World Journal of AIDS, 2013, 3, 201-206 Published Online September 2013 (
Copyright © 2013 SciRes. WJA
Characterization of Candida Species Isolated from Cases
of Lower Res piratory Tra ct Infection among HIV/AIDS
Patients in Calabar, Nigeria*
Ofonime Mark Ogba1, Lydia Nyong Abia-Bassey2, James Epoke2, Baki Idasa Mandor1,
Godwin Dickson Iwatt3
1Department of Medical Microbiology/Parasitology, University of Calabar Teaching Hospital, Calabar, Nigeria; 2Department of
Medical Laboratory Science, University of Calabar, Calabar, Nigeria; 3Department of Microbiology, University of Calabar, Calabar,
Received June 2nd, 2013; revised July 2nd, 2013; accepted August 2nd, 2013
Copyright © 2013 Ofonime Mark Ogba et al. This is an open access article distributed under the Creative Commons Attribution Li-
cense, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
This study was designed to identify and characterize the Candida species isolated from lower respiratory tract infections
among HIV positive patients and to determine the prevalence rates of Candida infections among these subjects. Two
early morning expectorate sputum samples were collected from 272 HIV pos itive subjects visiting the ART clinics and
DOTS centre with cases of lower respiratory tract infection, over a period of 14 months from May 2009 to July 2010 in
Calabar. Subjects were recruited for this study upon approval by the Ethical Research Committee of the University of
Calabar Teaching Hospital and obtaining written informed consent from the patients. Samples were processed by stan-
dard methods for isolation of Candida . Speciation was done by a germ tube test, chlamydospore production on corn
meal agar and sugar fermentation and assimilation tests using the Microexpr ess Candida identif ication kit (Tulip, India).
Out of the 544 sputum samples collected from 272 subjects, Candida species were isolated from 40 (14.7%) and identi-
fied after confirming the growth in the second sample. The majority of Candida species among the Candida isolates
were Candida albicans (80%) followed by Candida tropicalis 5 (12.5%), Candida dubliniensis 2 (5.0%) and Candida
guilliermondii 1 (2.5%). The isolation rate of Candida species from sputum samples was found to be highest among
subjects aged 25 - 34 years, followed by those aged 15 - 24 years. Twenty (7.3%) H IV seropositiv e subjec ts had bacte-
rial infections, while 4 (1.5%) subjects had mixed fungal and bacterial infections. This study is the first of its kind to be
carried out in Calabar and the South-South geopolitical region of Nigeria, and has shown that pulmonary candidiasis is
a health problem among HIV positive patients in Calabar.
Keywords: Candida Infections; Pulmonary; HIV/A IDS; Characterization
1. Introduction
Candida is a polymorphic fungus. It is a Gram positive,
oval, budding yeast cell that produces pseudohyphae both
in culture and in tissues and exudates [1]. They exhibit fi-
lamentous mycellial morphology in the saprophytic
phase, but have typical yeast morphology in the parasitic
phase, in tissue and when grown at 37˚C in the laboratory
[1]. They form pseudohyphae when the buds continue to
grow but fail to detach, producing chains of elongated
cells that are pinched or constricted at the septations be-
tween cells [2]. At temperatures below 26˚C in nutrition-
ally poor media such as cornmeal agar, it produces thick-
walled resting cells 7 to 17 mm in diameter, called chla-
mydospores [3]. It is a member of the normal flora of the
mucous membranes in the gastrointestinal, upper respira-
tory and female genital tracts [4].
There are about 68 species of Candida, the most path-
ogenic is C. albicans [5]. The other non-albicans Candida
(NAC) species include C. dubliniensis, C. glabrata, C.
guilliermondii, C. tropicalis, C. parapsilosis, C. krusei
and C. hisitaniae, C. kefyr, C. lipolytic and C. pelliculos
Candida pneumonia is one of the most challenging of
all the Candida infections. Primary Candida pneumonia
refers to infections limited to the lungs, while secondary
Candida pneumonia indicates lung involvement due to
Conflicts of Interests: None declared.
Characterization of Candida Species Isolated from Cases of Lower Respiratory
Tracr Infection among HIV/AIDS Patients in Calabar, Nigera
Copyright © 2013 SciRes. WJA
the movement of invasive Candida from other areas of
the body [5]. The criteria for the diagnosis of pulmonary
candidiasis are still controversial. The isolation of Can-
dida from culture of sputum, endotracheal aspirates, bron -
choscopic samples, percutaneous lung needle aspirates
and even from lung tissue may only represent coloniza-
tion of the trachea-bronchial tree [4]. Despite the debate
about the diagnosis of pulmonary candidiasis, the defini-
tive diagnosis is still resting on histological demonstra-
tion of the yeast in lung tiss ue with associated infla mma-
tory changes at autopsy [7,8].
The increase in the number of immunocompromised
patients during the last few decades, as a result of che-
motherapy or HIV/AIDS has resulted in a parallel in-
crease in the number of opportunistic infections, espe-
cially those due to Candida species [9,10].
Rapid identification and speciation of Candida species
are essential in clinical laboratories. However, no single
phenotypic test is highly ef fective in identifying Candida
species and the combination of tests is sometimes neces-
sary for identification. Molecular techniques have been
employed to characterize Candida spp. Although sensi-
tive and specific it is not cost effective for routine clini-
cal mycology laboratories in a resource constrained setup
like ours [11].
2. Aims and Objectives
The aim of the study was to determine the rate of iso-
lation of Candida species from sputum samples of HIV
positive patients with respiratory symptoms, to identify
and characterize the Candida species using various phe-
notypic methods such as Germ tube test, Chlamydospore
production and identification to specie level with Mi-
croxpress Candida identification kit (Tulip diagnostic
LTD, India), according to the manufacturer’s instruc-
3. Materials and Methods
3.1. Study Sites and Subjects Selection
The present study was carried out in the department of
Microbiology/Parasitology, University of Calabar Teach-
ing Hospital, Calabar. Subjects were recruited from two
tertiary hospitals; the University of Calabar Teaching
Hospital and Lawrence Henshaw Hospital located in Ca-
labar municipality and Calabar south local Government
areas respectively. The cases selected for the study inclu-
ded HIV positive subjects with respiratory symptoms
who were able to produce sputum. Sputum samples show-
ing less than 10 squamous epithelial cells and 25 or more
polymorphonuclear leukocytes per low power field (100×)
were included in this study.
3.2. Collection and Examination of Samples
A total of 272 sputum samples in duplicates were col-
lected from May 2009 to July 2010 from the subjects. All
sputum sp ecimens were processed by Gram staining, 10%
KOH mount, culture, germ tube test, detection of chla-
mydospore and sugars fermentation and assimilation
tests. A 10% KOH mount of sputum sample showing
plenty of Candida pseudohyphae were considered as po-
tential pathogens and not as colonizers. The isolates were
considered significant by correlation with microscopy
and growth of two consecutive cultures. The Candida
species were isolated repeatedly in pure culture from two
consecutive early mornings expectorate sputum samples
[4]. Speciation of Candida was by germ tube test, mor-
phology on corn meal agar, sugar fermentation and assi-
milation tests using Microexpress Candida id entification
kits (Tulip, India) according to the manufacturer’s in-
structions [4, 12].
3.3. Direct Examination of the Specimens
3.3.1. Gram Stain
Smears made from the most purulent: or mucopurulent
part of the sputum. Smears were examined for the pres-
ence of gram positive budding yeast cells with pseudohy-
phae. Specimen was considered as acceptable when 25 or
more polymorphonuclear leukocytes were seen per low
power field (100×) with few (less than 10) squamous epi-
thelial cells.
3.3.2. KOH Mount
Smears were prepared for each sample by adding a loop
full of sputum to a drop of 10% KOH on a clean, grease-
free slide and placing a cover slip over it. The prepara-
tions were slightly warmed to digest the materials and
examined under the microscope with X10 and X40 ob-
jective for yeast cells, pseudohyphae [12].
3.3.3. Culture
The most bloody, purulent, or mucus laden portions of
sputum samples were inoculated on Sabouraud Dextrose
Agar (SDA) with and without chloramphenicol (16
µgml1) in duplicates incubated at 37˚C and 25˚C. Cul-
tures were examined every other day for growth up to 2
weeks before discarding as negative [12,13]. The macro-
scopic features of the growth wer e opaque pasty glab rous
or membranous texture often with the sweet smell, remi-
niscent of ripe apples. The growth was confirmed by ob-
serving the characteristic budding with pseudohyphae in
the Gram stain [10]. Pure cultures of every isolate were
prepared before performing any physiological test. This
was done by sub-culturing individual isolates onto fresh
SDA plates and incubating at 37˚C and at room tempe-
Characterization of Candida Species Isolated from Cases of Lower Respiratory
Tracr Infection among HIV/AIDS Patients in Calabar, Nigera
Copyright © 2013 SciRes. WJA
rature (25˚C - 28˚C) for 24 - 48 hours [12]. Any signifi-
cant bacterial growth from SDA without chlorampheni-
col was purified on Cystein Lactose Electrolyte D eficient
(CLED) agar, for further biochemical analysis and iden-
tificatio n [13]. Ide ntification of i s ol a te s wa s ba s e d on gross
morphological characteristics, detailed study of stained
sampl e s and bi ochemical tests [14].
3.5. Identification of Candida Isolates
3.5.1. Germ Tube Test
All presumptive Candida species were subjected to germ
tube test. Colonies from the purity plate were picked to
perform the germ tube test. Small test tubes containing
about 0.5 ml human serum were inoculated with colonies
of test organisms in batches of three replicates per test.
Each batch included a known positive and negative con-
trol. Inoculated tubes were incubated at 37˚C for 2 - 3
hours. At the end of incubation, a drop of each serum
was transferred to a clean slide, and a cover slip placed
over it. These slides were examined microscopically un-
der high power (×40) objective to detect the presence of
germ tubes, which are short hyphal initials [4,9].
3.5.2. Chlamydospore Formation
All Candida isolates were tested for the production of
chlamydospores in corn meal agar (CMA) with 1% Tween
80. Subcultures on corn meal agar plates, was made from
SDA purity plate by furrowing the CMA plates (cut streak
method), and incubating at room temperature (25˚C -
28˚C) for 2 - 5 days after which they were examined for
the production of thick-walled chlamydospores in a lac-
tophenol cotton blue mount of samples taken from the
furrows of the corn meal agar plates [4,15].
3.5.3. Sugar Fermentation Test
All Candida isolates were subjected to carbohydrate fer-
mentation and utilization test using Candida identifica-
tion kit, Tulip Diagnostics Limited, India. Each kit con-
tained sterile media for colorimetric identification using
biochemical test and carbohydrate utilization tests based
on the principle of pH change and substrate utilization
designed to identify various metabolic properties of dif-
ferent Candida species, that can be used to differentiate
even closely related Candida species. The media were in-
oculated by adding 100 µl of the Candida suspension, in-
cubated at 20˚C - 25˚C and read after 24 - 48 hours in-
cubation. The Candidal suspension was prepared by puri-
fying on a Brain Heart Infusion Agar (BHIA) medium,
after which a single discrete colony was picked up and
streaked on to BHI agar slant for enrichment and incu-
bated at 20˚C - 25˚C (room temperature) for 24 - 48
hours. Th e growth on the slant was washed with 2 - 3 ml
of sterile saline and the turbidity of the suspension com-
pared with Mcfarland standard number 5. The results
were interpreted as per the standards given in the result
interpretation chart.
4. Results
A total of 272 sputum samples were collected from all
the HIV positive subjects enrolled during the study. Out
of which 40 (14.7%) Candida species were isolated and
identified after confirming the growth in the second sam-
ple. The majority of Candida species among the Candida
isolates were Candida albicans (80%) followed by Can-
dida tropicalis 5 (12.5%), Candida dubliniensis 2 (5.0%)
and Candida guilliermondii 1 (2.5%) (Table 1 ).
The isolation rate of Candida species from sputum
samples was found to be highest among subjects aged 25
- 34 years, followed by those aged 15 - 24 years. No
Candida species were isolated from subjects aged 65 - 74
years (Table 2). Table 3 shows the prevalence of bacte-
rial pathogens amongst the subjects. Twenty (7.3%) HIV
seropositive subjects had bacterial infections. Out of which
11 (4.0%) were infected with Klebsiella pneumoniae, 6
(2.2%) with Pseudomonas aeruginosa and 3 (1.1%) with
Proteus specie.
Table 4 shows the distribution of polymicrobial infec-
tions among the HIV-positive subjects. Out of the 4
(1.5%) subjects with mixed infections, 3 (75.0%) had
Candida albicans and Klebsiella pneumoniae infections,
while one subject (25.0%) had Klebsiella pneumoniae &
Candida tropicalis infection.
Table 5 shows the specific characteristics of isolates
of Candida species established with Microxpress Can-
dida identification kit (Tulip diagnostics LTD, India).
5. Discussion
The diagnosis of pulmonary candidiasis is difficult not
because it is difficult to demonstrate the organism in cli-
nical samples but because isolation of Candida species in
sputum does not necessarily mean that a person is suf-
fering from pulmonary candidiasis. A good clinical cor-
Table 1. Distribution of Candida isolates among subjects.
Candida species No of isolates
(n = 272) Percentage of
isolates (%)
Candida albicans 32 80
Candida tropical is 5 12.5
Candida dubliniensis 2 5.0
Candida guilliermondii 1 2.5
Total 40 14.7
Characterization of Candida Species Isolated from Cases of Lower Respiratory
Tracr Infection among HIV/AIDS Patients in Calabar, Nigera
Copyright © 2013 SciRes. WJA
Table 2. Age and gender distribution of Candida species
among subjects.
Age (years) Gender Candida species Total (%)
15 - 24 Female (F) 5 Candida albicans
2 Candida tropicalis 9 (22.5)
Male (M) 2 Candida albicans
25 - 34
Female (F) 12 Candida albicans
3 Candida tropicalis
19 (47.5)
Male (M) 3 Candida albicans
1 Candida
35 - 44
Female (F) 2 Candida albicans
4 (10.0)
Male (M) 1 Candida albicans
1 Candida dubliniensis
45 - 54
Female (F) 4 Candida albicans
7 (17.5)
Male (M) 2 Candida albicans
1 Candida dubliniensis
55 - 64 Female (F) - 1 (2.5)
Male (M) 1 Candida albicans
65 - 74 Female (F) - 0 (0.0)
Male (M) -
Total 40 (100)
Denotes n o Candida species was isolated.
Table 3. Distribution of bacterial pathogens from sputum
samples of subjects.
Bacteria pathogens No of isolates (n = 272)
K. pneumonia 11 (4.0)
P. aeruginosa 6 (2.2)
Proteus specie 3 (1.1)
Total 20 (7.3)
Table 4. Polymicrobial isolation from HIV positive subjects.
Types of isolates No of isolates (%)
(n = 272)
Candida albicans & Klebsiella pneumonia 3 (75.0)
Candida tropical is & klebsiella pneumonia 1 (25.0)
Total 4 (1.5%)
relation is therefore necessary to ascertain the clinical sig-
nificance of the isolate [4].
The total number of Candida species isolated during
the study was 40 (14.7%). These is higher than the 12.1%
prevalence reported in India by Jha et al. [3], but consid-
erably lower than 48% prevalence reported in New York,
USA by Diaz-Fuentes et al. [7]. The low prevalence rate
of candidiasis recorded in this study as compared to the
48% reported in America could have been due to t he fac t
that Diaz-Fu entes et al. [7] recovered the Candida iso-
lates at autopsy from lung tissues which is a definitive di-
agnostic technique for pulmonary candidiasis. It is likely
that none of their isolates were lost. Candida species ge-
nerally remains the most implicated opportunistic fungal
pathogen in HIV/AIDS infection probably because it is
an endogenous op portunist.
Candida albicans were found to be the most common
species with 32 (80%) isolates. This was followed in de-
scending order of prevalence by C. tropicalis 5 (12.5%),
C. dubliniensis 2 (5.0%) and C. guilliermondii 1 (2.5%)
(Table 1). Aluyi et al. [16] in Edo state, Nigeria found
the distribution of Candida species among patients to be
as follows: C. albicans (49.3%), C. stellatoidea (25.4%)
and C. parapsilosis (25.3%). A multicenter surveillance
study conducted in Quebec, Canada in 2001 reported a
distribution pattern for Candida as follows: C. albicans
(64%), C. tropicalis (17%), C. parapsilosis (8%), C. gla-
batra (6%) and C. krusei (2%) [17]. The findings of the
present study are different from the above studies. This
could be due to variation in geographical distribution of
various Candida species.
The isolation rate of Candida species from sputum
samples was found to be highest among subjects aged 25
- 34 years, followed by those aged 15 - 24 years. No
Candida species were isolated from subjects aged 65 - 74
years (Ta ble 2) . Jha et al. [3], found the iso lation rates of
Candida species highest among subjects in the seventh
decade of life followed by the fourth and fifth decade. In
this study, the high prevalence of Candida species among
subjects in the second and third decade of life could be
attributed to the high sexual activity of subjects in this
age group which leads to high HIV/AIDS transmission
with resultant immunosuppresion and opportunistic in-
fections which i nc l ude Candida infections.
Bhalla [18] noted that pneumonia of bacterial origin
occur at a rate many times higher in the HIV infected
patients than in the general population. In this study, the
20 (7.3%) prevalence of bacterial isolates is lower than
the 44.28% reported in Hyderabad by Shailaja et al. [19],
with K. pneumoniae as the most prevalent etiologic agent.
This study also encountered K. pneumoniae as the most
prevalent bacterial agent. Tchamran [20] in his study on
lung diseases of bacterial origin in HIV infected indivi-
duals in African adults, noted that 81% of infections
were due to S. pneumoniae and reported it to be the most
offending pathogen in HIV reactive patients. The differ-
ence in prevalence rates may be ascribed to the types of
culture media used during the present study. Sabouraud
Dextrose Agar was the primary isolation medium. Strep-
tococcus pneumoniae and other fastidious organisms do
Characterization of Candida Species Isolated from Cases of Lower Respiratory
Tracr Infection among HIV/AIDS Patients in Calabar, Nigera
Copyright © 2013 SciRes. WJA
Table 5. Characterization of Candida species with Microxpress Candida identifi cation kit.
utilisation Melibose
utilisation Lactose
utilization Sucrose
utilization Galactose
utilization Cellobiose
utilisation Inositol
utilization Xylose
utilization Dulcitol
utilization Raffinose
C. albicans + + +
dubliniensis + + V
C. tropicalis + + V + +
guilliemondii + + V + + + +
Key: + = positive; − = negative; v = variable.
not grow on this media, thus such organisms were not
Also the polymicrobial etiology (mixed Candida and
bacterial infections) in 4 (1.5%) of the HIV reactive sub-
jects indicates the severity and the effect of immunosup-
presion in this group.
6. Conclusion
Pulmonary candidiasis is a health problem among HIV
positive patients in Calabar, Nigeria. Microexpress can-
dida identification kit has been found to be useful in the
identification of Candida to species level, as PCR is ex-
pensive and not easily assessable. Periodic study of pul-
monary Candida infections among HIV infected patients
is the present day’s need, to know the changing pattern in
incidence of Candida species.
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List of Abbreviations
Abbreviation/Symbol Meaning
HIV: Human immunodeficiency syndrome
AIDS: Acquired immune deficiency syndrome
ART: Antiretroviral therap y
DOTS: Directly Observed Treatment Short
KOH: Potassium hydroxide
SDA: Sabouraud Dextrose Agar
CMA: Corn meal agar
BHIA: Brain Heart Infusion Agar
˚C: Degree Celsius
χ2: Chi Square
mg: Milligramme
ml: Milliliter
L: Litre
µl: Microliter
g: Gram
%: Percent
No: Number
TB: Tuberculosis