Rapid differentiation of Aspergillus species from other medically important opportunistic molds and yeasts by PCR-enzyme immunoassay

Journal of Clinical Microbiology

Volumn 42, Issue 8, 2004, Pages 3495-3504

  De Aguirre, Liliana ^a,c   Hurst, Steven F ^a   Choi, Jong Soo ^a,d   Shin, Jong Hee ^a,e   Hinrikson, Hans Peter ^a,f   Morrison, Christine J ^a,b  

^a NATIONAL CENTER FOR EMERGING AND ZOONOTIC INFECTIOUS DISEASES   (United States)

^b CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^c Inst de Investigations Veterinarias   (Venezuela)

^d Yeungnam University Hospital   (South Korea)

^e Chonnam National University Medical School   (South Korea)

^f LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; ASPERGILLOSIS; ASPERGILLUS; CELL DIFFERENTIATION; DNA EXTRACTION; DNA PROBE; ENZYME IMMUNOASSAY; MOULD; NONHUMAN; NUCLEOTIDE SEQUENCE; OPPORTUNISTIC INFECTION; PARASITE IDENTIFICATION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTOZOAL INFECTION; SPECIES DIFFERENTIATION; YEAST;

ANIMALS; ASPERGILLOSIS; ASPERGILLUS; BASE SEQUENCE; DNA PRIMERS; DNA PROBES; DNA, FUNGAL; DNA, RIBOSOMAL; FOOD MICROBIOLOGY; HUMANS; IMMUNOENZYME TECHNIQUES; POLYMERASE CHAIN REACTION; RABBITS; YEASTS;

ANIMALIA; ASPERGILLUS; ASPERGILLUS FLAVUS; ASPERGILLUS FUMIGATUS; ASPERGILLUS NIGER; ASPERGILLUS TERREUS; ASPERGILLUS USTUS; ASPERGILLUS VERSICOLOR; CANDIDA; EMERICELLA NIDULANS; EXOPHIALA; FUNGI; FUSARIUM; MUCOR; ORYCTOLAGUS CUNICULUS; PAECILOMYCES; PENICILLIUM; PROTOZOA; RHIZOPUS; SCEDOSPORIUM; SPOROTHRIX;

EID: 3843062469     PISSN: 00951137     EISSN: None     Source Type: Journal    
DOI: 10.1128/JCM.42.8.3495-3504.2004     Document Type: Article

References (72)

1. Ascioglu, S. J., H. Rex, B. de Pauw, J. E. Bennett, J. Bille, F. Crokaert, D. W. Denning, J. P. Donnelly, J. E. Edwards, Z. Erjavec, D. Fiere, O. Lortholary, J. Maertens, J. F. Meis, T. F. Patterson, J. Ritter, D. Selleslag, P. M. Shah, D. A. Stevens, T. J. Walsh, et al. 2002. Defining opportunistic invasive fungal infections in immunocompromised patients with cancer and hematopoietic stem cell transplants: an international consensus. Clin. Infect. Dis. 34:7-14.
2. Baddley, J. W., P. G. Pappas, A. C. Smith, and S. A. Moser. 2003. Epidemiology of Aspergillus terreus at a university hospital. J. Clin. Microbiol. 41:5525-5529.
3. Bialek, R., A. Feucht, C. Aepinus, G. Just-Nübling, V. J. Robertson, J. Knobloch, and R. Hohle. 2002. Evaluation of two nested PCR assays for detection of Histoplasma capsulatum DNA in human tissue. J. Clin. Microbiol. 40:1644-1647.
4. Blum, U., M. Windfuhr, C. Buitrago-Tellez, G. Sigmund, E. W. Herbst, and M. Langer. 1994. Invasive pulmonary aspergillosis: MRI, CT, and plain radiographic findings and their contribution for early diagnosis. Chest 106:1156-1161.
5. Bretagne, S., J. M. Costa, E. Bart-Delabesse, N. Dhedin, C. Rieux, and C. Cordonnier. 1998. Comparison of serum galactomannan antigen detection and competitive polymerase chain reaction for diagnosing invasive aspergillosis. Clin. Infect. Dis. 26:1407-1412.
6. Bretagne, S., J. M. Costa, A. Marmorat-Khuong, F. Poron, C. Cordonnier, M. Vidaud, and J. Fleury-Feith. 1995. Detection of Aspergillus species DNA in bronchoalveolar lavage samples by competitive PCR. J. Clin. Microbiol. 33:1164-1168.
7. Caillot, D., O. Cassanovas, A. Bernard, J. F. Couaillier, C. Durand, B. Cuisenierr, E. Solary, F. Piard, T. Petrella, A. Bonnin, G. Couaillault, M. Dumas, and H. Guy. 1997. Improved management of invasive pulmonary aspergillosis in neutropenic patients using early thoracic computed tomographic scan and surgery. J. Clin. Oncol. 15:139-147.
8. Catten, M., A. H. Murr, J. A. Goldstein, A. N. Mhatre, and A. K. Lalwani. 2001. Detection of fungi in the nasal mucosa using polymerase chain reaction. Laryngoscope 111:399-403.
9. Chang, J.-M., H. Oyaizu, and J. Sugiyama. 1991. Phylogenetic relationships among eleven selected species of Aspergillus and associated teleomorphic genera estimated from 18S ribosomal RNA partial sequences. J. Gen. Appl. Microbiol. 37:289-308.
10. Chen, S. C. A., C. L. Halliday, and W. Meyer. 2002. A review of nucleic acid-based diagnostic tests for systemic mycoses with an emphasis on polymerase chain reaction-based assays. Med. Mycol. 40:333-357.
11. Cornet, M., L. Fleury, C. Maslo, J. F. Bernard, G. Brucker, and the Invasive Aspergillosis Surveillance Network of the Assistance Publique-Hopitaux de Paris. 2002. Epidemiology of invasive aspergillosis in France: a six-year multicentric survey in the Greater Paris area. J. Hosp. Infect. 51:288-296.
12. Costa, C., D. Vidaud, M. Olivi, E. Bart-Delabesse, M. Vidaud, and S. Bretagne. 2001. Development of two real-time quantitative TaqMan PCR assays to detect circulating Aspergillus fumigatus DNA in serum. J. Microbiol. Methods 44:263-269.
13. Denning, D. W. 1998. Invasive aspergillosis. Clin. Infect. Dis. 26:781-803.
14. Denning, D. W. 1996. Therapeutic outcome in invasive aspergillosis. Clin. Infect. Dis. 23:608-615.
15. Einsele, H., H. Hebart, G. Roller, J. Loeffier, I. Rothenhofer, C. A. Muller, R. A. Bowden, J.-A. van Burik, D. Engelhard, L. Kanz, and U. Schumacher. 1997. Detection and identification of fungal pathogens in blood by using molecular probes. J. Clin. Microbiol. 35:1353-1360.
16. Elie, C. M., T. J. Lott, E. Reiss, and C. J. Morrison. 1998. Rapid identification of Candida species with species-specific DNA probes. J. Clin. Microbiol. 36:3260-3265.
17. Ellepola, A. N. B., S. F. Hurst, C. M. Elie, and C. J. Morrison. 2003. Rapid and unequivocal differentiation of Candida dubliniensis from other Candida species using species-specific DNA probes: comparison with phenotypic identification methods. Oral Microbiol. Immunol. 18:379-388.
18. Fortun, J., P. Martin-Davila, A. Sanchez-Souza, C. Quereda, E. Navas, R. Barcena, E. Vicente, A. Candelas, A. Honrubia, J. Nuno, V. Pintado, S. Moreno, et al. 2001. Aspergillus antigenemia sandwich-enzyme immunoassay test as a serodiagnostic method for invasive aspergillosis in liver transplant recipients. Transplantation 71:145-149.
19. Fujita, S.-I., B. A. Lasker, T. J. Lott, E. Reiss, and C. J. Morrison. 1995. Microtitration plate enzyme immunoassay to detect PCR-amplified DNA from Candida species in blood. J. Clin. Microbiol. 33:962-967.
20. Hall, L., S. Wohlfiel, and G. D. Roberts. 2003. Experience with the MicroSeq D2 large-subunit ribosomal DNA sequencing kit for the identification of commonly encountered, clinically important yeast species. J. Clin. Microbiol. 41:5099-5102.
21. Hashimoto, A., Y. Yamakami, P. Kamberi, E. Yamagata, R. Karashima, H. Nagaoka, and M. Nasu. 1998. Comparison of PCR, (1-3)-beta-glucan, and galactomannan assays in sera of rats with experimental invasive aspergillosis. J. Clin. Lab. Anal. 12:257-262.
22. Hayden, R. T., P. A. Isotalo, T. Parrett, D. M. Wolk, X. Qian, G. D. Roberts, and R. V. Lloyd. 2003. In situ hybridization for the differentiation of Aspergillus, Fusarium, and Pseudallescheria species in tissue section. Diagn. Mol. Pathol. 12:21-26.
23. Hayette, M.-P., D. Vaira, F. Susin, P. Boland, G. Christiaens, P. Melin, and P. De Mol. 2001. Detection of Aspergillus species DNA by PCR in bronchoalveolar lavage fluid. J. Clin. Microbiol. 39:2338-2340.
24. Henry, T., P. C. Iwen, and S. H. Hinrichs. 2000. Identification of Aspergillus species using internal transcribed spacer regions 1 and 2. J. Clin. Microbiol. 38:1510-1515.
25. Hung, C. C., S. C. Chang, P. C. Yang, and W. C. Hseigh. 1994. Invasive pulmonary pseudallescheriasis with direct invasion of the thoracic spine in an immunocompromised patient. Eur. J. Clin. Infect. Dis. 13:749-751.
26. Hurst, S. F., G. H. Reyes, D. W. McLaughlin, E. Reiss, and C. J. Morrison. 2000. Comparative evaluation of commercial latex agglutination and sandwich enzyme immunoassays with a competitive binding inhibition enzyme immunoassay to detect antigenemia and antigenuria for the rapid diagnosis of invasive aspergillosis. Clin. Diagn. Lab. Immunol. 7:477-485.
27. Iwen, P. C., M. E. Rupp, A. N. Langnas, E. C. Reed, and S. H. Hinrichs. 1998. Invasive pulmonary aspergillosis due to Aspergillus terreus: 12-year experience and review of the literature. Clin. Infect. Dis. 26:1092-1097.
28. Iwen, P. C., S. H. Hinrichs, and M. E. Rupp. 2002. Utilization of the internal transcribed spacer regions as molecular targets to detect and identify human fungal pathogens. Med. Mycol. 40:87-109.
29. Kambouris, M. E., U. Reichard, N. J. Legakis, and A. Velegraki. 1999. Sequences from the aspergillopepsin PEP gene of Aspergillus fumigatus: evidence on their use in selective PCR identification of Aspergillus species in infected clinical samples. FEMS Immunol. Med. Microbiol. 25:255-264.
30. Kami, M., T. Fukui, S. Ogawa, Y. Kazuyama, U. Machida, Y. Tanaka, Y. Kanda, T. Kashima, Y. Yamazaki, T. Hamaki, S.-I. Mori, H. Akiyama, Y. Mutou, H. Sakamaki, K. Osumi, S. Kimura, and H. Hirai. 2001. Use of real-time PCR on blood samples for diagnosis of invasive aspergillosis. Clin. Infect. Dis. 33:1504-1512.
31. Kappe, R., C. N. Okeke, C. Fauser, M. Maiwald, and H. G. Sonntag. 1998. Molecular probes for the detection of pathogenic fungi in the presence of human tissue. J. Med. Microbiol. 47:811-820.
32. Kaufman, L., P. G. Standard, M. Jalbert, and D. E. Kraft. 1997. Immunohistologic identification of Aspergillus spp. and other hyaline fungi by using polyclonal fluorescent antibodies. J. Clin. Microbiol. 35:2206-2209.
33. Kawamura, S., S. Maeski, T. Noda, Y. Hirakata, K. Tomono, T. Tashiro, and S. Kohno. 1999. Comparison between PCR and detection of antigen in sera for diagnosis of pulmonary aspergillosis. J. Clin. Microbiol. 37:218-220.
34. Kumeda, Y., and T. Asao. 1996. Single-strand conformational polymorphism analysis of PCR-amplified ribosomal DNA internal transcribed spacers to differentiate species of Aspergillus section Flavi. Appl. Environ. Microbiol. 62:2947-2952.
35. Kwok, S., and R. Higuichi. 1989. Avoiding false positives with PCR. Nature (London) 39:237-238.
36. Lass-Florl, C., J. Aigner, E. Gunsilius, A. Petzer, D. Nachbaur, G. Gastl, H. Einsele, J. Loffier, M. P. Dierich, and R. Wurzner. 2001. Screening for Aspergillus spp. using polymerase chain reaction of whole blood samples from patients with hematological malignancies. Br. J. Haematol. 113:180-184.
37. Lass-Florl, C., G. Kofler, G. Kropshofer, J. Hermans, A. Kreczy, M. P. Dierich, and D. Niederwieser. 1998. In vitro testing of susceptibility to amphotericin B is a reliable predictor of clinical outcome in invasive aspergillosis. J. Antimicrob. Chemother. 42:497-502.
38. Lin, S.-J., J. Schranz, and S. M. Teutsch. 2001. Aspergillosis case-fatality rate: systematic review of the literature. Clin. Infect. Dis. 32:358-366.
39. Lindsley, M. D., S. F. Hurst, N. J. Iqbal, and C. J. Morrison. 2001. Rapid identification of dimorphic and yeast-like fungal pathogens using specific DNA probes. J. Clin. Microbiol. 39:3505-3511.
40. Loeffler, J., K. Schmidt, H. Hebart, U. Schumacher, and H. Einsele. 2002. Automated extraction of genomic DNA from medically important yeast species and filamentous fungi by using the MagNA Pure LC system. J. Clin. Microbiol. 40:2240-2243.
41. Loeffler, J., N. Henke, H. Hebart, D. Schmidt, L. Hagmeyer, U. Schumacher, and H. Einsele. 2000. Quantification of fungal DNA by using fluorescence resonance energy transfer and the light cycler system. J. Clin. Microbiol. 38:586-590.
42. Loeffler, J., H. Hebart, R. Bialek, L. Hagmeyer, D. Schmidt, F. P. Serey, M. Hartmann, J. Eucker, and H. Einsele. 1999. Contaminations occurring in fungal PCR assays. J. Clin. Microbiol. 37:1200-1202.
43. Loeffler, J., H. Hebart, U. Schumacher, H. Reitze, and H. Einsele. 1997. Comparison of different methods for extraction of DNA of fungal pathogens from cultures and blood. J. Clin. Microbiol. 35:3311-3312.
44. Maertens, J., J. Verhaegen, H. Demuynck, P. Brock, G. Verhoef, P. Vandenberghe, J. Van Eldere, L. Verbist, and M. Boogaerts. 1999. Autopsy-controlled prospective evaluation of serial screening for circulating galactomannan by a sandwich enzyme-linked immunosorbent assay for hematological patients at risk for invasive aspergillosis. J. Clin. Microbiol. 37:3223-3228.
45. McNeil, M. M., S. L. Nash, R. A. Hajjeh, M. A. Phelan, L. A. Conn, B. D. Plikaytis, and D. W. Warnock. 2001. Trends in mortality due to invasive mycotic diseases in the United States, 1980-1997. Clin. Infect. Dis. 33:641-647.
46. Montone, K. T., and L. A. Litzky. 1995. Rapid method for detection of Aspergillus 5S ribosomal RNA using a genus-specific oligonucleotide probe. Am. J. Clin. Pathol. 103:48-51.
47. Morrison, C. J. 2002. Laboratory diagnosis of opportunistic infections in the intensive care unit, p. 55-104. In R. A. Barnes and D. W. Warnock (ed.), Fungal infection in the intensive care unit. Kluwer Academic Publishers, Norwell, Mass.
48. Morrison, C. J., S. F. Hurst, S. L. Bragg, R. J. Kuykendall, H. Diaz, J. Pohl, and E. Reiss. 1993. Heterogeneity of the purified extracellular aspartyl proteinase from Candida albicans: characterization with monoclonal antibodies and N-terminus amino acid sequence analysis. Infect. Immun. 61:2030-2036.
49. Morrison, C. J., S. F. Hurst, and E. Reiss. 2003. Competitive binding inhibition enzyme-linked immunosorbent assay that uses the secreted aspartyl proteinase of Candida albicans as an antigenic marker for diagnosis of disseminated candidiasis. Clin. Diagn. Lab. Immunol. 10:835-848.
50. Müller, F. M., K. E. Werner, M. Kasai, A. Francesconi, S. J. Chanock, and T. J. Walsh. 1998. Rapid extraction of genomic DNA from medically important yeasts and filamentous fungi by high-speed cell disruption. J. Clin. Microbiol. 36:1625-1629.
51. Nolan, C. 1989. Appendix E: Commonly used techniques in molecular cloning, p. E.1-E. 39. In J. Sambrook, E. F. Fritsch, and T. Maniatis (ed.), Molecular cloning: a laboratory manual, 2nd ed, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
52. O'Sullivan, C. E., M. Kasai, A. Francesconi, V. Petratis, R. Petraitiene, A. M. Kelaher, A. A. Sarafandi, and T. J. Walsh. 2003. Development and validation of a quantitative real-time PCR assay using fluorescence resonance energy transfer technology for detection of Aspergillus fumigatus in experimental invasive pulmonary aspergillosis. J. Clin. Microbiol. 41:5676-5682.
53. Park, C. S., J. Kim, and K. T. Montone. 1997. Detection of Aspergillus ribosomal RNA using biotinylated oligonucleotide probes. Diagn. Mol. Pathol. 6:255-260.
54. Peterson, S. W. 2000. Phylogenetic relationships in Aspergillus based on rDNA sequence analysis, p. 323-355. In R. A. Samson and J. I. Pitt (ed.), Integration of modern taxonomic methods for Penicillium and Aspergillus classification. Harwood Academic Publishers, Amsterdam, The Netherlands.
55. Pryce, T. M., S. Pallidino, D. Kay, and G. W. Coombs. 2003. Rapid identification of fungi by sequencing the ITS1 and ITS2 regions using an automated capillary electrophoresis system. Med. Mycol. 41:369-381.
56. Rath, P. M., and R. Ansorg. 2000. Identification of medically important Aspergillus species by single strand conformational polymorphism (SSCP) of the PCR-amplified intergenic spacer region. Mycoses 43:381-386.
57. Salonen, J., O. P. Lehtonen, M. R. Terasjarvi, and J. Nikoskelainen. 2000. Aspergillus antigen in serum, urine, and bronchoalveolar lavage specimens of neutropenic patients in relation to clinical outcome. Scand. J. Infect. Dis. 32:485-490.
58. Shin, J.-H., F. S. Nolte, B. P. Holloway, and C. J. Morrison. 1999. 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. 37:165-170.
59. Shin, J.-H., F. S. Nolte, and C. J. Morrison. 1997. Rapid identification of Candida species in blood cultures by a clinically useful PCR method. J. Clin. Microbiol. 35:1454-1459.
60. Skladny, H., D. Buchheidt, C. Baust, F. Krieg-Schneider, W. Seifarth, C. Leib-Mosch, and R. Hehlmann. 1999. Specific detection of Aspergillus species in blood and bronchoalveolar lavage samples of immunocompromised patients by two-step PCR. J. Clin. Microbiol. 37:3865-3871.
61. Stynen, D., J. Sarfati, A. Goris, M. C. Prevost, M. Lesourd, H. Kamphuis, V. Darras, and J. P. Latge. 1992. Rat monoclonal antibodies against Aspergillus galactomannan. Infect. Immun. 60:2237-2245.
62. Sutton, D. A., S. E. Sanche, S. G. Revankar, A. W. Fothergill, and R. G. Rinaldi. 1999. In vitro amphotericin B resistance in clinical isolates of Aspergillus terreus, with head-to-tail comparison to voriconazole. J. Clin. Microbiol. 37:2343-2345.
63. Turenne, C. Y., S. E. Sanche, D. J. Hoban, J. A. Karlowsky, and A. M. Kabani. 1999. Rapid identification of fungi by using the ITS2 genetic region and an automated fluorescent capillary electrophoresis system. J. Clin. Microbiol. 37:1846-1851.
64. Verweij, P. E., D. Poulain, T. Obayashi, T. F. Patterson, D. W. Denning, and J. Ponton. 1998. Current trends in the detection of antigenemia, metabolites, and cell markers for the diagnosis and therapeutic monitoring of fungal infections. Med. Mycol. 36(Suppl. 1):146-155.
65. Verweij, P. E., J. P. Latge, A. J. Rijs, W. J. Melchers, B. E. De Pauw, J. A. Hoogkamp-Korstanje, and J. F. Meis. 1995. Comparison of antigen detection and PCR assay using bronchoalveolar lavage fluid for diagnosing invasive pulmonary aspergillosis in patients receiving treatment for hematological malignancies. J. Clin. Microbiol. 33:3150-3153.
66. Wald, A., W. Leisenring, J. van Burik, and R. A. Bowden. 1997. Natural history of aspergillus infections in a large cohort of patients undergoing bone marrow transplantation. J. Infect. Dis. 175:1459-1466.
67. Walsh, T. J., A. Francesconi, M. Kasai, and S. J. Chanock. 1995. PCR and single-strand conformational polymorphism for recognition of medically important opportunistic fungi. J. Clin. Microbiol. 33:3216-3220.
68. White, T. J., T. D. Burns, S. B. Lee, and J. W. Taylor. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics, p. 315-322. In M. A. Innis, D, H. Helfand, J. J. Sninsky, and T. J. White (ed.), PCR protocols. Academic Press, Inc., San Diego, Calif.
69. Wu, Z., Y. Tsumura, G. Blomquist, and X.-R. Wang. 2003. 18S rRNA gene variation among common airborne fungi, and development of specific oligonucleotide probes for the detection of fungal isolates. Appl. Environ. Microbiol. 69:5389-5397.
70. Yamakami, Y., A. Hashimoto, I. Tokimatsu, and M. Nasu. 1996. PCR detection of DNA specific for Aspergillus species in serum of patients with invasive aspergillosis. J. Clin. Microbiol. 34:2464-2468.
71. Yeo, S. F., and B. Wong. 2002. Current status of nonculture methods for diagnosis of invasive fungal infections. Clin. Microbiol. Rev. 15:465-484.
72. Zhao, J., F. Kong, R. Li, X. Wang, Z. Wan, and D. Wang. 2001. Identification of Aspergillus fumigatus and related species by nested PCR targeting ribosomal DNA internal transcribed spacer regions. J. Clin. Microbiol. 39:2261-2266.