Distribution of fungal agents in the respiratory system of patients with underlying lung diseases; molecular identification and antifungal susceptibility profiles
-
Parviz Hassanpour
,
Seyed Jamal Hashemi
,
Sanam Nami
,
Roshanak Daie Ghazvini
,
Behrouz Naghili Hokmabadi
,
Abbas Rahimi Foroushani
,
Kazem Ahmadikia
,
Zahra Ramezanalipour
,
Saeid Firouzi Abriz
Abstract
Background and Objectives: Airway fungal infection is a severe clinical problem, especially in patients with compromised immune functions. Here, we examined the distribution and antifungal susceptibility profiles of fungal agents isolated from respiratory tract of symptomatic patients hospitalized in pulmonary units.
Materials and Methods: This descriptive cross-sectional study took place from 2023 to 2024, involving 360 patients. Bronchoalveolar lavage (BAL) or sputum specimens were collected and analyzed using mycological and molecular methods for this study. Antifungal susceptibility testing (AFST) was carried out using the broth micro dilution method.
Results: Of a total of 360 respiratory specimens, 114 (31.6%) were positive. The male-to-female ratio was 63:51 (1.3%). Candida albicans and Aspergillus flavus were the most common yeast and mold species. Chronic obstructive pulmonary disease (COPD) had the highest rate of colonization with fungal agents (47/114, 41%). The isolates associated with COPD in this study included Aspergillus species (4/12, 3.5%), Candida species (41/96, 36%), and other fungal species (2/6, 1.5%). Coughing (87%) was the predominant symptom, and malignancy (52%) was the predominant comorbidity factor. The result of AFST for antifungal agents showed that 9 (22.5%) Candida isolates were resistant, and the highest rate of resistance was related to voriconazole agent (5/9, 55.5%). Resistance to antifungal agents was not observed among Aspergillus isolates.
Conclusion: This study showed a significant relationship between the frequency of Aspergillus and Candida species in patients with underlying lung diseases. In addition, voriconazole was more effective than itraconazole, especially against Aspergillus flavus.
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3. Limper AH. The changing spectrum of fungal infections in pulmonary and critical care practice: clinical approach to diagnosis. Proc Am Thorac Soc 2010; 7: 163-168.
4. Kelly BT, Pennington KM, Limper AH. Advances in the diagnosis of fungal pneumonias. Expert Rev Respir Med 2020; 14: 703-714.
5. Biswas D, Agarwal S, Sindhwani G, Rawat J. Fungal colonization in patients with chronic respiratory diseases from Himalayan region of India. Ann Clin Microbiol Antimicrob 2010; 9: 28.
6. Ahmed MM, Farghaly AA, Raafata RH, Abd Elsattar WM. Study of the prevalence and pattern of fungal pneumonias in respiratory intensive care units. Egypt J Bronchol 2019; 13: 545-550.
7. Ardi P, Daie Ghazvini R, Hashemi SJ, Mobayen M, Pourheidari A, Khodavaisy S, et al. Identification of fungal agents isolated from burn lesions using mycological and molecular methods in patients admitted to Velayat burn hospital in Rasht city during 2022-2023. Iran J Microbiol 2024; 16: 490-496.
8. Hassanpour P, Spotin A, Morovati H, Aghebati-Maleki L, Raeisi M, Rezaee MA, et al. Molecular diagnosis, phylogenetic analysis, and antifungal susceptibility profiles of Candida species isolated from neutropenic oncological patients. BMC Infect Dis 2023; 23: 765.
9. Prabha TR, Revathi k, Vinod MS, Shanthakumar SP, Paul Bernard. A simple method for total genomic DNA extraction from water moulds. Curr Sci 2013; 104: 345-347.
10. Silva GAd, Bernardi TL, Schaker PDC, Menegotto M, Valente P. Rapid yeast DNA extraction by boiling and freeze-thawing without using chemical reagents and DNA purification. Braz Arch Biol Technol 2012; 55: 319-327.
11. Ezeonuegbu BA, Abdullahi MD, Whong CMZ, Sohunago JW, Kassem HS, Yaro CA, et al. Characterization and phylogeny of fungi isolated from industrial wastewater using multiple genes. Sci Rep 2022; 12: 2094.
12. Shokohi T, Hashemi Soteh MB, Saltanat Pouri Z, Hedayati MT, Mayahi S. Identification of Candida species using PCR-RFLP in cancer patients in Iran. Indian J Med Microbiol 2010; 28: 147-151.
13. Pfaller MA, Diekema DJ. Progress in antifungal susceptibility testing of Candida spp. by use of Clinical and Laboratory Standards Institute broth microdilution methods, 2010 to 2012. J Clin Microbiol 2012; 50: 2846-2856.
14. Wayne P. Reference method for broth dilution antifungal susceptibility testing of yeasts, approved standard. CLSI document M27-A2, 2002.
15. Fothergill AW (2012). Antifungal Susceptibility Testing: Clinical Laboratory and Standards Institute (CLSI) Methods. in (Ed: Hall GS), Interactions of Yeasts, Moulds, and Antifungal Agents. In: Interactions of Yeasts, Moulds, and Antifungal Agents. pp. 65-74.
16. Roudbary M, Keyvani H, Mousavi SAJ, Esghaei M, Roudbarmohammadi S, Hedayati N, et al. Investigation of fungal colonization among iranian patients with idiopathic pulmonary fibrosis; molecular identification and antifungal susceptibility pattern. Arch Clin Infect Dis 2019; 14(2): e65758.
17. CLSI. Epidemiological Cuttoff Values for Antifungal Susceptibility Testing, 2nd ed.; CLSI supplement M59; Clinical and Laboratory Standards Institute: Wayne, PA, USA, 2018.
18. Rafat Z, Hashemi SJ, Ashrafi K, Nikokar I, Jafari A, Rahimi Foroushani A, et al. Fungal isolates of the respiratory tract in symptomatic patients hospitalized in pulmonary units: a mycological and molecular epidemiologic study. J Multidiscip Healthc 2020; 13: 661-669.
19. Roohani AH, Fatima N, Shameem M, Khan HM, Khan PA, Akhtar A. Comparing the profile of respiratory fungal pathogens amongst immunocompetent and immunocompromised hosts, their susceptibility pattern and correlation of various opportunistic respiratory fungal infections and their progression in relation to the CD4+ T-cell counts. Indian J Med Microbiol 2018; 36: 408-415.
20. Shahi M, Ayatollahi Mousavi SA, Nabili M, Aliyali M, Khodavaisy S, Badali H. Aspergillus colonization in patients with chronic obstructive pulmonary disease. Curr Med Mycol 2015; 1: 45-51.
21. Taghizadeh Armaki M, Hedayati MT, Mahdavi Omran S, Saber S, Abastabar M, Hosseinnejad A. Identification and antifungal susceptibility testing of Candida species isolated from bronchoalveolar lavage samples. Int J Mol Clin Microbiol 2014; 1: 358-364.
22. Knoll MA, Steixner S, Lass-Flörl C. How to use direct microscopy for diagnosing fungal infections. Clin Microbiol Infect 2023; 29: 1031-1038.
23. Moglad E, Saeed S, Saeed H, Ahmed H, Salih K, Altayb H, et al. Molecular characterization and antifungal susceptibility of Aspergillus spp. among patients with underlying lung diseases. Trop Med Infect Dis 2022; 7: 274.
24. Paugam A, Baixench MT, Lebuisson A, Dupouy-Camet J. Diagnosis of invasive pulmonary aspergillosis: value of bronchoalveolar lavage galactomannan for immunocompromised patients. Pathol Biol (Paris) 2009; 58: 100-103.
25. Agossou M, Inamo J, Ahouansou N, Dufeal M, Provost M, Badaran E, et al. Frequency and distribution of Broncho-Alveolar fungi in lung diseases in martinique. J Clin Med 2023; 12: 5480.
26. Njunda AL, Ewang AA, Kamga L-HF, Nsagha DC, Assob J-CN, Ndah DA, et al. Respiratory tract Aspergillosis in the sputum of patients suspected of tuberculosis in Fako division-Cameroon. J Microbiol Res 2012; 2: 68-72.
27. Khodavaisy S, Hedayati MT, Alialy M, Habibi MR, Badali H. Detection of galactomannan in bronchoalveolar lavage of the intensive care unit patients at risk for invasive aspergillosis. Curr Med Mycol 2015; 1: 12-17.
28. Markussen DL, Ebbesen M, Serigstad S, Knoop ST, Ritz C, Bjørneklett R, et al. The diagnostic utility of microscopic quality assessment of sputum samples in the era of rapid syndromic PCR testing. Microbiol Spectr 2023; 11(5): e0300223.
29. Spahr J, Weiner DJ, Stokes DC, Kurland G (2019). 64-Pulmonary Disease in the pediatric patient with acquired immunodeficiency states. In: Kendig’s Disorders of the Respiratory Tract in Children (Ninth Edition). Elsevier. pp. 923-943.e7. https://www.sciencedirect.com/science/article/abs/pii/B978032344887100064X
30. Mohammadi F, Hashemi SJ, Seyedmousavi SM, Akbarzade D. Isolation and characterization of clinical triazole resistance Aspergillus fumigatus in Iran. Iran J Public Health 2018; 47: 994-1000.
31. Badiee P, Boekhout T, Zarei Mahmoudabadi A, Mohammadi R, Ayatollahi Mousavi SA, Najafzadeh MJ, et al. Multicenter study of susceptibility of Aspergillus species isolated from Iranian university hospitals to seven antifungal agents. Microbiol Spectr 2022; 10(3): e0253921.
32. Chadeganipour M, Mohammadi R. A 9-Year experience of Aspergillus infections from Isfahan, Iran. Infect Drug Resist 2020; 13: 2301-2309.
33. Otu A, Kosmidis C, Mathioudakis AG, Ibe C, Denning DW. The clinical spectrum of Aspergillosis in chronic obstructive pulmonary disease. Infection 2023; 51: 813-829.
34. Muni S, Rajpal K, Kumar R, Kumari R, Sinha R, Kumar S, et al. Identification of fungal isolates in patients with pulmonary tuberculosis treated at a tertiary Care hospital. Cureus 2023; 15(4): e37664.
35. Sethi S. Infection as a comorbidity of COPD. Eur Respir J 2010; 35: 1209-1215.
36. Guinea J, Torres-Narbona M, Gijón P, Muñoz P, Pozo F, Peláez T, et al. Pulmonary aspergillosis in patients with chronic obstructive pulmonary disease: incidence, risk factors, and outcome. Clin Microbiol Infect 2010; 16: 870-877.
37. Delisle MS, Williamson DR, Perreault MM, Albert M, Jiang X, Heyland DK. The clinical significance of Candida colonization of respiratory tract secretions in critically ill patients. J Crit Care 2008; 23: 11-17.
38. Yenisehirli G, Bulut N, Yenisehirli A, Bulut Y. In vitro susceptibilities of Candida albicans isolates to antifungal agents in Tokat, Turkey. Jundishapur J Microbiol 2015; 8(9): e28057.
39. Kan S, Song N, Pang Q, Mei H, Zheng H, Li D, et al. In vitro antifungal activity of azoles and other antifungal agents against pathogenic yeasts from vulvovaginal Candidiasis in China. Mycopathologia 2023; 188: 99-109.
40. Mora-Lee D, Jaikel-Víquez D, Gross NT. In vitro antifungal susceptibility of Candida spp. Acta Méd Costarric 2023; 65: 77-84.
41. Lestrade PPA, Meis JF, Melchers WJG, Verweij PE. Triazole resistance in Aspergillus fumigatus: recent insights and challenges for patient management. Clin Microbiol Infect 2019; 25: 799-806.
42. Rivero-Menendez O, Alastruey-Izquierdo A, Mellado E, Cuenca-Estrella M. Triazole resistance in Aspergillus spp.: a worldwide problem? J Fungi (Basel) 2016; 2: 21.
43. Meis JF, Chowdhary A, Rhodes JL, Fisher MC, Verweij PE. Clinical implications of globally emerging azole resistance in Aspergillus fumigatus. Philos Trans R Soc Lond B Biol Sci 2016; 371: 20150460.
44. Jafari Z, Motamedi M, Jalalizand N, Shokoohi GR, Charsizadeh A, Mirhendi H. Comparison of CHROMagar, polymerase chain reaction-restriction fragment length polymorphism, and polymerase chain reaction-fragment size for the identification of Candida species. Curr Med Mycol 2017; 3: 10-15.
45. Al-jader ZW, Ado JM. Molecular detection and identification of Candida Species isolates from oral by RFLP-PCR. J Res Appl Sci Biotechnol 2023; 2: 137-144.
46. Ashtiani NM, Kachuei R, Yalfani R, Harchegani AB, Nosratabadi M. Identification of Aspergillus sections Flavi, Nigri, and fumigati and their differentiation using specific primers. Infez Med 2017; 25: 127-132.
47. Machowicz-Matejko E, Furmańczyk A, Zalewska ED. Aspergillus penicillioides speg. implicated in keratomycosis. Pol J Microbiol 2018; 67: 407-416.
48. Samson RA, Visagie CM, Houbraken J, Hong SB, Hubka V, Klaassen CH, et al. Phylogeny, identification and nomenclature of the genus Aspergillus. Stud Mycol 2014; 78: 141-173.
2. Tonui J, Mureithi M, Jaoko W, Bii C. In vitro antifungal susceptibility of yeasts and molds isolated from sputum of tuberculosis relapse and retreatment patients. Pan Afr Med J 2021; 38: 227.
3. Limper AH. The changing spectrum of fungal infections in pulmonary and critical care practice: clinical approach to diagnosis. Proc Am Thorac Soc 2010; 7: 163-168.
4. Kelly BT, Pennington KM, Limper AH. Advances in the diagnosis of fungal pneumonias. Expert Rev Respir Med 2020; 14: 703-714.
5. Biswas D, Agarwal S, Sindhwani G, Rawat J. Fungal colonization in patients with chronic respiratory diseases from Himalayan region of India. Ann Clin Microbiol Antimicrob 2010; 9: 28.
6. Ahmed MM, Farghaly AA, Raafata RH, Abd Elsattar WM. Study of the prevalence and pattern of fungal pneumonias in respiratory intensive care units. Egypt J Bronchol 2019; 13: 545-550.
7. Ardi P, Daie Ghazvini R, Hashemi SJ, Mobayen M, Pourheidari A, Khodavaisy S, et al. Identification of fungal agents isolated from burn lesions using mycological and molecular methods in patients admitted to Velayat burn hospital in Rasht city during 2022-2023. Iran J Microbiol 2024; 16: 490-496.
8. Hassanpour P, Spotin A, Morovati H, Aghebati-Maleki L, Raeisi M, Rezaee MA, et al. Molecular diagnosis, phylogenetic analysis, and antifungal susceptibility profiles of Candida species isolated from neutropenic oncological patients. BMC Infect Dis 2023; 23: 765.
9. Prabha TR, Revathi k, Vinod MS, Shanthakumar SP, Paul Bernard. A simple method for total genomic DNA extraction from water moulds. Curr Sci 2013; 104: 345-347.
10. Silva GAd, Bernardi TL, Schaker PDC, Menegotto M, Valente P. Rapid yeast DNA extraction by boiling and freeze-thawing without using chemical reagents and DNA purification. Braz Arch Biol Technol 2012; 55: 319-327.
11. Ezeonuegbu BA, Abdullahi MD, Whong CMZ, Sohunago JW, Kassem HS, Yaro CA, et al. Characterization and phylogeny of fungi isolated from industrial wastewater using multiple genes. Sci Rep 2022; 12: 2094.
12. Shokohi T, Hashemi Soteh MB, Saltanat Pouri Z, Hedayati MT, Mayahi S. Identification of Candida species using PCR-RFLP in cancer patients in Iran. Indian J Med Microbiol 2010; 28: 147-151.
13. Pfaller MA, Diekema DJ. Progress in antifungal susceptibility testing of Candida spp. by use of Clinical and Laboratory Standards Institute broth microdilution methods, 2010 to 2012. J Clin Microbiol 2012; 50: 2846-2856.
14. Wayne P. Reference method for broth dilution antifungal susceptibility testing of yeasts, approved standard. CLSI document M27-A2, 2002.
15. Fothergill AW (2012). Antifungal Susceptibility Testing: Clinical Laboratory and Standards Institute (CLSI) Methods. in (Ed: Hall GS), Interactions of Yeasts, Moulds, and Antifungal Agents. In: Interactions of Yeasts, Moulds, and Antifungal Agents. pp. 65-74.
16. Roudbary M, Keyvani H, Mousavi SAJ, Esghaei M, Roudbarmohammadi S, Hedayati N, et al. Investigation of fungal colonization among iranian patients with idiopathic pulmonary fibrosis; molecular identification and antifungal susceptibility pattern. Arch Clin Infect Dis 2019; 14(2): e65758.
17. CLSI. Epidemiological Cuttoff Values for Antifungal Susceptibility Testing, 2nd ed.; CLSI supplement M59; Clinical and Laboratory Standards Institute: Wayne, PA, USA, 2018.
18. Rafat Z, Hashemi SJ, Ashrafi K, Nikokar I, Jafari A, Rahimi Foroushani A, et al. Fungal isolates of the respiratory tract in symptomatic patients hospitalized in pulmonary units: a mycological and molecular epidemiologic study. J Multidiscip Healthc 2020; 13: 661-669.
19. Roohani AH, Fatima N, Shameem M, Khan HM, Khan PA, Akhtar A. Comparing the profile of respiratory fungal pathogens amongst immunocompetent and immunocompromised hosts, their susceptibility pattern and correlation of various opportunistic respiratory fungal infections and their progression in relation to the CD4+ T-cell counts. Indian J Med Microbiol 2018; 36: 408-415.
20. Shahi M, Ayatollahi Mousavi SA, Nabili M, Aliyali M, Khodavaisy S, Badali H. Aspergillus colonization in patients with chronic obstructive pulmonary disease. Curr Med Mycol 2015; 1: 45-51.
21. Taghizadeh Armaki M, Hedayati MT, Mahdavi Omran S, Saber S, Abastabar M, Hosseinnejad A. Identification and antifungal susceptibility testing of Candida species isolated from bronchoalveolar lavage samples. Int J Mol Clin Microbiol 2014; 1: 358-364.
22. Knoll MA, Steixner S, Lass-Flörl C. How to use direct microscopy for diagnosing fungal infections. Clin Microbiol Infect 2023; 29: 1031-1038.
23. Moglad E, Saeed S, Saeed H, Ahmed H, Salih K, Altayb H, et al. Molecular characterization and antifungal susceptibility of Aspergillus spp. among patients with underlying lung diseases. Trop Med Infect Dis 2022; 7: 274.
24. Paugam A, Baixench MT, Lebuisson A, Dupouy-Camet J. Diagnosis of invasive pulmonary aspergillosis: value of bronchoalveolar lavage galactomannan for immunocompromised patients. Pathol Biol (Paris) 2009; 58: 100-103.
25. Agossou M, Inamo J, Ahouansou N, Dufeal M, Provost M, Badaran E, et al. Frequency and distribution of Broncho-Alveolar fungi in lung diseases in martinique. J Clin Med 2023; 12: 5480.
26. Njunda AL, Ewang AA, Kamga L-HF, Nsagha DC, Assob J-CN, Ndah DA, et al. Respiratory tract Aspergillosis in the sputum of patients suspected of tuberculosis in Fako division-Cameroon. J Microbiol Res 2012; 2: 68-72.
27. Khodavaisy S, Hedayati MT, Alialy M, Habibi MR, Badali H. Detection of galactomannan in bronchoalveolar lavage of the intensive care unit patients at risk for invasive aspergillosis. Curr Med Mycol 2015; 1: 12-17.
28. Markussen DL, Ebbesen M, Serigstad S, Knoop ST, Ritz C, Bjørneklett R, et al. The diagnostic utility of microscopic quality assessment of sputum samples in the era of rapid syndromic PCR testing. Microbiol Spectr 2023; 11(5): e0300223.
29. Spahr J, Weiner DJ, Stokes DC, Kurland G (2019). 64-Pulmonary Disease in the pediatric patient with acquired immunodeficiency states. In: Kendig’s Disorders of the Respiratory Tract in Children (Ninth Edition). Elsevier. pp. 923-943.e7. https://www.sciencedirect.com/science/article/abs/pii/B978032344887100064X
30. Mohammadi F, Hashemi SJ, Seyedmousavi SM, Akbarzade D. Isolation and characterization of clinical triazole resistance Aspergillus fumigatus in Iran. Iran J Public Health 2018; 47: 994-1000.
31. Badiee P, Boekhout T, Zarei Mahmoudabadi A, Mohammadi R, Ayatollahi Mousavi SA, Najafzadeh MJ, et al. Multicenter study of susceptibility of Aspergillus species isolated from Iranian university hospitals to seven antifungal agents. Microbiol Spectr 2022; 10(3): e0253921.
32. Chadeganipour M, Mohammadi R. A 9-Year experience of Aspergillus infections from Isfahan, Iran. Infect Drug Resist 2020; 13: 2301-2309.
33. Otu A, Kosmidis C, Mathioudakis AG, Ibe C, Denning DW. The clinical spectrum of Aspergillosis in chronic obstructive pulmonary disease. Infection 2023; 51: 813-829.
34. Muni S, Rajpal K, Kumar R, Kumari R, Sinha R, Kumar S, et al. Identification of fungal isolates in patients with pulmonary tuberculosis treated at a tertiary Care hospital. Cureus 2023; 15(4): e37664.
35. Sethi S. Infection as a comorbidity of COPD. Eur Respir J 2010; 35: 1209-1215.
36. Guinea J, Torres-Narbona M, Gijón P, Muñoz P, Pozo F, Peláez T, et al. Pulmonary aspergillosis in patients with chronic obstructive pulmonary disease: incidence, risk factors, and outcome. Clin Microbiol Infect 2010; 16: 870-877.
37. Delisle MS, Williamson DR, Perreault MM, Albert M, Jiang X, Heyland DK. The clinical significance of Candida colonization of respiratory tract secretions in critically ill patients. J Crit Care 2008; 23: 11-17.
38. Yenisehirli G, Bulut N, Yenisehirli A, Bulut Y. In vitro susceptibilities of Candida albicans isolates to antifungal agents in Tokat, Turkey. Jundishapur J Microbiol 2015; 8(9): e28057.
39. Kan S, Song N, Pang Q, Mei H, Zheng H, Li D, et al. In vitro antifungal activity of azoles and other antifungal agents against pathogenic yeasts from vulvovaginal Candidiasis in China. Mycopathologia 2023; 188: 99-109.
40. Mora-Lee D, Jaikel-Víquez D, Gross NT. In vitro antifungal susceptibility of Candida spp. Acta Méd Costarric 2023; 65: 77-84.
41. Lestrade PPA, Meis JF, Melchers WJG, Verweij PE. Triazole resistance in Aspergillus fumigatus: recent insights and challenges for patient management. Clin Microbiol Infect 2019; 25: 799-806.
42. Rivero-Menendez O, Alastruey-Izquierdo A, Mellado E, Cuenca-Estrella M. Triazole resistance in Aspergillus spp.: a worldwide problem? J Fungi (Basel) 2016; 2: 21.
43. Meis JF, Chowdhary A, Rhodes JL, Fisher MC, Verweij PE. Clinical implications of globally emerging azole resistance in Aspergillus fumigatus. Philos Trans R Soc Lond B Biol Sci 2016; 371: 20150460.
44. Jafari Z, Motamedi M, Jalalizand N, Shokoohi GR, Charsizadeh A, Mirhendi H. Comparison of CHROMagar, polymerase chain reaction-restriction fragment length polymorphism, and polymerase chain reaction-fragment size for the identification of Candida species. Curr Med Mycol 2017; 3: 10-15.
45. Al-jader ZW, Ado JM. Molecular detection and identification of Candida Species isolates from oral by RFLP-PCR. J Res Appl Sci Biotechnol 2023; 2: 137-144.
46. Ashtiani NM, Kachuei R, Yalfani R, Harchegani AB, Nosratabadi M. Identification of Aspergillus sections Flavi, Nigri, and fumigati and their differentiation using specific primers. Infez Med 2017; 25: 127-132.
47. Machowicz-Matejko E, Furmańczyk A, Zalewska ED. Aspergillus penicillioides speg. implicated in keratomycosis. Pol J Microbiol 2018; 67: 407-416.
48. Samson RA, Visagie CM, Houbraken J, Hong SB, Hubka V, Klaassen CH, et al. Phylogeny, identification and nomenclature of the genus Aspergillus. Stud Mycol 2014; 78: 141-173.
| Files | ||
| Issue | Vol 16 No 6 (2024) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v16i6.17258 | |
| Keywords | ||
| Lung infection; Underlying lung diseases; Antifungal; Fungal agents; Polymerase chain reaction; Iran | ||
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How to Cite
1.
Hassanpour P, Hashemi SJ, Nami S, Daie Ghazvini R, Naghili Hokmabadi B, Rahimi Foroushani A, Ahmadikia K, Ramezanalipour Z, Firouzi Abriz S. Distribution of fungal agents in the respiratory system of patients with underlying lung diseases; molecular identification and antifungal susceptibility profiles. Iran J Microbiol. 2024;16(6):792-802.
