INTRODUCTION
Vaginal candidiasis is one of the major fungal infections of the mucosa
of lower female genital tract at the reproductive age of 20 - 40 years,
worldwide (Rasti et al., 2014). It causes inflammation of the
vagina (vaginitis), after bacterial vaginosis, which is usually characterized
by vaginal itching, a thick white abnormal vaginal discharge, burning, smelly,
and inflammation and redness of the vulva (Hainer and Gibson,
2011).
It is known that approximately 85 to 95% of yeast strains isolated from
the vagina are C. albicans strains (Jang et al., 2019). Non- C. albicans isolates, particularly Candida glabrata,
infect approximately 10% to 30% of females in different parts of the world (Sobel et al., 2011). The prevalence of Vulvovaginal candidiasis
(VVC) caused by non- C. albicans species has been suggested to be
increasing (Jang et al., 2019). VVC is highly prevalent among women with diabetes or after using
antibiotics for a long period (Abdul-Aziz et al.,
2019). Vaginal candidiasis is
characterized as uncomplicated or complicated based on the clinical
presentations and antifungal response (Hainer and Gibson,
2011). The most common cause of
uncomplicated vaginal candidiasis is C. albicans, which causes mild to
severe symptoms of vaginitis. However, non-albicans Candida species produce
complex vaginal candidiasis, which is more common in immunocompromised patients
and pregnant women (Kalaiarasan et al., 2017). It is
previously reported that about 75% of all women suffer from at least one attack
of C. albicans during their lifetime and roughly half of them suffer
from vaginitis many times (Yuan et al., 2021). Depending on the locality, age, and socioeconomic status; the rate of
vaginal yeast isolates among women has been revealed between 5 to 48.4% and C. albicans was the dominant
isolated species (51.37%) (Anh et al., 2021). Another study conducted in Nigeria reported that the prevalence of C.
albicans was around 41% (Enweani et al., 2001). Another
recent study conducted at Maternity Hospital in Erbil City; Iraq found that the
prevalence of vulvovaginal candidiasis using culture was 54.66%. The highest
number of positive cases 71 (63.4%) was found among the age group of 30 –34
years (Shekhany, 2021)
The absolute
diagnosis of C. albicans depends on
the clinical manifestations is difficult due to mixed with other infections
affecting vaginal, including Bacterial vaginosis, Neisseria gonorrhoea and
Trichomonas vaginalis. Thus, mycological examinations of vaginal
discharges are critical for the initial diagnosis of infection and detection of
definitive causative agents (Anderson et al.,
2004).
It is
important to note that Candida spp. have fundamental resistance to
several antifungal drugs (ElFeky et al., 2016). These
problems in addition to exerting psychological adverse effects in the treatment
of C. albicans in women, can increase the probability of infertility, pelvic
abscess, pelvic inflammatory disease, and also during pregnancy they may lead
to premature infant birth, abortion, postpartum infections, and systemic
inflammation (Hedayati et al., 2015). Several
studies have been conducted on the major causes of abortion and miscarriage
among pregnant women in our region (Naqid et al., 2020a, Naqid et al., 2020b, Naqid et al., 2019, Haydar and Naqid, 2022) but no study has been done yet
on C. albicans. Due to the lack of sufficient
information in terms of the prevalence rate of different kinds of VVC and the
type of causative species especially C. albicans in Zakho City,
therefore, the aim of this study was to evaluate the prevalence of C.
albicans and associated risk factors in women with signs and symptoms of
vaginitis referring to Obstetrics and Gynaecological Hospital at Zakho City,
Iraq.
MATERIALS AND METHODS
2.1 Study design and subjects
The current study was conducted as a cross-sectional study among
married women attending Obstetrics and Gynaecological Hospital at Zakho City,
Kurdistan Region-Iraq. From October 2021-to April 2022, 150 symptomatic married
women with vaginal discharge and itching was collected and analysed for
Candidiasis. The participants ages ranged from 18 to 48 years old
2.2
Study tool and sampling technique
Data was collected from each patient
using a designed structured questionnaire such as sociodemographic, and
clinical characteristics of participants. Demographic characteristics such as
age, educational levels, residence, smoking, contraceptives use, past medical
history and recurrent infection were recorded. Clinical characteristics of
patients including vaginal discharges, and pH of vagina were also reported.
Women suffered from vaginal discharge, painful intercourse, vaginal itching or
painful urination were regarded as symptomatic.
2.3 Ethics
The study procedure and protocol were approved by the ethical
committee of the Shekhan Technical College of Health,
Duhok Polytechnic University, Iraq. The study protocol was also approved by the
Duhok Governorate's Research Ethical Committee (Reference number:
15092021-9-4). Informed consent was acquired from each participant before the
collection of data.
2.4 Criteria
The inclusion criteria were married women who presented with clinical
features of the diseases and agreed to participate in this study and the
exclusion criteria were unmarried women, not agreed to participate, and older
than 48 years old
2.5 Genital
swab collection and processing
Aseptically, vaginal discharge swabs
were collected by a physician from the cervix and high vaginal swabs (HVS) using
two sterile cotton swabs, and a speculum. Firstly, the endocervix was cleaned
with a cotton swab to remove mucous and blood. Secondly, another cotton swab
was inserted at a distance of 2-3 cm into the endocervix and rotated for 5–10
seconds to allow exudates to be absorbed.
2.6 Diagnosis
of Candida albicans
Abnormal vaginal discharge and pH of
vaginal <4.5 were characteristics of candidiasis. 10% KOH Wet mount was
performed from one swab on the clean slide and examined microscopically. The
slide was then incubated for 5 to 15 min at 37°C and then microscopically
examined for the seen of budding yeast cells, and pseudo-hyphae suggested by Candida
infection (Emeribe et al., 2015).
For characterisation of colony
morphology, the second swab was directly inoculated on the Sabouraud
dextrose agar (NEOGEN-USA) by streaking the cotton swab on the plate and then
incubated aerobically at 37 °C (24-48 hrs. Suggestive C. albicans colonies
were further confirmed by the germ tube test (Fajoyomi
Bridget et al., 2022). For this purpose, 3 colonies were
mixed with 0.5 ml of human serum in a test tube and incubated for 3hrs at 37
°C. Light microscopic (Olympus, Japan) examination was done under oil immersion
(100X).
2.7 Statistic
GraphPad Prism version 8 was
used for the statistical analysis. The significant association between
variables was reported using descriptive information and expressed as
number (%). Univariate logistic regression analysis was used to analysis
the relationship between Candidiasis and their risk factors according
to demographic and clinical characteristics.
Odds ratios (ORs) and 95% confidence intervals (CIs) were also assessed. p value < 0.05 is considered significant.
RESULTS
3.1 Patients’ characteristics
The demographic characteristic of 150 married women participated in
the current study presented in Table 1. The average age of recruited subjects
was 32.64 years (±8.01 SD). The majority of the age group of participants was
in 31-40 years 60 (40%), followed by 21-30 years old 49 (32.7%) (Table 1). The
highest percentage rate of studied participants was uneducated 64 (42.7%) and
about 104 (69.3%) of the study subjects lived in the urban area. Nearly 80
(53%) of participants used contraceptives and 70 (46.6%) not used any type of
contraceptive. Other characteristics of participant were presented in Table 1.
3.2 Morphology characteristics of C. albican
DISCUSSION
Vaginal candidiasis is a common fungal infection of female genital tract
caused largely by C. albicans, which can influence a large number of
healthy women of reproductive age. It is previously reported that roughly three
- quarters of all women suffer from at least one episode of this infection
during their lifetime and half of them suffer from vaginitis several times
during their life (Yuan et al., 2021). The aims of present study were
to evaluate the frequency of C. albicans and associated risk factors
among married women of reproductive age.
Worldwide, there is a variation in the
distribution of Candida spp. identified from vaginal swabs and depends
largely on the location as well as the population studied. The frequency rate
of Candidiasis reported by several studies was 16.5%, and 19% (Aring et al., 2013). The prevalence rate of infection in the present study was 38.67%
using culture. This relatively higher frequency of C. albicans infection
among married women could be highly attributed to poor personal hygiene,
inadequate knowledge, and abnormal levels of estrogen
and corticoids (Fernández Limia et
al., 2004). Similar to our study, a study conducted in Iraq
reported that the rate of Candidiasis
was 38% of the studied groups (Al-Obadi and Al-Abidi, 2000). A very recent study performed among women at Duhok province, Iraq,
found a higher infection rate of C.
albicans (47%) based on PCR detection than our results (Oufi et al., 2022).
The frequency of infection in our
study is also higher than the rates reported in Indian (20.4%) (Ahmad and Khan,
2009), and Turkish (16%) (Ozcan et al., 2006). However, another study conducted in North-West Nigeria reported a
very high prevalence of vaginal candidiasis (84.5%) (Ugwa, 2015). This difference could be due to the population size of each district,
the health status of women, the socioeconomic status of participants, and
personal hygiene. This variation may also be due to inaccuracy in the detection
of pathogens, sensitivity of diagnostic tests in different laboratories, ethnic
groups and cultures, incomplete course of therapy, drug resistance, and
inappropriate health habits (Ahmad and Khan,
2009).
Generally,
the frequency of C. albicans among the women depends on age, level of
education, pregnancy status, uses of contraceptive and any other risk factors
for its transmission of infection. In the present
study, C. albicans infection were observed frequently in the age
reproductive group 31-40 years (45%) and the least among those less than 20
years (33.33%), however, no age-group was
absolutely free of vaginal candidiasis. This high frequency of infection in
this age group may be due to an increase sexual activity, physiological and
hormonal changes, vaginal flora changes, higher vaginal discharges, poor
personal hygiene, the use of drug abuse and contraceptives among this age-group
(Arfiputri
et al., 2018). Our findings
are similar to the study of Alo et al. (2012), who found a higher rate of C. albicans
(33.33%) within age group of 36-40 years, while the lowest prevalence reported
between 20-25 years (20.42%). A study conducted in Iraq found a higher incidence rate of vaginal candidiasis among female age
group 16-28 years (Abdulla et al.,
2001). Another study conducted in Iran also reported
similar results, the highest rate of Candia infection was observed in patients
with <40 years old, while patients aged >40 years old had the lowest rate
of infection (Kiasat et al., 2019). Several
studies explained the factors that are responsible for the low percentage of
candidiasis infection in aged women, these may be due to reducing the effect of
estrogen hormone, reaching menopause, less or no
sexual activity, no contraceptive use, and also good vaginal immunity because
they have low estrogen and corticoids (Menza
et al., 2013). We also found the highest prevalence of C.
albicans among higher education qualification (50%) followed by uneducated
people (37.5%), but there was no significant difference between different
levels of education (p=0.48). Likewise,
possible explanations for the difference in infection rates between illiterates
and those with a higher level of education include improvements in personal
hygiene and economic standing. On the
other hand, the obtained results revealed that the high frequency of C.
albicans was reported among women who had low number of birth and
significantly associated with it (p=0.028).
This difference would be partially due to the number of samples recruited in
the present study. More studies are needed to recruit a larger number of
samples to explore this area.
We also found a higher occurrence of infection among married women who
used oral contraceptive pills (45.45%), but the difference was also not
significantly associated (p = 0.46). The IUCD users reported 44.44% isolation
of C. albicans in our study. This could be due to local changes and
secretions resulting from foreign subject presence in the vagina. Similarly, a
study conducted in Bangladesh found that the highest prevalence of vaginal
candidiasis was reported in oral contraceptive pills (OCP) (85.7%) patients (Yusuf et al., 2007). This was followed by injectables
(12.2%) and intra-uterine
contraceptive device (IUCD) (2.1%), users. There was a clear significant
association between the type of contraceptive used and the occurrence of
Candida vaginal infections (p=0.002) (Yusuf et al., 2007). Previously, estrogen
and progesterone hormones have been suggested to be present in oral
contraceptives, which could increase glycogen levels in the vagina and increase
lactobacilli activities Candida (Enweani et al., 2001). It is well known that
lactobacilli play an important role to convert glycogen into lactic acid thus
decreasing vaginal pH. Subsequently, the decreased pH
reduces the bacterial biota activities which is favours for the growth of yeast
of Candida (Enweani et al., 2001).
In our study, it was also found accounted around 37 % of C. albicans do
not use contraceptives. This result explored that there may be other causes of
the high occurrence of vaginal infections in women rather than contraceptive
use. It might also be ascribed to the predisposition to sexual behavioural
activity. This is adapted to another study suggesting that natural factors
predispose to Candida infections (Yusuf et al., 2007). In our study, the illiteracy and
poor practice in personal hygiene may partially explain this high prevalence of
candida among women. Additionally, we also reported a higher rate of C.
albicans among women who had recurrent infection (48.65%), but was not significantly
associated (p=0.07) and used antimicrobial therapy for
a long time (36.84%). This result was in conformity with the fact that
prolonged antibacterial used for recurrent infections usually affects the
population of vaginal microflora and biochemical activity, which therefore
increases the pH of the vagina as a result of decreased CO2 production.
This characteristic together with hormonal factors could promotes overgrowth of
Candida, which lead to vaginitis (Bauters et al., 2002). Although overusing antibiotics
has been proposed as one of the significant factors contributing to the
increasing in the prevalence rate of Candia. Therefore, for efficient preventive
control of candidiasis among women, it is recommended first to identify the Candida
spp. alongside clinical symptoms before starting treatment of this
infection.
As the vulva is involved in C. albicans infection, this disease
is usually accompanied by vaginal itching, burning, and erythema of the vagina
and vulva, which are regarded as a major clinical manifestation of Candida
vaginitis. In the current study, there was a significant relationship between
vaginal itching and the frequency of C. albicans (p=0.001). The invasion
of epithelial cells in the female reproductive tract by Candida may cause
causes widespread inflammation and itching due to the release of enzymes or
toxins that are important for the pathogenesis of Candida (Ilkit and Guzel, 2011). However, the rate of infection among other
clinical characteristics was not significantly associated (p>0.05). The
typical C. albicans signs such as whitish discharges, and yellow green
discharges, pH>4.5 were significantly related to C. albicans
infection. A similar study conducted in Iran reported that vaginal itching as
the most common symptom in Candida infection (Hedayati et al., 2015). However, same study reported
that cheesy discharge and erythema were not significantly associated to Candida
Vaginalis (Hedayati et al., 2015). This variation of results may be
related to higher sexual activity, hormonal and physiological changes, health
habits and vaginal flora changes.
The value of the present study lies in the samples collected from married
women who suffered from vaginitis and treated many times without any responses.
Our study also found the major risk factors associated with C. albicans and
this will help physician to manage the case infected with this fungus. Our study has some limitations or weakness
which include the lower number of samples recruited in the present study, which
may reduce the evaluation of number size and may indirectly influence the
statistical analysis of significance. Secondly, the lack of screening for other
species of Candida in women and the lack of facility of molecular
techniques for the detection of candida. Another limitation of study Finally,
the lack of using molecular diagnosis by sequencing the ITS region of rDNA or
using Candida chromogenic agar to confirm the isolates.
CONCLUSION
The results of our study showed a relatively
higher occurrence of C. albicans in married women in our area. C. albicans is one of the common causes of vaginal discharge and itching among
childbearing age women in our study and this could be a problem for health
among this age in the area. A high frequency of infection was also reported
among women who use oral contraceptive and intrauterine contraceptive device.
Findings of this study highlight the importance of the different risk factors
that play an essential role in C. albicans infection. These results call
for preventive measures to protect women against vaginal candidiasis. Further study
is required to
investigate more about risk factors for C.
albicans infection in order to improve the health condition of
women. Therefore,
public health education and campaign should be implemented.
ACKNOWLEDGEMENTS
We would like to thank all
participants recruited in this study for their voluntary cooperation and
support for providing essential information
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