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The impact of maternal periodontitis in the development of asthma in the offspring

Published online by Cambridge University Press:  21 April 2020

Grazielle Rodrigues
Affiliation:
Department of Biophotonics Applied to Health Sciences, University Nove de Julho (UNINOVE), São Paulo, Brazil
Alexandre do Valle Wuo
Affiliation:
Department of Biophotonics Applied to Health Sciences, University Nove de Julho (UNINOVE), São Paulo, Brazil
Simone Klein
Affiliation:
Department of Biophotonics Applied to Health Sciences, University Nove de Julho (UNINOVE), São Paulo, Brazil
Patrícia de Almeida
Affiliation:
Department of Biophotonics Applied to Health Sciences, University Nove de Julho (UNINOVE), São Paulo, Brazil
Amilcar Sabino Damazo
Affiliation:
Department of Health Sciences, Faculty of Medicine, Mato Grosso, Brazil
Rodrigo Labat Marcos
Affiliation:
Department of Biophotonics Applied to Health Sciences, University Nove de Julho (UNINOVE), São Paulo, Brazil
Anna Carolina Ratto Tempestini Horliana
Affiliation:
Department of Biophotonics Applied to Health Sciences, University Nove de Julho (UNINOVE), São Paulo, Brazil
Adriana Lino-dos-Santos-Franco*
Affiliation:
Department of Biophotonics Applied to Health Sciences, University Nove de Julho (UNINOVE), São Paulo, Brazil
*
Address for correspondence: Adriana Lino-dos-Santos-Franco, PhD, Department of Biophotonics Applied to Health Sciences, University Nove de Julho (UNINOVE), Rua Vergueiro, 239/245, São Paulo, SPCEP 01504-000, Brazil. Email: alsantosfranco@gmail.com

Abstract

Clinical and experimental studies show an association between maternal periodontitis and adverse outcomes during gestation. On the other hand, there were no studies evaluating the impact of maternal periodontitis on the offspring. Thus, our objective was to investigate the repercussion of maternal periodontitis on the development of asthma in the offspring. Pregnant rats were submitted or not to periodontitis by ligature technique. Thirty days after birth, the puppies were sensitized and challenged with ovalbumin (OVA) in order to induce asthmatic response. Our results showed that maternal periodontitis reduced cellular infiltrate in the parenchyma of offspring, tracheal responsiveness, lung edema, and anti-OVA antibodies, without alter mucus as well as cytokines production. We concluded that periodontitis has relevant impact on the offspring’s immune system, blunting the response to allergic and inflammatory stimulus. This study shows the important role of oral health during pregnancy and opens possibilities for future studies in order to explain the effects of periodontitis during pregnancy in the offspring.

Type
Original Article
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2020

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References

Di Benedetto, A, Gigante, I, Colucci, S, Grano, M. Periodontal disease: linking the primary inflammation to bone loss. Clin Dev Immunol. 2013; 2013, 503754.CrossRefGoogle ScholarPubMed
Yucel-Lindberg, T, Bage, T. Inflammatory mediators in the pathogenesis of periodontitis. Expert Rev Mol Med. 2013; 15, e7.CrossRefGoogle Scholar
Warren, J, Watkins, CA Cowen, HJ, Hand, JS, Levy, SM, Kuthy, RA. Tooth loss in the very old: 13-15-year incidence among elderly Iowans. Comm Dent Oral Epidemiol. 2002; 30, 2937.CrossRefGoogle ScholarPubMed
Page, RC, Eke, PI, Jin, Y, Liu, D, Lin, X. IL-35 may maintain homeostasis of the immune microenvironment in periodontitis. Exp Ther Med. 2017; 14(6), 56055610. Case definitions for use in population-based surveillance of periodontitis. J Periodontol. 2007;78(7 Suppl):1387-99.Google Scholar
Shah, R, Thomas, R, Mehta, DS. Neutrophil priming: Implications in periodontal disease. J Indian Soc Periodontol. 2017; 21(3), 180185.CrossRefGoogle ScholarPubMed
Fredriksson, MI. Effect of priming in subpopulations of peripheral neutrophils from patients with chronic periodontitis. J Periodontol. 2012; 83, 11921199.CrossRefGoogle ScholarPubMed
Cardoso, EM, Reis, C, Manzanares-Céspedes, MC. Chronic periodontitis, inflammatory cytokines, and interrelationship with other chronic diseases. Postgrad Med. 2018; 130(1), 98104.CrossRefGoogle ScholarPubMed
González-Jaranay, M, Téllez, L, Roa-López, A, Gómez-Moreno, G, Moreu, G. Periodontal status during pregnancy and postpartum. PLoS One 2017; 12(5), e0178234.CrossRefGoogle ScholarPubMed
Corbella, S, Taschieri, S, Francetti, L, De Siena, F, Del Fabbro, M. Periodontal disease as a risk factor for adverse pregnancy outcomes: a systematic review and meta-analysis of case-control studies. Odontology 2012; 232240.CrossRefGoogle ScholarPubMed
Srinivas, SK, Sammel, MD, Stamilio, DM, et al. Periodontal disease and adverse pregnancy outcomes: is there an association? Am J Obstet Gynecol. 2009; 200, e491498.CrossRefGoogle ScholarPubMed
Ibrahim, BS, Barioni, ÉD, Heluany, C, et al. Beneficial effects of vitamin C treatment on pregnant rats exposed to formaldehyde: reversal of immunosuppression in the offspring. Toxicol Appl Pharmacol. 2016; 300, 7781.CrossRefGoogle ScholarPubMed
Silva Ibrahim, B, Miranda da Silva, C, Barioni, ÉD, et al. Formaldehyde inhalation during pregnancy abolishes the development of acute innate inflammation in offspring. Toxicol Lett. 2015; 235(2), 147154.CrossRefGoogle ScholarPubMed
Maiellaro, M, Correa-Costa, M, Vitoretti, LB et al. Exposure to low doses of formaldehyde during pregnancy suppresses the development of allergic lung inflammation in offspring. Toxicol Appl Pharmacol. 2014; 278(3), 266274.CrossRefGoogle ScholarPubMed
Candeo, LC, Rigonato-Oliveira, NC, Brito, AA, et al. Effects of periodontitis on the development of asthma: the role of photodynamic therapy. PLoS One 2017; 12(11), e0187945.CrossRefGoogle ScholarPubMed
Mota, I, Wong, D. Homologous and heterologous passive cutaneous anaphylactic activity of mouse antisera during the course of immunization. Life Sci. 1969; 8(16), 813820.CrossRefGoogle ScholarPubMed
Iheozor-Ejiofor, Z, Middleton, P, Esposito, M, Glenny, AM. Treating periodontal disease for preventing adverse birth outcomes in pregnant women. Cochrane Database Syst Rev. 2017; 12(6), CD005297.Google Scholar
Ide, M, Papanou, PN. Epidemiology of association between maternal periodontal disease and adverse pregnancy outcomes--systematic review. J Periodontol. 2013; 4, S181S194.Google Scholar
Ren, H, Du, M. Role of maternal periodontitis in preterm birth. Front Immunol. 2017; 8, 139.CrossRefGoogle ScholarPubMed
Chen, CC, Chang, KL, Huang, JF, Huang, JS, Tsai, CC. Correlation of interleukin-1 beta, interleukin-6, and periodontitis. Kaohsiung J Med Sci. 1997; 13(10), 609617.Google ScholarPubMed
Hwang, YP, Jin, SW, Choi, JH et al. Inhibitory effects of l-theanine on airway inflammation in ovalbumin-induced allergic asthma. Food Chem Toxicol. 2017; 99, 162169.CrossRefGoogle ScholarPubMed
Wang, J, Fu, Y, Wei, Z, et al. Anti-asthmatic activity of osthole in an ovalbumin-induced asthma murine model. Respir Physiol Neurobiol. 2017; 239, 6469.CrossRefGoogle Scholar
Abuelezz, SA. Nebivolol attenuates oxidative stress and inflammation in a guinea pig model of ovalbumin-induced asthma: a possible mechanism for its favorable respiratory effects. Can J Physiol Pharmacol. 2018; 96(3), 258265.CrossRefGoogle Scholar
Casaro, M, Souza, VR, Oliveira, FA, Ferreira, CM. OVA-Induced allergic airway inflammation mouse model. Methods Mol Biol. 2019; 1916, 297301.CrossRefGoogle ScholarPubMed
Siqueira, VPC, Evangelista, MIS, Dos Santos, A, et al., Light-Emitting Diode treatment ameliorates allergic lung inflammation in experimental model of asthma induced by ovalbumin. J Biophotonics. 2017; 10(12), 16831693.CrossRefGoogle ScholarPubMed
Hannson, MA, Gluckman, PD. Developmental origins of health and disease: new insights. Basic Clin Pharmacol Toxicol, 2008; 102(2), 9093.CrossRefGoogle Scholar
Hamasato, EK, de Lima, AP, de Oliveira, AP, dos Santos Franco, AL, de Lima, WT, Palermo-Neto, J. Cohabitation with a sick partner increases allergic lung inflammatory response in mice. Brain Behav Immun. 2014; 42, 109117.CrossRefGoogle ScholarPubMed