Candidemia among Hospitalized Pediatric Patients Caused by Several Clonal Lineages of Candida parapsilosis
Abstract
:1. Introduction
2. Materials and Methods
3. Results
4. Discussion
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Mirhendi, H.; Charsizadeh, A.; Eshaghi, H.; Nikmanesh, B.; Arendrup, M.C. Species distribution and antifungal susceptibility profile of Candida isolates from blood and other normally sterile foci from pediatric ICU patients in Tehran, Iran. Med. Mycol. 2019, 58, 201–206. [Google Scholar] [CrossRef] [PubMed]
- Warris, A.; Pana, Z.-D.; Oletto, A.; Lundin, R.; Castagnola, E.; Lehrnbecher, T.; Groll, A.H.; Roilides, E. Etiology and Outcome of Candidemia in Neonates and Children in Europe. Pediatr. Infect. Dis. J. 2020, 39, 114–120. [Google Scholar] [CrossRef] [PubMed]
- Steinbach, W.J.; Roilides, E.; Berman, D.; Hoffman, J.A.; Groll, A.H.; Bin-Hussain, I.; Palazzi, D.L.; Castagnola, E.; Halasa, N.; Velegraki, A.; et al. Results From a Prospective, International, Epidemiologic Study of Invasive Candidiasis in Children and Neonates. Pediatr. Infect. Dis. J. 2012, 31, 1252–1257. [Google Scholar] [CrossRef] [PubMed]
- Pinhati, H.M.S.; Casulari, L.A.; Souza, A.C.R.; Siqueira, R.A.; Damasceno, C.M.G.; Colombo, A.L. Outbreak of candidemia caused by fluconazole resistant Candida parapsilosis strains in an intensive care unit. BMC Infect. Dis. 2016, 16, 433. [Google Scholar] [CrossRef] [PubMed]
- Hernández-Castro, R.; Arroyo-Escalante, S.; Carrillo-Casas, E.M.; Moncada-Barrón, D.; Álvarez-Verona, E.; Hernández-Delgado, L.; Torres-Narváez, P.; Lavalle-Villalobos, A. Outbreak of Candida parapsilosis in a neonatal intensive care unit: A health care workers source. Eur. J. Pediatr. 2010, 169, 783–787. [Google Scholar] [CrossRef]
- Arastehfar, A.; Hilmioğlu-Polat, S.; Daneshnia, F.; Pan, W.; Hafez, A.; Fang, W.; Liao, W.; Şahbudak-Bal, Z.; Metin, D.Y.; De Almeida, J.N., Jr.; et al. Clonal Candidemia Outbreak by Candida parapsilosis Carrying Y132F in Turkey: Evolution of a Persisting Challenge. Front. Cell Infect. Microbiol. 2021, 11, 1–10. [Google Scholar] [CrossRef]
- Govender, N.P.; Patel, J.; Magobo, R.E.; Naicker, S.; Wadula, J.; Whitelaw, A.; Coovadia, Y.; Kularatne, R.; Govind, C.; Lockhart, S.R.; et al. Emergence of azole-resistant Candida parapsilosis causing bloodstream infection: Results from laboratory-based sentinel surveillance in South Africa. J. Antimicrob. Chemother. 2016, 71, 1994–2004. [Google Scholar] [CrossRef] [Green Version]
- Singh, A.; Singh, P.K.; de Groot, T.; Kumar, A.; Mathur, P.; Tarai, B.; Sachdeva, N.; Upadhyaya, G.; Sarma, S.; Meis, J.F.; et al. Emergence of clonal fluconazole-resistant Candida parapsilosis clinical isolates in a multicentre laboratory-based surveillance study in India. J. Antimicrob. Chemother. 2019, 74, 1260–1268. [Google Scholar] [CrossRef] [Green Version]
- Choi, Y.J.; Kim, Y.-J.; Yong, D.; Byun, J.; Kim, T.S.; Chang, Y.S.; Choi, M.J.; Byeon, S.A.; Won, E.J.; Kim, S.H.; et al. Fluconazole-Resistant Candida parapsilosis Bloodstream Isolates with Y132F Mutation in ERG11 Gene, South Korea. Emerg. Infect. Dis. 2018, 24, 1768–1770. [Google Scholar] [CrossRef] [Green Version]
- Asadzadeh, M.; Ahmad, S.; Al-Sweih, N.; Khan, Z. Epidemiology and Molecular Basis of Resistance to Fluconazole Among Clinical Candida parapsilosis Isolates in Kuwait. Microb. Drug Resist. 2017, 23, 966–972. [Google Scholar] [CrossRef]
- Corzo-Leon, D.E.; Peacock, M.; Rodriguez-Zulueta, P.; Salazar-Tamayo, G.J.; MacCallum, D.M. General hospital outbreak of invasive candidiasis due to azole-resistant Candida parapsilosis associated with an Erg11 Y132F mutation. Med. Mycol. 2021, 59, 664–671. [Google Scholar] [CrossRef] [PubMed]
- Castanheira, M.; Deshpande, L.M.; Messer, S.A.; Rhomberg, P.R.; Pfaller, M.A. Analysis of global antifungal surveillance results reveals predominance of Erg11 Y132F alteration among azole-resistant Candida parapsilosis and Candida tropicalis and country-specific isolate dissemination. Int. J. Antimicrob. Agents 2020, 55, 105799. [Google Scholar] [CrossRef] [PubMed]
- Sarvikivi, E.; Lyytikäinen, O.; Soll, D.R.; Pujol, C.; Pfaller, M.A.; Richardson, M.; Koukila-Kähkölä, P.; Luukkainen, P.; Saxén, H. Emergence of Fluconazole Resistance in a Candida parapsilosis Strain That Caused Infections in a Neonatal Intensive Care Unit. J. Clin. Microbiol. 2005, 43, 2729–2735. [Google Scholar] [CrossRef] [Green Version]
- Arastehfar, A.; Daneshnia, F.; Hilmioğlu-Polat, S.; Fang, W.; Yaşar, M.; Polat, F.; Metin, D.Y.; Rigole, P.; Coenye, T.; Ilkit, M.; et al. First Report of Candidemia Clonal Outbreak Caused by Emerging Fluconazole-Resistant Candida parapsilosis Isolates Harboring Y132F and/or Y132F+K143R in Turkey. Antimicrob. Agents Chemother. 2020, 64, 1–11. [Google Scholar] [CrossRef] [PubMed]
- Thomaz, D.Y.; de Almeida, J.N.; Sejas, O.N.E.; Del Negro, G.M.B.; Carvalho, G.O.M.H.; Gimenes, V.M.F.; de Souza, M.; Arastehfar, A.; Camargo, C.; Motta, A.; et al. Environmental Clonal Spread of Azole-Resistant Candida parapsilosis with Erg11-Y132F Mutation Causing a Large Candidemia Outbreak in a Brazilian Cancer Referral Center. J. Fungi 2021, 7, 259. [Google Scholar] [CrossRef]
- Chakrabarti, A.; Sood, P.; Rudramurthy, S.M.; Chen, S.; Kaur, H.; Capoor, M.; Chhina, D.; Rao, R.; Eshwara, V.K.; Xess, I.; et al. Incidence, characteristics and outcome of ICU-acquired candidemia in India. Intensive Care Med. 2015, 41, 285–295. [Google Scholar] [CrossRef]
- Arastehfar, A.; Daneshnia, F.; Najafzadeh, M.J.; Hagen, F.; Mahmoudi, S.; Salehi, M.; Zarrinfar, H.; Namvar, Z.; Zareshahrabadi, Z.; Khodavaisy, S.; et al. Evaluation of Molecular Epidemiology, Clinical Characteristics, Antifungal Susceptibility Profiles, and Molecular Mechanisms of Antifungal Resistance of Iranian Candida parapsilosis Species Complex Blood Isolates. Front. Cell Infect. Microbiol. 2020, 10, 1–13. [Google Scholar] [CrossRef]
- Magobo, R.E.; Lockhart, S.R.; Govender, N.P.; Wadula, J.; Rensburg, V.; van Rensburg, C.J.; Whitelaw, A.; Zietsman, I.; Miller, N.; Smith, P.; et al. Fluconazole-resistant Candida parapsilosis strains with a Y132F substitution in the ERG11 gene causing invasive infections in a neonatal unit, South Africa. Mycoses 2020, 63, 471–477. [Google Scholar] [CrossRef]
- Vatanshenassan, M.; Boekhout, T.; Mauder, N.; Robert, V.; Maier, T.; Meis, J.F.; Berman, J.; Then, E.; Kostrzewa, M.; Hagen, F. Evaluation of microsatellite typing, ITS sequencing, AFLP fingerprinting, MALDI-TOF MS, and Fourier-Transform Infrared Spectroscopy Analysis of Candida auris. J. Fungi 2020, 6, 146. [Google Scholar] [CrossRef]
- Hubisz, M.J.; Falush, D.; Stephens, M.; Pritchard, J.K. Inferring weak population structure with the assistance of sample group information. Mol. Ecol. Resour. 2009, 9, 1322–1332. [Google Scholar] [CrossRef] [Green Version]
- Butler, G.; Rasmussen, M.D.; Lin, M.F.; Santos, M.A.S.; Sakthikumar, S.; Munro, C.A.; Rheinbay, E.; Grabherr, M.; Forche, A.; Reedy, J.L.; et al. Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature 2009, 459, 657–662. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pryszcz, L.P.; Németh, T.; Gácser, A.; Gabaldón, T. Unexpected genomic variability in clinical and environmental strains of the pathogenic yeast Candida parapsilosis. Genome Biol. Evol. 2013, 5, 2382–2392. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jombart, T.; Bateman, A. Adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics 2008, 24, 1403–1405. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Charsizadeh, A.; Mirhendi, H.; Nikmanesh, B.; Eshaghi, H.; Makimura, K. Microbial epidemiology of candidaemia in neonatal and paediatric intensive care units at the Children’s Medical Center, Tehran. Mycoses 2018, 61, 22–29. [Google Scholar] [CrossRef] [PubMed]
- Arastehfar, A.; Khodavaisy, S.; Daneshnia, F.; Najafzadeh, M.-J.; Mahmoudi, S.; Charsizadeh, A.; Salehi, M.-R.; Zarrinfar, H.; Raeisabadi, A.; Dolatabadi, S.; et al. Molecular Identification, Genotypic Diversity, Antifungal Susceptibility, and Clinical Outcomes of Infections Caused by Clinically Underrated Yeasts, Candida orthopsilosis, and Candida metapsilosis: An Iranian Multicenter Study (2014–2019). Front. Cell. Infect. Microbiol. 2019, 9. [Google Scholar] [CrossRef] [Green Version]
- Diab-Elschahawi, M.; Forstner, C.; Hagen, F.; Meis, J.F.; Lassnig, A.M.; Presterl, E.; Klaassen, C.H.W. Microsatellite genotyping clarified conspicuous accumulation of Candida parapsilosis at a cardio-thoracic surgery intensive care unit. J. Clin. Microbiol. 2012, 50, 3422–3426. [Google Scholar] [CrossRef] [Green Version]
- Kamvar, Z.N.; Tabima, J.F.; Grünwald, N.J. Poppr: An R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2014, 2014, 1–14. [Google Scholar] [CrossRef] [Green Version]
- Bruvo, R.; Michiels, N.K.; D’Souza, T.G.; Schulenburg, H. A simple method for the calculation of microsatellite genotype distances irrespective of ploidy level. Mol. Ecol. 2004, 13, 2101–2106. [Google Scholar] [CrossRef]
- Agapow, P.-M.; Burt, A. Indices of multilocus linkage disequilibrium. Mol. Ecol. Notes 2001, 1, 101–102. [Google Scholar] [CrossRef]
- Slatkin, M. A measure of population subdivision based on microsatellite allele frequencies. Genetics 1995, 139, 457–462. [Google Scholar] [CrossRef]
- Fekkar, A.; Blaize, M.; Bouglé, A.; Normand, A.-C.; Raoelina, A.; Kornblum, D.; Kamus, L.; Piarroux, R.; Imbert, S. Hospital Outbreak of Fluconazole-Resistant Candida parapsilosis: Arguments for Clonal Transmission and Long-Term Persistence. Antimicrob. Agents Chemother. 2021, 65. [Google Scholar] [CrossRef] [PubMed]
- Desnos-Ollivier, M.; Bórmida, V.; Poirier, P.; Nourrisson, C.; Pan, D.; Bretagne, S.; Puime, A.; Dromer, F.; Uruguayan Invasive Fungal Infection Network. Population Structure of Candida parapsilosis: No Genetic Difference Between French and Uruguayan Isolates Using Microsatellite Length Polymorphism. Mycopathologia 2018, 183, 381–390. [Google Scholar] [CrossRef] [PubMed]
- Prugnolle, F.; De Meeûs, T. The impact of clonality on parasite population genetic structure. Parasite 2008, 15, 455–457. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Arastehfar, A.; Daneshnia, F.; Salehi, M.; Yaşar, M.; Hoşbul, T.; Ilkit, M.; Pan, W.; Hagen, F.; Arslan, N.; Türk-Dağı, H.; et al. Low level of antifungal resistance of Candida glabrata blood isolates in Turkey: Fluconazole minimum inhibitory concentration and FKS mutations can predict therapeutic failure. Mycoses 2020, 63, 911–920. [Google Scholar] [CrossRef] [PubMed]
Cluster | No. Isolates | No. Patients | Wards Involved | Time Span of Obtained Isolates | Reference Strains in Cluster, Origin |
---|---|---|---|---|---|
G1-P | 44 | 36 | 12 (PICU, NICU, NICU-OH, CICU, EICU, Cardiac, Neurology, Surgery, Immunology, Infectious, GI, BMT) | 2 years and 9 months | CBS 1818, CL CBS 1954, IT CBS 604, PR |
G2-P | 6 | 5 | 4 (NICU, EICU, PICU, Surgery) | 2 years and 3 months | CBS 2197, DK CBS 2915, NO CBS 2194, AT CBS 2196, DOM |
G1-Orth | 3 | 3 | 3 (Immunology, PICU, NICU) | 1 month | CBS 10906 |
G2-Orth | 3 | 2 | 1 (PICU) | 10 months | No |
Source | df | SS | MS | Est. Var. | % |
---|---|---|---|---|---|
Among Pops | 1 | 268.378 | 268.378 | 1.604 | 1% |
Within Pops | 160 | 22,871.048 | 142.944 | 142.944 | 99% |
Total | 161 | 23,139.426 | 144.548 | 100% | |
Stat | Value | P(rand ≥ data) | |||
RST | 0.011 | 0.143 |
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Hare, R.K.; Arastehfar, A.; Rosendahl, S.; Charsizadeh, A.; Daneshnia, F.; Eshaghi, H.; Mirhendi, H.; Boekhout, T.; Hagen, F.; Arendrup, M.C. Candidemia among Hospitalized Pediatric Patients Caused by Several Clonal Lineages of Candida parapsilosis. J. Fungi 2022, 8, 183. https://doi.org/10.3390/jof8020183
Hare RK, Arastehfar A, Rosendahl S, Charsizadeh A, Daneshnia F, Eshaghi H, Mirhendi H, Boekhout T, Hagen F, Arendrup MC. Candidemia among Hospitalized Pediatric Patients Caused by Several Clonal Lineages of Candida parapsilosis. Journal of Fungi. 2022; 8(2):183. https://doi.org/10.3390/jof8020183
Chicago/Turabian StyleHare, Rasmus Krøger, Amir Arastehfar, Søren Rosendahl, Arezoo Charsizadeh, Farnaz Daneshnia, Hamid Eshaghi, Hossein Mirhendi, Teun Boekhout, Ferry Hagen, and Maiken Cavling Arendrup. 2022. "Candidemia among Hospitalized Pediatric Patients Caused by Several Clonal Lineages of Candida parapsilosis" Journal of Fungi 8, no. 2: 183. https://doi.org/10.3390/jof8020183