JCM Accepted Manuscript Posted Online 26 July 2017 J. Clin. Microbiol. doi:10.1128/JCM.00920-17 Copyright © 2017 American Society for Microbiology. All Rights Reserved.
Ustilago and Cryptococcal Antigen Tests
1
Cheng et al.
Cross-reacting Ustilago maydis Causing False-Positive Cryptococcal Antigen Tests.
3
Matthew P. Cheng*1, Tien T. Nguyen1, Leighanne O. Parkes1, Philippe J. Dufresne2, Donald C.
4
Sheppard1,3
5 6
1
7
Health Centre, Montreal, Canada
8
2
9
Montreal, Canada
Division of Infectious Diseases and Department of Medical Microbiology, McGill University
Institute national de santé publique du Québec, Laboratoire de santé publique du Québec,
10
3
11
Health Centre, Montreal, Canada.
Infectious Diseases in Global Health Program, Research Institute of the McGill University
12 13
Pages: 7
14
Tables: 1
15
Boxes: 0
16
Figures: 0
17
References: 16
18
Word count: 571
19
Key Words (5): “Ustilago”, “Rhodotorula”, “Sporobolomyces”, “Cryptococcus”, “Antigen”
20 21
*Correspondence to: Dr. Matthew P. Cheng, Division of Infectious Diseases and Department of
22
Medical Microbiology, Glen site, McGill University Health Centre, 1001 Boulevard Décarie,
23
room E05. 1811.2, Montreal, Canada H4A 3J1
24
Tel.: +1 514 934 1934; E-mail: [email protected]
25
Downloaded from http://jcm.asm.org/ on July 26, 2017 by TUFTS UNIV LIBRARIES
1 2
Ustilago and Cryptococcal Antigen Tests
26
2
Cheng et al.
TO THE EDITOR Cryptococcus neoformans is a yeast within the division Basidiomycota that may cause
28
pulmonary and central nervous system (CNS) disease. Detection of cryptococcal polysaccharide
29
antigen by latex agglutination (LA) and lateral flow assay (LFA) are sensitive and specific tests
30
for the diagnosis of invasive disease (1, 2), however cross-reactivity has been described with
31
Trichosporon asahii (3). Our objective was to determine if there is cross reactivity with other
32
Basidiomycete yeasts, including rare agents of human disease, such as Rhodotorula,
33
Sporobolomyces and Ustilago spp. (4-8).
34
Clinical isolates of Trichosporon, Rhodotorula, Sporobolomyces, and Ustilago species
35
were retrieved from the Quebec provincial reference laboratory (LSPQ). Sporobolomyces spp., T.
36
asahii, R. glutinis, R. minuta, and R. mucilaginosa isolates were taxonomically confirmed by
37
MALDI-TOF (VITEK MS, bioMérieux, Inc. QC, Canada). Ustilago spp. and R. sloofiae were
38
confirmed by sequencing their ribosomal DNA D1D2 and ITS regions. Cryptococcus neoformans
39
(LSPQ-16-A479650) and Candida albicans (ATCC strain 60433) strains were used as positive
40
and negative controls, respectively. Growth in Sabouraud dextrose broth was confirmed by
41
measuring an increase in optical density after 24 hours (DensiCHEK™ Plus, bioMérieux, Inc.).
42
Turbidity was adjusted to a 0.5 MacFarland (MF) standard equivalent, and organism count/ml
43
was determined by hemocytometer. This turbidity corresponded to an average of 3.2
44
organisms/ml (standard deviation 0.9 organisms/ml), which is similar to the organism burden
45
reported in the cerebrospinal fluid of patients with cryptococcal meningitis (9). Serial two-fold
46
dilutions were performed to determine the cut-off of positivity.
47
LA testing was performed using the CALAS™ cryptococcal antigen latex agglutination
48
kit (Meridian Bioscience, Inc., OH, USA). Flocculation was graded on a scale from 0 to 4, with 2
Downloaded from http://jcm.asm.org/ on July 26, 2017 by TUFTS UNIV LIBRARIES
27
Ustilago and Cryptococcal Antigen Tests
3
Cheng et al.
or more representing a positive result. LFA testing was performed using the IMMY cryptococcal
50
lateral flow assay (Immuno-Mycologics, Inc., OK, USA). Testing for both assays was done per
51
the manufacturer's instructions and assessed in a blinded fashion. In total, 23 samples were tested,
52
including nine isolates of Rhotodorula spp., five isolates of Sporobolomyces salmonicolor, three
53
isolates of Trichosporon asahii, and three isolates of Ustilago maydis (Table 1). Only C.
54
neoformans, Trichosporon and Ustilago isolates were unequivocally positive on both assays. One
55
Rhodotorula mucilaginosa and one Sporobolomyces salmonicolor isolate had discordant results;
56
both were weakly positive results on the LA assay at titers of 1:1 and 1:4 respectively, but were
57
negative on the LFA. All other isolates had concordant results between assays at 0.5 MF,
58
although some with different cut-offs for positivity (Table 1).
59
Our findings demonstrate that unlike Rhodotorula and Sporobolomyces spp.,
60
Trichosporon asahii and Ustilago maydis yield positive results on cryptococcal antigen assays at
61
clinically relevant concentrations, with excellent inter-assay agreement. The plant pathogens
62
Ustilago spp. (the agent of corn smut), and the closely related Pseudozyma spp. are ubiquitous in
63
the environment and are commonly regarded as laboratory contaminants. However, these
64
organisms can be transmitted by the airborne route and have occasionally caused fungemia and
65
central venous catheter infections in humans (5, 7, 10-16).
66
In conclusion, our results validate the cross-reactivity of Trichosporon asahii as
67
previously reported, and help delineate the limitations in specificity of cryptococcal antigen
68
testing for the detection of other basidiomycetous yeasts. Although this study is limited to in vitro
69
observations, our results suggest that these tests should not be used as an adjunct to diagnose
70
invasive infections caused by Rhodotorula or Sporobolomyces species, but may be considered for
71
Trichosporon asahii and Ustilago maydis. The fact that not all Basidiomycetes tested produced a
Downloaded from http://jcm.asm.org/ on July 26, 2017 by TUFTS UNIV LIBRARIES
49
Ustilago and Cryptococcal Antigen Tests
4
Cheng et al.
cross-reaction in the two assays suggests there is no conserved cross-reacting antigen produced
73
by all members of the division Basidiomycota.
74
CONTRIBUTORS AND ACKNOWLEDGEMENTS
75
Contributors: MPC, TTN and LOP performed literature searches, devised the experiments, and
76
drafted the manuscript. PJD and DCS were responsible for the overall content.
77 78
Potential conflicts of interest: We declare that we have no conflicts of interest.
79 80
Source of funding: This project was done as part of routine work. DCS was supported by a
81
Research Chair from the Fonds de Recherche Quebec Santé
Downloaded from http://jcm.asm.org/ on July 26, 2017 by TUFTS UNIV LIBRARIES
72
Ustilago and Cryptococcal Antigen Tests
82
5
Cheng et al.
TABLE 1: Inter-assay agreement Sample
Number Cryptococcal of isolates Antigen Latex N/A 1+
Titer
Cryptococcal Titer LFA N/A
84
test that was positive at a 1:1 dilution.
85
**A single Sporobolomyces salmonicolor isolate gave a weakly positive cryptococcal antigen
86
latex test that was positive at a 1:4 dilution.
87 88
Downloaded from http://jcm.asm.org/ on July 26, 2017 by TUFTS UNIV LIBRARIES
83
Control (-): Sabbouraud N/A dextrose broth Control (-): C. albicans 1 1+ N/A N/A (ATCC strain 60433) Control (+): C. neoformans 1 4+ 1:1024 + 1:256 1 1+ N/A N/A Rhodotorula glutinis 2 1+ N/A N/A Rhodotorula minuta 5 1+ N/A N/A Rhodotorula mucilaginosa* 1 1+ N/A N/A Rhodotorula sloofiae 5 1+ N/A N/A Sporobolomyces salmonicolor** 3 4+ 1:32 + 1:32 Trichosporon asahii 3 4+ 1:32 + 1:16 Ustilago maydis *A single Rhodotorula mucilaginosa isolate gave a weakly positive cryptococcal antigen latex
Ustilago and Cryptococcal Antigen Tests
89
REFERENCES
90
1.
6
Cheng et al.
Hansen J, Slechta ES, Gates-Hollingsworth MA, Neary B, Barker AP, Bauman S, Kozel TR, Hanson KE. 2013. Large-scale evaluation of the immuno-mycologics lateral
92
flow and enzyme-linked immunoassays for detection of cryptococcal antigen in serum
93
and cerebrospinal fluid. Clin Vaccine Immunol 20:52-55.
94
2.
Kauffman CA, Bergman AG, Severance PJ, McClatchey KD. 1981. Detection of
95
cryptococcal antigen. Comparison of two latex agglutination tests. Am J Clin Pathol
96
75:106-109.
97
3.
McManus EJ, Jones JM. 1985. Detection of a Trichosporon beigelii antigen cross-
98
reactive with Cryptococcus neoformans capsular polysaccharide in serum from a patient
99
with disseminated Trichosporon infection. J Clin Microbiol 21:681-685.
100
4.
Arendrup MC, Boekhout T, Akova M, Meis JF, Cornely OA, Lortholary O,
101
European Society of Clinical M, Infectious Diseases Fungal Infection Study G,
102
European Confederation of Medical M. 2014. ESCMID and ECMM joint clinical
103
guidelines for the diagnosis and management of rare invasive yeast infections. Clin
104
Microbiol Infect 20 Suppl 3:76-98.
105
5.
106 107
McGhie TA, Huber TW, Kassis CE, Jinadatha C. 2013. Ustilago species as a cause of central line-related blood stream infection. Am J Med Sci 345:254-255.
6.
Moore M, Russell WO, Sachs E. 1946. Chronic Leptomeningitis and Ependymitis
108
Caused by Ustilago, Probably U. Zeae (Corn Smut): Ustilagomycosis, the Second
109
Reported Instance of Human Infection. Am J Pathol 22:761-777.
Downloaded from http://jcm.asm.org/ on July 26, 2017 by TUFTS UNIV LIBRARIES
91
Ustilago and Cryptococcal Antigen Tests
110
7.
111 112
7
Cheng et al.
Patel R, Roberts GD, Kelly DG, Walker RC. 1995. Central venous catheter infection due to Ustilago species. Clin Infect Dis 21:1043-1044.
8.
Stewart E, Waldman S, Sutton DA, Sanders C, Lindner J, Fan H, Wiederhold NP, Thompson GR, 3rd. 2016. Ustilago echinata: Infection in a Mixed Martial Artist
114
Following an Open Fracture. Mycopathologia 181:311-314.
115
9.
Jarvis JN, Bicanic T, Loyse A, Namarika D, Jackson A, Nussbaum JC, Longley N,
116
Muzoora C, Phulusa J, Taseera K, Kanyembe C, Wilson D, Hosseinipour MC,
117
Brouwer AE, Limmathurotsakul D, White N, van der Horst C, Wood R, Meintjes G,
118
Bradley J, Jaffar S, Harrison T. 2014. Determinants of mortality in a combined cohort
119
of 501 patients with HIV-associated Cryptococcal meningitis: implications for improving
120
outcomes. Clin Infect Dis 58:736-745.
121
10.
Herb A, Sabou M, Delhorme JB, Pessaux P, Mutter D, Candolfi E, Letscher-Bru V.
122
2015. Pseudozyma aphidis fungemia after abdominal surgery: First adult case. Med
123
Mycol Case Rep 8:37-39.
124
11.
Joo H, Choi YG, Cho SY, Choi JK, Lee DG, Kim HJ, Jo I, Park YJ, Lee KY. 2016.
125
Pseudozyma aphidis fungaemia with invasive fungal pneumonia in a patient with acute
126
myeloid leukaemia: case report and literature review. Mycoses 59:56-61.
127
12.
Lin SS, Pranikoff T, Smith SF, Brandt ME, Gilbert K, Palavecino EL, Shetty AK.
128
2008. Central venous catheter infection associated with Pseudozyma aphidis in a child
129
with short gut syndrome. J Med Microbiol 57:516-518.
Downloaded from http://jcm.asm.org/ on July 26, 2017 by TUFTS UNIV LIBRARIES
113
Ustilago and Cryptococcal Antigen Tests
130
13.
8
Cheng et al.
Orecchini LA, Olmos E, Taverna CG, Murisengo OA, Szuzs W, Vivot W, Cordoba S, Bosco-Borgeat ME, Montanaro PC. 2015. First Case of Fungemia Due to
132
Pseudozyma aphidis in a Pediatric Patient with Osteosarcoma in Latin America. J Clin
133
Microbiol 53:3691-3694.
134
14.
Pande A, Non LR, Romee R, Santos CA. 2017. Pseudozyma and other non-Candida
135
opportunistic yeast bloodstream infections in a large stem cell transplant center. Transpl
136
Infect Dis 19.
137
15.
Prakash A, Wankhede S, Singh PK, Agarwal K, Kathuria S, Sengupta S, Barman P,
138
Meis JF, Chowdhary A. 2014. First neonatal case of fungaemia due to Pseudozyma
139
aphidis and a global literature review. Mycoses 57:64-68.
140
16.
Siddiqui W, Ahmed Y, Albrecht H, Weissman S. 2014. Pseudozyma spp catheter-
141
associated blood stream infection, an emerging pathogen and brief literature review. BMJ
142
Case Rep 2014.
143
Downloaded from http://jcm.asm.org/ on July 26, 2017 by TUFTS UNIV LIBRARIES
131
Ustilago and Cryptococcal Antigen Tests
1
Cheng et al.
Cross-reacting Ustilago maydis Causing False-Positive Cryptococcal Antigen Tests.
3
Matthew P. Cheng*1, Tien T. Nguyen1, Leighanne O. Parkes1, Philippe J. Dufresne2, Donald C.
4
Sheppard1,3
5 6
1
7
Health Centre, Montreal, Canada
8
2
9
Montreal, Canada
Division of Infectious Diseases and Department of Medical Microbiology, McGill University
Institute national de santé publique du Québec, Laboratoire de santé publique du Québec,
10
3
11
Health Centre, Montreal, Canada.
Infectious Diseases in Global Health Program, Research Institute of the McGill University
12 13
Pages: 7
14
Tables: 1
15
Boxes: 0
16
Figures: 0
17
References: 16
18
Word count: 571
19
Key Words (5): “Ustilago”, “Rhodotorula”, “Sporobolomyces”, “Cryptococcus”, “Antigen”
20 21
*Correspondence to: Dr. Matthew P. Cheng, Division of Infectious Diseases and Department of
22
Medical Microbiology, Glen site, McGill University Health Centre, 1001 Boulevard Décarie,
23
room E05. 1811.2, Montreal, Canada H4A 3J1
24
Tel.: +1 514 934 1934; E-mail: [email protected]
25
Downloaded from http://jcm.asm.org/ on July 26, 2017 by TUFTS UNIV LIBRARIES
1 2
Ustilago and Cryptococcal Antigen Tests
26
2
Cheng et al.
TO THE EDITOR Cryptococcus neoformans is a yeast within the division Basidiomycota that may cause
28
pulmonary and central nervous system (CNS) disease. Detection of cryptococcal polysaccharide
29
antigen by latex agglutination (LA) and lateral flow assay (LFA) are sensitive and specific tests
30
for the diagnosis of invasive disease (1, 2), however cross-reactivity has been described with
31
Trichosporon asahii (3). Our objective was to determine if there is cross reactivity with other
32
Basidiomycete yeasts, including rare agents of human disease, such as Rhodotorula,
33
Sporobolomyces and Ustilago spp. (4-8).
34
Clinical isolates of Trichosporon, Rhodotorula, Sporobolomyces, and Ustilago species
35
were retrieved from the Quebec provincial reference laboratory (LSPQ). Sporobolomyces spp., T.
36
asahii, R. glutinis, R. minuta, and R. mucilaginosa isolates were taxonomically confirmed by
37
MALDI-TOF (VITEK MS, bioMérieux, Inc. QC, Canada). Ustilago spp. and R. sloofiae were
38
confirmed by sequencing their ribosomal DNA D1D2 and ITS regions. Cryptococcus neoformans
39
(LSPQ-16-A479650) and Candida albicans (ATCC strain 60433) strains were used as positive
40
and negative controls, respectively. Growth in Sabouraud dextrose broth was confirmed by
41
measuring an increase in optical density after 24 hours (DensiCHEK™ Plus, bioMérieux, Inc.).
42
Turbidity was adjusted to a 0.5 MacFarland (MF) standard equivalent, and organism count/ml
43
was determined by hemocytometer. This turbidity corresponded to an average of 3.2
44
organisms/ml (standard deviation 0.9 organisms/ml), which is similar to the organism burden
45
reported in the cerebrospinal fluid of patients with cryptococcal meningitis (9). Serial two-fold
46
dilutions were performed to determine the cut-off of positivity.
47
LA testing was performed using the CALAS™ cryptococcal antigen latex agglutination
48
kit (Meridian Bioscience, Inc., OH, USA). Flocculation was graded on a scale from 0 to 4, with 2
Downloaded from http://jcm.asm.org/ on July 26, 2017 by TUFTS UNIV LIBRARIES
27
Ustilago and Cryptococcal Antigen Tests
3
Cheng et al.
or more representing a positive result. LFA testing was performed using the IMMY cryptococcal
50
lateral flow assay (Immuno-Mycologics, Inc., OK, USA). Testing for both assays was done per
51
the manufacturer's instructions and assessed in a blinded fashion. In total, 23 samples were tested,
52
including nine isolates of Rhotodorula spp., five isolates of Sporobolomyces salmonicolor, three
53
isolates of Trichosporon asahii, and three isolates of Ustilago maydis (Table 1). Only C.
54
neoformans, Trichosporon and Ustilago isolates were unequivocally positive on both assays. One
55
Rhodotorula mucilaginosa and one Sporobolomyces salmonicolor isolate had discordant results;
56
both were weakly positive results on the LA assay at titers of 1:1 and 1:4 respectively, but were
57
negative on the LFA. All other isolates had concordant results between assays at 0.5 MF,
58
although some with different cut-offs for positivity (Table 1).
59
Our findings demonstrate that unlike Rhodotorula and Sporobolomyces spp.,
60
Trichosporon asahii and Ustilago maydis yield positive results on cryptococcal antigen assays at
61
clinically relevant concentrations, with excellent inter-assay agreement. The plant pathogens
62
Ustilago spp. (the agent of corn smut), and the closely related Pseudozyma spp. are ubiquitous in
63
the environment and are commonly regarded as laboratory contaminants. However, these
64
organisms can be transmitted by the airborne route and have occasionally caused fungemia and
65
central venous catheter infections in humans (5, 7, 10-16).
66
In conclusion, our results validate the cross-reactivity of Trichosporon asahii as
67
previously reported, and help delineate the limitations in specificity of cryptococcal antigen
68
testing for the detection of other basidiomycetous yeasts. Although this study is limited to in vitro
69
observations, our results suggest that these tests should not be used as an adjunct to diagnose
70
invasive infections caused by Rhodotorula or Sporobolomyces species, but may be considered for
71
Trichosporon asahii and Ustilago maydis. The fact that not all Basidiomycetes tested produced a
Downloaded from http://jcm.asm.org/ on July 26, 2017 by TUFTS UNIV LIBRARIES
49
Ustilago and Cryptococcal Antigen Tests
4
Cheng et al.
cross-reaction in the two assays suggests there is no conserved cross-reacting antigen produced
73
by all members of the division Basidiomycota.
74
CONTRIBUTORS AND ACKNOWLEDGEMENTS
75
Contributors: MPC, TTN and LOP performed literature searches, devised the experiments, and
76
drafted the manuscript. PJD and DCS were responsible for the overall content.
77 78
Potential conflicts of interest: We declare that we have no conflicts of interest.
79 80
Source of funding: This project was done as part of routine work. DCS was supported by a
81
Research Chair from the Fonds de Recherche Quebec Santé
Downloaded from http://jcm.asm.org/ on July 26, 2017 by TUFTS UNIV LIBRARIES
72
Ustilago and Cryptococcal Antigen Tests
82
5
Cheng et al.
TABLE 1: Inter-assay agreement Sample
Number Cryptococcal of isolates Antigen Latex N/A 1+
Titer
Cryptococcal Titer LFA N/A
84
test that was positive at a 1:1 dilution.
85
**A single Sporobolomyces salmonicolor isolate gave a weakly positive cryptococcal antigen
86
latex test that was positive at a 1:4 dilution.
87 88
Downloaded from http://jcm.asm.org/ on July 26, 2017 by TUFTS UNIV LIBRARIES
83
Control (-): Sabbouraud N/A dextrose broth Control (-): C. albicans 1 1+ N/A N/A (ATCC strain 60433) Control (+): C. neoformans 1 4+ 1:1024 + 1:256 1 1+ N/A N/A Rhodotorula glutinis 2 1+ N/A N/A Rhodotorula minuta 5 1+ N/A N/A Rhodotorula mucilaginosa* 1 1+ N/A N/A Rhodotorula sloofiae 5 1+ N/A N/A Sporobolomyces salmonicolor** 3 4+ 1:32 + 1:32 Trichosporon asahii 3 4+ 1:32 + 1:16 Ustilago maydis *A single Rhodotorula mucilaginosa isolate gave a weakly positive cryptococcal antigen latex
Ustilago and Cryptococcal Antigen Tests
89
REFERENCES
90
1.
6
Cheng et al.
Hansen J, Slechta ES, Gates-Hollingsworth MA, Neary B, Barker AP, Bauman S, Kozel TR, Hanson KE. 2013. Large-scale evaluation of the immuno-mycologics lateral
92
flow and enzyme-linked immunoassays for detection of cryptococcal antigen in serum
93
and cerebrospinal fluid. Clin Vaccine Immunol 20:52-55.
94
2.
Kauffman CA, Bergman AG, Severance PJ, McClatchey KD. 1981. Detection of
95
cryptococcal antigen. Comparison of two latex agglutination tests. Am J Clin Pathol
96
75:106-109.
97
3.
McManus EJ, Jones JM. 1985. Detection of a Trichosporon beigelii antigen cross-
98
reactive with Cryptococcus neoformans capsular polysaccharide in serum from a patient
99
with disseminated Trichosporon infection. J Clin Microbiol 21:681-685.
100
4.
Arendrup MC, Boekhout T, Akova M, Meis JF, Cornely OA, Lortholary O,
101
European Society of Clinical M, Infectious Diseases Fungal Infection Study G,
102
European Confederation of Medical M. 2014. ESCMID and ECMM joint clinical
103
guidelines for the diagnosis and management of rare invasive yeast infections. Clin
104
Microbiol Infect 20 Suppl 3:76-98.
105
5.
106 107
McGhie TA, Huber TW, Kassis CE, Jinadatha C. 2013. Ustilago species as a cause of central line-related blood stream infection. Am J Med Sci 345:254-255.
6.
Moore M, Russell WO, Sachs E. 1946. Chronic Leptomeningitis and Ependymitis
108
Caused by Ustilago, Probably U. Zeae (Corn Smut): Ustilagomycosis, the Second
109
Reported Instance of Human Infection. Am J Pathol 22:761-777.
Downloaded from http://jcm.asm.org/ on July 26, 2017 by TUFTS UNIV LIBRARIES
91
Ustilago and Cryptococcal Antigen Tests
110
7.
111 112
7
Cheng et al.
Patel R, Roberts GD, Kelly DG, Walker RC. 1995. Central venous catheter infection due to Ustilago species. Clin Infect Dis 21:1043-1044.
8.
Stewart E, Waldman S, Sutton DA, Sanders C, Lindner J, Fan H, Wiederhold NP, Thompson GR, 3rd. 2016. Ustilago echinata: Infection in a Mixed Martial Artist
114
Following an Open Fracture. Mycopathologia 181:311-314.
115
9.
Jarvis JN, Bicanic T, Loyse A, Namarika D, Jackson A, Nussbaum JC, Longley N,
116
Muzoora C, Phulusa J, Taseera K, Kanyembe C, Wilson D, Hosseinipour MC,
117
Brouwer AE, Limmathurotsakul D, White N, van der Horst C, Wood R, Meintjes G,
118
Bradley J, Jaffar S, Harrison T. 2014. Determinants of mortality in a combined cohort
119
of 501 patients with HIV-associated Cryptococcal meningitis: implications for improving
120
outcomes. Clin Infect Dis 58:736-745.
121
10.
Herb A, Sabou M, Delhorme JB, Pessaux P, Mutter D, Candolfi E, Letscher-Bru V.
122
2015. Pseudozyma aphidis fungemia after abdominal surgery: First adult case. Med
123
Mycol Case Rep 8:37-39.
124
11.
Joo H, Choi YG, Cho SY, Choi JK, Lee DG, Kim HJ, Jo I, Park YJ, Lee KY. 2016.
125
Pseudozyma aphidis fungaemia with invasive fungal pneumonia in a patient with acute
126
myeloid leukaemia: case report and literature review. Mycoses 59:56-61.
127
12.
Lin SS, Pranikoff T, Smith SF, Brandt ME, Gilbert K, Palavecino EL, Shetty AK.
128
2008. Central venous catheter infection associated with Pseudozyma aphidis in a child
129
with short gut syndrome. J Med Microbiol 57:516-518.
Downloaded from http://jcm.asm.org/ on July 26, 2017 by TUFTS UNIV LIBRARIES
113
Ustilago and Cryptococcal Antigen Tests
130
13.
8
Cheng et al.
Orecchini LA, Olmos E, Taverna CG, Murisengo OA, Szuzs W, Vivot W, Cordoba S, Bosco-Borgeat ME, Montanaro PC. 2015. First Case of Fungemia Due to
132
Pseudozyma aphidis in a Pediatric Patient with Osteosarcoma in Latin America. J Clin
133
Microbiol 53:3691-3694.
134
14.
Pande A, Non LR, Romee R, Santos CA. 2017. Pseudozyma and other non-Candida
135
opportunistic yeast bloodstream infections in a large stem cell transplant center. Transpl
136
Infect Dis 19.
137
15.
Prakash A, Wankhede S, Singh PK, Agarwal K, Kathuria S, Sengupta S, Barman P,
138
Meis JF, Chowdhary A. 2014. First neonatal case of fungaemia due to Pseudozyma
139
aphidis and a global literature review. Mycoses 57:64-68.
140
16.
Siddiqui W, Ahmed Y, Albrecht H, Weissman S. 2014. Pseudozyma spp catheter-
141
associated blood stream infection, an emerging pathogen and brief literature review. BMJ
142
Case Rep 2014.
143
Downloaded from http://jcm.asm.org/ on July 26, 2017 by TUFTS UNIV LIBRARIES
131
