Characterization of Candida Species Isolated from Cases of Lower Respiratory Tract Infection among HIV/AIDS Patients in Calabar, Nigeria

doi:10.4236/wja.2013.33027

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World Journal of AIDS, 2013, 3, 201-206

http://dx.doi.org/10.4236/wja.2013.33027 Published Online September 2013 (http://www.scirp.org/journal/wja)

201

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,

Nigeria.

Email: [email protected]

Received June 2nd, 2013; revised July 2nd, 2013; accepted August 2nd, 2013

cense, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

ABSTRACT

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

[6,7].

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

202

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-

tions.

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

µg∙ml−1) 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

203

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

204

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

guilliermondii

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

205

Table 5. Characterization of Candida species with Microxpress Candida identifi cation kit.

SPECIES Urease

utilisation Melibose

utilisation Lactose

utilization

Maltose

utilization Sucrose

utilization Galactose

utilization Cellobiose

utilisation Inositol

utilization Xylose

utilization Dulcitol

utilization Raffinose

utilization

C. albicans − − − + − + − − + − −

dubliniensis − − − + − + − − V − −

C. tropicalis − − − + + V + − + − −

guilliemondii − + − − + V + − + + +

Key: + = positive; − = negative; v = variable.

not grow on this media, thus such organisms were not

isolated.

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

Course

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