Vaginal Yeasts and the Antifungal Action of Red Propolis Extract

Authors

  • Kévia Katiúcia Santos Bezerra Federal University of Campina Grande.
  • Maria do Carmo Andrade Duarte de Farias Federal University of Campina Grande.
  • Patrício Borges Maracajá Federal University of Campina Grande.
  • Alfredina dos Santos Araújo Federal University of Campina Grande.
  • Rosilene Agra da Silva Federal University of Campina Grande.
  • Antônio Fernandes Filho Federal University of Campina Grande.
  • Anne Milane Formiga Bezerra Nurse in a Mobile Emergency Service, MSU, Sousa, PB, Brazil.
  • Aucelia Cristina Soares Belchior Teacher of Faculty Santa Maria, Cajazeiras, Paraíba, Brazil; and Faculties Integrated of Patos, PB, Brazil.
  • Francisco Alírio da Silva Federal University of Campina Grande.
  • Wilma Katia Trigueiro Bezerra Nurse in a Mobile Emergency Service, MSU, Sousa, PB, Brazil.
  • Cláudia Sarmento Gadelha Federal University of Campina Grande.
  • Joyce Carolle Bezerra Cavalcante Federal University of Campina Grande.

DOI:

https://doi.org/10.3823/1753

Keywords:

Propolis, Candida, Vulvovaginitis, Products with antimicrobial action.

Abstract

Introduction: Vulvovaginitis is an inflammatory process that affects the vulva, vagina and cervix, most of the times of infectious cause. Vulvovaginal candidiasis is the second most frequent cause in Brazil, in Europe ranks first. Candida spp can be found in the vagina up to 20% of asymptomatic women.

Objective: Understanding the occurrence of vaginal yeasts and evaluating the antifungal action of a red propolis extract.

Method: This is a clinical study in vitro with vaginal secretion samples collected from 197 patients treated at the Health Center Frei Damiao in Patos-PB, Brazil. The species were identified using a chromogenic medium CHROMagar Candida®. At the end, the antifungal activity of the red propolis extract in four different concentrations was observed: 25%, 50%, 75% and 100%, by test disc Agar diffusion. The study was approved by the Research Ethics Committee of the Federal University of Campina Grande, CAAE 35203614.8.0000.5575.

Results: Of the samples analyzed other species identified by the medium used were the most prevalent corresponding to 59.8%, followed by C. albicans, with 21.7%. The antifungal activity was observed in 81.25% of the tested samples. According to the average and standard deviation of the inhibition zone of the four concentrations, the one that presented the smallest variation was the concentration at 50%, followed by concentration to 75%.

Conclusions: The results of this research showed that there was antifungal action of red propolis extract, since occurred inhibition in 81.25% of the analyzed samples. However did not show clearance regarding this action, since positivity tendency was not growing by increasing or decreasing the concentration of propolis extract.

Author Biographies

Kévia Katiúcia Santos Bezerra, Federal University of Campina Grande.

Academic Unit of Life Sciences, Teacher training center,

Maria do Carmo Andrade Duarte de Farias, Federal University of Campina Grande.

Academic Unit of Life Sciences, Teacher training center,

Patrício Borges Maracajá, Federal University of Campina Grande.

Graduate-degree in Agroindustrial Systems, Pombal, PB, Brazil.

Alfredina dos Santos Araújo, Federal University of Campina Grande.

Graduate-degree in Agroindustrial Systems, Pombal, PB, Brazil.

Rosilene Agra da Silva, Federal University of Campina Grande.

Graduate-degree in Agroindustrial Systems, Pombal, PB, Brazil.

Antônio Fernandes Filho, Federal University of Campina Grande.

Academic Unit of Nursing, Teacher training center,

Anne Milane Formiga Bezerra, Nurse in a Mobile Emergency Service, MSU, Sousa, PB, Brazil.

Nurse in a Mobile Emergency Service, MSU, Sousa, PB, Brazil.

Aucelia Cristina Soares Belchior, Teacher of Faculty Santa Maria, Cajazeiras, Paraíba, Brazil; and Faculties Integrated of Patos, PB, Brazil.

Teacher of Faculty Santa Maria, Cajazeiras, Paraíba, Brazil; and Faculties Integrated of Patos, PB, Brazil.

Francisco Alírio da Silva, Federal University of Campina Grande.

Academic Unit of Life Sciences, Teacher training center,

Wilma Katia Trigueiro Bezerra, Nurse in a Mobile Emergency Service, MSU, Sousa, PB, Brazil.

Nurse in a Mobile Emergency Service, MSU, Sousa, PB, Brazil.

Cláudia Sarmento Gadelha, Federal University of Campina Grande.

Academic Unit of Life Sciences, Cajazeiras, Paraíba, Brasil.

Joyce Carolle Bezerra Cavalcante, Federal University of Campina Grande.

Student of Medicine, Academic Unit of Life Sciences, Cajazeiras, Paraíba, Brasil.

References

Dalazen D, Zanrosso D, Wanderley L, Silva NL, Fuentefria AM. Comparação do perfil de suscetibilidade entre isolados clínicos de Candida spp. orais e vulvovaginais no Sul do Brasil. J Bras Patol Med Lab [Internet]. 2011 Feb; 47(1): 33-8. Available from: <http://www.scielo.br/pdf/jbpml/v47n1/04.pdf>. doi: http://dx.doi.org/10.1590/S1676-24442011000100004

Consolaro ME, Albertoni TA, Svidzinski AE, Peralta RM, Svidzinski TI. Vulvovaginal Candidasis is associated with the production of germ tubes by Candida albicans. Mycopathologia [Internet]. 2005 Jun; 159(4):501-7. Available from: <http://www.ncbi.nlm.nih.gov/pubmed/15983735>. doi: http://dx.doi.org/10.1007/s11046-005-1149-0. PubMed PMID: 15983735.

Dota KFD, Shinobu CS, Patussi EV, Consolaro MEL, Svidzinski TIE. Susceptibility to vaginal yeast in most used antifungical in Maringá, Paraná, Brazil. Acta Bioquim Clin Latinoam [Internet]. 2008 Oct; 110:66–72. Available from: <http://www.scielo.org.ar/pdf/abcl/v42n4/v42n4a08.pdf>

Nunes LCC, Lima MAR, Sousa KMH, Prado AIO, Soares-Sobrinho JL, Rolim-Neto PJ. Desenvolvimento de gel vaginal contendo extrato de própolis vermelha. Rev Bras Farm [Internet]. 2012; 93(2): 179-85. Available from: <http://www.rbfarma.org.br/files/rbf-2012-93-2-8.pdf>.

Butts A, Krysan DJ. Antifungal drug discovery: something old and something new. PLOS Pathogens [Internet]. 2012 Sep; 8(9). Available from: <http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3435257/>. doi: http://dx.doi.org/ http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3435257/. PubMed Central PMCID: PMC3435257.

Portilho DR, Melo IA, Guerra RC, Batista HL, Fernandes CHC. Avaliação da atividade antibacteriana e antifúngica da própolis produzida no estado do Tocantins. Rev Cient do ITPAC [Internet]. 2013 Apr; 6(2). Available from: <http://www.itpac.br/arquivos/Revista/62/1.pdf>.

Oliveira KAM, Oliveira GV, Batalini C, Rosalem JA, Ribeiro LS. Atividade antimicrobiana e quantificação de flavonoides e fenóis totais em diferentes extratos de própolis. Semina: Ciênc Biol Saúde [Internet]. 2012 Jul/Dec; 33(2): 211-22. Available from: <http://www.uel.br/revistas/uel/index.php/seminabio/article/view/10827/12168>. doi: http://dx.doi.org/10.5433/1679-0367.2012v33n2p211

Park YK, Ikegaki M, Alencar SM. Evaluation of brazilian propolis by both physicochemical methods and biological activity. Honeybee Science [Internet]. 2000; 21(2): 85-90. Available from: <http://www.cabdirect.org/abstracts/20000508894.html;jsessionid=257A25DA65F7139693018667252A362F>.

Batista LLV, Campesatto EA, Assis MLB, Barbosa APF, Grillo LAM, Dornelas CB. Estudo comparativo do uso tópico de própolis verde e vermelha na reparação de feridas em ratos. Rev Col Bras Cir [Internet]. 2012 Nov/Dec; 39(6): 515-20. Available from: <http://www.scielo.br/scielo.php?pid=S0100-69912012000600012&script=sci_arttext>. doi: http://dx.doi.org/10.1590/S0100-69912012000600012

Daugsch A, Moraes CS, Fort P, Pacheco E, Lima IB, Abreu JA, et al. Própolis vermelha e sua origem botânica. Mensagem Doce [Internet]. 2006; 89: 2-8. Available from: http://www.apacame.org.br/mensagemdoce/89/artigo.htm>.

Krol W, Schller S, Czuba Z, Matsuno T, Zydowicz G, Shani J, et al. Inhibition of neutrophils' chemiluminescence by ethanol extract of propolis (EEP) and its phenolic components. J of Ethnopharmacology [Internet]. 1996 Dec; 55: 19-25. Available from: <http://www.ncbi.nlm.nih.gov/pubmed/9121163>. PubMed PMID: 9121163.

Oliveira AC, Shinobu CS, Longhini R, Franco SL, Svidzinski TI. Antifungal activity of propolis extract against yeasts isolated from onychomycosis lesions. Mem Inst Oswaldo Cruz [Internet]. 2006 Aug; 101(5): 493-7. Available from: <http://www.scielo.br/pdf/mioc/v101n5/v101n5a02.pdf>. doi: http://dx.doi.org/10.1590/S0074-02762006000500002. PubMed PMID: 17072451.

Scazzocchio F, D'Auria FD, Alessandrini D, Pantanella F. Multifactorial aspects of antimicrobial activity of propolis. Microbiol Res [Internet]. 2006 Jan; 161(4): 327-33. Available from: <http://www.sciencedirect.com/science/article/pii/S0944501305001230>. doi: http://dx.doi.org/10.1016/j.micres.2005.12.003. PubMed PMID: 16427259.

Bastos EMAF, Santana RA, Calaça-Costa AGF, Thiago PS. Interaction between Apis melliferaL and Baccharis dracunculifolia DC, that favours green propolis production in Minas Gerais. Braz J Biol [Internet]. 2011 Aug; 71(3): 727-34. Available from: <http://www.scielo.br/scielo.php?pid=S1519-69842011000400018&script=sci_arttext>. doi: http://dx.doi.org/10.1590/S1519-69842011000400018

Lacaz CS, Porto E, Martins JEC, Heins-Vaccari EM, Takahashi MN.Tratado de micologia médica. São Paulo: Sarvier; 2002. 9 ed. São Paulo: Sarvier; 2002.

Sidrim JJC, Rocha MFG. Micologia médica a luz de autores contemporâneos. Rio de Janeiro: Guanabara Koogan; 2004.

Quindós G, Alonso-Vargas R, Helou S, Arechavala A, Martín-Mazuelos E, Negroni R. Evaluación de un nuevo medio de cultivo cromógeno (Candida ID) para el aislamiento e identiï¬cación presuntiva de Candida albicans y otras levaduras de interés médico. Rev Iberoam Micol [Internet]. 2001; 18: 23-8. Available from: <http://www.reviberoammicol.com/2001-18/023028.pdf>.

Odds FC, Bernaerts R. CHROMagar Candida, a new differential isolation medium for presuntive identiï¬cation of clinically important Candida species. J Clin Microbiol [Internet]. 1995 Aug; 32(8): 1923-9. Available from: <http://www.ncbi.nlm.nih.gov/pmc/articles/PMC263904/>. doi: http://dx.doi.org/10.1128/JCM.39.5.2015-2016.2001. PubMed PMID: PMC88073.

Duarte S, Koo H, Bowen WH, Hayacibara MF, Cury JA, Ikegaki M, Rosalen PL. Effect of a novel type of propolis and its chemical fractions on glucosyltransferases and on growth and adherence of mutans streptococci. Biol Pharm Bull [Internet]. 2003 Apr; 26(4):527-31. Available from: <http://www.ncbi.nlm.nih.gov/pubmed/12673037>. PubMed PMID: 12673037.

Ferrazza MHSH, Maluf MLF, Consolaro MEL, Shinobu CS, Svidzinski TIE, Batista MR. Caracterização de leveduras isoladas da vagina e sua associação com candidíase vulvovaginal em duas cidades do Sul do Brasil. Rev Bras Ginecol Obstet [Internet]. 2005 Feb; 27(2): 58-63. Available from: <http://www.scielo.br/pdf/rbgo/v27n2/24297.pdf>. doi: http://dx.doi.org/10.1590/S0100-72032005000200003

Gygax SE, Vermitsky JP, Chadwick SG, Self MJ, Zimmerman JA, Mordechai E, et al. Antifungal resistance of Candida glabrata vaginal isolates and development of a quantitative reverse transcription-PCR-based azole susceptibility assay. Antimicrob Agents Chemother [Internet]. 2008 Sep; 52(9): 3424-6. Available from: <http://aac.asm.org/content/52/9/3424.full.pdf#page=1&view=FitH>. doi: http://dx.doi.org/10.1128/AAC.00462-08. PubMed PMID: 18591262. PubMed Central PMCID: PMC2533493.

Schaller M. Candida albicans-interactions with the mucosa and the immune system. J Dtsch Dermatol Ges [Internet]. 2006 Apr; 4(4): 328-36. Available from: <http://onlinelibrary.wiley.com/doi/10.1111/j.1610-0387.2006.05935.x/pdf>. doi: http://dx.doi.org/10.1111/j.1610-0387.2006.05935.x

Barrenetxea Z. Vulvovaginitis candidiasica. Rev Iberoam Micol [Internet]. 2002; 19(1): 22-4. Available from: <http://www.reviberoammicol.com/2002-19/022024.pdf>.

Parazzini F, Di Cintio E, Chiantera V, Guaschino S. Determinants of different Candida species infection of the genital tract in women. Sporachrom study Group. Eur J Obstet Reprod Biol [Internet]. 2000; 93(2): 141-5. Available from: <http://europepmc.org/abstract/MED/11074134>. doi: http://dx.doi.org/10.1016/S0301-2115(00)00289-X

Baldim IM, Pereira MA, Rufino RLA, Oliveira NMS, Fiorini JE. Teste de sensibilidade ao quefir de cepas de Candida spp. isoladas de vulvovaginites. Rev Ciênc Farm Básica Apl [Internet]. 2012; 33(3): 379-383. Available from: <http://serv-bib.fcfar.unesp.br/seer/index.php/Cien_Farm/article/viewFile/2078/1263>

Toloi MRT, Candido RC, Franceschini SA. Vaginal candidiasis: risk factors. Rev Chil Cienc Méd Biol [Internet]. 2001; 11(1): 11-4.

Holanda AAR, Fernandes ACS, Bezerra CM, Ferreira MAF, Holanda MRR, Holanda JCP, et al. Candidíase vulvovaginal: sintomatologia, fatores de risco e colonização anal concomitante. Rev Bras Ginecol Obstet [Internet]. 2007 Jan; 29(1): 3-9. Available from: <http://www.scielo.br/pdf/rbgo/v29n1/a02v29n1.pdf>. doi: http://dx.doi.org/10.1590/S0100-72032007000100002

Colombo AL, Nucci M, Park BJ, Nouér SA, Arthington-Skaggs B, da Matta DA, et al. Epidemiology of candidemia in Brazil: a Nationwide sentinel surveillance of candidemia in eleven medical centrs. J Clin Microbiol [Internet]. 2006 Aug; 44(8): 2816-23. Available from: <http://jcm.asm.org/content/44/8/2816.long>.

Bassetti M, Ansaldi F, Nicolini L, Malfatto E, Molinari MP, Mussap M, et al. Incidence of candidemia and relationship with fluconazole use in an intensive care unit. J Antimicrob Chemother. 2009 Sep; 64(3): 625-9. Available from: <http://jac.oxfordjournals.org/content/64/3/625.full.pdf>. doi: http://dx.doi.org/10.1093/jac/dkp251

Spinillo A, Capuzzo E, Gulminetti R, Marone P, Colonna L, Piazzi G. Prevalence of and risk factors for jungal vaginitis caused by non-albicans species. Am J Obstet Gynecol [Internet]. 1997 Feb; 176(1): 138-41. Available from: < http://www.ajog.org/article/S0002-9378(97)80026-9/abstract>. doi: http://dx.doi.org/10.1016/S0002-9378(97)80026-9

Simões JA. Sobre o diagnóstico da candidíase vaginal. Rev Bras Ginecol Obstet [Internet]. 2005 May; 27(5): 233-4. Available from: <http://www.scielo.br/pdf/rbgo/v27n5/25637.pdf>. doi: http://dx.doi.org/10.1590/S0100-72032005000500001

Lopes-Consolaro ME, Albertoni T, Yoshida C, Mazucheli J, Peralta RM, Svidzinski TI.. Correlation of candida species and symptoms among patients with vulvovaginal candidasis in Maringa Paraná, Brasil. Rev Iberoam Micol [Internet]. 2004 Dec; 21(4): 202-5. Available from: < http://www.ncbi.nlm.nih.gov/pubmed/15709802>.

Corrêa PR, David PRS, Peres NP, Cunha KC, Almeida MTG. Caracterização fenotípica de leveduras isoladas da mucosa vaginal em mulheres adultas. Rev Bras Ginecol Obstet [Internet]. 2009; 31(4): 177-81. Available from: <http://www.scielo.br/pdf/rbgo/v31n4/04.pdf>. doi: http://dx.doi.org/10.1590/S0100-72032009000400004

Sá MCN, Sousa HR, Amaro CSO, Pinheiro DN, Oliveira MMM, Pinheiro MCN. Isolamento de Candida no esfregaço cérvico-vaginal de mulheres não gestantes residentes em área ribeirinha do Estado do Maranhão, Brasil, 2012. Rev Pan-Amaz Saude [Internet]. 2014 Mar; 5(1): 25-34. Available from: <http://scielo.iec.pa.gov.br/scielo.php?script=sci_arttext&pid=S2176-62232014000100003&lng=pt>.

Andrioli JL, Oliveira GSA, Barreto CS, Sousa ZL, Oliveira MCH, Cazorla IM, et al. Frequência de leveduras em fluido vaginal de mulheres com e sem suspeita clínica de candidíase vulvovaginal. Rev Bras Ginecol Obstet [Internet]. 2009 Jun; 31(6): 300-4. Available from: <http://www.scielo.br/pdf/rbgo/v31n6/06.pdf>. doi: http://dx.doi.org/10.1590/S0100-72032009000600006

Rosa MI, Rumel D. Fatores associados à candidíase vulvovaginal: estudo exploratório. Rev Bras Ginecol Obstet [Internet]. 2004 Jan/Feb; 26(1): 65-70. Available from: <http://www.scielo.br/pdf/rbgo/v26n1/19547.pdf>. doi: http://dx.doi.org/10.1590/S0100-72032004000100010

Ota C, Unterkircher C, Fantinato V, Shimizu MT. Antifungical activity of propolis on different species of candida. Mycoses [Internet]. 2001 Nov; 44(9-10): 375-8. Available from: < http://onlinelibrary.wiley.com/doi/10.1046/j.1439-0507.2001.00671.x/abstract>. doi: http://dx.doi.org/10.1046/j.1439-0507.2001.00671.x

Longhini R, Raksa S M, Oliveira ACP, Svidzinski TIE, Franco SL. Obtenção de extratos de própolis sob diferentes condições e avaliação de sua atividade antifúngica. Rev bras farmacogn [Internet]. 2007 Sep; 17(3): 388-95. Available from: <http://www.scielo.br/scielo.php?script=sci_arttext&pid=S0102-695X2007000300015&lng=en>. doi: http://dx.doi.org/10.1590/S0102-695X2007000300015.

Monzote L, Cuesta-Rubio O, Campo FM, Márquez HI, Fraga J, Pérez Kl, et al. In vitro antimicrobial assessment of Cuban propolis extracts. Mem Inst Oswaldo Cruz [Internet]. 2012 Dec; 107(8): 978–84. Available from: <http://www.scielo.br/pdf/mioc/v107n8/03.pdf>. doi: http://dx.doi.org/10.1590/S0074-02762012000800003

Kujumgiev A, Tsvetkova I, Serkedjieva Y, Bankova V, Christov R, Popov S. Antibacterial, antifungal and antiviral activity of propolis of different geographic origin. J Ethnopharmacol [Internet]. 1999 Mar; 64(3): 235-40. Available from: <http://www.ncbi.nlm.nih.gov/pubmed/10363838>. doi: http://dx.doi.org/10.1016/S0378-8741(98)00131-7. PubMed PMID: 10363838.

Negri M, Salci TP, Shinobu-Mesquita CS, Capoci IR, Svidzinski TI, Kioshima ES. Early state research on antifungal natural products. Molecules [Internet]. 2014 Mar; 19(3): 2925-56. Available from: <http://www.mdpi.com/1420-3049/19/3/2925>. doi: http://dx.doi.org/10.3390/molecules19032925. PubMed PMID: 24609016.

Quintero-Mora ML, Londoño-Orozco A, Hernández-Hernández F, Manzano-Gayosso P, López-Martínez R, Soto-Zárate CI. Efecto de extratos propóleos mexicanos de Apis mellifera sobre el crecimiento in vitro de Candida albicans. Rev Iberoam Micol [Internet]. 2008; 25(1): 22-6. Available from: <http://www.reviberoammicol.com/2008-25/022026.pdf>.

Dota KFD, Freitas AR, Consolaro MEL, Svidzinski TIE. A challenge for clinical laboratories: detection of antifungal resistance in Candida Species causing vulvovaginal candidiasis. Lab medicine [Internet]. 2011 Feb; 42(2): 87-93. Available from: <http://labmed.ascpjournals.org/content/42/2/87.full.pdf#page=1&view=FitH>. doi: http://dx.doi.org/10.1309/LMDFCA8YEZ0MQULA

Dalben-Dota KF, Faria MG, Bruschi ML, Pelloso SM, Lopes-Consolaro ME, Svidzinski TI. Antifungical activity of propolis extract against yeast isolated from vaginal exudates. J Altern Complement Med [Internet]. 2010 Mar; 16(3): 285-90. Available from: <http://online.liebertpub.com/doi/abs/10.1089/acm.2009.0281>. doi: http://dx.doi.org/10.1089/acm.2009.0281

Tamura NK, Negri MFN, Bonassoli LA, Svidzinski TIE. Fatores de virulência de candida spp isoladas de cateteres venosos e mãos de servidores hospitalares. Rev Soc Bras Med Trop [Internet]. 2007 Jan/Feb; 40(1): 91-3. Available from: <http://www.scielo.br/pdf/rsbmt/v40n1/a21v40n1.pdf>. doi: http://dx.doi.org/10.1590/S0037-86822007000100021

Sousa RP, Lopes ME, editors. Eficácia in vivo de diferentes formulas farmacêuticas de propolis em infeccção vaginal por Candida sp em comparação com nistatina e fluconazol. Anais do XIX EAIC; 2010 Oct 28-30; Guarapuava, BR. Guarapuava: UNICENTRO; 2010.

Uzel A, Sorkun K, Onçağ O, Cogŭlu D, Gençay O, Salih B. Chemical compositions and antimicrobial activities of four different Anatolian propolis samples. Microbiol Res [Internet]. 2005; 160(2): 189-95. Available from: <http://www.sciencedirect.com/science/article/pii/S094450130500011X>. doi: http://dx.doi.org/10.1016/j.micres.2005.01.002

Downloads

Published

2015-07-07

Issue

Section

Microbiology

Most read articles by the same author(s)

1 2 3 > >>