Bacterial Sexually Transmitted Infections and Syndromic Approach: A Study Conducted on Women at Moroccan University Hospital
by
Safae Karim
1,
Chahrazed Bouchikhi
2,
Abdelaziz Banani
2,
Hinde El Fatemi
3,
Tiatou Souho
1,
Sanaa Erraghay
2 and
Bahia Bennani
1,* 
1
URL-CNRST, Laboratory of Human Pathology, Biomedicine and Environment, Faculty of Medicine and Pharmacy Fez, Sidi Mohammed Ben Abdellah University, Sidi Harazem Road, Fez 30070, Morocco
2
Department of Gynecology, Hassan II University Hospital Center, Sidi Harazem Road, Fez 30070, Morocco
3
Department of Anatomopathology, Hassan II University Hospital Center, Sidi Harazem Road, Fez 30070, Morocco
*
Author to whom correspondence should be addressed.
GERMS 2021, 11(4), 544-553; https://doi.org/10.18683/germs.2021.1289
Submission received: 24 May 2021
/
Revised: 7 November 2021
/
Accepted: 15 November 2021
/
Published: 29 December 2021
Abstract
Introduction: In Morocco, a syndromic approach has been implemented for sexually transmitted infections (STIs) management. However, those infections can be asymptomatic and the use of the syndromic approach to their management can be inappropriate and lead to dissemination of infection. Therefore, it would be important to determine the epidemiology and risk factors of bacterial STIs (Neisseria gonorrhoeae (NG), Chlamydia trachomatis (CT) and Mycoplasma genitalium (MG)) in a Moroccan population and their association with symptoms to assess the appropriacy of the use of the syndromic approach. Methods: Cervical samples were collected from symptomatic and asymptomatic consenting women attending the University Hospital of Fez and were tested by PCR for NG, CT and MG using specific primers. We assessed the infection status and its association with different risk factors and genital STIs-related symptoms. Results: Of 809 tested for CT, NG and MG, 16.6% tested positive for at least one STI. Of the 134 participants who tested positive for at least one bacterial STI, 74.2% had no genital STIs-related symptoms. Moreover, the results showed a significantly high rate of NG and MG infections in asymptomatic women. However, the determined risk factors for NG, MG and CT infections were menopause (p = 0.002), oral contraception (p = 0.036) and a high number of parities (p = 0.048), respectively. Conclusions: This investigation shows a predominance of NG infection and a high prevalence of STIs in asymptomatic patients. These results highlight that the adopted syndromic approach will not be adapted in the management of these STIs. Thus, the implementation of a systematic diagnostic program in order to enhance their management is needed.
Introduction
Sexually transmitted infections (STIs) are among the most threatening public health problems in the world because of the gravity of their associated diseases with 357 million new cases per year [1]. The leading infectious agents are Chlamydia trachomatis (CT), Neisseria gonorrhoeae (NG), herpes simplex virus (HSV), human immunodeficiency virus (HIV) and human papillomavirus (HPV) [2,3]. Most of these infections are asymptomatic or present mild symptoms. However, they can cause serious complications if not treated on time. Therefore, CT and NG can cause cervicitis, endometritis, pelvic inflammatory disease and even infertility [4,5]. Mycoplasma species, notably Mycoplasma genitalium (MG) can be responsible for pregnancy complications, cervicitis, postpartum sepsis, post-birth fever, non-gonococcal and non-chlamydial urethritis [6]. These infections are prevalent in low and middle-income countries where diagnosis is not routinely practiced and can associate the emergence of antibiotic resistant species.
In developing countries, women visit preferably pharmacists or traditional healers to get their treatment based on symptoms and even if they attend hospitals, the diagnosis of STIs is rarely prescribed. Therefore, STIs cases are mainly clinically diagnosed (based on clinical symptoms), and information on prevalent germs and symptoms are deficient. In Morocco, a recent analysis using the spectrum-STIs model, concluded that the prevalence of CT and NG has declined from 1995 to 2016 [7]. But this conclusion was based on the use of STI-spectrum models, which is just an estimation tool. Also, the authors used only data extracted from three studies, which included women aged 15–49 years attending antenatal care or family planning clinics in economically developed cities that are not representative of the whole Moroccan population. So, there is a lack of data on the real prevalence of CT and NG in Morocco and the epidemiology of these bacterial STIs is still undetermined. Also, no data about the prevalence of MG infection is available. In fact, except for syphilis and HIV, there is no systematic diagnosis for STIs and it is still difficult to determine their real prevalence and that of each germ. In addition, the STIs management is based on syndromic approach that consists of the identification of coherent groups of clinical symptoms and signs (syndromes) [7]. However, this approach will be useful only when most cases are symptomatic, such as in the case of urethral discharge in males (caused by CT and NG infections) but not in the case of vaginal discharge in women. Thus, the disadvantages of this approach are on the one hand its inability to detect and treat asymptomatic STIs increasing the risk of complications and spread of STIs and on the other hand, antibiotics (ceftriaxone, doxycycline and metronidazole) can be prescribed to healthy patients (who presented symptoms that were considered as associated with STIs but who actually did not have an STI), leading to potential antibiotic resistance.
This study aims to determine the prevalence and risk factors of NG, CT and MG infections and their association with symptoms among women consulting at the University Hospital of Fez, Morocco to assess the appropriacy of the use of the syndromic approach in our context.
Methods
Patients and sampling
A prospective study was conducted between February 2015 and March 2017. It included consecutive women attending the department of Obstetrics and Gynecology or the Anatomo-pathology laboratory of University Hospital Center Hassan II of Fez, Morocco for routine gynecological examination or for Pap smears test, respectively. All patients (symptomatic or asymptomatic) were eligible for inclusion except those who were less than 18 years old, pregnant, infertile, virgin, HIV positive, those who used antibiotic treatment during the past 3 months, were currently menstruating, and those who refused to participate. Written informed consent was obtained from women before their enrollment in the study. The Institutional Review Board of Fez, Morocco approved this study (N ̊ 02/15).
After clinical examination, the women underwent physician cervical sampling and a face-to-face questionnaire was used to collect information about their demographics, history of medication and infection information. Also, all relevant clinical information was noted.
Sample collection
Cervical samples were collected using a cytobrush and were stored in phosphate buffered saline (PBS) at −80 °C until deoxyribonucleic acid (DNA) extraction.
DNA extraction
Genomic DNA was extracted with proteinase K, purified using a phenol/chloroform protocol [8], and then stored at −20 °C until molecular analysis.
STIs detection
In order to detect the studied bacterial infectious agents (NG, CT and MG), polymerase chain reactions (PCRs) were performed using specific primers for each germ [9]. The primers delimited a region of 200 bp, 346 bp and 281 bp for CT, MG and NG, respectively. Negative (sterile distilled water in spite of DNA) and positive controls (DNA of each germ (NG, CT and MG)) were used for each reaction and the PCR products were visualized under ultraviolet light after electrophoresis in 2% agarose gel containing ethidium bromide.
Statistical analysis
Statistical analysis was performed using SPSS (version 20, SPSS Inc., USA) software. A descriptive analysis was performed and the results were presented as median for age with interquartile range (IQR) and number (percentage) for qualitative variables. The Chi-square or Fisher exact tests were performed when appropriate in univariate analyses to establish all correlations between variables and infection. Multivariate analyses were done by binary logistic regression and variables included in the final model were those with p-value ≤0.200 to determine the risk factors associated with bacterial STIs. The results were expressed as odds ratio (OR), 95% confidence intervals (CI) and p-values. In addition, in all tests and models, a p-value <0.050 was considered significant.
In order to determine the infection rate according to symptoms and to deduce the appropriacy of the syndromic approach, the recruited patients were categorized into two groups based on clinical examination and questionnaire information. The first group, of “symptomatic women”, included all women presenting at least one of the following symptoms: leucorrhea, pelvic pain/dyspareunia, pruritus, menorrhagia, metrorrhagia or dysuria. The second group was considered “asymptomatic”, and it included all women with none of the above-mentioned complaints/symptoms. The association of presence/absence of symptoms with infection status was analyzed.
To determine the risk factors of infection, several variables were analyzed and included socio-demographic factors, medical history and sexual behaviors (age, education level, menopause, relationship status, passive smoking, number of pregnancies, parity, oral contraception, history of miscarriages, age at first sexual intercourse and number of lifetime sexual partners).
Results
Study population
A total of 809 women were enrolled in this study. The participants were aged 19 to 85 years old with a median age of 45 years (IQR, 38–52 years) and 38.5% (n=306) of them were menopausal. The majority of women declared having had only one sexual partner in their lifetime, who is her husband (94.4%). None of the women was an active smoker and only 26.2% were passive smokers. The majority of them were illiterate (69.5%), 26.7% had used oral contraception and 34.8% of them had more than four pregnancies. The demographics, sexual behavior and clinical characteristics of the study population are presented in Table 1.
STIs prevalence
Molecular analysis showed that 16.6% (134/809) of recruited patients were infected with at least one of the bacterial infectious agents. The most predominant detected bacteria was NG [14.2% (115/809)], followed by CT [1.6% (13/809)] and MG [1% (8/809)]. CT/NG co-infections were detected only in 0.25% (2/809) cases.
Discussion
STIs are considered a worldwide burden for public health. They compromise many lives’ quality with serious impact on the sexual behavior of infected patients and their partners as well as on their reproductive and child health.
In Morocco and in an effort to manage the related STIs, the syndromic approach was implemented 21 years ago. But it has been proven that this approach shows several limits. So, the real prevalence of STIs and that of different related bacteria (CT, NG and MG) are still undetermined. To the best of our knowledge, this is the first study conducted in Morocco to determine the prevalence and risk factors of bacterial STIs and to explore their association with genital STIs-related symptoms in order to deduce the appropriacy of the used syndromic approach.
In an attempt to identify NG, CT and MG infections among 809 recruited women, we adopted a PCR-based approach. Women consulting the department of Obstetrics and Gynecology and the Laboratory of Pathological Anatomy of the University Hospital Center Hassan II of Fez, Morocco were recruited. Among them, 16.6% tested positive for at least one STI and multiple infections were identified in two cases. The global prevalence of STIs seems to be high compared with western populations such as Italian (2.4%—Area of Apulia [10], but similar to that of African population (15.5%—Ghana, STIs clinic) [11]. In fact, reasons that could explain these differences include: targeted population, samples size, geographical area, cultural environments and STIs management strategy. In our study, the obtained rate, even if similar to that of Ghana [11], is alarming since the Ghanaian study was conducted in an STIs clinic that is supposed to be attended by STIs high-risk population. So, in our study, since most women declared they had no extra marital relations (related to cultural environment), the main factor that can explain the high rate of infection is the failure of diagnosis particularly if it is based on syndromic approach; a high rate of asymptomatic women was also seen. In fact, this approach used in both men and women is more useful in men with urethral discharge syndrome than in women with vaginal discharge [12].
The detected MG rate (1%) was quite similar to that reported in different countries (UK 0.3% and Korea 0.6%) [13,14]. However, the distribution of the other STIs (NG and CT) was different from the rates reported in several countries. In fact, the detected rate of NG is higher (14.2%) than that reported in France (3.1%) [15]. CT is the most common bacterial STIs worldwide with an estimated rate of 9.1 million adults in the African region [3], its determined prevalence (1.6%) is comparable to that reported in an Italian study (1.8%) [10]. This disparity in the prevalence and distribution of the bacterial STIs can be due to diagnostic techniques [16], management strategies and STIs patient awareness (taboo subject).
Using the spectrum-STIs model (1995 to 2016) [7], the estimated infection rates in the Moroccan population were 0.37% for NG and 3.80% for CT. Those data were different from the ones obtained in this study. In fact, the rate of NG and CT infection was marked by high prevalence of NG and low prevalence of CT with rates of 14.2% and 1.6%, respectively. The low rate of detected CT infection might be related to the fact that only the cervical site was explored. However, the high rate of NG indicates that the distribution of this species may be different from an area to another in the same countries, that the rate of infection is underestimated when using the spectrum-STIs model or that there is a change in the epidemiology of this infection over time. This highlights the need for a periodic surveillance in order to evaluate the evolution of STIs.
Studies conducted in populations from Réunion Island [17,18] China, India, Peru, Russia, and Zimbabwe [19] showed that MG, NG and CT were more noticed in asymptomatic than in symptomatic women. These data were in agreement with the obtained results. In fact, 74.2% of infections are asymptomatic implying that the use of the syndromic approach for STIs management will not be sufficient. Their diagnosis and the identification of responsible agents is still necessary and will help to avoid both infection complications and spread.
The association of infection with age shows that the prevalence of each bacteria varies according to the age groups. The highest prevalence of MG was obtained in the younger group (≤45 years, p=0.004). This result is not surprising as STIs are related to sexual activities. However, CT and NG were most prevalent in the age group >45 years and menopause was significantly associated with NG infection. It is possible that the psychological, physiological and hormonal changes related to menopause lead to a decrease in the immune system [20], that can allow an increase of the risk of infections. The pH change at this stage can impact the susceptibility to infection and can favor its occurrence [21]. In fact, the acidic environment, associated with the metabolism of lactobacilli, has been shown to be extremely effective in countering the growth of NG [22]. Physiological changes occurring during menopause include a decrease in lactobacilli, which induces an increase in pH, which may lead to increased risk of STIs and their persistence. Assuming the fact that those women have had only one sexual partner, this infection can most likely be related to sexual behavior of their partner or instead to contamination pathways other than sexual. However, the hypothesis that women had acquired those STIs and particularly NG infection a long time ago (before menopause) is plausible especially that they were in most cases asymptomatic and were not tested for STIs (lack of screening program). In this case, the questions that rise are about the infection timing and the possible occurrence of complications. Thus, a particular attention will be paid to those patients and studies will be conducted to determine the infection status of their respective partners and also to determine the behaviors that can lead to infection.
In the present study, CT infection was found to be associated with a high number of parities, which is in agreement with data reported in India [23]. The multivariate analysis shows also that women who use oral contraception are four times more likely to be infected with MG compared to the others. These results are in accordance with studies suggesting that changes in hormones (during pregnancy or because of contraceptive use) may increase the risk of STIs acquisition [24] by altering the immune system [20], and/or the genital tract epithelial structure, thus making the tissue more susceptible to infection [25].
Several studies have consistently reported an increased risk for MG, CT and NG infection with higher numbers of recent sexual partners. However, the association between sexual behavior and the different STIs in Morocco could not be studied due to the socio-cultural and religious context. In fact, according to their responses, most of the recruited patients confirmed having had one sexual partner in their lifetime who is her husband (having more than one sexual partner designates an ex-marriage and not extramarital or multiple relationship). Assuming the fact that those women have had only one sexual partner, the high rate of infection can most likely be related to sexual behavior of their spouses. Accordingly, further studies are needed to understand the influence of behavioral and socio-economic factors on bacterial STIs especially in men.
It is necessary to note that the data derived from this region may not appropriately reflect the situation of other geographical regions since women participating in this study are representative of this region but not of whole Moroccan population and further larger studies are needed. However, the high rate of infection and the absence of a significant association between STIs and symptoms highlight the fact that the use of a syndromic approach is not appropriate. Even though this approach can avoid the expensive laboratory tests and could be easily implemented at the healthcare centers, it is unable to detect STIs in most cases. Additionally, not all symptomatic patients had STIs, and based on the syndromic approach they might receive antibiotics (ceftriaxone, doxycycline and metronidazole), which constitutes an overuse of antibiotics. Such misuse of antibiotics has a health and economic impact. Thus, it constitutes a factor for resistance development.
The results obtained in this study provide data on STIs etiology and highlight the fact that the adopted syndromic approach will not be sufficient for the diagnosis and treatment of STIs. The rate of STIs is alarming and highlights the utility of routine screening for CT, NG and MG infections in order to prevent complications, transmission to partners (propagation) and re-infection. Both symptomatic and asymptomatic patients should be diagnosed to prevent on the one hand the abusive treatment (in symptomatic-STIs negative patients) and STIs propagation (in asymptomatic-STIs positive patients) and on the other hand, adapted STIs prevention programs including awareness campaigns are necessary to limit the infection risks.
Conclusions
Based on the data from this study, it is clear that STIs constitute a public health problem in Morocco. The obtained rate of bacterial STIs, especially NG, is alarming and the prevalence of patients with no genital STIs-related symptoms (asymptomatic patients) is high. Even if the data derived from this study and the studied population may not reflect the situation of other regions, the results highlight that the adopted syndromic approach will not be sufficient for the diagnosis and treatment of STIs. In fact, its use can lead to the failure of STIs management increasing the risk of infection complications and potentially contributing to infection spread. Thus, we propose that the diagnosis of infections with those bacteria should routinely be performed in sexually active females especially those with the determined risk factors (menopause, oral contraception use, high number of parity).
Also, the high rate of infection detected in women with presumably one sexual partner highlights the necessity of conducting diagnosis in their partner and suggests the presence of other contamination pathways (other than the sexual one). Besides, it seems to be necessary to establish an STIs prevention program, to implement STI education for women, and to pay more attention to menopausal women. A periodic surveillance is required to evaluate the evolution of STIs.
Author Contributions
SK and BB conceived and designed the experiments. SK, CB, SE, HEF, TS and BB performed the experiments. SK and BB analyzed the data. AB and BB contributed reagents/materials/analysis tools. SK and BB wrote the paper. All authors read and approved the final version of the manuscript.
Funding
None to declare.
Institutional Review Board Statement
This study was approved by the Institutional Review Board of Fez, Morocco (N ̊ 02/15).
Acknowledgments
The authors would like to thank the staff of the Obstetrics and Gynecology Department and the Anatomo-pathology Laboratory of CHU Hassan II of Fez for their help in clinical examination and the specimen collection respectively.
Conflicts of Interest
All authors—none to declare.
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Table 1.
Demographics and clinical characteristics of the study population.
| Variable | N | % |
|---|---|---|
| Age (years), N=803 | ||
| ≤45 | 402 | 50.1 |
| >45 | 401 | 49.9 |
| Education level, N=794 | ||
| Illiterate | 552 | 69.5 |
| Literate | 242 | 30.5 |
| Menopause, N=794 | ||
| No | 488 | 61.5 |
| Yes | 306 | 38.5 |
| Age at first sexual intercourse (years), N=787 | ||
| <20 | 434 | 55.1 |
| ≥20 | 353 | 44.9 |
| Relationship status, N=795 | ||
| Married | 696 | 87.5 |
| Widowed or divorced | 99 | 12.5 |
| Number of lifetime sexual partners, N=784 | ||
| 1 | 740 | 94.4 |
| ≥2 | 44 | 5.6 |
| Passive smoking, N=789 | ||
| No | 582 | 73.8 |
| Yes | 207 | 26.2 |
| Oral contraception, N=786 | ||
| No | 576 | 73.3 |
| Yes | 210 | 26.7 |
| Number of pregnancies, N=792 | ||
| ≤4 | 516 | 65.2 |
| >4 | 276 | 34.8 |
| Parity, N=794 | ||
| ≤3 | 465 | 58.6 |
| >3 | 329 | 41.4 |
| History of miscarriages, N=790 | ||
| No | 560 | 70.9 |
| Yes | 230 | 29.1 |
Table 2.
Association between infection and symptoms.
| Bacterial infections | NG | CT | MG | |||||
|---|---|---|---|---|---|---|---|---|
| Symptoms | BI+, N=132* | Crude OR (95%CI) | NG+, N=113* | Crude OR (95%CI) | CT+, N=11* | Crude OR (95%CI) | MG+, N=8 | Crude OR (95%CI) |
| Absent, N (%) | 98 (74.2) | 1.66 | 83 (73.5) | 1.56 | 7 (63.6) | 1.07 | 8 (100) | - |
| (1.09–2.53) | (1.00–2.44) | (0.31–3.68) | ||||||
| Present, N (%) | 34 (25.8) | 1.00 (Ref) | 30 (26.5) | 1.00 (Ref) | 4 (36.4) | 1.00 (Ref) | 0 (0.0) | - |
| Statistical test results | p=0.017, df=1, χ2=5.71 | p=0.047, df=1, χ2=3.96 | p=0.914, df=1, χ2=0.01 | p=0.038, df=1, χ2=4.31 | ||||
*Excluding the two cases of co-infection. P-value for χ2 or Fisher’s exact test. BI—bacterial infections; CT—Chlamydia trachomatis; df—degrees of freedom; MG—Mycoplasma genitalium; NG—Neisseria gonorrhoeae; OR—odds ratio; 95%CI—95% confidence interval.
Table 3.
Prevalence of detected bacterial infections according to different variables.
| Variable | BI, N (%) | Crude OR (95%CI) | NG, N (%) | Crude OR (95%CI) | CT, N (%) | Crude OR (95%CI) | MG, N (%) | Crude OR (95%CI) |
|---|---|---|---|---|---|---|---|---|
| Age group (years) | ||||||||
| ≤45, N=401 | 61 (15.2) | 0.83 (0.57–1.20) | 50 (12.5) | 0.76 (0.51–1.13) | 3 (0.7) | 0.36 (0.09–1.40) | 8 (2.0) | 0.00 |
| >45, N=400 | 71 (17.8) | 1.00 (Ref) | 63 (15.8) | 1.00 (Ref) | 8 (2.0) | 1.00 (Ref) | 0 (0.0) | |
| Statistical test results | p=0.333, df=1, χ2=0.93 | p=0.182, df=1, χ2=1.77 | p=0.128, df=1, χ2=2.31 | p=0.004, df=1, χ2=8.05 | ||||
| Education level | ||||||||
| Illiterate, N=551 | 93 (16.9) | 1.08 (0.71–1.63) | 79 (14.3) | 1.05 (0.68–1.63) | 11 (2.0) | 0.00 | 3 (0.5) | 0.25 (0.06–1.09) |
| Literate, N=241 | 38 (15.8) | 1.00 (Ref) | 33 (13.7) | 1.00 (Ref) | 0 (0.00) | 5 (2.1) | 1.00 (Ref) | |
| Statistical test results | p=0.699, df=1, χ2=0.15 | p=0.811, df=1, χ2=0.05 | p=0.018, df=1, χ2=4.87 | p=0.060, df=1, χ2=3.92 | ||||
| Menopause | ||||||||
| No, N=487 | 65 (13.3) | 1.00 (Ref) | 53 (10.9) | 1.00 (Ref) | 4 (0.8) | 1.00 (Ref) | 8 (1.6) | |
| Yes, N=305 | 64 (21.0) | 1.72 (1.17–2.52) | 57 (18.7) | 1.88 (1.25–2.82) | 7 (2.3) | 2.83 (0.82–9.77) | 0 (0.0) | 0.00 |
| Statistical test results | p=0.005, df=1, χ2=8.02 | p=0.002, df=1, χ2=9.55 | p=0.081, df=1, χ2=2.97 | p=0.020, df=1, χ2=5.05 | ||||
| Age at first sexual intercourse (years) | ||||||||
| <20, N=434 | 81 (18.7) | 1.41 (0.96–2.08) | 69 (15.0) | 1.39 (0.92–2.10) | 6 (1.4) | 0.97 (0.29–3.20) | 6 (1.4) | 2.44 (0.49–12.19) |
| ≥20, N=351 | 49 (14.0) | 1.00 (Ref) | 42 (12.0) | 1.00 (Ref) | 5 (1.4) | 1.00 (Ref) | 2 (0.6) | 1.00 (Ref) |
| Statistical test results | p=0.078, df=1, χ2=3.10 | p=0.116, df=1, χ2=2.47 | p=0.596, df=1, χ2=0.00 | p=0.224, df=1, χ2=1.26 | ||||
| Relationship status | ||||||||
| Married, N=694 | 116 (16.7) | 1.00 (Ref) | 99 (14.3) | 1.00 (Ref) | 9 (1.3) | 1.00 (Ref) | 8 (1.2) | |
| Widowed or divorced, N=99 | 14 (14.1) | 0.82 (0.45–1.49) | 12 (12.1) | 0.82 (0.43–1.57) | 2 (2.0) | 1.56 (0.33–7.37) | 0 (0.0) | 0.00 |
| Statistical test results | p=0.518, df=1, χ2=0.41 | p=0.565, df=1, χ2=0.33 | p=0.408, df=1, χ2=0.33 | p=0.342, df=1, χ2=1.15 | ||||
| Number of lifetime sexual partners | ||||||||
| 1, N=742 | 122 (16.4) | 1.00 (Ref) | 104 (14.0) | 1.00 (Ref) | 10 (1.3) | 1.00 (Ref) | 8 (1.1) | |
| ≥2, N=44 | 7 (15.9) | 0.96 (0.41–2.20) | 6 (13.6) | 0.96 (0.40–2.34) | 1 (2.3) | 1.70 (0.21–13.60) | 0 (0.0) | 0.00 |
| Statistical test results | p=0.926, df=1, χ2=0.00 | p=0.944, df=1, χ2=0.00 | p=0.472, df=1, χ2=0.25 | p=0.629, df=1, χ2=0.47 | ||||
| Passive smoking | ||||||||
| No, N=580 | 94 (16.2) | 1.00 (Ref) | 81 (14.0) | 1.00 (Ref) | 7 (1.2) | 1.00 (Ref) | 6 (1.0) | 1.00 (Ref) |
| Yes, N=207 | 35 (16.9) | 1.05 (0.68–1.61) | 29 (14.0) | 1.00 (0.63–1.58) | 4 (1.9) | 1.61 (0.46–5.57) | 2 (1.0) | 0.93 (0.18–4.66) |
| Statistical test results | p=0.815, df=1, χ2=0.05 | p=0.987, df=1, χ2=0.00 | p=0.322, df=1, χ2=0.58 | p=0.646, df=1, χ2=0.93 | ||||
| Oral contraception | ||||||||
| No, N=575 | 98 (17.0) | 1.00 (Ref) | 85 (14.8) | 1.00 (Ref) | 10 (1.7) | 1.00 (Ref) | 3 (0.5) | 1.00 (Ref) |
| Yes, N=209 | 31 (14.0) | 0.84 (0.54–1.31) | 25 (12.0) | 0.78 (1.68–1.26) | 1 (0.5) | 0.272 (0.03–2.13) | 5 (2.4) | 4.67 (1.10–19.72) |
| Statistical test results | p=0.460, df=1, χ2=0.545 | p=0.315, df=1, χ2=1.01 | p=0.163, df=1, χ2=1.759 | p=0.035, df=1, χ2=5.30 | ||||
| Number of pregnancies | ||||||||
| ≤4, N=516 | 86 (16.7) | 1.00 (Ref) | 72 (14.0) | 1.00 (Ref) | 6 (1.2) | 1.00 (Ref) | 8 (1.6) | |
| >4, N=274 | 42 (15.3) | 0.90 (0.60–1.35) | 37 (13.5) | 0.96 (0.62–1.47) | 5 (1.8) | 1.580 (0.47–5.22) | 0 (0.0) | 0.00 |
| Statistical test results | p=0.627, df=1, χ2=0.23 | p=0.861, df=1, χ2=0.03 | p=0.323, df=1, χ2=0.57 | p=0.033, df=1, χ2=4.28 | ||||
| Parity | ||||||||
| ≤3, N=464 | 79 (17.0) | 1.00 (Ref) | 68 (14.7) | 1.00 (Ref) | 3 (0.6) | 1.00 (Ref) | 8 (1.7) | |
| >3, N=328 | 49 (14.9) | 0.85 (0.58–1.36) | 41 (12.5) | 0.83 (0.54–1.26) | 8 (2.4) | 3.84 (1.01–14.59) | 0 (0.0) | 0.00 |
| Statistical test results | p=0.432, df=1, χ2=0.61 | p=0.386, df=1, χ2=0.75 | p=0.035, df=1, χ2=4.50 | p=0.014, df=1, χ2=5.70 | ||||
| History of miscarriages | ||||||||
| No, N=559 | 87 (15.6) | 1.00 (Ref) | 75 (13.4) | 1.00 (Ref) | 6 (1.1) | 1.00 (Ref) | 6 (1.1) | 1.00 (Ref) |
| Yes, N=229 | 41 (17.9) | 1.18 (0.78–1.77) | 34 (14.8) | 1.12 (0.72–1.74) | 5 (2.2) | 2.05 (0.62–6.80) | 2 (0.9) | 0.81 (1.16–4.05) |
| Statistical test results | p=0.419, df=1, χ2=0.65 | p=0.597, df=1, χ2=0.27 | p=0.189, df=1, χ2=1.45 | p=0.576, df=1, χ2=0.06 | ||||
P-value for χ2 or Fisher’s exact test. BI—bacterial infections; CT—Chlamydia trachomatis; df—degrees of freedom; MG—Mycoplasma genitalium; NG—Neisseria gonorrhoeae; OR—odds ratio; 95%CI—95% confidence interval.
Table 4.
Risk factors associated with bacterial infections (multivariate analysis).
| STIs | Variable | Adjusted OR | 95%CI | p-value | |
|---|---|---|---|---|---|
| NG | Menopause | No | 1.00 | ||
| Yes | 1.88 | 1.25–2.82 | 0.002 | ||
| CT | Parity | ≤3 | 1.00 | ||
| >3 | 3.84 | 1.01–14.59 | 0.048 | ||
| MG | Oral | No | 1.00 | ||
| contraception | Yes | 4.67 | 1.10–19.72 | 0.036 | |
CT—Chlamydia trachomatis; MG—Mycoplasma genitalium; NG—Neisseria gonorrhoeae; OR—odds ratio; STIs—sexually transmitted infections; 95%CI—95% confidence interval.
© 2021 by the authors.
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MDPI and ACS Style
Karim, S.; Bouchikhi, C.; Banani, A.; El Fatemi, H.; Souho, T.; Erraghay, S.; Bennani, B. Bacterial Sexually Transmitted Infections and Syndromic Approach: A Study Conducted on Women at Moroccan University Hospital. GERMS 2021, 11, 544-553. https://doi.org/10.18683/germs.2021.1289
AMA Style
Karim S, Bouchikhi C, Banani A, El Fatemi H, Souho T, Erraghay S, Bennani B. Bacterial Sexually Transmitted Infections and Syndromic Approach: A Study Conducted on Women at Moroccan University Hospital. GERMS. 2021; 11(4):544-553. https://doi.org/10.18683/germs.2021.1289
Chicago/Turabian StyleKarim, Safae, Chahrazed Bouchikhi, Abdelaziz Banani, Hinde El Fatemi, Tiatou Souho, Sanaa Erraghay, and Bahia Bennani. 2021. "Bacterial Sexually Transmitted Infections and Syndromic Approach: A Study Conducted on Women at Moroccan University Hospital" GERMS 11, no. 4: 544-553. https://doi.org/10.18683/germs.2021.1289
APA StyleKarim, S., Bouchikhi, C., Banani, A., El Fatemi, H., Souho, T., Erraghay, S., & Bennani, B. (2021). Bacterial Sexually Transmitted Infections and Syndromic Approach: A Study Conducted on Women at Moroccan University Hospital. GERMS, 11(4), 544-553. https://doi.org/10.18683/germs.2021.1289
