The prevalence of pediatric nosocomial fungal infections
,
Abstract
Background and Objectives: The aim of this study was to identify the incidence of nosocomial fungal infections in pediatric patients and evaluate the etiological agents, risk factors, and sites of infections.
Materials and Methods: Clinical samples were cultured to assess fungal colonization. When fungal nosocomial infections were suspected according to the European Organization for Research and Treatment of Cancer criteria, clinical samples were evaluated using direct microscopic, culture, and molecular methods. Susceptibility patterns of the isolates were evaluated according to the Clinical and Laboratory Standard Institute.
Results: From the 1450 patients, 190 cases (5.5%) were evaluated for nosocomial fungal infections. Candida colonization was observed in 35 (18.4%) patients. The rate of nosocomial fungal infections in pediatrics was 2.69% (12 cases with proven and 27 cases with probable infections, 39/1450). Bloodstream and lungs were the frequent infected sites of patients’ body. Aspergillus species (Aspergillus flavus and Aspergillus fumigatus), Candida species (Candida albicans, Candida parapsilosis, Candida glabrata) and Mucorales were the etiologic agents of infections. Caspofungin and luliconazole were effective antifungal agents for isolated fungi. The rate of mortality in infected patients suffering from proven and probable infections was 15.4% (6/39 cases).
Conclusion: Due to the high mortality rates of fungal infections in pediatrics, it is essential to identify modifiable risk factors, and implement control measures along with early detection techniques in pediatric populations.
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3. Zingg W, Hopkins S, Gayet-Ageron A, Holmes A, Sharland M, Suetens C, et al. Health-care-associated infections in neonates, children, and adolescents: an analysis of paediatric data from the European centre for disease Prevention and control point-prevalence survey. Lancet Infect Dis 2017; 17: 381-389.
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5. Reddy GKK, Padmavathi AR, Nancharaiah YV. Fungal infections: Pathogenesis, antifungals and alternate treatment approaches. Curr Res Microb Sci 2022; 3: 100137.
6. Badiee P, Hashemizadeh Z. Opportunistic invasive fungal infections: diagnosis & clinical management. Indian J Med Res 2014; 139: 195-204.
7. Bassetti M, Azoulay E, Kullberg BJ, Ruhnke M, Shoham S, Vazquez J, et al. EORTC/MSGERC Definitions of Invasive Fungal diseases: Summary of Activities of the Intensive care unit working group. Clin Infect Dis 2021; 72(Suppl 2): S121-S127.
8. Donnelly JP, Chen SC, Kauffman CA, Steinbach WJ, Baddley JW, Verweij PE, et al. Revision and update of the Consensus Definitions of Invasive Fungal disease from the European Organization for Research and Treatment of cancer and the Mycoses study group Education and Research Consortium. Clin Infect Dis 2020; 71: 1367-1376.
9. Suleyman G, Alangaden GJ. Nosocomial Fungal infections: Epidemiology, infection control, and prevention. Infect Dis Clin North Am 2021; 35: 1027-1053.
10. Lamberink H, Wagemakers A, Sigaloff KCE, van Houdt R, de Jonge NA, van Dijk K. The impact of the updated EORTC/MSG criteria on the classification of hematological patients with suspected invasive pulmonary aspergillosis. Clin Microbiol Infect 2022; 28: 1120-1125.
11. Shin JH, Nolte FS, Holloway BP, Morrison CJ. Rapid identification of up to three Candida species in a single reaction tube by a 5' exonuclease assay using fluorescent DNA probes. J Clin Microbiol 1999; 37: 165-170.
12. Kami M, Fukui T, Ogawa S, Kazuyama Y, Machida U, Tanaka Y, et al. Use of real-time PCR on blood samples for diagnosis of invasive aspergillosis. Clin Infect Dis 2001; 33: 1504-1512.
13. CLSI (2008). Reference method for broth dilution antifungal susceptibility testing of filamentous fungi; approved standard, 2nd ed. CLSI document M38-A2.
14. CLSI (2017). M61 Performance standards for antifungal susceptibility testing of filamentous fungi, 1st ed.
15. CLSI (2018). Epidemiological cutoff values for antifungal susceptibility testing, 2nd ed. M59.
16. CLSI (2017). Performance standards for antifungal susceptibility testing of yeasts, 1st ed. M60.
17. Terlizzi V, Motisi MA, Pellegrino R, Galli L, Taccetti G, Chiappini E. Management of pulmonary aspergillosis in children: a systematic review. Ital J Pediatr 2023; 49: 39.
18. Guery BP, Arendrup MC, Auzinger G, Azoulay E, Borges Sá M, Johnson EM, et al. Management of invasive candidiasis and candidemia in adult non-neutropenic intensive care unit patients: Part II. Treatment. Intensive Care Med 2009; 35: 206-214.
19. Pfaller M, Neofytos D, Diekema D, Azie N, Meier-Kriesche H-U, Quan S-P, et al. Epidemiology and outcomes of candidemia in 3648 patients: data from the Prospective Antifungal Therapy (PATH Alliance®) registry, 2004–2008. Diagn Microbiol Infect Dis 2012; 74: 323-331.
20. Tragiannidis A, Fegeler W, Rellensmann G, Debus V, Muller V, Hoernig-Franz I, et al. Candidaemia in a European Paediatric University Hospital: a 10-year observational study. Clin Microbiol Infect 2012; 18: E27-E30.
21. Harrington R, Kindermann SL, Hou Q, Taylor RJ, Azie N, Horn DL. Candidemia and invasive candidiasis among hospitalized neonates and pediatric patients. Curr Med Res Opin 2017; 33: 1803-1812.
22. Obeed FK, Al-Saad LA, Alrubayae IMN. The prevalence of Hospital-acquired fungal infections in some Hospitals of basrah province. Health Educ Health Promot 2022; 10: 193-200.
23. Badiee P, Choopanizadeh M, Moghadam AG, Nasab AH, Jafarian H, Shamsizadeh A, et al. Antifungal susceptibility patterns of colonized Candida species isolates from immunocompromised pediatric patients in five university hospitals. Iran J Microbiol 2017; 9: 363-371.
24. Badiee P, Alborzi A, Joukar M. Molecular assay to detect nosocomial fungal infections in intensive care units. Eur J Intern Med 2011; 22: 611-615.
25. Burgos A, Zaoutis TE, Dvorak CC, Hoffman JA, Knapp KM, Nania JJ, et al. Pediatric invasive aspergillosis: a multicenter retrospective analysis of 139 contemporary cases. Pediatrics 2008; 121(5): e1286-e1294.
26. Crassard N, Hadden H, Pondarre C, Hadden R, Galambrun C, Piens MA, et al. Invasive aspergillosis and allogeneic hematopoietic stem cell transplantation in children: a 15-year experience. Transpl Infect Dis 2008; 10: 177-183.
27. Kontoyiannis DP, Marr KA, Park BJ, Alexander BD, Anaissie EJ, Walsh TJ, et al. Prospective surveillance for invasive fungal infections in hematopoietic stem cell transplant recipients, 2001–2006: overview of the Transplant-Associated Infection Surveillance Network (TRANSNET) Database. Clin Infect Dis 2010; 50: 1091-1100.
28. Zaoutis TE, Heydon K, Chu JH, Walsh TJ, Steinbach WJ. Epidemiology, outcomes, and costs of invasive aspergillosis in immunocompromised children in the United States, 2000. Pediatrics 2006; 117(4): e711-e716.
29. Badiee P, Alborzi A, Karimi M, Pourabbas B, Haddadi P, Mardaneh J, et al. Diagnostic potential of nested PCR, galactomannan EIA, and beta-D-glucan for invasive aspergillosis in pediatric patients. J Infect Dev Ctries 2012; 6: 352-357.
30. Prado-Calleros HM, Brito-Vera JP, Moreno-Coutino G, Andrade-Morelos LE, Escobedo-Torres MP, Vazquez-Zavala G, et al. Rhino-Orbital mucormycosis in an immunocompetent pediatric patient with hyperglycemia of the hospitalized patient. J Infect Dev Ctries 2021; 15: 1035-1038.
31. Badiee P, Arastefar A, Jafarian H. Comparison of histopathological analysis, culture and polymerase chain reaction assays to detect mucormycosis in biopsy and blood specimens. Iran J Microbiol 2013; 5: 406-410.
32. Francis JR, Villanueva P, Bryant P, Blyth CC. Mucormycosis in children: review and recommendations for management. J Pediatric Infect Dis Soc 2018; 7: 159-164.
33. Amanati A, Barzegar H, Pouladfar G, Sanaei Dashti A, Abtahi MB, Khademi B, et al. Orbital mucormycosis in immunocompetent children; review of risk factors, diagnosis, and treatment approach. BMC Infect Dis 2020; 20: 770.
34. Badiee P, Boekhout T, Haddadi P, Mohammadi R, Ghadimi-Moghadam A, Soltani J, et al. Epidemiology and antifungal susceptibility of Candida species isolated from 10 tertiary care Hospitals in Iran. Microbiol Spectr 2022; 10(6): e0245322.
35. 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.
2. Suleyman G, Alangaden GJ. Nosocomial fungal infections: Epidemiology, infection control, and Prevention. Infect Dis Clin North Am 2016; 30: 1023-1052.
3. Zingg W, Hopkins S, Gayet-Ageron A, Holmes A, Sharland M, Suetens C, et al. Health-care-associated infections in neonates, children, and adolescents: an analysis of paediatric data from the European centre for disease Prevention and control point-prevalence survey. Lancet Infect Dis 2017; 17: 381-389.
4. Hlophe ST, Jeena PM, Mahabeer Y, Ajayi OR, Govender NP, Ogunsakin RE, et al. Invasive fungal infections in a paediatric intensive care unit in a low-to middle-income country. Afr J Thorac Crit Care Med 2022; 28: 10.7196/AJTCCM.2022.v28i3.200.
5. Reddy GKK, Padmavathi AR, Nancharaiah YV. Fungal infections: Pathogenesis, antifungals and alternate treatment approaches. Curr Res Microb Sci 2022; 3: 100137.
6. Badiee P, Hashemizadeh Z. Opportunistic invasive fungal infections: diagnosis & clinical management. Indian J Med Res 2014; 139: 195-204.
7. Bassetti M, Azoulay E, Kullberg BJ, Ruhnke M, Shoham S, Vazquez J, et al. EORTC/MSGERC Definitions of Invasive Fungal diseases: Summary of Activities of the Intensive care unit working group. Clin Infect Dis 2021; 72(Suppl 2): S121-S127.
8. Donnelly JP, Chen SC, Kauffman CA, Steinbach WJ, Baddley JW, Verweij PE, et al. Revision and update of the Consensus Definitions of Invasive Fungal disease from the European Organization for Research and Treatment of cancer and the Mycoses study group Education and Research Consortium. Clin Infect Dis 2020; 71: 1367-1376.
9. Suleyman G, Alangaden GJ. Nosocomial Fungal infections: Epidemiology, infection control, and prevention. Infect Dis Clin North Am 2021; 35: 1027-1053.
10. Lamberink H, Wagemakers A, Sigaloff KCE, van Houdt R, de Jonge NA, van Dijk K. The impact of the updated EORTC/MSG criteria on the classification of hematological patients with suspected invasive pulmonary aspergillosis. Clin Microbiol Infect 2022; 28: 1120-1125.
11. Shin JH, Nolte FS, Holloway BP, Morrison CJ. Rapid identification of up to three Candida species in a single reaction tube by a 5' exonuclease assay using fluorescent DNA probes. J Clin Microbiol 1999; 37: 165-170.
12. Kami M, Fukui T, Ogawa S, Kazuyama Y, Machida U, Tanaka Y, et al. Use of real-time PCR on blood samples for diagnosis of invasive aspergillosis. Clin Infect Dis 2001; 33: 1504-1512.
13. CLSI (2008). Reference method for broth dilution antifungal susceptibility testing of filamentous fungi; approved standard, 2nd ed. CLSI document M38-A2.
14. CLSI (2017). M61 Performance standards for antifungal susceptibility testing of filamentous fungi, 1st ed.
15. CLSI (2018). Epidemiological cutoff values for antifungal susceptibility testing, 2nd ed. M59.
16. CLSI (2017). Performance standards for antifungal susceptibility testing of yeasts, 1st ed. M60.
17. Terlizzi V, Motisi MA, Pellegrino R, Galli L, Taccetti G, Chiappini E. Management of pulmonary aspergillosis in children: a systematic review. Ital J Pediatr 2023; 49: 39.
18. Guery BP, Arendrup MC, Auzinger G, Azoulay E, Borges Sá M, Johnson EM, et al. Management of invasive candidiasis and candidemia in adult non-neutropenic intensive care unit patients: Part II. Treatment. Intensive Care Med 2009; 35: 206-214.
19. Pfaller M, Neofytos D, Diekema D, Azie N, Meier-Kriesche H-U, Quan S-P, et al. Epidemiology and outcomes of candidemia in 3648 patients: data from the Prospective Antifungal Therapy (PATH Alliance®) registry, 2004–2008. Diagn Microbiol Infect Dis 2012; 74: 323-331.
20. Tragiannidis A, Fegeler W, Rellensmann G, Debus V, Muller V, Hoernig-Franz I, et al. Candidaemia in a European Paediatric University Hospital: a 10-year observational study. Clin Microbiol Infect 2012; 18: E27-E30.
21. Harrington R, Kindermann SL, Hou Q, Taylor RJ, Azie N, Horn DL. Candidemia and invasive candidiasis among hospitalized neonates and pediatric patients. Curr Med Res Opin 2017; 33: 1803-1812.
22. Obeed FK, Al-Saad LA, Alrubayae IMN. The prevalence of Hospital-acquired fungal infections in some Hospitals of basrah province. Health Educ Health Promot 2022; 10: 193-200.
23. Badiee P, Choopanizadeh M, Moghadam AG, Nasab AH, Jafarian H, Shamsizadeh A, et al. Antifungal susceptibility patterns of colonized Candida species isolates from immunocompromised pediatric patients in five university hospitals. Iran J Microbiol 2017; 9: 363-371.
24. Badiee P, Alborzi A, Joukar M. Molecular assay to detect nosocomial fungal infections in intensive care units. Eur J Intern Med 2011; 22: 611-615.
25. Burgos A, Zaoutis TE, Dvorak CC, Hoffman JA, Knapp KM, Nania JJ, et al. Pediatric invasive aspergillosis: a multicenter retrospective analysis of 139 contemporary cases. Pediatrics 2008; 121(5): e1286-e1294.
26. Crassard N, Hadden H, Pondarre C, Hadden R, Galambrun C, Piens MA, et al. Invasive aspergillosis and allogeneic hematopoietic stem cell transplantation in children: a 15-year experience. Transpl Infect Dis 2008; 10: 177-183.
27. Kontoyiannis DP, Marr KA, Park BJ, Alexander BD, Anaissie EJ, Walsh TJ, et al. Prospective surveillance for invasive fungal infections in hematopoietic stem cell transplant recipients, 2001–2006: overview of the Transplant-Associated Infection Surveillance Network (TRANSNET) Database. Clin Infect Dis 2010; 50: 1091-1100.
28. Zaoutis TE, Heydon K, Chu JH, Walsh TJ, Steinbach WJ. Epidemiology, outcomes, and costs of invasive aspergillosis in immunocompromised children in the United States, 2000. Pediatrics 2006; 117(4): e711-e716.
29. Badiee P, Alborzi A, Karimi M, Pourabbas B, Haddadi P, Mardaneh J, et al. Diagnostic potential of nested PCR, galactomannan EIA, and beta-D-glucan for invasive aspergillosis in pediatric patients. J Infect Dev Ctries 2012; 6: 352-357.
30. Prado-Calleros HM, Brito-Vera JP, Moreno-Coutino G, Andrade-Morelos LE, Escobedo-Torres MP, Vazquez-Zavala G, et al. Rhino-Orbital mucormycosis in an immunocompetent pediatric patient with hyperglycemia of the hospitalized patient. J Infect Dev Ctries 2021; 15: 1035-1038.
31. Badiee P, Arastefar A, Jafarian H. Comparison of histopathological analysis, culture and polymerase chain reaction assays to detect mucormycosis in biopsy and blood specimens. Iran J Microbiol 2013; 5: 406-410.
32. Francis JR, Villanueva P, Bryant P, Blyth CC. Mucormycosis in children: review and recommendations for management. J Pediatric Infect Dis Soc 2018; 7: 159-164.
33. Amanati A, Barzegar H, Pouladfar G, Sanaei Dashti A, Abtahi MB, Khademi B, et al. Orbital mucormycosis in immunocompetent children; review of risk factors, diagnosis, and treatment approach. BMC Infect Dis 2020; 20: 770.
34. Badiee P, Boekhout T, Haddadi P, Mohammadi R, Ghadimi-Moghadam A, Soltani J, et al. Epidemiology and antifungal susceptibility of Candida species isolated from 10 tertiary care Hospitals in Iran. Microbiol Spectr 2022; 10(6): e0245322.
35. 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.
| Files | ||
| Issue | Vol 17 No 4 (2025) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v17i4.19258 | |
| Keywords | ||
| Pediatrics Fungal drug resistance Colonization Fungal infection Candida Aspergillus | ||
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How to Cite
1.
Badiee P, Jafarian H. The prevalence of pediatric nosocomial fungal infections. Iran J Microbiol. 2025;17(4):644-652.
