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313316
0095-1137/97/$04.0010
Copyright q 1997, American Society for Microbiology
AND
M. R. MCGINNIS3
Department of Bacteriology and Mycology, Janssen Research Foundation, 2340-Beerse, Belgium ; Fungus Testing Laboratory,
University of Texas Health Science Center, San Antonio, Texas 782842; and Medical Mycology Research Center, Center for
Tropical Diseases and Department of Pathology, University of Texas Medical Branch, Galveston, Texas 775553
Received 26 January 1996/Returned for modification 12 April 1996/Accepted 16 October 1996
The genera Candida and Torulopsis have traditionally contained asexual yeasts that have no distinguishing morphologic
or other characteristics to facilitate a more precise classification. They are essentially heterogeneous-form genera whose
members are defined by negative rather than positive properties (1, 9, 10). Classification within the genus Candida or Torulopsis does not necessarily imply close taxonomic relationships
among member species.
The taxonomic status of the genera Candida and Torulopsis
has been a source of controversy for many years. The two
genera have been distinguished by their ability (Candida) or
lack of ability (Torulopsis) to form pseudohyphae when cultured under microaerophilic conditions or on an appropriate
agar medium by the so-called Dalmau technique, which involves scoring the inoculum into the agar (4). In an influential
monograph on yeast taxonomy published in 1970, Van Uden
and Buckley considered that the distinction between Candida
and Torulopsis spp. was arbitrary and artificial but retained
the separation to avoid the confusion and justified irritation
that abolition of the generic distinction would create among
those who use or encounter species in these genera (9).
Nevertheless, in 1978 Yarrow and Meyer (12) formally proposed deletion of the genus Torulopsis and the transfer of
Torulopsis spp. into the genus Candida. This proposal was
rejected in two later publications (3, 5). Because 18 years have
passed since the proposal to merge Torulopsis spp. into the
genus Candida was made, we felt that a scientific reappraisal of
the validity of separate identifications of Candida and Torulopsis spp. was appropriate. The intention of the study was to
assess the consistency of recording observations of pseudohypha formation by personnel experienced and inexperienced in
* Corresponding author. Mailing address: Department of Bacteriology and Mycology, Janssen Research Foundation, B-2340 Beerse, Belgium. Phone: 32 14-603004. Fax: 32 14-605403.
313
Seventy yeast isolates representing species in the genera Candida and Torulopsis but excluding Candida
albicans were examined in three laboratories for production of pseudohyphae in Dalmau cultures. The microscopic morphology of the isolates was scrutinized by four individuals experienced in yeast identification and
three inexperienced persons, all of whom were blinded as to the putative identification of the yeasts. For 49
(70%) of the 70 isolates, the seven observers recorded comparable scores for morphology, but 5 (7%) of the
isolates showed extreme variation in recorded morphologies, from true hyphae formed to no pseudohyphae
formed. Isolates of Candida parapsilosis and Torulopsis glabrata consistently did and did not form pseudohyphae, respectively: however, other Candida and Torulopsis spp. did not always express their expected morphologies. In 48 (19%) of 252 readings (seven observers), 36 isolates of Candida spp. were scored as forming no
pseudohyphae, and in 22 (9.2%) of 238 readings, 34 isolates of Torulopsis spp. were recorded as forming true
hyphae or pseudohyphae. These results show that pseudohypha formation is not a reliable characteristic for
identification of yeasts at the genus level; we suggest that the merger of Torulopsis spp. into the genus Candida
should be finally accepted.
314
NOTES
J. CLIN. MICROBIOL.
NOTES
TABLE 1Continued
Laboratory A
Laboratory B
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
61
62
63
64
T. glabrata
C. krusei
C. norvegensis
C. parapsilosis
T. glabrata
C. lusitaniae
T. glabrata
No identification
C. lipolytica
C. lusitaniae
C. krusei
T. glabrata
T. glabrata
T. glabrata
C. krusei
T. glabrata
C. parapsilosis
T. glabrata
C. parapsilosis
C. krusei
T. glabrata
T. glabrata
C. parapsilosis
T. glabrata
C. parapsilosis
C. krusei
T. glabrata
C. guilliermondii
T. candida
C. valida
C. lambica
T. inconspicua
S. cerevisiae
C. pelliculosa
T. candida
C. norvegensis
T. pintolopesiid
T. inconspicuab
T. glabrata
C. guilliermondii
T. candidab
T. candida
C. guilliermondii
C. guilliermondiib
T. inconspicua
C. pelliculosa
C. pelliculosa
T. glabrata
T. glabrata
T. glabrata
C. parapsilosis
C. krusei
T. glabrata
T. glabrata
T. glabrata
C. parapsilosis
T. glabrata
C. parapsilosis
C. parapsilosis
T. glabrata
T. glabrata
C. parapsilosis
T. glabrata
C. parapsilosis
T. glabrata
C. krusei
C. kruseib
C. parapsilosis
T. glabrata
C. lusitaniae
T. glabrata
W. dermatitidisc
C. lipolytica
C. lusitaniae
C. krusei
T. glabrata
T. glabrata
T. glabrata
C. krusei
T. glabrata
C. parapsilosis
T. glabrata
C. parapsilosis
C. krusei
T. glabrata
T. glabrata
C. parapsilosis
T. glabrata
C. parapsilosis
C. krusei
T. glabrata
C. guilliermondii
T. candida
C. krusei
C. lambica
C. kruseib
S. cerevisiae
H. anomala
T. candida
C. kruseib
No identification
C. krusei
T. glabrata
C. guilliermondii
C. guilliermondii
T. candida
C. guilliermondii
T. candida
C. kruseib
H. anomala
H. anomala
T. glabrata
T. glabrata
T. glabrata
C. parapsilosis
C. krusei
T. glabrata
T. glabrata
T. glabrata
C. parapsilosis
T. glabrata
C. parapsilosis
C. parapsilosis
T. glabrata
T. glabrata
C. parapsilosis
T. glabrata
C. parapsilosis
4
3
2
2
4
4
4
2
2
4
3
4
4
4
2
4
2
4
2
2
4
4
2
4
2
2
4
2
3
4
2
4
2
4
3
4
2
4
4
4
3
4
2
3
4
4
4
4
4
4
2
4
4
4
3
2
4
2
2
4
4
2
4
2
4
3
2
2
4
4
4
2
1
4
3
4
4
4
3
3
2
4
2
2
4
4
2
4
2
2
4
2
4
2
2
2
4
3
4
2
4
4
4
2
3
4
2
4
2
3
3
4
4
4
2
2
4
4
3
2
3
2
2
4
4
2
4
2
4
2
1
2
4
4
4
4
1
2
2
4
4
4
2
3
2
4
2
1
4
4
2
4
2
2
4
3
2
2
2
2
2
2
2
4
2
2
4
2
2
3
2
2
2
2
2
4
4
4
2
2
4
4
3
2
4
2
2
3
4
2
4
2
4
4
1
2
4
4
3
4
2
4
3
4
4
4
4
3
2
4
2
4
4
4
2
4
2
1
4
2
4
1
1
1
4
3
4
2
4
4
4
1
4
4
1
4
1
3
3
4
4
4
2
3
4
4
4
2
4
2
2
3
4
2
4
2
4
4
1
2
4
4
4
1
1
3
4
3
3
4
2
2
2
4
2
3
4
4
2
3
2
3
2
2
4
3
2
4
2
2
2
2
3
4
4
3
4
2
2
4
4
2
2
4
3
4
1
4
4
4
4
2
4
2
2
2
4
2
4
2
4
4
1
2
3
4
4
4
2
4
4
4
4
4
4
3
2
4
2
4
4
4
2
4
1
1
3
1
4
1
1
1
3
2
4
2
3
2
2
4
3
4
1
4
1
4
3
3
4
4
4
4
3
4
3
2
4
2
2
3
3
2
4
2
4
2
1
2
4
4
4
4
1
3
2
4
4
4
2
3
2
4
2
2
4
4
2
4
2
2
4
3
4
1
2
1
2
3
3
4
4
3
4
3
3
4
2
3
1
3
3
4
4
4
2
1
4
4
4
2
4
2
2
3
3
2
4
2
Continued
Yeast
reference
no.
65
66
67
68
69
70
71
72
Yeast identification
Laboratory A
C. parapsilosis
T. glabrata
C. lusitaniae
T. glabrata
C. lusitaniae
C. tropicalis
T. glabrata
T. glabrata
Laboratory B
C. parapsilosis
T. glabrata
C. lusitaniae
T. glabrata
C. lusitaniae
C. tropicalis
T. glabrata
T. glabrata
2
4
3
4
2
2
4
4
2
4
4
4
4
1
4
4
2
4
2
4
4
2
4
4
2
4
4
4
4
1
4
4
2
4
3
4
2
1
4
4
2
3
4
4
3
1
4
4
2
4
4
4
4
1
4
4
a
Scores are as follows: 1, true hypha formation; 2, unequivocal pseudohypha
formation; 3, equivocal pseudohypha formation; 4, no pseudohyphae formed.
b
Correct identification based on traditional tests.
c
An albino, mutant strain (Mel3 [ATCC44504]) of this normally darkly pigmented yeast was employed in this study.
d
This identification was confirmed by the Centraalbureau voor Schimmelcultures at Delft, The Netherlands.
Yeast
reference
no.
Yeast identification
315
316
NOTES
J. CLIN. MICROBIOL.
Yeast species
C. guilliermondii
C. krusei
C. lambica
C. lipolytica
C. lusitaniae
C. parapsilosis
C. pelliculosa
C. tropicalis
C. valida
T. candida
T. glabrata
T. inconspicua
T. pintolopesii
With experienced
observers, no. of
times morphology
received the
following scores:
No. of
isolates
4
10
1
1
4
12
3
1
1
4
27
1
1
With inexperienced
observers, no. of
times morphology
received the
following scores:
2
6
1
2
0
0
0
2
1
0
0
0
0
9
19
3
2
3
48
3
2
2
3
0
1
2
2
7
0
0
1
0
6
0
0
5
10
0
0
3
8
0
0
12
0
3
0
1
8
98
3
2
2
9
1
2
0
2
0
3
2
0
0
0
0
3
8
2
1
1
33
4
0
0
2
4
1
0
4
2
0
0
4
0
4
0
1
3
16
2
2
3
11
0
0
7
1
1
0
0
7
61
0
1
a
The numbers of times that isolates within each species were scored as 1, 2, 3,
or 4 by four experienced and three inexperienced observers are tabulated.