Cervicovaginal infections are common in clinical medicine, and one of the most important causes of illness in women of reproductive age. They can lead to mortality and complications such as miscarriage, cervical cancer, preterm delivery, and infertility,1 and also contribute to high costs in the healthcare system every year.2 A variety of infectious organisms can affect the female genital system and are divided into two main groups: sexually transmitted infection and overgrowth of vaginal flora.3 Almost 95% of vaginitis are caused by one of the three microorganisms: Candida albicans, Gardnerella vaginalis, or Trichomonas vaginalis.4,5 The prevalence of sexually transmitted infections dramatically varies across the world and is affected by demographic features such as population distribution, age, race, and socioeconomics.6 According to a report by the World Health Organization (WHO), nearly 500 million new cases of sexually transmitted infections are added each year throughout the world caused by four agents of Chlamydia trachomatis, Neisseria gonorrhea, syphilis, and trichomoniasis.7 Hepatitis, syphilis, genital herpes, and acquired immune deficiency syndrome (AIDS) are among the most fatal sexually transmitted diseases, and each can increase the odds of comorbidity.8,9 Furthermore, the human papillomavirus (HPV) has been recognized as a risk factor for cervical cancer.10,11

Genital infections are often asymptomatic, yet they may be identified with such symptoms as vaginal discharge, burning, itching, and a foul smell.12 These infections may be diagnosed in different ways.13 Specific methods have been proposed to diagnose genital infections, but are mostly impracticable. Diagnosis of sexually transmitted infections requires available and cost-effective tests.14,15 The Pap smear was first proposed by George Papa Nicolaou in 1943 for early detection of changes in cervical cells.12 The Pap smear is not a specific or sensitive test for detecting genital infections but is used for women of childbearing age to screen for cervical cancer and identify genital infections. It is used to look for specific cellular changes caused by microorganisms and to observe the microorganisms present in specimens.16,17 Many women undergo an annual Pap smear test,18 which is a simple, quick, cheap, and painless method for diagnosing cervicovaginal infections. 13,14 It can also be used as an appropriate method to detect genital infections, especially in developing countries.19 Using Pap smear finding to determine the amount of genital infection can benefit interventions in these countries.

Several studies have been conducted across the world to determine the prevalence of genital infections based on Pap smear samples. A study in India reported the prevalence of genital infections as 50.07%. 13 Another study from Pakistan found that 38.3% of women had at least one genital infection.12 Both studies used Pap smear samples to determine the prevalence.

Various studies have been conducted in Iran to determine the prevalence of genital and sexually transmitted infections in different populations. However, the majority of these studies were conducted among high-risk populations or symptomatic women, or on those attending hospitals or specialist clinics and not on a large and representative population.20,21 There is a need to identify the effect of genital infections on women’s health and the demographic factors of those affected to identify the prevalence and risk factors of genital infections and conduct appropriate interventions. Therefore, we sought to determine the prevalence of genital and sexually transmitted infections in married women in Iran living in the Zanjan province and the associated risk factors.

METHODS

We conducted a cross-sectional study of 4 274 married women living in urban and rural areas of the Zanjan province from 2012 to 2013. Zanjan is 21 773 square kilometers and has 1 015 734 residents. It is located in Northwestern Iran and has eight large cities and 978 villages. According to Iranian law and culture, women lose their virginity after marriage. Early marriage, especially in rural areas, is common. Our study population included 20–65-year-old, married, divorced, and widowed women living in urban and rural areas. A sample size of 4 861 women was estimated based on 8% prevalence of genital infections in Iran reported by Maria et al21 with 99% confidence and accuracy of 0.01. We aimed for a sample size of 5 000 to cover possible withdrawals. Of the 5 000 prepared samples, 726 samples were excluded from the study due to unsatisfactory or inadequate specimens. Finally, 4 274 samples remained for interpretation and examination. To prevent the loss of Pap smear results, we did not exclude smears that lacked associated demographic or reproductive data. The study protocol was approved by Zanjan University of Medical Sciences and Health Services (UNI20PRJ532 ID Code).

Women who had not performed a Pap smear test during the past eight weeks and were eligible to obtain Pap smear were included in the study.22 Patients who married under the age of 18 for at least three years and those who had not had a hysterectomy and no history of cancer or chronic diseases were selected for inclusion by the stratified cluster sampling method. Those who did not fit the selection criteria for obtaining a cervical smear, or who were unwilling to participate in the study were excluded. To conduct the stratified cluster sampling method, each of the cities of Zanjan province (Zanjan, Soltanieh, Abhar, Khoramdeh, Tarom, Ijrood, Mahneshan, and Khodabande) were considered a cluster. Urban and rural clinics were classified based on population distribution in each cluster, and one to 10 health centers were selected based on their covered populations. In each center, samples were selected from medical records using systematic random sampling. The percentage of women of reproductive age, according to the last census, in each city were: 44% in Zanjan, 17% each in Khodabande and Abhar, 6% in Khoramdeh, 5% in Tarom, 4% each in Ijrood and Mahneshan, and 3% in Soltanieh. Selected subjects were called and invited to participate in the study. The data collection tool was a checklist of demographic and reproductive characteristics and cervical cytology results.

After obtaining written consent from each woman, their demographic and reproductive information was obtained via interviews with trained midwives. Specimens of the cervix were obtained using a cervical brush (Rovers Cervix Brush, Rovers Medical Devices B.V., The Netherlands) by the standard method.

An expert pathologist interpreted and reported the Pap smear findings, which included direct examination of specimens and cytological examination using conventional staining procedures, with an emphasis on identifying infectious agents in the samples. Of the samples, 99.6% were good quality.

The prevalence of genital and sexually transmitted infections in all samples was separately investigated according to infection type. For reporting mixed infections, which may occur during sampling, we considered criteria based on at least one or more genital or sexually transmitted infection. Factors associated with genital infections and sexually transmitted infections (infected vs. uninfected) were assessed using univariate and multivariate logistic regression models. We included variables such as place of residence, contraceptive method, vaginal discharge, menopause, age at first intercourse, and education in the final model. Data were analyzed using SPSS Statistics (SPSS Statistics Inc., Chicago, US) version 17. A p-value < 0.010 was considered statistically significant.

RESULTS

The mean age of participants was 35.6±9.3. The mean age of marriage and first intercourse were 16.4±10.3 and 19.2±4.3 years, respectively. The majority of participants were housewives (94.6%) and educated to primary and junior high school level (65.8%). About half of women lived in rural areas and half in urban areas. The majority (57.4%) had a monthly income of US$ 58–142 [Table 1]. More than 96% of women had a history of pregnancy and childbirth. Almost 40% of women complained about vaginal discharge, and 26.3% had previously had a Pap smear [Table 2].

Of the participants in this study, 850 (19.9%) were infected with at least one genital infection and 168 (3.9%) with at least one sexually transmitted infection. Bacterial vaginosis (8.2%) and trichomoniasis (1.4%) were the most common vaginal and sexually transmitted infections [Table 3]. Place of residence (p < 0.001), contraceptive method (p < 0.001), and vaginal discharge (p < 0.001) were significantly related to the risk of vaginal and sexually transmitted infections [Table 4]. In women who used an IUD as a contraceptive, the odds of having genital infection was 1.48 times greater than other contraceptive types (99% CI 1.21–1.82; p < 0.001). The odds of having genital infection was 1.46 times greater in women living in urban areas compared to rural areas (99% CI 1.23–1.73; p < 0.001), and 2.25 times greater in women with vaginal discharge (99% CI 1.9-2.65; p < 0.001). Additionally, the odds of having a sexually transmitted infection in women who used an IUD as a contraception was 1.74 times greater than those using other contraceptive types (99% CI 1.17–2.59; p < 0.006). The odds of having sexually transmitted infection was 1.85 times greater in women living in urban areas compared to rural areas (99% CI 1.29–2.65; p < 0.001), and 3.73 times greater in women with vaginal discharge (99% CI 2.60–5.35; p < 0.001) [Table 5].

DISCUSSION

The overall prevalence of genital and sexually transmitted infections was 19.9% and 3.9%, respectively. The most common genital infections were bacterial vaginosis (8.2%), candidiasis (6.5%), and trichomoniasis (1.4%). In addition, women who used IUD as a contraceptive, lived in urban areas, and had vaginal discharge, had a greater risk of genital or sexually transmitted infections.

The prevalence of genital infections was consistent with a study conducted in Gorgan (19.3%),20 but higher than that reported in the Ahwaz (10.4%), Khozestan (8.8%), and Kalantari (7.5%) provinces of Iran.1,21,23 Inconsistencies in the prevalence of genital infections could be due to differences in social, cultural, and sexual behaviors as well as the clinical conditions of the population. In our study, the prevalence of genital infections was higher than those living in urban areas and those with vaginal discharge.

The most common genital infections were bacterial vaginosis, candidiasis, and trichomoniasis, which is consistent with several other studies conducted in Iran, China, and India.1,4,13,24 According to the results of various studies, the prevalence of Gardnerella vaginalis ranged from 8% to 75%, Candida albicans from 2.2% to 30%, and Trichomoniasis vaginalis from 0% to 34%.23,25 Bacterial vaginosis is the most common cause of abnormal vaginal odor and discharge. It is due to a change in the type of bacteria found in the vagina and often occurs during pregnancy. It may cause premature labor and delivery, premature rupture of membranes, postnatal uterine infections, urinary tract infections, and postpartum endometritis.26 It can also increase the risk of HIV infection.27 We reported a prevalence of 8.2%, which was less than that reported in India (18.34%),13 but greater than that reported in a study conducted in the Khuzestan province of Iran.21

Candida albicans is identified by observing thin-walled blastospores and pseudohyphae in Pap smears. The prevalence of candidiasis was reported at 16.11% in India and 6.5% in China.13,24 We reported a prevalence of 6.5%, which is similar to results obtained in Ahwaz (8.2%)1 and in Khuzestan (6%),21 but lower than that in Gorgan (14.5%).20 The higher prevalence of candidiasis in Gorgan may be due to the climate and higher humidity of this city compared to Zanjan. In many cases, candidiasis is asymptomatic and does not require antifungal treatment, but clinical examination is required to determine the need for treatment.28

Trichomoniasis was the most common sexually transmitted infection. The prevalence of trichomoniasis has been reported as 5.9% in India, 2.5% in China,13,24 1.4% in Ahwaz, and 3.6% in Gorgan.1,20 A study in Jordan reported that 0.7% and 0.5% of women with trichomoniasis were symptomatic or asymptomatic, respectively.29 Diagnosis of trichomoniasis is vital, as it may have adverse effects on pregnancy outcomes, including premature rupture of membrane, preterm delivery, and low birth weight.30 It may also facilitate transmission of HIV infection and increase its risk.27

The prevalence of chlamydia infection was the second highest sexually transmitted infection in this study (1.0%). Previous studies found a higher prevalence in symptomatic and asymptomatic women compared to our results (0.6% and 0.5%, respectively).29 Chlamydia is one of the most common sexually transmitted diseases in the United States. This infection is easily spread because it often causes no symptoms and may be unknowingly passed to sexual partners. If left untreated, chlamydia infection can cause pelvic inflammatory disease. Studies have also suggested that Chlamydia trachomatis is considered a potential cofactor in the development of cervical intraepithelial neoplasia (CIN).31

Our results showed that there were greater odds of infection in women using IUD as a contraceptive, living in urban areas, and in those with clinical symptoms.32 This is consistent with the results obtained in other studies, which confirmed that lifestyle and socioeconomic factors are related to genital infection in Iran and other countries.21,24,33

According to the WHO, in countries where specific tests cannot be easily or economically performed, the Pap smear test, detecting patients’ complaints, or a combination of both may be used to determine appropriate treatment. Although we did not use a specific method to detect a variety of vaginal infections, we used clinical examination to evaluate infection, which may enhance the accuracy of our results. Other strong points of this study included sampling from rural and urban areas and a large sample size. However, there were limitations. Firstly, the prevalence of the infections may be under-reported due to the poor sensitivity of Pap smear tests in detecting genital infections. Secondly, chronic diseases such as diabetes mellitus and other risk factors may not have been detected due to the self-reported nature of the study. Finally, we had cases of incomplete demographic and reproductive data due to the self-reported nature of the study. Therefore, generalization of our results is limited. It seems that demographic, economic, and cultural changes in cities and the greater influence of media such as the internet and their inappropriate use exposes women to a higher risk of genital and sexually transmitted infections. Considering people’s lifestyle changes and the importance of controlling the spread of sexually transmitted infections, we suggest introducing primary and secondary preventive interventions to raise awareness of transmission and disease control, provide condom use training, and vaccination and screening to vulnerable groups (especially women living in urban areas that use IUDs).

CONCLUSION

A large proportion of married women living in Zanjan, Iran, suffered from genital and sexually transmitted infections. We identified many factors that affected the risk of getting infection including the use of IUDs and living in urban areas. Primary and secondary preventive and planning policies are needed to control the transmission of such infections.

Disclosure

The authors declared no conflicts of interest. The study was funded by the Deputy of Research and Technology of Zanjan University of Medical Sciences, and the Zanjan province general governor.

Acknowledgements

The authors would like to thank the Deputy of Research and Technology of Zanjan University of Medical sciences, and the Zanjan province general governor for their contribution to the study. We would also like to thank the staff of the health center for their collaboration, and women for their participation

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