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Erschienen in: Clinical Oral Investigations 6/2018

29.12.2017 | Original Article

Anti-inflammatory and antiresorptive effects of Calendula officinalis on inflammatory bone loss in rats

verfasst von: Joanna Trycia M. Alexandre, Luzia Hermínia Teixeira Sousa, Mario Roberto Pontes Lisboa, Flávia A. C. Furlaneto, Danielle Rocha do Val, Mirna Marques, Hellíada C. Vasconcelos, Iracema Matos de Melo, Renata Leitão, Gerly Anne Castro Brito, Paula Goes

Erschienen in: Clinical Oral Investigations | Ausgabe 6/2018

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Abstract

Objective

The aim of this work was to evaluate the anti-inflammatory and antiresorptive effects of Calendula officinalis (CLO) on alveolar bone loss (ABL) in rats.

Material and methods

Male Wistar rats were subjected to ABL by ligature with nylon thread around the second upper left molar. The contralateral hemimaxillae were used as control. Rats received saline solution (SAL) or CLO (10, 30, or 90 mg/kg) 30 min before ligature and daily until the 11th day. The maxillae were removed and prepared for macroscopic, radiographic, micro-tomographic, histopathologic, histometric analysis, and immunohistochemical localization of receptor activator of nuclear factor kappa-B ligand (RANKL) and osteoprotegerin (OPG). The gingival tissues were used to quantify the myeloperoxidase (MPO) activity, tumor necrosis factor-alpha (TNF-α), and interleukin-1β (IL-1β) concentrations by ELISA. Blood samples were collected for leukogram and to evaluate the bone-specific alkaline phosphatase (BALP) activity and serum levels of aspartate and alanine transaminases (AST/ALT).

Results

The bone loss induced by 11 days of ligature induced bone loss, reduced levels of BALP, leukocyte infiltration, increased MPO activity, gingival concentrations of TNF-α and IL-1β, and RANKL while reduced OPG immunoexpressions in the periodontal tissue and leukocytosis. Of the CLO, 90 mg/kg reduced bone loss, neutrophilia, the levels of pro-inflammatory mediators, and RANKL expression, while it increased OPG immunopositive cells and BALP serum levels, when compared to SAL. CLO did not affect either kidney or liver function, indicated by serum AST/ALT levels.

Conclusion

The present data suggests that CLO reduced inflammatory bone resorption in experimental periodontitis, which may be mediated by its anti-inflammatory properties and its effects on bone metabolism.

Clinical relevance

CLO can be a potential therapeutical adjuvant in the treatment of periodontitis.
Literatur
1.
4.
Zurück zum Zitat Kayal RA (2013) The role of osteoimmunology in periodontal disease. Biomed Res Int 2013:1–12CrossRef Kayal RA (2013) The role of osteoimmunology in periodontal disease. Biomed Res Int 2013:1–12CrossRef
5.
Zurück zum Zitat Souza PP, Lerner UH The role of cytokines in inflammatory bone loss. Immunol Investig 42:555–622 Souza PP, Lerner UH The role of cytokines in inflammatory bone loss. Immunol Investig 42:555–622
6.
Zurück zum Zitat Norlindh T (1946) Studies in the Calenduleae II. Phytogeography and interrelation. Botaniska Notiser 4:471–506 Norlindh T (1946) Studies in the Calenduleae II. Phytogeography and interrelation. Botaniska Notiser 4:471–506
7.
Zurück zum Zitat Ukiya M, Akihisa T, Yasukawa K, Tokuda H, Suzuki T, Kimura Y (2006) Anti-inflammatory, anti-tumorpromoting, and cytotoxic activities of constituents of marigold (Calendula officinalis) flowers. J Nat Prod 69:1692–1696CrossRefPubMed Ukiya M, Akihisa T, Yasukawa K, Tokuda H, Suzuki T, Kimura Y (2006) Anti-inflammatory, anti-tumorpromoting, and cytotoxic activities of constituents of marigold (Calendula officinalis) flowers. J Nat Prod 69:1692–1696CrossRefPubMed
8.
Zurück zum Zitat Saini P, Al-Shibani N, Sun J et al (2012) Effects of Calendula officinalis on human gingival fibroblasts. Homeopathy 101:92–98CrossRefPubMed Saini P, Al-Shibani N, Sun J et al (2012) Effects of Calendula officinalis on human gingival fibroblasts. Homeopathy 101:92–98CrossRefPubMed
9.
Zurück zum Zitat Khairnar MS, Pawar B, Marawar PP, Mani A (2013) Evaluation of Calendula officinalis as an anti-plaque and anti-gingivitis agent. J Indian Soc Periodontol 17:741–747CrossRefPubMedPubMedCentral Khairnar MS, Pawar B, Marawar PP, Mani A (2013) Evaluation of Calendula officinalis as an anti-plaque and anti-gingivitis agent. J Indian Soc Periodontol 17:741–747CrossRefPubMedPubMedCentral
10.
Zurück zum Zitat Bezerra MM, de Lima V, Alencar VB et al (2000) Selective cyclooxygenase-2 inhibition prevents alveolar bone loss in experimental periodontitis in rats. J Periodontol 71:1009–1014CrossRefPubMed Bezerra MM, de Lima V, Alencar VB et al (2000) Selective cyclooxygenase-2 inhibition prevents alveolar bone loss in experimental periodontitis in rats. J Periodontol 71:1009–1014CrossRefPubMed
11.
Zurück zum Zitat Preethi KC, Kuttan R (2009) Wound healing activity of flower extract of Calendula officinalis. J Basic Clin Physiol Pharmacol 20:73–79aCrossRefPubMed Preethi KC, Kuttan R (2009) Wound healing activity of flower extract of Calendula officinalis. J Basic Clin Physiol Pharmacol 20:73–79aCrossRefPubMed
12.
Zurück zum Zitat Goes P, Lima AP, Melo IM, Rêgo RO, Lima V (2010) Effect of Atorvastatin in radiographic density on alveolar bone loss in wistar rats. Braz Dent J 21:193–198CrossRefPubMed Goes P, Lima AP, Melo IM, Rêgo RO, Lima V (2010) Effect of Atorvastatin in radiographic density on alveolar bone loss in wistar rats. Braz Dent J 21:193–198CrossRefPubMed
13.
Zurück zum Zitat Lisboa MR, Gondim DV, Ervolino E et al (2015) Effects of electroacupuncture on experimental periodontitis in rats. J Periodontol 86:801–811CrossRefPubMed Lisboa MR, Gondim DV, Ervolino E et al (2015) Effects of electroacupuncture on experimental periodontitis in rats. J Periodontol 86:801–811CrossRefPubMed
14.
Zurück zum Zitat Leitão RF, Ribeiro RA, Chaves HV, Rocha FA, Lima V, Brito GA (2005) Nitric oxide synthase inhibition prevents alveolar bone resorption in experimental periodontitis in rats. J Periodontol 76:956–963CrossRefPubMed Leitão RF, Ribeiro RA, Chaves HV, Rocha FA, Lima V, Brito GA (2005) Nitric oxide synthase inhibition prevents alveolar bone resorption in experimental periodontitis in rats. J Periodontol 76:956–963CrossRefPubMed
15.
Zurück zum Zitat Goes P, Melo IM, Silva LM et al (2014) Low-dose combination of alendronate and atorvastatin reduces ligature-induced alveolar bone loss in rats. J Periodontal Res 49:45–54CrossRefPubMed Goes P, Melo IM, Silva LM et al (2014) Low-dose combination of alendronate and atorvastatin reduces ligature-induced alveolar bone loss in rats. J Periodontal Res 49:45–54CrossRefPubMed
16.
Zurück zum Zitat Moss DW, Whitby LG (1975) A simplified heat-inactivation method for investigating alkaline phosphatase isoenzymes in serum. Clin Chim Acta 61:63–71CrossRefPubMed Moss DW, Whitby LG (1975) A simplified heat-inactivation method for investigating alkaline phosphatase isoenzymes in serum. Clin Chim Acta 61:63–71CrossRefPubMed
17.
Zurück zum Zitat Goes P, Melo IM, Dutra CS, Lima AP, Lima V (2012) Effect of alendronate on bone-specific alkaline phosphatase on periodontal bone loss in rats. Arch Oral Biol 57:1537–1544CrossRefPubMed Goes P, Melo IM, Dutra CS, Lima AP, Lima V (2012) Effect of alendronate on bone-specific alkaline phosphatase on periodontal bone loss in rats. Arch Oral Biol 57:1537–1544CrossRefPubMed
18.
Zurück zum Zitat Sousa LH, Linhares EV, Alexandre JT et al (2016) Effects of atorvastatin on periodontitis of rats subjected to glucocorticoid-induced osteoporosis. J Periodontol 87:1206–1216CrossRefPubMed Sousa LH, Linhares EV, Alexandre JT et al (2016) Effects of atorvastatin on periodontitis of rats subjected to glucocorticoid-induced osteoporosis. J Periodontol 87:1206–1216CrossRefPubMed
19.
Zurück zum Zitat Dalcico R, de Menezes AM, Deocleciano OB et al (2013) Protective mechanisms of simvastatin in experimental periodontal disease. J Periodontol 84:1145–1157CrossRefPubMed Dalcico R, de Menezes AM, Deocleciano OB et al (2013) Protective mechanisms of simvastatin in experimental periodontal disease. J Periodontol 84:1145–1157CrossRefPubMed
20.
Zurück zum Zitat de Barros Silva PG, de Oliveira CC, Brizeno L et al (2016) Immune cellular profile of bisphosphonaterelated osteonecrosis of the jaw. Oral Dis 22:649–657CrossRefPubMed de Barros Silva PG, de Oliveira CC, Brizeno L et al (2016) Immune cellular profile of bisphosphonaterelated osteonecrosis of the jaw. Oral Dis 22:649–657CrossRefPubMed
21.
22.
Zurück zum Zitat Tanideh N, Tavakoli P, Saghiri MA et al (2013) Healing acceleration in hamsters of oral mucositis induced by 5-fluorouracil with topical Calendula officinalis. Oral Surg Oral Med Oral Pathol Oral Radiol 115:332–338CrossRefPubMed Tanideh N, Tavakoli P, Saghiri MA et al (2013) Healing acceleration in hamsters of oral mucositis induced by 5-fluorouracil with topical Calendula officinalis. Oral Surg Oral Med Oral Pathol Oral Radiol 115:332–338CrossRefPubMed
23.
Zurück zum Zitat Garnero P (2008) Biomarkers for osteoporosis management: utility in diagnosis, fracture risk prediction and therapy monitoring. Mol Diagn Ther 12:157–170CrossRefPubMed Garnero P (2008) Biomarkers for osteoporosis management: utility in diagnosis, fracture risk prediction and therapy monitoring. Mol Diagn Ther 12:157–170CrossRefPubMed
24.
Zurück zum Zitat Forte L, Torricelli P, Boanini E et al (2016) Antioxidant and bone repair properties of quercetinfunctionalized hydroxyapatite: an in vitro osteoblast-osteoclast-endothelial cell co-culture study. Acta Biomater 32:298–308CrossRefPubMed Forte L, Torricelli P, Boanini E et al (2016) Antioxidant and bone repair properties of quercetinfunctionalized hydroxyapatite: an in vitro osteoblast-osteoclast-endothelial cell co-culture study. Acta Biomater 32:298–308CrossRefPubMed
25.
Zurück zum Zitat Zhou Y, Wu Y, Jiang X et al (2016) The effect of quercetin on the osteogenesic differentiation and angiogenic factor expression of bone marrow-derived mesenchymal stem cells. PLoS One 10:e0129605CrossRef Zhou Y, Wu Y, Jiang X et al (2016) The effect of quercetin on the osteogenesic differentiation and angiogenic factor expression of bone marrow-derived mesenchymal stem cells. PLoS One 10:e0129605CrossRef
26.
Zurück zum Zitat Srivastava S, Bankar R, Roy P (2013) Assessment of the role of flavonoids for inducing osteoblast differentiation in isolated mouse bone marrow derived mesenchymal stem cells. Phytomedicine 20:683–690CrossRefPubMed Srivastava S, Bankar R, Roy P (2013) Assessment of the role of flavonoids for inducing osteoblast differentiation in isolated mouse bone marrow derived mesenchymal stem cells. Phytomedicine 20:683–690CrossRefPubMed
27.
Zurück zum Zitat Wang XC, Zhao NJ, Guo C, Chen JT, Song JL, Gao L (2014) Quercetin reversed lipopolysaccharide-induced inhibition of osteoblast differentiation through the mitogen-activated protein kinase pathway in MC3T3-E1 cells. Mol Med Rep 10:3320–3326CrossRefPubMed Wang XC, Zhao NJ, Guo C, Chen JT, Song JL, Gao L (2014) Quercetin reversed lipopolysaccharide-induced inhibition of osteoblast differentiation through the mitogen-activated protein kinase pathway in MC3T3-E1 cells. Mol Med Rep 10:3320–3326CrossRefPubMed
28.
Zurück zum Zitat Araújo AA, Souza TO, Moura LM et al (2013) Effect of telmisartan on levels of IL-1, TNF-α, downregulated COX-2, MMP-2, MMP-9 and RANKL/RANK in an experimental periodontitis model. J Clin Periodontol 40:1104–1111CrossRefPubMedPubMedCentral Araújo AA, Souza TO, Moura LM et al (2013) Effect of telmisartan on levels of IL-1, TNF-α, downregulated COX-2, MMP-2, MMP-9 and RANKL/RANK in an experimental periodontitis model. J Clin Periodontol 40:1104–1111CrossRefPubMedPubMedCentral
29.
Zurück zum Zitat Araújo AA, Varela H, Brito GA et al (2014) Azilsartan increases levels of IL-10, down-regulates MMP-2, MMP-9, RANKL/RANK, Cathepsin K and up-regulates OPG in an experimental periodontitis model. PloS One 9:e96750CrossRefPubMedPubMedCentral Araújo AA, Varela H, Brito GA et al (2014) Azilsartan increases levels of IL-10, down-regulates MMP-2, MMP-9, RANKL/RANK, Cathepsin K and up-regulates OPG in an experimental periodontitis model. PloS One 9:e96750CrossRefPubMedPubMedCentral
30.
Zurück zum Zitat Gonçalves DC, Evangelista RC, da Silva RR et al (2014) Infliximab attenuates inflammatory osteolysis in a model of periodontitis in Wistar rats. Exp Biol Med 239:442–453CrossRef Gonçalves DC, Evangelista RC, da Silva RR et al (2014) Infliximab attenuates inflammatory osteolysis in a model of periodontitis in Wistar rats. Exp Biol Med 239:442–453CrossRef
31.
Zurück zum Zitat Preethi KC, Kuttan G, Kuttan R (2009) Anti-inflammatory activity of flower extract of Calendula officinalis Linn. and its possible mechanism of action. Indian J Exp Biol 47:113–120bPubMed Preethi KC, Kuttan G, Kuttan R (2009) Anti-inflammatory activity of flower extract of Calendula officinalis Linn. and its possible mechanism of action. Indian J Exp Biol 47:113–120bPubMed
32.
Zurück zum Zitat Schwingel TE, Klein CP, Nicoletti NF et al (2014) Effects of the compounds resveratrol, rutin, quercetin, and quercetin nanoemulsion on oxaliplatin-induced hepatotoxicity and neurotoxicity in mice. Naunyn Schmiedebergs Arch Pharmacol 387:837–848CrossRefPubMed Schwingel TE, Klein CP, Nicoletti NF et al (2014) Effects of the compounds resveratrol, rutin, quercetin, and quercetin nanoemulsion on oxaliplatin-induced hepatotoxicity and neurotoxicity in mice. Naunyn Schmiedebergs Arch Pharmacol 387:837–848CrossRefPubMed
33.
Zurück zum Zitat Napimoga MH, Clemente-Napimoga JT, Macedo CG et al (2013) Quercetin inhibits inflammatory bone resorption in a mouse periodontitis model. J Nat Prod 76:2316–2321CrossRefPubMed Napimoga MH, Clemente-Napimoga JT, Macedo CG et al (2013) Quercetin inhibits inflammatory bone resorption in a mouse periodontitis model. J Nat Prod 76:2316–2321CrossRefPubMed
34.
Zurück zum Zitat Hajishengallis G, Chavakis T, Hajishengallis E, Lambris JD (2015) Neutrophil homeostasis and inflammation: novel paradigms from studying periodontitis. J Leukoc Biol 98:539–548CrossRefPubMed Hajishengallis G, Chavakis T, Hajishengallis E, Lambris JD (2015) Neutrophil homeostasis and inflammation: novel paradigms from studying periodontitis. J Leukoc Biol 98:539–548CrossRefPubMed
37.
Zurück zum Zitat de Araújo RF Jr, Reinaldo MP, Brito GA (2014) Olmesartan decreased levels of IL-1β and TNF-α, downregulated MMP-2, MMP-9, COX-2, RANK/RANKL and up-regulated SOCs-1 in an intestinal mucositis model. PLoS One 9:e114923CrossRefPubMedPubMedCentral de Araújo RF Jr, Reinaldo MP, Brito GA (2014) Olmesartan decreased levels of IL-1β and TNF-α, downregulated MMP-2, MMP-9, COX-2, RANK/RANKL and up-regulated SOCs-1 in an intestinal mucositis model. PLoS One 9:e114923CrossRefPubMedPubMedCentral
Metadaten
Titel
Anti-inflammatory and antiresorptive effects of Calendula officinalis on inflammatory bone loss in rats
verfasst von
Joanna Trycia M. Alexandre
Luzia Hermínia Teixeira Sousa
Mario Roberto Pontes Lisboa
Flávia A. C. Furlaneto
Danielle Rocha do Val
Mirna Marques
Hellíada C. Vasconcelos
Iracema Matos de Melo
Renata Leitão
Gerly Anne Castro Brito
Paula Goes
Publikationsdatum
29.12.2017
Verlag
Springer Berlin Heidelberg
Erschienen in
Clinical Oral Investigations / Ausgabe 6/2018
Print ISSN: 1432-6981
Elektronische ISSN: 1436-3771
DOI
https://doi.org/10.1007/s00784-017-2308-7

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