JOURNAL OF CLINICAL MICROBIOLOGY, Jan. 1997, p.

313316
0095-1137/97/$04.0010
Copyright q 1997, American Society for Microbiology

Vol. 35, No. 1

Candida and Torulopsis: a Blinded Evaluation of Use of Pseudohypha

Formation as Basis for Identification of Medically Important Yeasts
F. C. ODDS,1* M. G. RINALDI,2 C. R. COOPER, JR.,3 A. FOTHERGILL,2 L. PASARELL,3

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

evaluating growth on Dalmau cultures and who were blinded

as to the likely identification of the isolates.
The three participating laboratories followed similar protocols. Each laboratory prepared triplicate subcultures from single colonies of 24 yeasts selected to provide 11 to 12 isolates
representative of species in the genus Torulopsis and 11 to 12
representatives of Candida spp. Inclusion of one yeast isolate
from a genus other than Candida or Torulopsis was permitted
in each panel as a general control for identifications to the
genus level. Isolates of Candida albicans were specifically excluded, since this species is particularly distinctive by microscopic examination. The yeast cultures were randomly coded
and distributed to all participants. Dalmau plate cultures were
set up according to the methods routinely used in that laboratory, and the plates were examined microscopically after 48 h
of incubation by at least two individuals, one of whom was
experienced and the other of whom was inexperienced in reading yeast and pseudohyphal morphologies.
Techniques used for Dalmau cultures were as follows. In
laboratory A, yeasts from an overnight culture at 308C on
diluted casein hydrolysate-yeast extract-glucose medium (6)
were cross-streaked with an inoculating loop on plates of 1%
cream of rice1% Tween 80 agar with firmness sufficient to
scrape the agar surface lightly during inoculation. Sterile glass
coverslips were pressed over an inoculated area. The plates
were incubated at 258C. In laboratories B and C, yeasts from
24- to 48-h cultures incubated at 308C on Sabouraud glucose
agar were lightly streaked onto the surface of cornmeal agar
containing Tween 80. Sterile glass coverslips were placed over
the streak marks, and the plates were incubated at 308C for
48 h.
In two of the participating laboratories, the isolates were
fully identified to the species level, when possible, on the basis
of physiological profiles and according to the methods routinely used in each laboratory. Laboratory A used the API
ID32C identification galleries (Biomerieux, Marcy-lEtoile,
France). When the measured API profile led to a result de-

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

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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

tendency to elicit unexpected scores of 3 and 4, regardless of

observer experience.
The definition of a Candida species as one that forms
pseudohyphae and of a Torulopsis species as one that forms no
pseudohyphae predicts that isolates of Candida spp. should
never receive a score of 4, while scores of 1 and 2 are compatible with the genus definition, and a score of 3 indicates observer indecision. Similarly, isolates of Torulopsis spp. should
never be scored as 1 or 2, since unequivocal formation of true
or pseudohyphae is incompatible with the genus definition. In
the present study, scores of 4 were assigned to yeasts identified
as Candida spp. on 46 occasions, representing 18.8% of 245
total readings (35 isolates and seven observers), and scores of
1 or 2 were assigned to yeasts identified as Torulopsis spp. on
23 occasions, representing 9.8% of 245 total readings.
Reidentifications of yeasts by laboratories A and B were
concordant for 62 (89%) of the 70 Candida and Torulopsis
isolates. Discrepancies were noted as follows: two C. krusei
isolates identified as Candida norvegensis, two C. krusei isolates
identified as Torulopsis inconspicua, one T. inconspicua isolate
identified as C. krusei, one T. candida isolate identified as
Candida guilliermondii, one C. guilliermondii isolate identified
as T. candida, and one Torulopsis pintolopesii (not identified in
laboratory B). Identifications of Candida pelliculosa in one
laboratory and Hansenula anomala in the other were not regarded as discrepant, since the former species is the anamorph of
the other. The species C. parapsilosis (13 isolates) and T. glabrata
(26 isolates) were the two most frequently represented among
those tested, and agreement for identification of these species
was 100% between laboratories A and B. Single isolates of
Candida lambica, Candida lipolytica, Candida tropicalis, and
Candida valida and four isolates of C. lusitaniae were also
identified concordantly by both laboratories. These results
show that identifications of yeasts based predominantly on
commercially supplied kits can lead to confusion, particularly
between the triad C. krusei, C. norvegensis, and T. inconspicua.
Confusion between identifications of C. guilliermondii and T.
candida is often difficult to avoid, since these biologically different species share indistinguishable physiological properties
(1); only careful and exhaustive morphological examination for
pseudohypha formation can successfully discriminate between
these species at the phenotypic level.
Two of the three laboratories submitted only isolates of the
species C. glabrata as representatives of the genus Torulopsis.
Neither laboratory routinely isolates yeasts from samples such
as skin and nails or from veterinary sources, where other Torulopsis species are often found. Although T. glabrata is the most
commonly encountered representative of the genus Torulopsis
among clinically isolated yeasts, it is not representative of the
whole genus, as indicated by the difficulties and inconsistencies
encountered with the isolates of T. candida, T. inconspicua,
and T. pintolopesii in the study. The last species, which is the
predominant commensal yeast found in rodents, could not
even be identified with the commercial kits used for clinical
yeast isolates because it was not included in their databases.
(The identity of the isolate of C. pintolopesii used in this study
was in fact determined by the Centraalbureau voor Schimmelcultures in Delft, The Netherlands.)
This study was designed to assess whether pseudohypha formation is a reliable criterion for distinguishing among yeasts.
McGinnis defined a pseudohypha as a series of blastoconidia
that have remained attached to each other, forming a hyphalike filament (4). Van der Walts description of formation of a filamentous structure consisting of cells which arise
exclusively by budding (8) is essentially identical. However,
scrutiny of the illustrations of various Candida spp. in the

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scribed as excellent identification in the reference chart and

the morphology of the yeast conformed to the ID32C results,
that identification was recorded; when the API ID32C-based
identification was less than excellent, further physiological profiles on API 20C yeast galleries (Biomerieux) and classical
assimilation broth tests were utilized to establish the identification of the isolate. Laboratory B used the API20C identification system (BioMerieux Vitek, Hazelwood, Mo.) as well as
additional tests as necessary according to the manufacturers
instructions. Pseudohypha formation as a criterion for identification of yeasts was set up and read independently of the
blinded evaluation. When laboratories A and B disagreed over
an identification, the isolates were subjected to traditional fermentation and assimilation tests to establish the correct identity, in consultation with a yeast reference laboratory in one
instance.
Table 1 lists the 72 yeast isolates examined, the species
identifications as determined by laboratories A and B, and the
morphology scores for each isolate according to each of seven
observers. A total of four experienced (A to D) and three
inexperienced (E to G) observers recorded the morphology of
each isolate with a score of from 1 to 4, as follows: 1, unequivocal true hyphae seen; 2, unequivocal pseudohyphae (but not
true hyphae) seen; 3, pseudohyphae possibly present but equivocal; 4, definitely no formation of pseudohyphae (Table 1).
One of the isolates identified as Saccharomyces cerevisiae and
another as a yeast-like variant of Wangiella dermatitidis were
excluded from further study.
On the basis of the data in Table 1, it was calculated that
experienced observers of yeast microscopic morphology recorded a score of 3 (equivocal pseudohypha formation) 31
times, 11.1% of all 280 scores they recorded, compared with
inexperienced observers, who recorded 37 equivocal scores
(17.6% of 210 total scores). These differences were not statistically significant. Agreement between morphology scores recorded for individual isolates was perfect (identical scores) or
differed by only 1 point for 49 (70%) of the isolates when
examined by experienced observers and for 51 (73%) of the
isolates when examined by inexperienced observers. The numbers (percentages) of isolates for which morphology scores
over the entire range (1 to 4) were recorded by different observers were five (7%) and four (6%) for experienced and
inexperienced individuals, respectively.
Table 2 summarizes the score data according to the species
of yeast examined. For both experienced and inexperienced
observers, most isolates of Candida parapsilosis and Torulopsis
glabrata were given morphology scores indicating consistent
pseudohypha formation and no pseudohypha formation, respectively, by these two species. T. glabrata isolates were scored
as forming unequivocal pseudohyphae, i.e., a score of 2, in 4 of
a total of 189 readings, and all 4 of these aberrant readings
were from inexperienced observers. Similarly, for C. parapsilosis isolates, nothing was given a score of 1 (true hyphae) from
the 52 total readings from experienced observers, compared
with 2 of 36 readings by inexperienced observers.
For several of the less frequently represented species in the
study, the scores given for pseudohypha formation were more
often wide-ranging or inappropriate (on the basis of no
pseudohypha formation by Torulopsis spp.), regardless of the
experience of the observer in judging yeast cell morphology.
All four isolates of Candida lusitaniae were scored principally
as morphology level 3 or 4, i.e., equivocal or no pseudohypha
formation, while the expected score of 2 (unequivocal pseudohyphae) was recorded for only 4 of 28 observations. Isolates of
Candida krusei showed a similar although less pronounced

J. CLIN. MICROBIOL.

VOL. 35, 1997

NOTES

TABLE 1. Details of the 72 yeast isolates studied, the results of

their reidentifications in two laboratories, and the morphology
scores reported by each of seven observersa

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

Morphology scored by the

following observers:

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

Morphology scored by the

following observers:
A

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.

monograph by Van Uden and Buckley (9) shows that the

definition embraces weakly organized chains of nearly spherical yeast cells as well as highly organized branched filaments
made up of greatly elongated component cells. In much older
yeast taxonomies, different styles and appearances of pseudohyphae were used to distinguish yeast taxa (11); however, these
characteristics were later abandoned, largely because of their
variability.
In a numerical taxonomic analysis of Candida and Torulopsis
spp. (7), no natural separation between the two genera was
evident on the basis of the combined phenotypic characteristics
of the yeasts. Moreover, pseudohypha formation did not appear as a significant taxonomic marker for any of the clusters
of species that emerged from that analysis. The terms primitive pseudomycelium, rudimentary pseudomycelium, and
sparse pseudomycelium can be found in standard descriptions for several species in the genus Candida (9) and the genus
Torulopsis (10). Our study showed that inexperienced observers recorded equivocal morphologies (score of 3) more often
than experienced observers (17 versus 11%) and that the
former were responsible for almost all of the inappropriate
morphology scores recorded for the otherwise well-recognized
species C. parapsilosis and T. glabrata. Nevertheless, the differences in observer equivocation were not statistically significant,
and a generally high level of variability was seen for pseudohypha scores regardless of the experience of the observer; 19 to
21 of 70 isolates showed ranges of two or three score differences, and inappropriate morphology scores (pseudohyphae
for a Torulopsis sp. and no pseudohyphae for a Candida sp.)
were recorded overall for 69 (14%) of the 490 readings made.
Therefore, we conclude that pseudohypha formation is too
unreliable a characteristic to allow for dependable identification of medically important yeasts in the separate genera Candida and Torulopsis.
For differentiation of some species, e.g., C. guilliermondii
and Torulopsis famata, pseudohypha formation remains the
only reliable characteristic. However, it is clear from the present study that correct observation of pseudohypha formation is
vulnerable to both observer variation and technical artifacts
that emphasize the need for care beyond the norms of rapid
throughput in clinical microbiology laboratories in the identification of such difficult species.
We suggest that the proposal of Yarrow and Meyer (12) to
merge isolates previously classified as Torulopsis spp. into the

Downloaded from jcm.asm.org by on June 25, 2008

Yeast
reference
no.

Yeast identification

315

316

NOTES

J. CLIN. MICROBIOL.

TABLE 2. Summary of morphology scores for 70 yeast isolates

in the genus Candida or Torulopsisa

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.

We acknowledge the technical assistance of Leanna Jackson and

Marc Van Der Flaes.
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identification, 2nd ed. Cambridge University Press, Cambridge, United
Kingdom.
2. Davis, C. 1986. Torulopsis glabrata. Mycopathologia 96:191193.
3. Kane, J., S. Krajden, and R. C. Summerbell. 1986. Torulopsis: still legitimate
name for medically important yeast. Can. Med. Assoc. J. 135:274275.
4. McGinnis, M. R. 1980. Laboratory handbook of medical mycology. Academic Press, New York.
5. McGinnis, M. R., L. Ajello, E. S. Beneke, E. Drouhet, N. L. Goodman, C. J.
Halde, L. D. Haley, J. Kane, G. A. Land, A. A. Padhye, D. H. Pincus, M. G.
Rinaldi, A. L. Rogers, I. F. Slakin, W. A. Schell, and I. Weitzman. 1984.
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genus Candida for the reasons outlined by those authors and

by Davis (2) be accepted. We recognize that many medical
mycologists will be reluctant to abandon the name Torulopsis
and that much of the reluctance is based on the conspicuously
different morphology of T. glabrata from that of clinically encountered Candida spp. Our study has shown that, even within
the small subset of species represented by clinical yeast isolates, pseudohypha formation is not a dependable distinguishing character for routine yeast identification at the generic
level. Because of this, and because the endlessly continued
controversy over classification and nomenclature of medical

yeasts is unhelpful to medical practitioners unspecialized in

mycology, we encourage taxonomists to redress present uncertainties over the status of precedence of the name Torulopsis by
formally proposing the conservation of Candida over Torulopsis.