Download PDF
CC BY 4.0 · Eur J Dent 2024; 18(02): 624-631
DOI: 10.1055/s-0043-1768466
Original Article

Marine Ascomycetes Extract Antifungal Susceptibility against Candida spp. Isolates from Oral Candidiasis HIV/AIDS Patient: An In Vitro Study

Alexander Patera Nugraha
1   Department of Orthodontic, Faculty of Dental Medicine - Universitas Airlangga, Surabaya, Indonesia
2   Immunology Study Programme, Postgraduate School, Universitas Airlangga, Surabaya, Indonesia
,
Mada Triandala Sibero
3   Department of Marine Science, Fac. of Fisheries and Marine Science, Diponegoro University, Semarang, Indonesia
,
Kindi Farabi
4   Department of Chemistry, Faculty of Mathematics and Natural Sciences, Universitas Padjadjaran, Indonesia
,
Meircurius Dwi Condro Surboyo 
5   Department of Oral Medicine, Faculty of Dental Medicine - Universitas Airlangga, Surabaya, Indonesia
,
Diah Savitri Ernawati
5   Department of Oral Medicine, Faculty of Dental Medicine - Universitas Airlangga, Surabaya, Indonesia
,
Tengku Natasha Eleena binti Tengku Ahmad Noor
6   Membership of Faculty of Dental Surgery, Royal Collage of Surgeon, Edinburgh University, United Kingdom
› Author Affiliations
› Further Information
Also available at
   Permissions and Reprints

Abstract

Objective The etiology of oral candidiasis (OC) was Candida albicans, C. krusei, C. dubliniensis, C. tropicalis that are frequently found in human immunodeficiency virus/ acquired immunodeficiency syndrome (HIV/AIDS) patients. Marine ascomycetes (MA) have been widely reported as an important producer of various antibiotic compounds. However, there is limited study of antifungal compounds from MA against Candida species. The aim of this study was to investigate the antifungal susceptibility of MA against Candida spp. isolates from OC HIV/AIDS patient.

Materials and Methods Trichoderma sp. is a sponge-associated fungus collected from Karimunjawa National Park, Central Java, Indonesia. The validation of C. albicans, C. krusei, C. dubliniensis, C. tropicalis. was done by ChromAgar. This study was true experimental with post-test only control group design; the sample was four replications for each group. Nystatin administration (K +), the golden standard antifungal drug, was used. The minimum fungicidal concentration (MFC), minimum inhibitory concentration (MIC), and diffusion zone methods were done. Analysis of variance difference test, and post-hoc Tukey's honest significant different were done to analyze the significant different between groups (p ≤ 0.05).

Results The MFC and MIC of MA against C. albicans, C. krusei, C. dubliniensis, and C. tropicalis were found at 12.5%. In addition, the greatest diffusion zone of MA against C. albicans, C. krusei, C. dubliniensis, and C. tropicalis was found at 12.5%. There is no appreciable difference in antifungal activity between K + and 12.5% of MA extract (p ≥ 0.05).

Conclusion Concentration of 12.5% MA extract has antifungal susceptibility against Candida spp. isolates from OC HIV/AIDS patient.

Keywords

Medicine - HIV/AIDS - Oral candidiasis - Marine Ascomycetes - Antifungal


Publication History

Article published online:
22 February 2024

© 2024. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution License, permitting unrestricted use, distribution, and reproduction so long as the original work is properly cited. (https://creativecommons.org/licenses/by/4.0/)

Thieme Medical and Scientific Publishers Pvt. Ltd.
A-12, 2nd Floor, Sector 2, Noida-201301 UP, India

 

  • References

  • 1 Nugraha AP, Ernawati DS, Parmadiati AE. et al. Prevalence of Candida species in oral candidiasis and correlation with CD4+ count in HIV/AIDS patients at Surabaya, Indonesia. J Int Dent Med Res 2018; 11 (01) 81-85
    Search in Google Scholar
  • 2 Mensana MP, Ernawati DS, Nugraha AP. et al. Oral candidiasis profile of the Indonesian HIV-infected pediatric patients at UPIPI Dr. Soetomo General Hospital, Surabaya, Indonesia. HIV AIDS Rev 2018; 17 (04) 272-277
    CrossrefSearch in Google Scholar
  • 3 Wicaksono S, Rezkita F, Wijaya FN, Nugraha AP, Winias S. Ellagic acid: an alternative for antifungal drugs resistance in HIV/AIDS patients with oropharyngeal candidiasis. HIV AIDS Rev 2020; 19 (03) 153-156
    CrossrefSearch in Google Scholar
  • 4 Mensana MP, Nugraha AP, Ernawati DS. et al. Correlation of Oral Hairy Leukoplakia, HAART and CD4+ in HIV-infected Pediatric Patients at UPIPI Soetomo Hospital Surabaya, Indonesia. J Int Dent Med Res 2019; 12 (01) 165-169
    Search in Google Scholar
  • 5 Nugraha AP, Mensana MP, Soebadi B. et al. Sensitivity and specificity of linear gingival erythema as immune suppression marker in pediatric HIV-infected at UPIPI Soetomo General Hospital Surabaya, Indonesia. Indian J Public Health Res Dev 2019; 10 (02) 575-580
    Search in Google Scholar
  • 6 Nugraha AP, Mensana MP, Soebadi B. et al. Correlation of low CD4+ counts with high dental caries prevalence in children living with perinatal HIV/AIDS undergoing antiretroviral therapy. Pesqui Bras Odontopediatria Clin Integr 2019; 19 (e4819): 1-7
    CrossrefSearch in Google Scholar
  • 7 Nugraha AP, Triyono EA, Prahasanti C, Sufiawati I, Prasetyo RA, Ernawati DS. The correlation of pathognomonic periodontal manifestation with CD4+ level in people live with human immunodeficiency virus/acquired immunodeficiency syndrome in a tertiary hospital, Surabaya, Indonesia. J Int Oral Health 2019; 11: 137-140
    CrossrefSearch in Google Scholar
  • 8 Baumgardner DJ. Oral fungal microbiota: to thrush and beyond. J Patient Cent Res Rev 2019; 6 (04) 252-261
    CrossrefPubMedSearch in Google Scholar
  • 9 Hu L, He C, Zhao C, Chen X, Hua H, Yan Z. Characterization of oral candidiasis and the Candida species profile in patients with oral mucosal diseases. Microb Pathog 2019; 134: 103575
    CrossrefPubMedSearch in Google Scholar
  • 10 Vila T, Sultan AS, Montelongo-Jauregui D, Jabra-Rizk MA. Oral candidiasis: a disease of opportunity. J Fungi (Basel) 2020; 6 (01) 1
    CrossrefPubMedSearch in Google Scholar
  • 11 Shekatkar M, Kheur S, Gupta AA. et al. Oral candidiasis in human immunodeficiency virus-infected patients under highly active antiretroviral therapy. Dis Mon 2021; 67 (09) 101169
    CrossrefPubMedSearch in Google Scholar
  • 12 Du X, Xiong H, Yang Y, Yan J, Zhu S, Chen F. Dynamic study of oral Candida infection and immune status in HIV infected patients during HAART. Arch Oral Biol 2020; 115: 104741
    CrossrefPubMedSearch in Google Scholar
  • 13 Murtiastutik D, Maharani CS, Rahmadewi R. Profile of Candida resistancy to fluconazole in male patient with oral candidiasis and HIV/AIDS. J AIDS Clin Res 2019; 10: 790
    Search in Google Scholar
  • 14 Paul S, Kannan I. Molecular identification and antifungal susceptibility pattern of Candida species isolated from HIV infected patients with candidiasis. Curr Med Mycol 2019; 5 (01) 21-26
    PubMedSearch in Google Scholar
  • 15 Revianti S, Andriani D, Pargaputri AF, Hartono MR. Acanthus ilicifolius methanolic extract for oral candidiasis treatment through tongue epithelial STAT3 and cell death evaluation. Eur J Dent 2023; 17 (04) 1201-1206
    Thieme ConnectPubMedSearch in Google Scholar
  • 16 de Barros PP, Rossoni RD, de Souza CM, Scorzoni L, Fenley JC, Junqueira JC. Candida biofilms: an update on developmental mechanisms and therapeutic challenges. Mycopathologia 2020; 185 (03) 415-424
    CrossrefPubMedSearch in Google Scholar
  • 17 Kean R, Ramage G. Combined antifungal resistance and biofilm tolerance: the global threat of Candida auris . mSphere 2019; 4 (04) e00458-e19
    CrossrefPubMedSearch in Google Scholar
  • 18 Hadadi-Fishani M, Shakerimoghaddam A, Khaledi A. Candida coinfection among patients with pulmonary tuberculosis in Asia and Africa; a systematic review and meta-analysis of cross-sectional studies. Microb Pathog 2020; 139: 103898
    CrossrefPubMedSearch in Google Scholar
  • 19 Segrelles-Calvo G, de S Araújo GR, Llopis-Pastor E. et al. Candida spp. co-infection in COVID-19 patients with severe pneumonia: prevalence study and associated risk factors. Respir Med 2021; 188: 106619
    CrossrefPubMedSearch in Google Scholar
  • 20 Tarapan S, Matangkasombut O, Trachootham D. et al. Oral Candida colonization in xerostomic postradiotherapy head and neck cancer patients. Oral Dis 2019; 25 (07) 1798-1808
    CrossrefPubMedSearch in Google Scholar
  • 21 Nugraha AP, Ernawati DS, Parmadiati AE. et al. Study of drug utilization within an anti-fungal therapy for HIV/AIDS patients presenting oral candidiasis at UPIPI RSUD, Dr. Soetomo Hospital Surabaya. J Int Dent Med Res 2018; 11 (01) 131-134
    Search in Google Scholar
  • 22 Kharisma VD, Widyananda MH, Ansori ANM, Nege AS, Naw SW, Nugraha AP. Tea catechin as antiviral agent via apoptosis agonist and triple inhibitor mechanism against HIV-1 infection: a bioinformatics approach. J Pharm Pharmacogn Res 2021; 9 (04) 435-445
    CrossrefSearch in Google Scholar
  • 23 Indraningrat AA, Smidt H, Sipkema D. Bioprospecting sponge-associated microbes for antimicrobial compounds. Mar Drugs 2016; 14 (05) 87
    CrossrefPubMedSearch in Google Scholar
  • 24 Procópio RE, Silva IR, Martins MK, Azevedo JL, Araújo JM. Antibiotics produced by Streptomyces. Braz J Infect Dis 2012; 16 (05) 466-471
    CrossrefPubMedSearch in Google Scholar
  • 25 Mahmoud HM, Kalendar AA. Coral-associated actinobacteria: diversity, abundance, and biotechnological potentials. Front Microbiol 2016; 7: 204
    CrossrefPubMedSearch in Google Scholar
  • 26 Sun W, Peng C, Zhao Y, Li Z. Functional gene-guided discovery of type II polyketides from culturable actinomycetes associated with soft coral Scleronephthya sp. PLoS One 2012; 7 (08) e42847
    CrossrefPubMedSearch in Google Scholar
  • 27 Zhang Z, Sibero MT, Kai A, Fukaya K, Urabe D, Igarashi Y. TMKS8A, an antibacterial and cytotoxic chlorinated α-lapachone, from a sea slug-derived actinomycete of the genus Streptomyces. J Antibiot (Tokyo) 2021; 74 (07) 464-469
    CrossrefPubMedSearch in Google Scholar
  • 28 Zhang Z, Zhou T, Harunari E, Oku N, Igarashi Y. Iseolides A-C, antifungal macrolides from a coral-derived actinomycete of the genus Streptomyces. J Antibiot (Tokyo) 2020; 73 (08) 534-541
    CrossrefPubMedSearch in Google Scholar
  • 29 Zhang B, Zhang T, Xu J. et al. Marine sponge-associated fungi as potential novel bioactive natural product sources for drug discovery: a review. Mini Rev Med Chem 2020; 20 (19) 1966-2010
    CrossrefPubMedSearch in Google Scholar
  • 30 Kusumawati P, Murti YB, Wijayanti N. Screening of anti-Candida albicans metabolites produced by marine sponge-associated bacteria. Mar Res Indones 2020; 45 (02) 47-58
    CrossrefSearch in Google Scholar
  • 31 Cheng Y, Chen N, Li J. et al. Antimicrobial chlorinated carbazole alkaloids from the sponge-associated actinomycete Streptomyces diacarni LHW51701. Chin J Chem 2021; 39: 1188-1192
    CrossrefSearch in Google Scholar
  • 32 Sibero MT, Zhou T, Fukaya K. et al. Two new aromatic polyketides from a sponge-derived Fusarium . Beilstein J Org Chem 2019; 15: 2941-2947
    CrossrefPubMedSearch in Google Scholar
  • 33 Balouiri M, Sadiki M, Ibnsouda SK. Methods for in vitro evaluating antimicrobial activity: a review. J Pharm Anal 2016; 6 (02) 71-79
    CrossrefPubMedSearch in Google Scholar
  • 34 Clinical and Laboratory Standards Institute. Performance Standards for Antifungal Susceptibility Testing of Yeasts. 2nd ed. Wayne, Pennsylvania, United States: Clinical and Laboratory Standard Institute; 2020
    Search in Google Scholar
  • 35 Jakubiec-Krzesniak K, Rajnisz-Mateusiak A, Guspiel A, Ziemska J, Solecka J. Secondary metabolites of actinomycetes and their antibacterial, antifungal and antiviral properties. Pol J Microbiol 2018; 67 (03) 259-272
    CrossrefPubMedSearch in Google Scholar
  • 36 Santajit S, Indrawattana N. Mechanisms of antimicrobial resistance in ESKAPE pathogens. BioMed Res Int 2016; 2016: 2475067
    CrossrefPubMedSearch in Google Scholar
  • 37 Prompanya C, Fernandes C, Cravo S. et al. A new cyclic hexapeptide and a new isocoumarin derivative from the marine sponge-associated fungus Aspergillus similanensis KUFA 0013. Mar Drugs 2015; 13 (03) 1432-1450
    CrossrefPubMedSearch in Google Scholar
  • 38 Saadouli I, Zendah El Euch I, Trabelsi E. et al. Isolation, characterization and chemical synthesis of large spectrum antimicrobial cyclic dipeptide (l-leu-l-pro) from Streptomyces misionensisV16R3Y1 Bacteria Extracts. A novel 1H NMR metabolomic approach. Antibiotics (Basel) 2020; 9 (05) 270
    CrossrefPubMedSearch in Google Scholar
  • 39 Raissa G, Waturangi DE, Wahjuningrum D. Screening of antibiofilm and anti-quorum sensing activity of Actinomycetes isolates extracts against aquaculture pathogenic bacteria. BMC Microbiol 2020; 20 (01) 343
    CrossrefPubMedSearch in Google Scholar
  • 40 Sibero MT, Sabdaningsih A, Cristianawati O. et al. Isolation, identification and screening antibacterial activity from marine sponge-associated fungi against multidrug- resistant (MDR) Escherichia coli. IOP Conf Ser Earth Environ Sci 2017; 55: 012028
    CrossrefSearch in Google Scholar
  • 41 Zhao X, Yu Z, Ding T. Quorum-sensing regulation of antimicrobial resistance in bacteria. Microorganisms 2020; 8 (03) 425
    CrossrefPubMedSearch in Google Scholar
  • 42 Sibero MT, Herdikiawan D, Radjasa OK, Sabdono A, Trianto A, Triningsih DW. Antibacterial activity of sponge associated fungi against vibriosis agents in shrimp and its toxicity to Litopenaeus vannamei. AAC Bioflux 2018; 11 (01) 10-18
    Search in Google Scholar
  • 43 Norouzi H, Danesh A, Mohseni M, Rabbani Khorasgani M. Marine actinomycetes with probiotic potential and bioactivity against multidrug-resistant bacteria. Int J Mol Cell Med 2018; 7 (01) 44-52
    PubMedSearch in Google Scholar
  • 44 Fairlamb AH, Gow NA, Matthews KR, Waters AP. Drug resistance in eukaryotic microorganisms. Nat Microbiol 2016; 1 (07) 16092
    CrossrefPubMedSearch in Google Scholar
  • 45 van der Linden JW, Arendrup MC, Melchers WJ, Verweij PE. Azole resistance of Aspergillus fumigatus in immunocompromised patients with invasive Aspergillosis. Emerg Infect Dis 2016; 22 (01) 158-159
    CrossrefPubMedSearch in Google Scholar
  • 46 Clardy J, Fischbach MA, Currie CR. The natural history of antibiotics. Curr Biol 2009; 19 (11) R437-R441
    CrossrefPubMedSearch in Google Scholar
  • 47 Newman DJ, Cragg GM. Natural products as sources of new drugs over the nearly four decades from 01/1981 to 09/2019. J Nat Prod 2020; 83 (03) 770-803
    CrossrefPubMedSearch in Google Scholar
  • 48 Saputra G, Nugraha AP, Rosari FS. et al. Mangrove ethanol extract (Aegiceras corniculatum) failed to inhibit Candida albicans growth isolated from oral candidiasis HIV/AIDS patient in vitro. J Int Dental Medical Res 2022; 15 (03) 1236-1241
    Search in Google Scholar
  • 49 Asnani A, Luviriani E, Oedjijono O. Activity of actinomycetes isolated from Mangrove Segara Anakan Cilacap toward Methicillin-resistant Staphylococcus aureus (MRSA). Journal Kimia Sains Dan Aplikasi 2020; 23 (01) 1-7
    CrossrefSearch in Google Scholar
  • 50 Geraldi A, Wardana AP, Aminah NS. et al. Tropical medicinal plant extracts from Indonesia as antifungal agents against Candida Albicans . Front Biosci 2022; 27 (09) 274
    CrossrefPubMedSearch in Google Scholar
  • 51 Hassan SSU, Shaikh AL. Marine actinobacteria as a drug treasure house. Biomed Pharmacother 2017; 87: 46-57
    CrossrefPubMedSearch in Google Scholar