New short tandem repeat-based molecular typing method for Pneumocystis jirovecii reveals intrahospital transmission between patients from different wards

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Gits Muselli, Maud ^a   Peraldi, Marie Noelle ^a,b   De Castro, Nathalie ^a   Delcey, Véronique ^a   Menotti, Jean ^a,b,c,d   Guigue, Nicolas ^a,b   Hamane, Samia ^a   Raffoux, Emmanuel ^a   Bergeron, Anne ^a,b   Valade, Sandrine ^a   Molina, Jean Michel ^a,b   Bretagne, Stéphane ^a,b,c,d   Alanio, Alexandre ^a,b,c,d  

^a SAINT LOUIS HOSPITAL   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c INSTITUT PASTEUR   (France)

^d CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADOLESCENT; ADULT; AGED; ALLELE; ARTICLE; BACTERIAL GENOME; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE TRANSMISSION; FEMALE; GENOTYPE; GRAFT RECIPIENT; HUMAN; KIDNEY GRAFT; MALE; MOLECULAR TYPING; NONHUMAN; PATHOPHYSIOLOGY; PNEUMOCYSTIS JIROVECI; PNEUMOCYSTIS PNEUMONIA; POLYMERASE CHAIN REACTION; SHORT TANDEM REPEAT; FUNGAL GENOME; GENETICS; INFANT; MICROBIOLOGY; MIDDLE AGED; OPPORTUNISTIC INFECTION; PATHOGENICITY; PHYLOGEOGRAPHY; PNEUMOCYSTIS CARINII; PRESCHOOL CHILD; SPUTUM; TRANSMISSION; VERY ELDERLY;

FUNGI; PNEUMOCYSTIS; PNEUMOCYSTIS JIROVECII;

FUNGAL DNA; MICROSATELLITE DNA;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; CHILD; CHILD, PRESCHOOL; DNA, FUNGAL; GENOME, FUNGAL; GENOTYPE; HUMANS; INFANT; MICROSATELLITE REPEATS; MIDDLE AGED; OPPORTUNISTIC INFECTIONS; PHYLOGEOGRAPHY; PNEUMOCYSTIS CARINII; PNEUMONIA, PNEUMOCYSTIS; SPUTUM;

EID: 84928799243     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0125763     Document Type: Article

References (53)

1. Cushion MT (2010) Are members of the fungal genus Pneumocystis (a) commensals; (b) opportunists; (c) pathogens; or (d) all of the above? PLOS Pathog 6: e1001009. doi: 10.1371/journal.ppat.1001009 PMID: 20885786
2. Gigliotti F, Wright TW (2012) Pneumocystis: where does it live? PLOS Pathog 8: e1003025. doi: 10.1371/journal.ppat.1003025.g001 PMID: 23209406
3. Roblot F, Le Moal G, Godet C, Hutin P, Texereau M, Boyer E, et al. (2003) Pneumocystis carinii pneumonia in patients with hematologic malignancies: a descriptive study. J Infect 47: 19-27. doi: 10.1016/S0163-4453(03)00038-0 PMID: 12850158
4. Tasaka S, Tokuda H (2012) Pneumocystis jirovecii pneumonia in non-HIV-infected patients in the era of novel immunosuppressive therapies. J Infect Chemother 18: 793-806. doi: 10.1007/s10156-012-0453-0 PMID: 22864454
5. Reid AB, Chen SCA, Worth LJ (2011) Pneumocystis jirovecii pneumonia in non-HIV-infected patients: new risks and diagnostic tools. Curr Opin Infect Dis 24: 534-544. Available: http://eutils.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom = pubmed&id = 21986616&retmode = ref&cmd = prlinks. doi: 10.1097/QCO.0b013e32834cac17 PMID: 21986616
6. Wissmann G, Morilla R, Martín-Garrido I, Friaza V, Respaldiza N, Povedano J, et al. (2010) Pneumocystis jirovecii colonization in patients treated with infliximab. Eur J Clin Invest 41: 343-348. doi: 10.1111/j.1365-2362.2010.02415.x PMID: 21299548
7. Catherinot E, Lanternier F, Bougnoux M-E, Lecuit M, Couderc L-J, Lortholary O (2010) Pneumocystis jirovecii pneumonia. Infect Dis Clin North Am 24: 107-138. doi: 10.1016/j.idc.2009.10.010 PMID: 20171548
8. Mori S, Sugimoto M (2012) Pneumocystis jirovecii infection: an emerging threat to patients with rheumatoid arthritis. Rheumatology (Oxford) 51: 2120-2130. doi: 10.1093/rheumatology/kes244 PMID: 23001613
9. Pagano L, Fianchi L, Mele L, Girmenia C, Offidani M, Ricci P, et al. (2002) Pneumocystis carinii pneumonia in patients with malignant haematological diseases: 10 years' experience of infection in GIMEMA centres. Br J Haematol 117: 379-386. PMID: 11972521
10. Chabé M, Dei-Cas E, Creusy C, Fleurisse L, Respaldiza N, Camus D et al. (2004) Immunocompetent hosts as a reservoir of Pneumocystis organisms: histological and rt-PCR data demonstrate active replication. Eur J Clin Microbiol Infect Dis 23: 89-97. doi: 10.1007/s10096-003-1092-2 PMID: 14712369
11. Gigliotti F, Harmsen AG, Wright TW (2003) Characterization of transmission of Pneumocystis carinii f. sp. muris through immunocompetent BALB/c mice. Infect Immun 71: 3852-3856. PMID: 12819069
12. Choukri F, Menotti J, Sarfati C, Lucet JC, Nevez G, Garin JF, et al. (2010) Quantification and spread of Pneumocystis jirovecii in the surrounding air of patients with Pneumocystis pneumonia. Clin Infect Dis 51: 259-265. doi: 10.1086/653933 PMID: 20572759
13. Yazaki H, Goto N, Uchida K, Kobayashi T, Gatanaga H, Oka S, et al. (2009) Outbreak of Pneumocystis jiroveci pneumonia in renal transplant recipients: P. jiroveci is contagious to the susceptible host. Transplantation 88: 380-385. doi: 10.1097/TP.0b013e3181aed389 PMID: 19667941
14. de Boer MGJ, Bruijnesteijn van Coppenraet LES, Gaasbeek A, Berger SP, Gelinck LBS, van Houwelongen HC, et al. (2007) An outbreak of Pneumocystis jiroveci pneumonia with 1 predominant genotype among renal transplant recipients: interhuman transmission or a common environmental source? Clin Infect Dis 44: 1143-1149. doi: 10.1086/513198 PMID: 17407029
15. Pliquett RU, Asbe-Vollkopf A, Hauser PM, Presti LL, Hunfeld KP, Berger A, et al. (2012) A Pneumocystis jirovecii pneumonia outbreak in a single kidney-transplant center: role of cytomegalovirus co-infection. Eur J Clin Microbiol Infect Dis 31: 2429-2437. doi: 10.1007/s10096-012-1586-x PMID: 22402816
16. Le Gal S, Damiani C, Rouillé A, Grall A, Tréguer L, Virmaux M, et al. (2012) A cluster of Pneumocystis infections among renal transplant recipients: molecular evidence of colonized patients as potential infectious sources of Pneumocystis jirovecii. Clin Infect Dis 54: e62-e71. doi: 10.1093/cid/cir996 PMID: 22337822
17. Olsson M, Eriksson BM, Elvin K, Strandberg M, Wahlgren M (2001) Genotypes of clustered cases of Pneumocystis carinii pneumonia. Scand J Infect Dis 33: 285-289. PMID: 11345221
18. Gianella S, Haeberli L, Joos B, Ledergerber B, Wüthrich RP, Weber R, et al. (2010) Molecular evidence of interhuman transmission in an outbreak of Pneumocystis jirovecii pneumonia among renal transplant recipients. Transplant infectious disease: an official journal of the Transplantation Society 12: 1-10. doi: 10.1111/j.1399-3062.2009.00447.x
19. Höcker B, Wendt C, Nahimana A, Tönshoff B, Hauser PM (2005) Molecular evidence of Pneumocystis transmission in pediatric transplant unit. Emerg Infect Dis 11: 330-332. doi: 10.3201/eid1102.040820 PMID: 15752458
20. Phipps LM, Chen SCA, Kable K, Halliday CL, Firacative C, Meyer W, et al. (2011) Nosocomial Pneumocystis jirovecii pneumonia: lessons from a cluster in kidney transplant recipients. Transplantation 92: 1327-1334. doi: 10.1097/TP.0b013e3182384b57 PMID: 22129760
21. de Castro N, Xu F, Porcher R, Pavie J, Molina JM, Peraldi MN, et al. (2010) Pneumocystis jirovecii pneumonia in renal transplant recipients occurring after discontinuation of prophylaxis: a case-control study. Clin Microbiol Infect 16: 1375-1377. doi: 10.1111/j.1469-0691.2009.03143.x PMID: 20041898
22. Rabodonirina M, Vanhems P, Couray-Targe S, Gillibert R-P, Ganne C, Nizard N, et al. (2004) Molecular evidence of interhuman transmission of Pneumocystis pneumonia among renal transplant recipients hospitalized with HIV-infected patients. Emerg Infect Dis 10: 1766-1773. doi: 10.3201/eid1010.040453 PMID: 15504262
23. Vargas SL, Hughes WT, Santolaya ME, Ulloa AV, Ponce CA, Cabrera CE, et al. (2001) Search for primary infection by Pneumocystis carinii in a cohort of normal, healthy infants. Clin Infect Dis 32: 855-861. doi: 10.1086/319340 PMID: 11247708
24. Schildgen V, Mai S, Khalfaoui S, Lusebrink J, Pieper M, Tillmann RL, et al. (2014) Pneumocystis jirovecii can be productively cultured in differentiated cufi-8 airway cells. mBio 5: e01186-14-e01186-14. doi: 10.1128/mBio.01186-14 PMID: 24825015
25. Hauser PM, Blanc DS, Bille J, Telenti A, Francioli P (1996) Development of a molecular typing method for Pneumocystis carinii sp.f. hominis. J Euk Microbiol 43: 34S. PMID: 8822837
26. Hauser PM (2004) The development of a typing method for an uncultivable microorganism: the example of Pneumocystis jirovecii. Infect Genet Evol 4: 199-203. PMID: 15450199
27. Hauser PM, Francioli P, Bille J, Telenti A, Blanc DS (1997) Typing of Pneumocystis carinii f. sp. hominis by single-strand conformation polymorphism of four genomic regions. J Clin Microbiol 35: 3086-3091. PMID: 9399499
28. Maitte C, Leterrier M, Le Pape P, Miegeville M, Morio F (2013) Multilocus sequence typing of pneumocystis jirovecii from clinical samples: how many and which loci should be used? J Clin Microbiol 51: 2843-2849. doi: 10.1128/JCM.01073-13 PMID: 23784120
29. Angulo B, García-García E, Martínez R, Suárez-Gauthier A, Conde E, Hidalgo M, et al. (2010) A commercial real-time PCR kit provides greater sensitivity than direct sequencing to detect KRAS mutations: a morphology-based approach in colorectal carcinoma. J Mol Diagn 12: 292-299. doi: 10.2353/jmoldx.2010.090139 PMID: 20203003
30. Esteves F, Gaspar J, de Sousa B, Antunes F, Mansinho K, Matos O (2011) Clinical relevance of multiple single-nucleotide polymorphisms in Pneumocystis jirovecii pneumonia: development of a multiplex PCR-single-base-extension methodology. J Clin Microbiol 49: 1810-1815. doi: 10.1128/JCM.02303-10 PMID: 21389160
31. de Valk HA, Meis JFGM, Curfs IM, Muehlethaler K, Mouton JW, Klaassen CHW (2005) Use of a novel panel of nine short tandem repeats for exact and high-resolution fingerprinting of Aspergillus fumigatus isolates. J Clin Microbiol 43: 4112-4120. doi: 10.1128/JCM.43.8.4112-4120.2005 PMID: 16081958
32. Botterel F, Desterke C, Costa C, Bretagne S (2001) Analysis of microsatellite markers of Candida albicans used for rapid typing. J Clin Microbiol 39: 4076-4081. doi: 10.1128/JCM.39.11.4076-4081.2001 PMID: 11682532
33. Enache-Angoulvant A, Bourget M, Brisse S, Stockman-Pannier C, Diancourt L, François N, et al. (2010) Multilocus microsatellite markers for molecular typing of Candida glabrata: application to analysis of genetic relationships between bloodstream and digestive system isolates. J Clin Microbiol 48: 4028-4034. doi: 10.1128/JCM.02140-09 PMID: 20844221
34. Illnait-Zaragozi M-T, Martínez-Machín GF, Fernández-Andreu CM, Boekhout T, Meis JFGM, Klaassen CHW (2010) Microsatellite typing of clinical and environmental Cryptococcus neoformans var. grubii isolates from Cuba shows multiple genetic lineages. PLOS One 5: e9124. doi: 10.1371/journal.pone.0009124 PMID: 20161737
35. Garcia-Hermoso D, Cabaret O, Lecellier G, Desnos-Ollivier M, Hoinard D, Raoux D, et al. (2007) Comparison of microsatellite length polymorphism and multilocus sequence typing for DNA-based typing of Candida albicans. J Clin Microbiol 45: 3958-3963. doi: 10.1128/JCM.01261-07 PMID: 17928418
36. Garcia-Hermoso D, MacCallum DM, Lott TJ, Sampaio P, Serna M-JB, Grenouillet F, et al. (2010) Multicenter collaborative study for standardization of Candida albicans genotyping using a polymorphic microsatellite marker. J Clin Microbiol 48: 2578-2581. doi: 10.1128/JCM.00040-10 PMID: 20427694
37. de Valk HA, Meis JFGM, Bretagne S, Costa JM, Lasker BA, Balajee SA, et al. (2009) Interlaboratory reproducibility of a microsatellite-based typing assay for Aspergillus fumigatus through the use of allelic ladders: proof of concept. Clin Microbiol Infect 15: 180-187. doi: 10.1111/j.1469-0691.2008.02656.x PMID: 19154486
38. de Valk HA, Meis JFGM, Klaassen CHW (2007) Microsatellite based typing of Aspergillus fumigatus: strengths, pitfalls and solutions. J Microbiol Methods 69: 268-272. doi: 10.1016/j.mimet.2007.01.009 PMID: 17328980
39. Cissé OH, Pagni M, Hauser PM (2012) De novo assembly of the Pneumocystis jirovecii genome from a single bronchoalveolar lavage fluid specimen from a patient. mBio 4. doi: 10.1128/mBio.00428-12 PMID: 23269830
40. Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27: 573-580. PMID: 9862982
41. Alanio A, Desoubeaux G, Sarfati C, Hamane S, Bergeron A, Azoulay E, et al. (2011) Real-time PCR assay-based strategy for differentiation between active Pneumocystis jirovecii pneumonia and colonization in immunocompromised patients. Clin Microbiol Infect 17: 1531-1537. doi: 10.1111/j.1469-0691.2010.03400.x PMID: 20946413
42. Feil EJ (2004) Small change: keeping pace with microevolution. Nat Rev Micro 2: 483-495. doi: 10.1038/nrmicro904
43. Hunter PR, Gaston MA (1988) Numerical index of the discriminatory ability of typing systems: an application of Simpson's index of diversity. J Clin Microbiol 26: 2465-2466. PMID: 3069867
44. Parobek CM, Jiang LY, Patel JC, Alvarez-Martinez MJ, Miro JM, Worodria W, et al. (2014) Multilocus microsatellite genotyping array for investigation of genetic epidemiology of Pneumocystis jirovecii. J Clin Microbiol 52: 1391-1399. doi: 10.1128/JCM.02531-13 PMID: 24523468
45. Davidson S, Starkey A, MacKenzie A (2009) Evidence of uneven selective pressure on different subsets of the conserved human genome; implications for the significance of intronic and intergenic DNA. BMC Genomics 10: 614. doi: 10.1186/1471-2164-10-614 PMID: 20015390
46. Nahimana A, Blanc DS, Francioli P, Bille J, Hauser PM (2000) Typing of Pneumocystis carinii f. sp. hominis by PCR-SSCP to indicate a high frequency of co-infections. J Med Microbiol 49: 753-758. PMID: 10933262
47. Esteves F, Gaspar J, Tavares A, Moser I, Antunes F, Mansinha K, et al. (2010) Population structure of Pneumocystis jirovecii isolated from immunodeficiency virus-positive patients. Infect Genet Evol 10: 192-199. doi: 10.1016/j.meegid.2009.12.007 PMID: 20060502
48. Hauser PM, Blanc DS, Sudre P, Senggen Manoloff E, Nahimana A, Bille J, et al. (2001) Genetic diversity of Pneumocystis carinii in HIV-positive and-negative patients as revealed by PCR-SSCP typing. AIDS 15: 461-466. PMID: 11242142
49. de Castro N, Neuville S, Sarfati C, Ribaud P, Derouin F, Gluckman E, et al. (2005) Occurrence of Pneumocystis jiroveci pneumonia after allogeneic stem cell transplantation: a 6-year retrospective study. Bone Marrow Transplant 36: 879-883. doi: 10.1038/sj.bmt.1705149 PMID: 16151423
50. Hauser P, Rabodonirina M, Nevez G (2009) Hypothetical Pneumocystis jirovecii transmission from immunocompetent carriers to infant. Emerg Infect Dis 15: 506-7-authorreply507. doi: 10.3201/eid1503.081350 PMID: 19239784
51. Garcia-Hermoso D, Janbon G, Dromer F (1999) Epidemiological evidence for dormant Cryptococcus neoformans infection. J Clin Microbiol 37: 3204-3209. PMID: 10488178
52. Helweg-Larsen J, Lundgren B, Lundgren JD (2001) Heterogeneity and compartmentalization of Pneumocystis carinii f. sp. hominis genotypes in autopsy lungs. J Clin Microbiol 39: 3789-3792. doi: 10.1128/JCM.39.10.3789-3792.2001 PMID: 11574620
53. de Castro N, Scemla A, Gallien S, Molina JM (2012) Pneumonie à Pneumocystis jirovecii chez les patients infectés par le VIH. Revue des maladies respiratoires 29: 793-802. doi: 10.1016/j.rmr.2011.10.975 PMID: 22742466