African Journal of Microbiology Research Vol. 7(1), pp.

27-34, 1 January, 2013

Available online at http://www.academicjournals.org/AJMR
DOI: 10.5897/AJMR12.651
ISSN 1996-0808 ©2013 Academic Journals

Full Length Research Paper

Aetiology and frequency of cervico-vaginal infections

among Mexican women
Fabiola Hernández-Martínez, Juan A Hernández-García, Marcos D Martínez-Peña, Brenda L
Muñíz-Becerril, Cecilia Hernández-Cortez, Graciela Castro-Escarpulli and
M. G Aguilera-Arreola*
Laboratorio de Bacteriología médica, departamento de Microbiología, Escuela Nacional de Ciencias Biológicas, Instituto
Politécnico Nacional (IPN). Ciudad de México, D.F. México.
Accepted 24 September, 2012

There are major concerns worldwide regarding sexually transmitted infections (STI), bacterial vaginosis
(BV), and candidiasis as a major cause of morbidity as they result in significant health and economic
consequences, particularly in developing countries. This study was intended to obtain information
about the prevalence of these pathologies in women considered to be at low risk using both traditional
and in-house NAAT methods. Cervical and vaginal samples were collected all volunteers signed an
informed consent form and completed a survey. BV, trichomoniasis, candidiasis, genital mycoplasmas
colonization and Chlamydia trachomatis or Neisseria gonorrhoeae cervicitis were diagnosed.
Candidiasis and abnormal vaginal flora associated with BV were very frequent. The high colonization
with micoplasmas was detected. C. trachomatis cervicitis was found in 10.67% from which a third of the
cases were of asymptomatic woman. No cases of gonorrhoea or trichomoniasis were diagnosed. In
house NAAT’s used seems to viable tools for the cheap and reliable test for the diagnosis of gonorrhoea
and chlamydial infections. Increased awareness of the importance of protected sexual intercourse is
imperative to prevent the transmission of sexually transmitted. Further studies for a comprehensive
understanding of the rates of these infections in Mexican women are necessary and should be an
impulse for make community-based assessment of STI and RTI.

Key words: Bacterial vaginosis, candidosis, STI, cervicitis, gonorrhoea.

INTRODUCTION

There are major concerns worldwide regarding sexually
transmitted infections (STI) as a major cause of morbidity
as they result in significant health and economic
consequences, particularly in developing countries. In
women, STI like gonorrhoea, clamidial infection or
trichomonosis are often chronic and present with few
*Corresponding author. E-mail: lupita_aguilera@hotmail.com.
Tel: (+0052) 55-57-29-60-00. Ext. 62374, 62567. Fax: (+0052)
55-57-29-62-07.
symptoms or asymptomatic, but they can eventually lead
to severe repercussions such as chronic pelvic
inflammatory disease, ectopic pregnancy, and infertility
(Araújo et al., 2007; CDC, 2010; Kurewa et al., 2010).
Thorough screening for STI in women should be
performed on a routine basis world-wide to rapidly
diagnose and treat infected individuals since timely
treatment of STI will prevent further transmission and
help control the spread of infection (Da Ros and Schmitt,
2008).
Reliable epidemiological data on chlamydia bacterial
STI and other reproductive tract infections (RTI) as the
28 Afr. J. Microbiol. Res.
dysbiotic conditions bacterial vaginosis (BV) or
candidiasis is scanty and insufficient among Mexican
women (Ponce and Ronzón, 2001). Contributing to the
lack of appropriate epidemiological information, Mexican
public health services do not offer population-level
screening or monitoring for all these diseases; diagnosis
of these infections is available only for women who are
already presenting symptoms or serious consequences,
including infertility. Although gonorrhoea, trichomoniasis
and candidiasis are notifiable diseases, under-reporting
of cases is high. In contrast, better reliable
epidemiological overview of syphilis, HIV, AIDS,
congenital syphilis and other viral infections has been
built (Reyna-Figueroa et al., 2011; Avila-Ríos et al.,
2011). Asymptomatic infections caused by pathogens
such as Chlamydia trachomatis or Neiseria gonorrhoeae
make transmission easier and frequently these untreated
asymptomatic infections progress to sequel (Avila-Ríos et
al., 2011). This fact creates an environment whereby
proactive screening is not only vital for improving health
status but also represents a cost-effective measure
(Reyna-Figueroa et al., 2011).
Currently, nucleic acid amplification tests (NAAT’s)
have become widely used; either in-house or commercial
assays offer several advantages over culture and other
methods for the detection of these microorganisms in
clinical samples such as increased sensitivity, high
throughput, no requirement for viable organisms and the
use of non-invasive specimens. NAAT’s for the detection
of C. trachomatis and N. gonorrhoeae has some
limitations such as cost, risk of carryover contamination,
inhibition and inability to provide antibiotic resistance
data. However, the possibility of detection of genetic
material in urine, self-taken vaginal swabs, cervical and
urethral swabs, storage and transport of samples is
simpler, since at 5°C can be retained up to 60 days
without affecting the results overcome limitations
(Bañuelos-Pánuco et al., 2000; Van Dyck et al., 2001;
Whiley et al., 2006).
Thus, this study was intended to obtain evidence about
the prevalence of STI (Trichomonas vaginalis, C.
trachomatis and N. gonorrhoeae) and RTI (Candida spp.,
bacterial vaginosis and Mycoplasma) in women
considered to be at low risk using low cost methods
(traditional and in-house NAAT’s Secondarily describes
demographic characteristics, sexual behaviour and
clinical findings that present the enrolled participants.
MATERIALS AND METHODS
Details of ethical approval and recruitment process
This study protocol received ethical approval from the Institutional
Ethics Committee from Escuela Nacional de Ciencias Biológicas.
Results were reported to all participants, and those who tested
positive for an STI, BV or Candidiasis were referred to a physician.
Recruitment was undertaken by distribution of a leaflet inviting
women to participate in the study. Leaflet was handed out in public
places, including different locations surrounding the Lázaro
Cárdenas-IPN Campus, México City and it briefly described the
study and suggested that women interested in participating should
schedule an appointment for sample collection at the most
convenient date and time.
Data and sample collection
Informed consent was obtained for each participant prior to her
recruitment into the study, and a self-administered questionnaire
was gathered from each participant. The questionnaire gathered
information about demographic characteristics (Table 1). Vaginal
samples were obtained using either a plastic or a wooden Dacron
swab while a cervical brush was used to sample cervical cells for
DNA detection of N. gonorrhoeae and C. trachomatis.
Exclusion criteria
Women younger than 18 years old and older than 65 years old
were excluded from the study; participants younger than 18 years
old were excluded because of legal ramifications as they were
under the age of consent. In addition, we also excluded pregnant
women and women who had received a course of antibiotics in the
previous month. Participants were required to not have had sexual
intercourse in the three days prior to sample collection.
Vaginal samples
The presence of BV, candidiasis, trichomoniasis and mycoplasmas
was studied in vaginal samples. Women were diagnosed with
bacterial vaginosis if they presented three or more of Amsel’s
clinical criteria, a ≥7 score according to Nugent’s criteria, and/or G.
vaginalis growth on Casman plates, as previously described
(Money, 2005; Livengood, 2009). At least two of this criterion has to
be concurrent for a diagnosed BV. All together with the
questionnaire about symptomatic occurrence was taken account for
diagnosis. Observation of budding yeast and/or pseudomycelium
on wet mount in physiological saline solution, as well as culture in
BiGGY medium (MCD LAB, Tlalnepantla Edo. de México) were
used to identify candidiasis. Since almost 10 to 30% of women
have candida colonization without any symptoms, the presence of
microbiological findings was correlated with specific symptoms such
as itch, burning or increase of normal secretion volume or kind. T.
vaginalis was diagnosed by observation on wet mount in
physiological saline solution, the slide was evaluated immediately
that the vaginal sample was taken. The Mycoplasma IST 2 gallery
(bioMérieux, Inc., Marcy I’Etoile, France) was used for culture,
identification and evaluation of antibiotic susceptibility according to
the manufacturer’s instructions.
Cervical samples
C. trachomatis detection
Cervical samples were frozen in 2-sucrose phosphate medium (2-
 Hernández-Martínez et al. 29

Table 1. Demographic, behavioural and clinical answers of the enrolled

participants.

Variables (N = 105) Frequency (%)

Age group
18-25 44 41.9
26-33 24 22.9
34-41 9 8.6
42-49 14 13.3
>50 14 13.3
Reason for consultation
gynaecological check-up 67 63.8
symptomatic 30 28.6
without answer 8 7.6
Current partner type
monogamous 85 81.0
concurrent 3 2.8
without answer 17 16.2
Number of sexual partners in the past
less than 2 35 33.3
two o more 66 62.9
without answer 4 3.8
Use of condom
Yes 37 35.2
No 33 31.5
without answer 35 33.3
Main symptoms
Itching 13 12.4
Burning 0 0.0
Discharge 28 26.7
Painful intercourse 3 2.9
Urination pain 1 1.0
Two or more 25 76.3
without answers 35 33.3

SP) until use. Deoxyribonucleic acid (DNA) extraction for C.
trachomatis detection was performed by enzymatic cellular lysis
with lysozyme and proteinase K. Polymerase chain reaction (PCR)
amplification of the omp1 gene, which encodes the species-specific
major outer membrane protein (MOMP), was performed under
conditions previously described (Bañuelos-Pánuco et al., 2000).
The identity of a random positive PCR reaction was confirmed by
sequencing with ABI-PRISM™ 310 sequencer (Applied Biosystems,
Foster City, CA) following the standard methodology outlined by the
manufacturer.
N. gonorrhoeae culture and detection
N. gonorrhoeae was detected by PCR and culture on selective
gonococcal plates with Thayer-Martin medium (TM) immediately
after sampling. DNA extraction was performed from the sample
using the InstaGeneTM Matrix Kit (BioRad Laboratories, Inc.,
Hercules, and CA) according to the manufacturer’s instructions.
Genetic detection was performed by making small modifications to
PCR conditions proposed by Boel et al. (2005).
Statistical analysis
Data collection was performed with a statistical package for the
social sciences (SPSS version 17.0). The frequency of each
demographic, behavioural and clinical categorical variable in the
survey was obtained. In order to establish the statistical significance
all categorical variables were analysed by means of 2 x 2
30 Afr. J. Microbiol. Res.

Table 2. Frequency of STI and RTI in healthy and infected Mexican women enrolled.

Menarche women Menopausal women Total N (%)

Diagnosis Cases n = 77 Diagnosis Cases n = 28 105 (100)
Microbiologically healthy 34 Microbiologically healthy 17 51 (48.57)

Infected 43 Infected 11 54 (51.43)

A S A S
C. trachomatis 4 7 C. trachomatis 0 0 11 (10.47)
C. albicans 2 6 C. albicans 0 0 8 (7.61)
BV 4 11 BV 3 3 21 (20)
M. hominis 2 3 M. hominis 1 0 8 (7.61)
U. urealyticum 4 18 U. urealyticum 3 2 27 (25.71)
Total* 16 45 Total** 7 5
*Since in menarche woman 15 concurrent infections were founded the total was bigger than the cases number of infected
diagnosis. ** In menopausal woman 1 concurrent infection was founded so the total was bigger than the cases number of
colonized diagnosis. The division of asymptomatic (A) or symptomatic (S) was performed with basis of how the participant
described herself as well as other symptomatology detected by the technician during the sampling such as discharge, redness or
other signs of illness. The two asymptomatic participants with Candida were cases of colonized but not as active infections since
no budding yeast, pseudomicelium or other sign of infection was founded. The seven participants with asymptomatic bacterial
vaginosis (BV) have abnormal vaginal flora (Nugent >7) accompanied of other altered signs as pH, Whiff test positive and/or clue
cells. U. urealyticum was concurrent with BV in 5 cases and was present with increased polymorphonuclear cell counts in 11 of
22 remaining cases.

contingency tables using Cramer's V (V) and chi square (p<0.05).
RESULTS
After approval by the ethics committee a total of 105
samples were collected from the sexually active female
population. The main characteristics of the studied
population are shown in Table 1. The mean age of the
participants was 32 years. The major reason of the
participants for consultation was because they wanted to
have a gynaecological check up 63.8% (67/105) while
28.6% (30/105) complained of gynaecological symptoms;
the rest 7.6% (8/105) did not specify the reason.
Regarding the current partner type, 81% (85/105) had a
monogamous relationship and only 2.8% (3/105)
declared having a concurrent relationship. On the other
hand, the number of sexual partners in the past was one
or two in 61.9% (65/105) of the participants, 20.0%
(21/105) declared having had three to four partners,
10.50% (11/105) reported having had either five or six
partners, and four (4.9%) women reported having had
more than six sexual partners; the remaining 4.90%
(4/105) did not respond. The average number of sexual
partners was 3. Among the women in this study, only
35.2% (37/105) reported the use of condoms; 31.50%
(33/105) reported never using condom and 33.3%
(35/105) did not respond.
Most women reported that their first incidence of sexual
intercourse occurred before the age of 20: one participant
first had sexual intercourse when she was under 10 years
old, 3.8% (4/105) reported first having sexual intercourse
between 11 and 15 years, 67.61% (71/105) between 16
and 20 years, 23.8% (25/105) between 21 and 25 years
and 3.8% (4/105) between 26 and 30 years.
Among the symptoms that participants reported,
vaginal discharge was the most frequent one (26.7 to
28/105%), followed by itching (12.4 to 13/105%), painful
intercourse in 2.9% (3/105), urination pain only in one
case (1.0%), no cases of burning were declared and
33.3% (35/105) did not respond; it is important to
emphasize that 76.3% (25/105) presented two or more
concurrent symptoms (Table 1).
Age of first sexual intercourse and health status of the
participant were dependent variables (V = 0.302,
p<0.041) so in this population the early age of first sexual
intercourse was a predisposing factor for developing
some STI. Any other categorical variable analysed shows
statistical significance.
There were a total of 51 microbiologically healthy and
54 colonized women (Table 2). Two groups were
generated based on hormonal stadium in menarche
women and menopausal ones. BV was diagnosed in 21
cases, most of them in the group of menarche women. In
14 of these 21 cases symptoms were declared in the
survey. The remainder seven participants did not report

any symptomatology, nevertheless were declared with
asymptomatic BV because they had abnormal vaginal
flora (Nugent >7) accompanied of other altered signs
such as pH, positive Whiff test and/or clue cells in Gram
stain smear. The Gram stain smear was employed to
perform BV diagnosis with Nugent´s score, which allowed
us to divide the participants (n = 105) in three groups
according to the present vaginal flora.
According to this, 77 cases were declared as normal, 7
cases as intermediate and 21 with BV. Clinical findings
were taken into consideration in each group; from the 77
cases included in the normal group, 28 participants
declared having no symptoms, meanwhile, 49 cases
were symptomatic however the symptoms could be
associated to other noninfectious pathologies. In the
intermediate group (7 cases), 4 patients reported
symptomatology and 3 were asymptomatic. Finally, as
mentioned before, 21 participants were diagnosed with
BV.
C. albicans was founded in 8 cases (7.61%) only in
menarche women. Two asymptomatic participants with
Candida were found, but were declared as cases of
colonization not as active infections since no budding
yeast, pseudomicelia or other sign of infection was
founded. None case of trichomoniasis was detected.
M. hominis was detected in eight cases and always
concurrent with BV. M. hominis was resistant to ERY4
(66.6%), CIP2 (33.3%), AZI4 (66.6%) and CLA4 (33.3%).
U. urealyticum was detected in 27 cases mainly in
menarche women; this bacterium was concurrent with BV
in 5 cases. U. urealyticum was resistant to OFL4, JOS8
and CLA4 (4.76% each), TET8 (9.52%), ERY4 (14.28%)
and CIP2 (33.3%).
C. trachomatis was present in 11 menarche women
(10.47%) from which four cases were of asymptomatic
participants. Participants with C. trachomatis infection
shared similar demographic characteristics with the
uninfected patients (that is, they belonged to the same
age group and were between the ages of 18 and 20 at
the time of first sexual intercourse). PCR was employed
to test for N. gonorrhoeae infection in the subjects, but no
cases of gonococcal cervicitis were detected.
At least one STI or RTI was diagnosed in 51.43% of the
study participants. Additionally, there were 15 cases of
co-infection between two or more pathogens
microorganisms, mainly in patients with BV which was
found in concurrence in nine cases with microorganisms
such as G. vaginalis, U. urealyticum, M. hominis,
Candida spp. and C. trachomatis; an intermediate
Nugent´s score was found in association with G. vaginalis
and C. trachomatis in one case, co-infection of U.
urealyticum and Candida spp. in three cases and
concurrent infection with U. urealyticum and C.
trachomatis were detected in two cases (Table 2).
Hernández-Martínez et al. 31
DISCUSSION
The diagnosis of genital infections among women in low
income countries remains a major challenge. Although,
STI and other vaginal conditions primarily affect young
women worldwide (Bañuelos-Pánuco et al., 2000;
Kurewa et al., 2010; Avila-Ríos et al., 2011) in most
resource limited setting the high costs and technical
requirements of commercial laboratory test make their
routine use difficult and compromise STI control and
management (Vickerman et al., 2003). For this reason
conventional and in house design NAAT were preferred
at the present work.
The survey was an attempt to review the presence of
symptoms and riskier behaviour (e.g. earlier sexual
debut, unprotected sex, number of sexual partners).
Interestingly most of the participants attended to the
study because their desires a gynaecological check-up
but no reports have any symptoms. However, when
samples were taken the analyst observe abnormal
vaginal or cervical discharge and swollen and redness
areas. The low frequency of complaints associated with
STI or RTI in this group of women may be attributed to
the false interpretation of physiological signs and
symptoms as normal. Health education should be
directed to empower women to recognize symptoms and
signs related to STI/RTI as early as possible (Araújo et
al., 2007).
BV is an endogenous infectious and remarkably
prevalent condition in women occurring in up to 30% of
the female population (Livengood, 2009). Accurate
diagnosis of BV is important as it is associated with
adverse pregnancy outcome. In Mexico, some studies
have reported a BV prevalence of 12 to 25% in family
clinics, 20.4%, and 32 to 64% in Sexually Transmitted
Diseases (STD) clinics. The BV frequency observed in
our study (23.8% in the general population) is similar to
that reported in women presenting to healthcare services.
Because BV increases women’s risk of medical
complications as pelvic inflammatory disease or adverse
pregnancy outcomes the high prevalence results
displeasing. This issue should be attended, probably by
offering early screening and treatment in general
population not only in order to prevent complications but
also recurrent episodes (Ponce and Ronzón, 2001). In
addition, it should be considered that BV probably
enhances women’s likelihood of sexual acquisition of HIV
(Verstraelen et al., 2010; Marrazzo, 2011).
Currently the criteria as defined by Nugent et al. (1991)
are considered as the standard procedure to score
vaginal smears by Gram stain. In agreement with other
authors the Nugent’s criteria demonstrating the
usefulness for determination of BV in women (Livengood,
2009; Marrazzo, 2011).
32 Afr. J. Microbiol. Res.
In the population analysed only C. albicans was
isolated. This concurs with literature´s description that
between 85% and 95% of yeast strains isolated from the
vagina belong to the species C. albicans while the
remainder are non-albicans species, the commonest of
which is Candida glabrata (Torulopsis glabrata). Probably
the most important challenge in vulvovaginitis Candida
(VVC) diagnosis is to differentiate symptomatic Candida
vulvovaginitis, to the less frequent asymptomatic Candida
vaginal infection with positive microscopy and culture and
the carrier state, in which asymptomatic women without
signs of disease and with negative routine microscopy
are found to have positive vaginal yeast cultures (Sobel,
2008). In the present two asymptomatic participants with
Candida infection were found, these were declared as
cases of colonization (carries state) not as active
infections since no budding yeast, pseudomicelia or other
sign of infection was founded.
Mycoplasmas infections are associated with urethritis,
premature rupture of membranes, premature labour,
endometritis, BV and postpartum infections of mothers
and newborns. In the present study, we observed a 32%
frequency of vaginitis, mainly associated with U.
urealyticum and less frequently with M. hominis. It has
been reported that genital mycoplasmas can be isolated
from the cervix or vagina of 50-80% of sexually active
women and, as in the present study, U. urealyticum had
been the most frequently reported mycoplasma in these
cases (Ponce and Ronzon 2001; Castellano-González et
al., 2007). Nevertheless, their aetiological role is widely
controversial as colonization of the female genitourinary
tract hinders evolution of these microorganisms as
infectious agents. According to the IST 2 gallery
manufacturers, the genital mycoplasmas presence at a
concentration of ≥104 CFU is sufficient to presume that
they are involved as pathogens, but concentrations ≤104
CFU indicate that they are only as a part of the normal
flora (Castellano-González et al., 2007; Kechagia et al.,
2008; Ekiel et al., 2009).
In this study, in accordance with other authors,
mycoplasmas were frequently associated with other
pathogenic microorganisms such as G. vaginalis, an
indicator of BV. In cases of BV, the vaginal environment
is altered, allowing bacteria such as mycoplasmas to
flourish; thus concurrent infection by G. vaginalis, U.
urealyticum, and even M. hominis has been previously
reported (Livengood, 2009; Bayraktar et al., 2010;
Marrazzo, 2011). Also, it has been reported that genital
mycoplasmas can be isolated from the cervix or vagina of
50 to 80% of sexually active women and, as in the
present study, U. urealyticum has been the most
frequently reported mycoplasma in these cases (Ponce
and Ronzón, 2001; Castellano-González et al., 2007). In
a few cases U. urealyticum was present as a unique
agent along with inflammatory cells. In addition to co-
infection with multiple microorganisms, another important
issue in the diagnosis of genital mycoplasmas is their
antibiotic susceptibility pattern. Antibiotic susceptibility
must be defined because of the previously reported high
frequency of resistance, including mycoplasmas’ natural
resistance to penicillin and cephalosporins because of
their lack of a cell wall. The importance of identifying
antibiotic-resistant strains is underlined by the fact that M.
hominis resistance to erythromycin has been previously
reported and was identified in a significant proportion of
subjects in this study.
In general, the resistance profiles observed in this
report are consistent with the findings of other Mexican
studies, indicating the necessity of modifying
recommended treatments; genital mycoplasmas are
resistant to most of the antibiotics recommended for their
treatment in the official Mexican guidelines, causing
failures in patient recovery. This is a quite important issue
as newborns might get infected during childbirth with
multidrug resistance genital micoplasmas leading to
acute infections that may end up in death (Castellano-
González et al., 2007; Kechagia et al., 2008; Bayraktar et
al., 2010).
C. trachomatis infection was detected in 10.78% of the
population tested, a result closer to data reported by the
international community. However, in Mexico, there are
no previous studies of C. trachomatis prevalence that
screen general population. Other studies have provided
significant evidence of the importance of routine
screening for C. trachomatis; e.g. the number of cases
detected can be increased from 29.7% when testing
patients who ask for C. trachomatis screening to 62.5%
when population-level screening is implemented. These
studies support our assertion that screening for C.
trachomatis infection should be included in all routine
checkups or at least in checkups for women with high-risk
behaviours (Paavonen and Eggert-Kruse, 1999; Baker et
al., 2005; Pavlin et al., 2006; Shao et al., 2010; Carey
and Beagley, 2010). Several studies have reported that
50% of chlamydial cervicitis cases manifest no symptoms
of infection which agree with our results (Jalil et al., 2008;
Bébéar and de Barbeyrac, 2009; Shao et al., 2010; Carey
and Beagley, 2010; Balfe et al., 2010) emphasising and
reinforces the importance of routine screening for this
bacteria, which is generally only identified in patients
showing symptoms of chronic infection (Paavonen and
Eggert-Kruse, 1999; Boel et al., 2005; Pavlin et al.,
2006).
Although non-gonococcal cervicitis is not a notifiable
disease in Mexico, there is an official regulation (NOM-
039-SSA2-2002) that establishes a protocol for the
diagnosis of an STI, including gonococcal and non-
gonococcal cervicitis. Cultures have been the gold

standard for diagnosis of gonococcal and non-
gonococcal cervicitis, but disadvantages, such as the
time between collection of samples to culture, have led to
the widespread use of NAAT diagnostic methods.
Unfortunately, these molecular methods are not
affordable for small laboratories and some hospitals, a
problem that has restricted their broad adoption. We
believe that in-house PCR-based diagnosis not only
accurately detects nutritionally fastidious microorganisms
but also provides a more affordable technique for specific
diagnosis. In the present study, an in-house PCR assay
for the detection of the N. gonorrhoeae 16S rRNA gene
was used (van Dyck et al., 2001; Whiley et al., 2006;
Chui et al., 2008); we did not observe any signs of
inhibition when using DNA extracted from clinical
samples, suggesting that this PCR method has wide
utility. Moreover, the results obtained by PCR
corroborated those obtained by culture. The results
obtained in this study regarding gonococcal cervicitis are
consistent with the findings of several other studies
(Flores-Paz et al., 2003; Pavlin et al., 2006; Jalil et al.,
2008).
World Health Organization recommends the use of the
syndromic approach to the management of urethral
discharge in men and vaginal discharge and lower
abdominal pain in women. While the syndromic approach
appears to be satisfactory in men it has several important
limitations in women mainly due that a large proportion of
genital gonococcal and chlamydial infections are
asymptomatic in women. The development of cheap and
reliable test for the diagnosis of gonorrhoea and
chlamydial infections among women in developing
countries could greatly improve STI control and the in
house NAAT’s tested in the present work seems to viable
tools for this purpose however it is necessary to continue
testing and improving their diagnostic capabilities and
accuracy in wide at high at risk population.
We also examined the frequency of mixed infections;
as previous studies have demonstrated associations
between C. trachomatis and other microorganisms such
as M. hominis, U. urealyticum, G. vaginalis and Candida
spp. The presence of concurrent infections has a direct
impact on the course of treatment, as care must be taken
to avoid treating only one microorganism while the other
remains untreated (Pavlin et al., 2006; Balfe et al., 2010).
Most cases of infertility related to microbial infections
have been associated with multiple infections,
predominantly C. trachomatis and M. hominis and/or U.
urealyticum. In this study, we found a frequent
association of C. trachomatis with U. urealyticum, which
points out the relevance of accurate diagnosis to provide
an adequate treatment. There is still much to be learned
about the risk factors for C. trachomatis cervicitis
infection, especially in Mexico, where this infection is not
Hernández-Martínez et al. 33
a notifiable disease and the only information available is
from individual reports.
More studies must be performed to improve the early
diagnosis of bacterial STI in woman and other vulnerable
populations (men who have sex with men or women who
have sex with women). It is imperative to increase the
awareness of the importance of protected sexual
intercourse, and efforts must be made to inform more
Mexican women, about the possible risks and
consequences of not using protection against STI.
In summary, in the analysed population the results
show false interpretation of physiological signs and
symptoms as normal since low frequency of complaints
associated with STI or RT, reveal a high frequency of
asymptomatic Chlamydia cervicitis and RTI as bacterial
vaginosis. Also high frequency also of genital
mycoplasmas (U. urealyticum and M. hominis) was
founded; although the aetiological role of these bacteria
is widely controversial a relevant issue is concern about
their antibiotic susceptibility pattern, since newborns
might get infected during childbirth with multidrug
resistance genital micoplasmas leading to acute
infections that may end up in death. Finally, the in house
NAAT’s tested in the present work seems to viable tools
for the cheap and reliable test for the diagnosis of
gonorrhoea and chlamydial infections among women in
developing countries. Further studies for a
comprehensive understanding of the rates of these
infections in Mexican women are necessary and should
be an impulse for make community-based assessment of
STI and RTI.
ACKNOWLEDGEMENTS
This investigation received financial support from SIP
20100629 and PICDS08-77 grants from Instituto
Politécnico Nacional (IPN) and the Instituto de Ciencia y
Tecnología del Distrito Federal (ICyT-DF), respectively.
MG AGUILERA-ARREOLA and G CASTRO-
ESCARPULLI received COFAA, EDI, and SNI support.
REFERENCES
Araújo OF, Pfleger V, Lang K, Heukelbach J, Miralles I, Fraga F, Quiroz
SA, Stoffler-Meilicke M, Ignatius R, Franco SKL, Feldmeier H (2007).
Sexually transmitted infections, bacterial vaginosis, and candidiasis in
women of reproductive age in rural Northeast Brazil: a population-
based study. Mem. Inst. Oswaldo Cruz. 102:751-756.
Avila-Ríos S, García-Morales C, Garrido-Rodríguez D, Ormsby CE,
Hernández-Juan R, Andrade-Villanueva J, González-Hernández LA,
Torres-Escobar I, Navarro-Álvarez S, Reyes-Terán G; Mexican HIV
Molecular Epidemiology Project Group (2011). National prevalence
and trends of HIV transmitted drug resistance in Mexico. PLoS One,
6: e27812.
34 Afr. J. Microbiol. Res.
Baker M, Ortega-Benito J, Garret N, Bromhead C, Leslie K, MacDonald
J, McNicholas A (2005). Prevalence and risk factors for Chlamydia
trachomatis infection in female New Zealand university students. N.
Z. Med. J. 118:U1607.
Balfe M, Brugha R, O’Donovan D, O’Connoll E, Vaughan D (2010).
Young women’s decisions to accept chlamydia screening: influences
of stigma and doctor-patient interactions. BMC Pub. Health 10:425.
Bañuelos-Pánuco CA, Deleón-Rodríguez I, Hernández-Méndez JT,
Martínez-Guzmán LA, Akle-Fierro D, Miranda-Murillo J, Reyes-
Maldonado E (2000). Detection of Chlamydia trachomatis in pregnant
women by Papanicolaou technique, enzyme immunoassay and
polymerase chain reaction. Acta Cytol. 44:114-123.
Bayraktar MR, Ozerol IH, Gucluer N, Celik O (2010). Prevalence and
antibiotic susceptibility of Mycoplasma hominis and Ureaplasma
urealyticum in pregnant women. Int. J. Infect. Dis. 14:90-95.
Bébéar C, de Barbeyrac B (2009). Genital Chlamydia trachomatis
infections. Clin. Microbiol. Infect. 15:4-10.
Boel CH, van Herk CM, Berretty PJ, Onland GH, Van Den Brule AJC
(2005). Evaluation of conventional and real-time PCR assays using
two targets for confirmation of results of the COBAS AMPLICOR
Chlamydia trachomatis/Neisseria gonorrhoeae test for detection of
Neisseria gonorrhoeae in clinical samples. J. Clin. Microbiol.
43:2231-2235.
Carey AJ, Beagley KW (2010). Chlamydia trachomatis, a hidden
epidemic: Effects on female reproduction and options for treatment.
Am. J. Reprod. Immunol. 63:576-586.
Castellano-Gonzalez M, Ginestre-Pérez M, Perozo-Mena A, Alaña F,
Fernández-Bravo M, Rincón-Villalobos G (2007). Vaginal colonization
by genital mycoplasmas in pregnant and non-pregnant women.
Invest. Clin. 48:419-429.
CDC, Centers for Disease Control and Prevention (2010). Sexually
transmitted diseases treatment guidelines 2010. MMWR RR, 12:59.
Chui L, Cniu T, Kakulphimp J, Tyrrell GJ (2008). A comparison of three
real-time PCR assays for the confirmation of Neisseria gonorrhoeae
following detection of N. gonorrhoeae using Roche COBAS
AMPLICOR. Clin. Microbiol. Infect. 14:473-479.
Da Ros CT, Schmitt CS (2008). Global epidemiology of sexually
transmitted diseases. Asian J. Androl. 10:110-114.
Ekiel AM, Friedek DA, Romanik MK, Jozviak J, Martirosian G (2009).
Occurence of Ureaplasma parvum and Ureaplasma urealyticum in
women with cervical dysplasia in Katowice, Poland. J. Korean Med.
Sci. 24:1177-1181.
Flores-Paz R, Rivera SR, García-Jiménez E, Arriaga-Alba M (2003).
Etiology of cervical vaginal infection among patients of the Juárez
Hospital of Mexico. Salud Publica Mexico 45(5):694-697.
Jalil EM, Pinto VM, Benzaken AS, Ribeiro D, Oliveira EC, Garcia EG,
Moherdaui F, Barbosa MJ (2008). Prevalence of Chlamydia and
Neisseria gonorrhoeae infections in pregnant women in six Brazilian
cities. Rev. Bras. Gynecol. Obstet. 30:614-619.
Kechagia N, Bersimis S, Chatzipanagiotou S (2008). Incidence and
antimicrobial susceptibilities of genital mycoplasmas in outpatient
women with clinical vaginitis in Athens, Greece. J. Antimicrob.
Chemother. 62:122-125.
Kurewa NE, Mapingure MP, Munjoma MW, Chirenje MZ, Rusakaniko S,
Stray-Pedersen B (2010). The burden and risk factors of Sexually
Transmitted Infections and Reproductive Tract Infections among
pregnant women in Zimbabwe. BMC Infect. Dis. 10:127.
Livengood CH (2009). Bacterial Vaginosis: an Overview for 2009. Rev.
Obstet. Gynecol. 2:28-37.
Marrazzo JM (2011). Interpreting the epidemiology and natural history
of bacterial vaginosis: are we still confused? Anaerobe 17:186-190.
Money D (2005). The laboratory diagnosis of bacterial vaginosis. Can.
J. Infect. Dis. Med. Microbiol. 16:77-79.
Nugent RP, Krohn MA, Hillier SL (1991). Reliability of diagnosing
bacterial vaginosis is improved by a standardized method of gram
stain interpretation. J. Clin. Microbiol. 29:297-301.
Paavonen J, Eggert-Kruse W (1999). Chlamydia trachomatis: impact on
human reproduction. Hum. Reprod. Update 5:433-447.
Pavlin NL, Gunn JM, Parker R, Fairley CK, Hocking J (2006).
Implementing chlamydia screening: what do women think? A
systematic review of the literature. BMC Pub. Health 6:221.
Ponce GG, Ronzón FJB (2001). Genital studies: How to increase
positivity. Rev. Mex. Pathol. Clin. 48:46-48.
Reyna-Figueroa J, Esparza-Aguilar M, Hernández-Hernández L del C,
Fernández-Canton S, Richardson-Lopez CVL (2011). Congenital
syphilis, a reemergent disease in Mexico: its epidemiology during the
last 2 decades. Sex. Transm. Dis. 38:798-801.
Shao R, Zhang SX, Weijdegard B, Zou S, Egecioglu E, Norström A,
Brännström M, Billig H (2010). Nitric oxyde synthases and tubal
ectopic pregnancies induced by Chlamydia infection: basic and
clinical insights. Mol. Hum. Reprod. 16:907-915.
Sobel DJ (2008). Vulvovaginal Candidiasis. In Holmes et al. (eds)
Sexually transmitted diseases, The Mc Graw Hill companies, United
States of America, pp. 823-838.
Van Dyck E, Leven M, Pattyn S, Van Damme L, Laga M (2001).
Detection of Chlamydia trachomatis and Neisseria gonorrhoeae by
enzyme immunoassay, culture, and three nucleic acid amplification
tests. J. Clin. Microbiol. 39:1751-1756.
Verstraelen H, Verhelst R, Vaneechoutte M, Temmerman M (2010).
The epidemiology of bacterial vaginosis in relation to sexual
behaviour. BMC Infect. Dis. 10:81.
Vickerman P, Watts C, Alary M, Mabey D, Peeling RW (2003).
Sensitivity requirements for the point of care diagnosis of Chlamydia
trachomatis and Neisseria gonorrhoeae in women. Sex. Transm.
Infect. 79:363-367.
Whiley DM, Tapsall JW, Sloots TP (2006). Nucleic acid amplification
testing for Neisseria gonorrhoeae: an ongoing challenge. J. Mol.
Diagn. 8:3-15.