasitology 62, 460–465.CrossRefGoogle ScholarPubMed
Macpherson, CNL (2013) The epidemiology and public health importance of toxocariasis: a zoonosis of global importance. International Journal for Parasitology 43, 999–1008.CrossRefGoogle ScholarPubMed
Magnaval, JF and Glickman, LT (2006) Management and treatment options for human toxocariasis. pp. 113–126 in Holland, CV and Smith, HV (Eds) Toxocara the enigmatic parasite. London, CAB International.Google Scholar
Magnaval, JF, Glickman, LT, Dorchies, P and Morassin, B (2001) Highlights of human toxocariasis. The Korean Journal of Parasitology 39, 1–11.CrossRefGoogle ScholarPubMed
Mor, G and Cardenas, I (2010) The immune system in pregnancy: a unique complexity. American Journal of Reproductive Immunology 63, 425–433.CrossRefGoogle ScholarPubMed
Moura, MQ, Terto, WDS, Jeske, ST, de Castro, LM, Pinto, NB, Avila, LFC, Leivas Leite, FP and Berne, MEA (2017) Evaluation of the transcription of interleukin-12 in the intestinal mucosa of mice subjected to experimental toxocariasis and supplemented with Saccharomyces boulardii. Veterinary Parasitology 242, 59–62.CrossRefGoogle ScholarPubMed
Nauta, AJ, Ben Amor, K, Knol, J, Garssen, J and Van der Beek, EM (2013) Relevance of pre- and postnatal nutrition to development and interplay between the microbiota and metabolic and immune systems. The American Journal of Clinical Nutrition 98(2), 586s–593s.CrossRefGoogle ScholarPubMed
Oshima, T (1961) Influence of pregnancy and lactation on migration of the larvae of Toxocara canis in mice. The Journal of Parasitology 47, 657–660.CrossRefGoogle ScholarPubMed
Othman, AA (2012) Therapeutic battle against larval toxocariasis: are we still far behind? Acta Tropica 124, 171–178.CrossRefGoogle ScholarPubMed
Overgaauw, PAM and Knapen, FV (2013) Veterinary and public health aspects of Toxocara spp. Veterinary Parasitology 193, 398– 403CrossRefGoogle ScholarPubMed
Quattrocchi, G, Nicoletti, A, Marin, B, Bruno, E, Druet-Cabanac, M and Preux, PM (2012) Toxocariasis and epilepsy: systematic review and meta-analysis. PLoS Neglected Tropical Diseases 6, e1775.CrossRefGoogle ScholarPubMed
Reiterová, K, Tomašovicová, O and Dubinský, P (2003) Influence of maternal infection on offspring immune response in murine larval toxocariasis. Parasite Immunology 25, 361–368.CrossRefGoogle ScholarPubMed
Smith, H, Holland, C, Taylor, M, Magnaval, JF, Schantz, P and Maizels, R (2009) How common is human toxocariasis? Towards standardizing our knowledge. Trends in Parasitology 25, 182–188.CrossRefGoogle Scholar
Strube, C, Heuer, L and Janecek, E (2013) Toxocara spp infections in paratenic hosts. Veterinary Parasitology 193, 375–389.CrossRefGoogle ScholarPubMed
Walcher, DL, Cruz, LAX, Telmo, PL, Martins, LHR, Avila, LFC, Berne, MEA and Scaini, CJ (2018) Lactobacillus rhamnosus reduces parasite load on Toxocara canis experimental infection in mice, but has no effect on the parasite in vitro. Parasitology Research 117, 597–602.CrossRefGoogle ScholarPubMed
Xi, WG and Jin, LZ (1998) A novel method for the recovery of Toxocara canis in mice. Journal of Helminthology 72, 183–184.CrossRefGoogle ScholarPubMed