The emergence of decreased activity of amphotericin B and voriconazole against clinical isolates of Aspergillus species: a subtropical region of the Middle East
Main Article Content
Keywords
Aspergillosis, Aspergillus, MIC, Antifungal, Middle East
Abstract
Introduction: Aspergillus species are a group of opportunistic molds that can cause various types of aspergillosis in individuals, particularly those with weakened immune systems. In recent years, there have been increasing reports of antifungal resistance among clinical isolates of Aspergillus. Objective: This study aims to determine the in vitro antifungal susceptibility patterns of Aspergillus clinical isolates causing human infections in a subtropical region of the Middle East.
Methods: In this study, the minimum inhibitory/effective concentrations (MICs/MECs) of four antifungal agents (amphotericin B, itraconazole, voriconazole, and caspofungin) were determined using the CLSI M38-A2 broth microdilution method for 60 clinical Aspergillus isolates, including A. flavus (n=39), A. niger (n=9), A. fumigatus (n=6), A. tubingensis (n=5), and A. oryzae (n=1). Statistical analysis was performed using the Chi-square test in SPSS 20 software.
Results: The MEC range for caspofungin was 0.007-4 µg/ml, with a geometric mean (GM) of 0.45 µg/ml. For itraconazole, voriconazole, and amphotericin B, the MIC ranges were 0.031-4 µg/ml, 0.5-4 µg/ml, and 1-4 µg/ml, respectively, with GMs of 1.21 µg/ml, 2.51 µg/ml, and 3.43 µg/ml, respectively.
Conclusion: Among the antifungal agents tested, caspofungin was the most effective against all Aspergillus clinical isolates, while amphotericin B and voriconazole were the least effective. A. flavus, A. niger, and A. tubingensis were more susceptible to caspofungin, whereas A. fumigatus was more susceptible to itraconazole.
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Najafzadeh, Mohammad Javad, Somayeh Dolatabadi, Hossein Zarrinfar and Jos Houbraken. 2021b. "Molecular Diversity of Aspergilli in Two Iranian Hospitals." Mycopathologia:1-15.
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Shivaprakash, MR, Erik Geertsen, Arunaloke Chakrabarti, Johan W Mouton and Jacques F Meis. 2011. "In Vitro Susceptibility of 188 Clinical and Environmental Isolates of Aspergillus Flavus for the New Triazole Isavuconazole and Seven Other Antifungal Drugs." Mycoses 54(5):e583-e89.
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Silvanose, Christudas, TA Bailey and Antonio Di Somma. 2011. "In Vitro Sensitivity of Aspergillus Species Isolated from Respiratory Tract of Falcons." Online veterinary journal 6.
Taheri Rizi, Zahra, Mahdi Abastabar, Hamed Fakhim, Macit Ilkit, Fatemeh Ahangarkani, Javad Javidnia, Iman Haghani, Jacques F Meis and Hamid Badali. 2020. "Antifungal Activity of a Novel Triazole, Efinaconazole and Nine Comparators against 354 Molecularly Identified Aspergillus Isolates." Mycopathologia 185(2):357-65.
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Xu, Xue, Ali Naseri, Jos Houbraken, Farzaneh Akbari, Xiaodong Wang, Rongfen Zhao, Hong Zhang, Mohammad Javad Najafzadeh and Shuwen Deng. 2021. "Identification and in Vitro Antifungal Susceptibility of Causative Agents of Onychomycosis Due to Aspergillus Species in Mashhad, Iran." Scientific reports 11(1):1-8.
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Abastabar, Mahdi, Nooshin Rahimi, Jacques F Meis, Narges Aslani, Sadegh Khodavaisy, Mojtaba Nabili, Ali Rezaei-Matehkolaei, Koichi Makimura and Hamid Badali. 2016. "Potent Activities of Novel Imidazoles Lanoconazole and Luliconazole against a Collection of Azole-Resistant and-Susceptible Aspergillus Fumigatus Strains." Antimicrob Agents Chemother 60(11):6916-19.
Ahangarkani, F., Y. Puts and M. Nabili. 2020. "First Azole-Resistant Aspergillus Fumigatus Isolates with the Environmental Tr(46) /Y121f/T289a Mutation in Iran." 63(5):430-36. doi: 10.1111/myc.13064.
Al-Wathiqi, F., S. Ahmad and Z. Khan. 2013. "Molecular Identification and Antifungal Susceptibility Profile of Aspergillus Flavus Isolates Recovered from Clinical Specimens in Kuwait." BMC Infect Dis 13:126. doi: 10.1186/1471-2334-13-126.
Alborzi, Abdolvahab, Mahsa Moeini and Pedram Haddadi. 2012. "Antifungal Susceptibility of the Aspergillus Species by Etest and Clsi Reference Methods." Archives of Iranian medicine 15(7):429.
Arabatzis, Michael, Manousos Kambouris, Miltiades Kyprianou, Aikaterini Chrysaki, Maria Foustoukou, Maria Kanellopoulou, Lydia Kondyli, Georgia Kouppari, Chrysa Koutsia-Karouzou and Evangelia Lebessi. 2011. "Polyphasic Identification and Susceptibility to Seven Antifungals of 102 Aspergillus Isolates Recovered from Immunocompromised Hosts in Greece." Antimicrob Agents Chemother 55(6):3025-30.
Araujo, Ricardo, Cidalia Pina-Vaz and Acacio Gonçalves Rodrigues. 2007. "Susceptibility of Environmental Versus Clinical Strains of Pathogenic Aspergillus." International journal of antimicrobial agents 29(1):108-11.
Badali, Hamid, Hamed Fakhim, Fereshteh Zarei, Mojtaba Nabili, Afsane Vaezi, Nafiseh Poorzad, Somayeh Dolatabadi and Hossein Mirhendi. 2016. "In Vitro Activities of Five Antifungal Drugs against Opportunistic Agents of Aspergillus Nigri Complex." Mycopathologia 181(3-4):235-40.
Beardsley, Justin, Catriona L Halliday, Sharon CA Chen and Tania C Sorrell. 2018. "Responding to the Emergence of Antifungal Drug Resistance: Perspectives from the Bench and the Bedside." Future microbiology 13(10):1175-91.
Colozza, Camilla, Brunella Posteraro, Stefania Santilli, Elena De Carolis, Maurizio Sanguinetti and Corrado Girmenia. 2012. "In Vitro Activities of Amphotericin B and Ambisome against Aspergillus Isolates Recovered from Italian Patients Treated for Haematological Malignancies." International journal of antimicrobial agents 39(5):440-43.
Dagenais, Taylor RT and Nancy P Keller. 2009. "Pathogenesis of Aspergillus Fumigatus in Invasive Aspergillosis." Clin Microbiol Rev 22(3):447-65.
Diekema, DJ, SA Messer, RJ Hollis, RN Jones and MA Pfaller. 2003. "Activities of Caspofungin, Itraconazole, Posaconazole, Ravuconazole, Voriconazole, and Amphotericin B against 448 Recent Clinical Isolates of Filamentous Fungi." J Clin Microbiol 41(8):3623-26.
Erjavec, Z., H. Kluin-Nelemans and P. E. Verweij. 2009. "Trends in Invasive Fungal Infections, with Emphasis on Invasive Aspergillosis." Clin Microbiol Infect 15(7):625-33. doi: 10.1111/j.1469-0691.2009.02929.x.
Gheith, S., F. Saghrouni, W. Bannour, Y. Ben Youssef, A. Khelif, A. C. Normand, R. Piarroux, M. Ben Said, M. Njah and S. Ranque. 2014. "In Vitro Susceptibility to Amphotericin B, Itraconazole, Voriconazole, Posaconazole and Caspofungin of Aspergillus Spp. Isolated from Patients with Haematological Malignancies in Tunisia." Springerplus 3:19. doi: 10.1186/2193-1801-3-19.
Gonçalves, Sarah S, Alberto M Stchigel, Josep Cano, Josep Guarro and Arnaldo L Colombo. 2013. "In Vitro Antifungal Susceptibility of Clinically Relevant Species Belonging to Aspergillus Section Flavi." Antimicrob Agents Chemother 57(4):1944-47.
Hedayati, M. T., M. Taghizadeh-Armaki, H. Zarrinfar, A. Hoseinnejad, S. Ansari, M. Abastabar, H. Er, B. Özhak, D. Öğünç, M. Ilkit and S. Seyedmousavi. 2019. "Discrimination of Aspergillus Flavus from Aspergillus Oryzae by Matrix-Assisted Laser Desorption/Ionisation Time-of-Flight (Maldi-Tof) Mass Spectrometry." Mycoses 62(12):1182-88. doi: 10.1111/myc.13010.
Hoseinnejad, Akbar, Mohammad Taghi Hedayati, Maryam Moazeni, Mojtaba Taghizadeh Armaki, Mehdi Abastabar, Jabari Amiri, Mohammad Reza and Syed Mojtaba Syedmousavi. 2016. "Antifungal Susceptibility Testing of 90 Clinical and Environmental Isolates of Aspergillus Flavus to Voriconazole and Itraconazole." Journal of Mazandaran University of Medical Sciences 25(133):91-99.
Hosseinikargar, Neginsadat, Reza Basiri, Mohammad Asadzadeh, Mohammad Javad Najafzadeh and Hossein Zarrinfar. 2021. "First Report of Invasive Aspergillus Rhinosinusitis in a Critically Ill Covid-19 Patient Affected by Acute Myeloid Leukemia, Northeastern Iran." Clinical Case Reports 9(10):e04889. doi: https://doi.org/10.1002/ccr3.4889.
Hsueh, Po-Ren, Yeu-Jun Lau, Yin-Ching Chuang, Jen-Hsien Wan, Wen-Kuei Huang, Jainn-Ming Shyr, Jing-Jou Yan, Kwok-Woon Yu, Jiunn-Jong Wu and Wen-Chien Ko. 2005. "Antifungal Susceptibilities of Clinical Isolates of Candida Species, Cryptococcus Neoformans, and Aspergillus Species from Taiwan: Surveillance of Multicenter Antimicrobial Resistance in Taiwan Program Data from 2003." Antimicrob Agents Chemother 49(2):512-17.
Kashefi, Elham, Seyed Javad Seyedi, Kamiar Zomorodian, Zahra Zare Shahrabadi and Hossein Zarrinfar. 2021. "Successful Treatment of Pulmonary Aspergillosis Due to Aspergillus Fumigatus in a Child Affected by Systemic Lupus Erythematosus: A Case Report from Northeastern Iran." Clinical Case Reports 9(5):e04248-e48. doi: 10.1002/ccr3.4248.
Kousha, M, R Tadi and AO Soubani. 2011. "Pulmonary Aspergillosis: A Clinical Review." European Respiratory Review 20(121):156-74.
Li, Yali, Zhe Wan, Wei Liu and Ruoyu Li. 2015. "Identification and Susceptibility of Aspergillus Section Nigri in China: Prevalence of Species and Paradoxical Growth in Response to Echinocandins." J Clin Microbiol 53(2):702-05.
Lionakis, Michail S, Russell E Lewis, Harrys A Torres, Nathaniel D Albert, Issam I Raad and Dimitrios P Kontoyiannis. 2005. "Increased Frequency of Non-Fumigatus Aspergillus Species in Amphotericin B–or Triazole–Pre-Exposed Cancer Patients with Positive Cultures for Aspergilli." Diagnostic microbiology and infectious disease 52(1):15-20.
Meletiadis, Joseph, Rafal Al-Saigh, Aristea Velegraki, Thomas J Walsh, Emmanuel Roilides and Loukia Zerva. 2012. "Pharmacodynamic Effects of Simulated Standard Doses of Antifungal Drugs against Aspergillus Species in a New in Vitro Pharmacokinetic/Pharmacodynamic Model." Antimicrob Agents Chemother 56(1):403-10.
Mohammadi, Faezezeh, Seyed Jamal Hashemi, Seyed Mojtaba Seyedmousavi and Dorna Akbarzade. 2018. "Isolation and Characterization of Clinical Triazole Resistance Aspergillus Fumigatus in Iran." Iran J Public Health 47(7):994.
Nabili, Mojtaba, Tahereh Shokohi, Maryam Moazeni, Sadegh Khodavaisy, Masoud Aliyali, Parisa Badiee, Hossein Zarrinfar, Ferry Hagen and Hamid Badali. 2016. "High Prevalence of Clinical and Environmental Triazole-Resistant Aspergillus Fumigatus in Iran: Is It a Challenging Issue?". J Med Microbiol 65(6):468-75.
Najafzadeh, Mohammad Javad, Somayeh Dolatabadi, Hossein Zarrinfar and Jos Houbraken. 2021a. "Molecular Diversity of Aspergilli in Two Iranian Hospitals." Mycopathologia 186(4):519-33.
Najafzadeh, Mohammad Javad, Somayeh Dolatabadi, Hossein Zarrinfar and Jos Houbraken. 2021b. "Molecular Diversity of Aspergilli in Two Iranian Hospitals." Mycopathologia:1-15.
Nasrolahiomran, Ayatollah. 2018. "Evatuation of Drug Susceptibility of Aspergillus Species Isolated from Icu of Hospitals in Invitro." scientific journal of ilam university of medical sciences 25(6):130-40.
Oakley, Karen L, Caroline B Moore and David W Denning. 1998. "In Vitro Activity of the Echinocandin Antifungal Agent Ly303, 366 in Comparison with Itraconazole and Amphotericin B against Aspergillus Spp." Antimicrob Agents Chemother 42(10):2726-30.
Öz, Yasemin, Havva Gül Özdemir, Egemen Gökbolat, Nuri Kiraz, Macit Ilkit and Seyedmojtaba Seyedmousavi. 2016. "Time-Kill Kinetics and in Vitro Antifungal Susceptibility of Non-Fumigatus Aspergillus Species Isolated from Patients with Ocular Mycoses." Mycopathologia 181(3-4):225-33.
Pagano, Livio, Morena Caira, Anna Candoni, Massimo Offidani, Luana Fianchi, Bruno Martino, Domenico Pastore, Marco Picardi, Alessandro Bonini and Anna Chierichini. 2006. "The Epidemiology of Fungal Infections in Patients with Hematologic Malignancies: The Seifem-2004 Study." Haematologica 91(8):1068-75.
Pfaller, MA, SA Messer, L Boyken, C Rice, S Tendolkar, RJ Hollis and DJ Diekema. 2008. "In Vitro Survey of Triazole Cross-Resistance among More Than 700 Clinical Isolates of Aspergillus Species." J Clin Microbiol 46(8):2568-72.
Pfaller, Michael A. 2012. "Antifungal Drug Resistance: Mechanisms, Epidemiology, and Consequences for Treatment." The American journal of medicine 125(1):S3-S13.
Salah, H., M. Lackner, J. Houbraken, B. Theelen, C. Lass-Flörl, T. Boekhout, M. Almaslamani and S. J. Taj-Aldeen. 2019. "The Emergence of Rare Clinical Aspergillus Species in Qatar: Molecular Characterization and Antifungal Susceptibility Profiles." Front Microbiol 10:1677. doi: 10.3389/fmicb.2019.01677.
Salehi, M. and K. Ahmadikia. 2020. "Opportunistic Fungal Infections in the Epidemic Area of Covid-19: A Clinical and Diagnostic Perspective from Iran." 185(4):607-11. doi: 10.1007/s11046-020-00472-7.
Shivaprakash, MR, Erik Geertsen, Arunaloke Chakrabarti, Johan W Mouton and Jacques F Meis. 2011. "In Vitro Susceptibility of 188 Clinical and Environmental Isolates of Aspergillus Flavus for the New Triazole Isavuconazole and Seven Other Antifungal Drugs." Mycoses 54(5):e583-e89.
Shobana, Coimbatore Subramanian, A Mythili, Mónika Homa, L Galgóczy, R Priya, YR Babu Singh, K Panneerselvam, C Vágvölgyi, L Kredics and V Narendran. 2015. "In Vitro Susceptibility of Filamentous Fungi from Mycotic Keratitis to Azole Drugs." Journal de Mycologie Medicale 25(1):44-49.
Silvanose, Christudas, TA Bailey and Antonio Di Somma. 2011. "In Vitro Sensitivity of Aspergillus Species Isolated from Respiratory Tract of Falcons." Online veterinary journal 6.
Taheri Rizi, Zahra, Mahdi Abastabar, Hamed Fakhim, Macit Ilkit, Fatemeh Ahangarkani, Javad Javidnia, Iman Haghani, Jacques F Meis and Hamid Badali. 2020. "Antifungal Activity of a Novel Triazole, Efinaconazole and Nine Comparators against 354 Molecularly Identified Aspergillus Isolates." Mycopathologia 185(2):357-65.
Verweij, Paul E, Anuradha Chowdhary, Willem JG Melchers and Jacques F Meis. 2015. "Azole Resistance in Aspergillus Fumigatus: Can We Retain the Clinical Use of Mold-Active Antifungal Azoles?". Clinical Infectious Diseases 62(3):362-68.
Xu, Xue, Ali Naseri, Jos Houbraken, Farzaneh Akbari, Xiaodong Wang, Rongfen Zhao, Hong Zhang, Mohammad Javad Najafzadeh and Shuwen Deng. 2021. "Identification and in Vitro Antifungal Susceptibility of Causative Agents of Onychomycosis Due to Aspergillus Species in Mashhad, Iran." Scientific reports 11(1):1-8.
Zanganeh, Elnaz, Hossein Zarrinfar, Fariba Rezaeetalab, AbdolMajid Fata, Mohammad Tohidi, Mohammad Javad Najafzadeh, Majid Alizadeh and Seyedmojtaba Seyedmousavi. 2018. "Predominance of Non-Fumigatus Aspergillus Species among Patients Suspected to Pulmonary Aspergillosis in a Tropical and Subtropical Region of the Middle East." Microbial Pathogenesis 116:296-300.
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Jul 11, 2023
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Dehghani, R., Mohammadi, S., Zarrinfar, H., Jarahi, L., Najafzadeh, M. J., & Salah, H. (2023). The emergence of decreased activity of amphotericin B and voriconazole against clinical isolates of Aspergillus species: a subtropical region of the Middle East. Journal of Population Therapeutics and Clinical Pharmacology, 30(17), 146–154. https://doi.org/10.47750/jptcp.2023.30.17.011
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Author Biographies
Robabeh Dehghani
Department of Parasitology and Mycology, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran
Shirin Mohammadi
Department of Physiology, Faculty of Medicine, Kuwait University, Kuwait City, Kuwait
Hossein Zarrinfar
Associate professor of Medical Mycology, Allergy Research Center; Department of Medical Mycology and Parasitology; Faculty of Medicine; Mashhad University of Medical Sciences; Postal address: Ghaem Hospital, Mashhad, Iran
Lida Jarahi
Department of Community Medicine, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran
Mohammad Javad Najafzadeh
Department of Parasitology and Mycology, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran
Husam Salah
Division of Microbiology, Department of Laboratory Medicine and Pathology, Hamad Medical Corporation, Doha, Qatar