In vitro activity of ethanolic extract of propolis and chlorhexidine digluconate on Candida species isolated from the oral mucosa of patients hospitalized in the Intensive Care Unit (ICU)
Keywords:
Candida albicans, propolis, chlorhexidine
Abstract
The activity of propolis extract and chlorhexidine digluconate on Candida sp isolated from oral mucosa of patients in ICU was evaluated. The minimum fungicidal concentrations (MFC) were determined, and also the production of proteinase and phospholipase exoenzymes and the fringe formation. Seventy-two isolates were used and identified by the API 20C AUX® System. The antifungal activity was evaluated by “at base 2” serial microdilution technique. Also the exoenzymes production (proteinase and phospholipase), the fringes formation, before and after being exposed to propolis and chlorhexidine, were analysed. Of 72 isolates, 53 were C. albicans, 11 C. tropicalis, four C. guilhermondii and four suggestive C. dubliniensis. The MFC 90% of propolis extract was 5% C. albicans, 20% C. tropicalis, 0.625% C. guilhermondii; and 0.312% suggestive of C. dubliniensis. MFC 90% of chlorhexidine was 0.0018% C. albicans, 0.012% C. tropicalis, 0.0018% C. guilhermondii and 0.00375% suggestive of C. dubliniensis. The inhibition of exoenzymes and fringes occurred in the both products. Although the inhibition of chlorhexidine is lower than that showed by propolis, its daily use neither cause undesirable side effects as blemishes on the teeth and tongue, nor the loss of the taste and the burning sensation in the oral mucosa.References
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dx.doi.org/10.1590/S1517-83822002000400018
19. Huang M, Kao KC. Population dynamics and the evolution of anti fungal drug resistance in Candida albicans. FEMS Microbiol Lett. 2012;333(2):85-93. https://dx.doi.org/10.1111/j.1574-6968.2012.02587.x
20. Rüchel R, Tegeler R, Trost M.A comparison of secretory proteinases from different strains of Candida albicans. Sabouraudia: Journal of Medical and Veterinary Mycology. 1982; 20(3):233-44.
21. Price MF, Wilkinson ID, Gentry LO. Plate method for detection of phospholipase activity in Candida albicans. Sabouraudia. Journal of Medical and Veterinary Mycology.1982;20(1):7-14.
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24. Budzýnska A, Sadowska B, Lipowczan G, Maciag A, Kalemba D, Rózalska B. Activity of selected essential oils against Candida spp. strains. Evaluation of new aspects of their specific pharmacological properties, with special reference to lemon balm. Adv Microbiol. 2013;3(4):317-25.http://dx.doi.org/10.4236/aim.2013.34045
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26. Libério SA, Pereira AL, Araújo MJ, Dutra RP, Nascimento FR, Monteiro-Neto V et al. The potential use of propolis as a cariostatic agent and its actions on mutans group streptococci. JEthnopharmacol.2009:125(1):1-9. http://doi.org/10.1016/j.jep.2009.04.047
27. Abrantes MR, Lima EO, Medeiros MAP, Menezes CP, Guerra FQS, Milan EP. Atividade antifúngica de óleos essenciais sobre leveduras Candida não-albicans. Rev Bras Farm. 2013;94(3):227–33. [acesso 2018 Jun 17]. Disponível em: http://www.rbfarma.org.br/files/rbf-v94n3-05.pdf
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29. Matsuzaki Y, Tsujisawa T, Nishihara T, Nakamura M, Kakinoki Y. Antifungal activity of chemotype essential oils from rosemary against Candida
albicans. Open J Stomatol. 2013;3:176-82. http://dx.doi.org/10.4236/ojst.2013.32031 Silva BB, Rosalen PL, Cury JA, Ikegaki M, Souza VC, Esteves A et al. Chemical composition and botanical origin of red propolis, a new type of Brazilian propolis. Evid Based Complement Alternat Med. 2008;5(3):313-6. http://dx.doi.org/10.1093/ecam/nem059
31. Santos FA, Bastos EMA, Uzeda MC, Carvalho MA, Farias LM, Moreira ESA et al. Antibacterial activity of Brazilian propolis and fractions against oral
anaerobic bacteria. J. Ethnopharmacol. 2002;80:1-7. https://dx.doi.org/10.1016/S0378-8741(02)00003-X
32. Schett G. Effects of inflammatory and anti-inflammatory cytokines on the bone. Eur J Clin Invest.2011;41(12):1361–6. https://dx.doi.org/10.1111/j.1365-2362.2011.02545.x
33. Ota C, Valente PHM, Unterkicher CS, Shimizu MT. Atividade da própolis sobre bactérias isoladas da cavidade bucal. LECTA, Bragança Paulista.
1998;16:73-7.
34. Silici S, Kutluca S. Chemical composition and antibacterial activity of propolis collected by three different races of honeybees in the same region. J Ethnopharmacol. 2005;99(1):69-73. https://dx.doi.org/10.1016/j.jep.2005.01.046
35. Oliveira ACP, Shinobu CS, Longhini R, Franco SL, Svidzinski TIE. Antifungal activity of propolis extract against yeasts isolated from onychomycosis lesions. Mem Inst Oswaldo Cruz. 2006;101(5):493-7. http://dx.doi.org/10.1590/S0074-02762006000500002
36. Santos VR, Gomes RT, Mesquita RA, Moura MD, França EC, Aguiar EG et al. Efficacy of Brazilian propolis gel for the management of denture stomatitis: a pilot study. Phytother Res.2008;22(11):1544-7.https://dx.doi. org/10.1002/ptr.2541
37. Gomes RT, Teixeira KIR, Cortés ME, Santos VR. Antimicrobial activity of a propolis adhesive formulation on different oral pathogens. Braz J Oral Sci.
2007;6(22):1387-91. [acesso 2018 Jun 17]. Disponível em:https://periodicos.sbu.unicamp.br/ojs/index.php/bjos/article/view/8642997
38. Ota C, Unterkircher C, Fantinato V. Antifungal activity of propolis on different species of Candida. Mycoses. 2001;44(9-10):375-8.
39. Parker JF, Luz MMS. Método para avaliação e pesquisa da atividade antimicrobiana de produtos de origem natural. Rev Bras Farmacogn. 2007;17:102-7. http://dx.doi.org/10.1590/S0102-695X2007000100019
40. Fernandes Junior A, Lopes MR, Colombari V, Monteiro AV, Vieira EP. Atividade antimicrobiana de própolis de Apis mellifera obtidas em três regiões do Brasil. Cienc Rural [online]. 2006;36(1):294-7. http://dx.doi.org/10.1590/S0103-84782006000100047
41. Araujo MTB, Araujo RPC, Campos EJ. Estudo in vitro e in vivo da atividade bactericida da clorexidina 0,12% e 0,2% e dos produtos farmacológicos Listerine e Duplax. Rev Odonto Ciênc. 2001;16(33):187-201.
42. Batista AL, Lins RD, Coelho RS, Barbosa DN, Belém NM, Celestino FJA. Clinical efficacy analysis of the mouth rinsing with pomegranate and chamomile plant extracts in the gingival bleeding reduction. Complement Ther Clin Pract. 2014;(20):93-8. http://dx.doi.org/10.1016/j.ctcp.2013.08.002
43. Simões RCS, Merlini SP, Silva RPR, Bastos RS, Torres AS, Bastos JRM. Avaliação in vitro da atividade antimicrobiana de enxaguatórios bucais. Rev Bras Odontol. 2011;68(1):91-4.
44. Souza ELC. Comparação do digluconato de clorexidina 0,12% sem xilitol com álcool e com xilitol sem álcool para controle do biofilme oral e efeitos adversos associados. [dissertação de mestrado]. Rio de Janeiro (RJ): Universidade Veiga de Almeida; 2007.
45. Hortense SR, Carvalho ES, Carvalho FS, Silva RPR, Bastos JRM, Bastos RS. Uso de clorexidina como agente preventivo e terapêutico na odontologia. Rev Odontol Univ Cidade de São Paulo. 2010; 22,(2):178-84.
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48. Ferguson JW, Hatton JF, Gillespie MJ. Effectiveness of intracanal irrigants and medications against the yeast Candida albicans. J Endod. 2002;28(2):68-71. https://dx.doi.org/10.1097/00004770-200202000-00004
2. Pupulin ÁR, Carvalho PG, Nakamura CV- Susceptibility to antifungal and enzyme production by Candida yeasts isolated from HIV/AIDS patients. Salud(i)Ciencia. 2014; 20(5):471-6.
3. Sears D, Schwartz BS. Candida auris: an emerging multidrug-resistant pathogen. Int J Infect Dis. 2017;63:95–8. http;//dx.doi.org/10.1016/j.ijid.2017.08.017
4. Gonçalves PE, Rodrigues NALR, Seixas FL. Ações de promoção de saúde bucal no âmbito hospitalar. Rev. Ciênc. Méd., Campinas. 2014; 23(1):15-23. https://dx.doi.org/10.24220/2318-0897v23n1a2411
5. Martins ST, Moreira M, Furtado GHCF, Marino CGJ, Machado FR, Wey SB et al. Application of control measures for infections caused by multi-resistant gram-negative bacteria in intensive care unit patients. Mem Inst Oswaldo Cruz. 2004; 99(3):331-4. http://dx.doi.org/10.1590/S0074-2762004000300017
6. Wingeter MA, Guilhermetti E, Shinobu CS, Takaki I, Svidzinski TIE. Microbiological identification and in vitro sensitivity of Candida isolates from the oral cavity of HIV-positive individuals. Rev Soc Bras Med Trop. 2007;40(3):272-6. http://dx.doi.org/10.1590/S0037-86822007000300004
7. Nascimento PFC, Nascimento AC, Rodrigues CS, Antoniolli AR, Santos PO, Barbosa Júnior AM et al. Atividade antimicrobiana dos óleos essenciais: Uma abordagem multifatorial dos métodos. Rev Bras Farmacogn. 2007;17(1):108-13. http://dx.doi.org/10.1590/S0102-695X2007000100020
8. Lee SC, Li A, Calo S, Heitman J. Calcineurin plays key roles in the dimorphic transition and virulence of the human pathogenic zygomycete Mucor circinelloides. PloS Pathog. 2013;9(9):e1003625. http://dx.doi.org/ 10.1371/journal.ppat.1003625
9. Heizmann P, Klefisch F, Heizmann WR. Basic research - Significance of detection and clinical impact of Candida albicans in non-immunosuppressed patients. Pharmacol Pharm. 2011;2:354-60.
10. Khan MS, Malik A, Ahmad I. Anti-candidal activity of essential oils alone and in combination with amphotericin B or fluconazole against multi-drug resistant isolates of Candida albicans. Med Mycol. 2012;50(1):33-42. http://dx.doi.org/ 10.3109/13693786.2011.582890
11. López-Montéon A, Gómez-Figueroa FS, Ramos-Poceros G, Guzmán-Gómez D, Ramos-Ligonio A. Codetection of Trichomonas vaginalis and Candida albicans by PCR in urine samples in a low-risk population attended in a clinic first level in central Veracruz,Mexico.BiomeRes Int. 2013;2013:281892. http://dx.doi.org/ 10.1155/2013/281892
12. Salatino A, Teixeira EW, Negri G, Message D. Origin and chemical variation of Brazilian propolis. Evid Based Complement.Alternat Med. 2005;2(1):33–8. http;//dx.doi.org/10.1093/ecam/neh060
13. Sforcin JM. Propolis and the immune system: a re view. J Ethnopharmacol. 2007; 113(1):1-14. https://dx.doi.org/10.1016/j.jep.2007.05.012
14. Banskota AH, Tezuka Y, Kadota S. Recent progress in pharmacological research of propolis. Phytother Res. 2001;15(7):561-71.
15. Oliveira LC, Carneiro PP, Fischer RG, Tinoco EM. A presença de patógenos respiratórios no biofilme bucal de pacientes com pneumonia nosocomial. Rev Bras Ter Intensiva. 2007;19(4):428-33.
16. Chan GC, Cheung KW, Sze DM. The immunomodulatory and anticancer properties of propolis. Clin Rev Allergy Immunol. 2013;44(3):262-
73. https://dx.doi.org/doi:10.1007/s12016-012-8322-2
17. Simões CC, Araújo DB, Araújo RPC. Estudo in vitro e ex vivo da ação de diferentes concentrações de extratos de própolis frente aos microrganismos presentes na saliva de humanos. Ver Braz Farmacon. 2008;18(1):84-9. http://dx.doi.org/10.1590/S0102-695X2008000100016
18. Gebara ECE, Lima LA, Mayer MPA. Propolis antimicrobial activity against periodontopathic bacteria. Braz J Microbiol. 2002;33(4):365-9. http://
dx.doi.org/10.1590/S1517-83822002000400018
19. Huang M, Kao KC. Population dynamics and the evolution of anti fungal drug resistance in Candida albicans. FEMS Microbiol Lett. 2012;333(2):85-93. https://dx.doi.org/10.1111/j.1574-6968.2012.02587.x
20. Rüchel R, Tegeler R, Trost M.A comparison of secretory proteinases from different strains of Candida albicans. Sabouraudia: Journal of Medical and Veterinary Mycology. 1982; 20(3):233-44.
21. Price MF, Wilkinson ID, Gentry LO. Plate method for detection of phospholipase activity in Candida albicans. Sabouraudia. Journal of Medical and Veterinary Mycology.1982;20(1):7-14.
22. Hunter PR, Fraser CA. M. Application of a numerical index of discriminatory power to a comparison of four physiochemical typing methods for Candida albicans. J Clin Microbiol.1989;27(10):2156-60. [acesso 2018 Jun 17]. Disponível em: https://jcm.asm.org/content/jcm/27/10/2156.full.pdf
23. Colombo AL, Guimarães T. Epidemiologia das infecções hematogênicas por Candida spp. Rev Soc Bras Med Trop. 2003;36(5):599-07 http://dx.doi.org/10.1590/S0037-86822003000500010
24. Budzýnska A, Sadowska B, Lipowczan G, Maciag A, Kalemba D, Rózalska B. Activity of selected essential oils against Candida spp. strains. Evaluation of new aspects of their specific pharmacological properties, with special reference to lemon balm. Adv Microbiol. 2013;3(4):317-25.http://dx.doi.org/10.4236/aim.2013.34045
25. Williams D, Lewis D. Pathogenesis and treatment of oral candidosis. J Oral Microbiol. 2011;3:5771. https://dx.doi.org/10.3402/jom.v3i0.5771
26. Libério SA, Pereira AL, Araújo MJ, Dutra RP, Nascimento FR, Monteiro-Neto V et al. The potential use of propolis as a cariostatic agent and its actions on mutans group streptococci. JEthnopharmacol.2009:125(1):1-9. http://doi.org/10.1016/j.jep.2009.04.047
27. Abrantes MR, Lima EO, Medeiros MAP, Menezes CP, Guerra FQS, Milan EP. Atividade antifúngica de óleos essenciais sobre leveduras Candida não-albicans. Rev Bras Farm. 2013;94(3):227–33. [acesso 2018 Jun 17]. Disponível em: http://www.rbfarma.org.br/files/rbf-v94n3-05.pdf
28. Santana DP, Ribeiro TF, Ribeiro EL, Aquino GLB, Naves PLF. Ação de chalconas contra a formação de biofilme de Candida albicans. Rev Ciênc Farm Básica Apl. 2015;36(1):83-90. [acesso 2018 Jun 17]. Disponível em: http://seer.fcfar.unesp.br/rcfba/index.php/rcfba/article/view/211/119
29. Matsuzaki Y, Tsujisawa T, Nishihara T, Nakamura M, Kakinoki Y. Antifungal activity of chemotype essential oils from rosemary against Candida
albicans. Open J Stomatol. 2013;3:176-82. http://dx.doi.org/10.4236/ojst.2013.32031 Silva BB, Rosalen PL, Cury JA, Ikegaki M, Souza VC, Esteves A et al. Chemical composition and botanical origin of red propolis, a new type of Brazilian propolis. Evid Based Complement Alternat Med. 2008;5(3):313-6. http://dx.doi.org/10.1093/ecam/nem059
31. Santos FA, Bastos EMA, Uzeda MC, Carvalho MA, Farias LM, Moreira ESA et al. Antibacterial activity of Brazilian propolis and fractions against oral
anaerobic bacteria. J. Ethnopharmacol. 2002;80:1-7. https://dx.doi.org/10.1016/S0378-8741(02)00003-X
32. Schett G. Effects of inflammatory and anti-inflammatory cytokines on the bone. Eur J Clin Invest.2011;41(12):1361–6. https://dx.doi.org/10.1111/j.1365-2362.2011.02545.x
33. Ota C, Valente PHM, Unterkicher CS, Shimizu MT. Atividade da própolis sobre bactérias isoladas da cavidade bucal. LECTA, Bragança Paulista.
1998;16:73-7.
34. Silici S, Kutluca S. Chemical composition and antibacterial activity of propolis collected by three different races of honeybees in the same region. J Ethnopharmacol. 2005;99(1):69-73. https://dx.doi.org/10.1016/j.jep.2005.01.046
35. Oliveira ACP, Shinobu CS, Longhini R, Franco SL, Svidzinski TIE. Antifungal activity of propolis extract against yeasts isolated from onychomycosis lesions. Mem Inst Oswaldo Cruz. 2006;101(5):493-7. http://dx.doi.org/10.1590/S0074-02762006000500002
36. Santos VR, Gomes RT, Mesquita RA, Moura MD, França EC, Aguiar EG et al. Efficacy of Brazilian propolis gel for the management of denture stomatitis: a pilot study. Phytother Res.2008;22(11):1544-7.https://dx.doi. org/10.1002/ptr.2541
37. Gomes RT, Teixeira KIR, Cortés ME, Santos VR. Antimicrobial activity of a propolis adhesive formulation on different oral pathogens. Braz J Oral Sci.
2007;6(22):1387-91. [acesso 2018 Jun 17]. Disponível em:https://periodicos.sbu.unicamp.br/ojs/index.php/bjos/article/view/8642997
38. Ota C, Unterkircher C, Fantinato V. Antifungal activity of propolis on different species of Candida. Mycoses. 2001;44(9-10):375-8.
39. Parker JF, Luz MMS. Método para avaliação e pesquisa da atividade antimicrobiana de produtos de origem natural. Rev Bras Farmacogn. 2007;17:102-7. http://dx.doi.org/10.1590/S0102-695X2007000100019
40. Fernandes Junior A, Lopes MR, Colombari V, Monteiro AV, Vieira EP. Atividade antimicrobiana de própolis de Apis mellifera obtidas em três regiões do Brasil. Cienc Rural [online]. 2006;36(1):294-7. http://dx.doi.org/10.1590/S0103-84782006000100047
41. Araujo MTB, Araujo RPC, Campos EJ. Estudo in vitro e in vivo da atividade bactericida da clorexidina 0,12% e 0,2% e dos produtos farmacológicos Listerine e Duplax. Rev Odonto Ciênc. 2001;16(33):187-201.
42. Batista AL, Lins RD, Coelho RS, Barbosa DN, Belém NM, Celestino FJA. Clinical efficacy analysis of the mouth rinsing with pomegranate and chamomile plant extracts in the gingival bleeding reduction. Complement Ther Clin Pract. 2014;(20):93-8. http://dx.doi.org/10.1016/j.ctcp.2013.08.002
43. Simões RCS, Merlini SP, Silva RPR, Bastos RS, Torres AS, Bastos JRM. Avaliação in vitro da atividade antimicrobiana de enxaguatórios bucais. Rev Bras Odontol. 2011;68(1):91-4.
44. Souza ELC. Comparação do digluconato de clorexidina 0,12% sem xilitol com álcool e com xilitol sem álcool para controle do biofilme oral e efeitos adversos associados. [dissertação de mestrado]. Rio de Janeiro (RJ): Universidade Veiga de Almeida; 2007.
45. Hortense SR, Carvalho ES, Carvalho FS, Silva RPR, Bastos JRM, Bastos RS. Uso de clorexidina como agente preventivo e terapêutico na odontologia. Rev Odontol Univ Cidade de São Paulo. 2010; 22,(2):178-84.
46. Ministério da Saúde (BR). Agência Nacional de Vigilância Sanitária. Resolução no 7, de 24 de fevereiro de 2010. Dispõe sobre os requisitosmínimos para funcionamento de Unidades de Terapia Intensiva e dá outras providências. Diário Oficial da União. Brasília, DF, 2010. [acesso 2018 Jun 17]. Disponível em: http://bvsms.saude.gov.br/bvs/saudelegis/anvisa/2010/res0007_24_02_2010.html
47. Candido RC, Azevedo RVP, Ito IY. Determinação da Concentração Inibitória Mínima de Cepacol, Malvona e Periogard, Frente C. albicans Isoladasda Cavidade Bucal. Rev. Odontol. UNESP. 1996;25(1):79-84. [acesso 2018 Jun 17]. Disponível em:http://www.revodontolunesp.com.br/article/588017787f8c9d0a098b4742
48. Ferguson JW, Hatton JF, Gillespie MJ. Effectiveness of intracanal irrigants and medications against the yeast Candida albicans. J Endod. 2002;28(2):68-71. https://dx.doi.org/10.1097/00004770-200202000-00004
Published
2018-03-29
How to Cite
MAKABE, M. L., SANTOS, P. de S., & PIRES, M. de F. C. (2018). In vitro activity of ethanolic extract of propolis and chlorhexidine digluconate on Candida species isolated from the oral mucosa of patients hospitalized in the Intensive Care Unit (ICU). Revista Do Instituto Adolfo Lutz, 77, 1-11. Retrieved from https://periodicoshomolog.saude.sp.gov.br/index.php/RIAL/article/view/34185
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Section
ORIGINAL ARTICLE
