Prevalence of Sexually Transmitted Infections and Their Risk Factors among Female Sex Workers in Isfahan,Iran: A Cross-Sectional Study

Abstract

Objectives:

Female sex workers (FSWs) are at high risk of sexually transmitted infections (STIs) and form a core group to facilitate STI spreading. We aimed to estimate the prevalence of STIs among FSWs who attended Female Harm Reduction Center of Isfahan, Iran, and to determine the association between risky behaviors and STIs.

Study Design:

In a cross-sectional study, 99 FSWs were recruited and interviewed about demographic characteristics and risky behaviors. A trained midwife examined FSWs for genital ulcer, abnormal vaginal discharge, and cervicitis. Urine and genital specimens were collected and real-time polymerase chain reaction was performed to diagnose Neisseria gonorrhoeae, human papilloma virus (HPV), and Trichomonas Vaginalis. Data were analyzed via χ² test and logistic regression in StataCorp software (version 11) with 95% confidence interval.

Results:

Totally, 84.9% of FSWs reported STI symptoms, while 12.1% of them were infected with N gonorrhoeae, HPV, or T vaginalis. Human papilloma virus and gonorrhea prevalence rates were 5.7% and 8% in FSWs with STI-associated symptoms. Sexually transmitted infections showed significant association with duration of prostitution (odds ratio [OR]_HPV = 1.009 [95% confidence interval [95% CI: 1.004-1.01]; OR_gonorrhea = 1.01 [95% CI: 1.00-1.01]) and condom usage (OR_HPV = 0.11 [95% CI: 0.012-0.98]; OR_gonorrhea = 0.04 [95% CI: 0.005-0.33]).

Conclusion:

Due to the literature gap on the Iranian FSWs’ sexual health and the intense stigma around this subject, in Iran, our results would be useful for developing an efficient intervention program. The prevalence of STIs in Isfahan FSWs can be controlled with programs such as consistent condom use and STI treatment. In addition, as just one-tenth of FSWs with an STI symptom were positive for an STI, symptomatic diagnosis of STIs might be insufficient.

Keywords

sexually transmitted infections female sex worker epidemiology prevalence condoms risk behaviors

Introduction

Sexually transmitted infections (STIs) are among the most critical concerns of public health in both developed and developing nations. The asymptomatic nature of some STIs and difficult diagnosis procedure show that many STI cases remain undiagnosed. Many STIs are associated with serious sequelae such as pelvic inflammatory disease, infertility, ectopic pregnancy, cervical cancer, neonatal death, prematurity, and congenital deformities as well as facilitating HIV and Hepatitis B Virus (HBV) transmission.¹ Approximately, 448 million curable STIs, including syphilis, gonorrhea, chlamydia, and trichomoniasis, occur annually in the 15 to 49 age range.¹

Female sex workers (FSWs) are at higher risk of getting STIs and play a prominent role in the STI dynamics. Drug and alcohol abuse, inconsistent condom use, and more concurrent sexual partners are some types of the FSWs’ risky behaviors that contribute to transmission of STIs.² Female sex workers’ mobility (ie, relocation of FSWs to places where they can find more clients) is connected to the HIV/STI transmission; a complex social network between FSWs, their clients, and partners of clients assists the spreading STIs in the community.^3
–5

Previous studies estimated that the STI prevalence among FSWs ranges between 0.6% and 14.1% in various communities.⁶ An international survey in 2010 found the HIV prevalence of 4.5% among FSWs.⁷ A study on FSWs in Shiraz, Iran, reported the prevalence of 4.7%, 9%, 1.43%, and 9.7% for HIV, Chlamydia trachomatis, Neisseria gonorrhoeae, and Herpes Simplex Virus 2 (HSV2), respectively.⁸ The prevalence rates of syphilis, C trachomatis, and HSV2 among Isfahan-imprisoned FSWs were estimated as 7.2%, 19.8%, and 18%, respectively.⁹ The HIV prevalence was recently estimated to be 5% among Tehran FSWs.¹⁰

The hardship of STI diagnosis and treatment is even exacerbated in regions with a less efficient health-care system and in communities where there is a social stigma around STIs.1 Prostitution is illegal in Iran and is stigmatized in the Iranian society. However, the government impartially provides health-care services to FSWs. Female harm reduction centers (FHRCs) provide services to different types of vulnerable women, including drug users, prisoners, and FSWs. These centers provide education on HIV/STI prevention, condom use, reproductive health care, STI screening and treatment services, and life skills for FSWs and can help to control the STI/HIV epidemics.^11,12 A study showed that STI prevalence was significantly decreased after providing the mentioned services to FSWs at a drop-in center.¹¹ There are 35 accredited FHRCs in Iran (2 in Isfahan). However, the number of FSWs who attend FHRCs remains unevaluated.

We aimed to determine the prevalence of STIs among FSWs of Isfahan and to assess the association between risky behaviors and STI risk. The outcomes of this study would help to form efficient intervention programs to manage the Isfahan STI epidemics. This study seeks to reduce the prostitution-related harms by discovering potential intervention programs that can help FSWs.

Materials and Methods

Study Setting

This cross-sectional study was conducted between 2013 and 2014 to estimate the prevalence of N gonorrhoeae, human papilloma virus (HPV), and Trichomonas vaginalis among FSWs who attend the Isfahan FHRCs. The study was conducted on FSWs attending 2 FHRCs in Isfahan. Isfahan is the capital city of Isfahan province in central Iran. It has a population of 1 986 542 and most of them are Muslims. Study participants’ recruitment, clinical examination, and sampling procedures were conducted from November 2013 to March 2014.

Sampling and Sample Size

Considering the prevalence of 5%,⁸ 0.042 margin of error, and 95% confidence coefficient, 100 FSWs were enrolled using a convenience sampling technique. Women who were sex workers based on the World Health Organization definition, receiving money or goods in exchange for sexual services⁸ during the last 6 months, and refer to FHRCs in Isfahan were eligible to participate in the study. Participants taking antibiotic in the last month or unwilling to provide urine/vaginal samples were excluded from the study.

Data Collection Method

Interviews

Participants were interviewed face-to-face for demographic characteristics and risky behaviors (ie, duration of prostitution, number of sexual partners in a week, drug abuse and alcohol consumption, condom use, and STI-associated symptoms) by a trained female social worker. A gynecologist guided the clinical examination procedure by instructing a midwife to appropriately examine the FSWs. After the interview, a trained midwife examined FSWs for genital ulcer, abnormal vaginal discharge, and cervicitis. Finally, vaginal and urine sampling were performed, which are described hereunder.

Genital Sampling

Prior to genital sampling, cervical inspection was performed through a sterile speculum and the examination was processed under a sterile condition. Sterile Dacron (or Rayon) swabs were used for genital sampling. The swab was inserted 1 to 3 cm deep into endocervix and was rotated for 10 to 30 seconds to absorb the exudate fluid. There was neither bleeding nor antiseptic application at the sampling site. To reduce the possible inhibitory effects, swabs were immediately transferred to culture or transport media. Cytobrush was used for collection of endocervical samples in search for any possible T vaginalis or HPV infection.

Urine sampling

Urine specimens were collected in preservative-free urine collection cups. They were kept in a +4°C environment before transportation. Urine and genital samples were transported to the Infectious Diseases and Tropical Medicine Research Center laboratory at Isfahan University of Medical Sciences.

Laboratory tests

Real-time polymerase chain reaction (RT-PCR) technique was used for the detection of infectious agents. To extract DNA from genital and urine samples, High Pure Nucleic Acid Extraction kit (Roche, Germany) was used. Appropriate (HPV, N gonorrhoeae, and T vaginalis) specific primers and probes were used to perform RT-PCR in a Rotorgene-Q apparatus (QIAGEN, Hilden, Germany).^13,14 Positive and negative controls were included in all PCR runs.

Human papilloma virus, N gonorrhoeae, and T vaginalis were detected in vaginal samples, whereas urine samples were tested for N gonorrhoeae and T vaginalis. All the results and the relevant codes were supplied to the FHRC for appropriate health-care provision.

Statistical Analysis

Missing values in some quantitative variables were imputed (ie, simple mean imputation). We used descriptive statistical indicators, including frequency and percentage for qualitative variables and mean and standard deviation for the quantitative variables. To assess the effects of independent variables, such as demographic characteristics, risky behaviors (eg, duration of prostitution, drug abuse, and STI-associated symptoms), and condom use, on the dependent variable, such as, infections of gonorrhea, HPV, and/or T vaginalis, we used χ² test for qualitative variables and independent t test for quantitative variables in the primary statistical analysis. In addition, we implemented logistic regression and odds ratio (OR).

Furthermore, specificity, sensitivity, and positive predictive value (PPV) of STI-associated symptoms for clinical diagnosis of the mentioned STIs were evaluated in our secondary statistical analysis. StataCorp software (version 11) was used for statistical analysis. Statistical significance level of .05 was considered.

Ethical Consideration

The study protocol was approved by the ethical committee of Isfahan University of Medical Sciences (project number: 291198-202). Participants were informed about the study’s objectives and were assured about confidentiality and anonymity. Written informed consents were obtained.

Results

Sociodemographic Characteristics

Of the 100 FSWs who participated in the study, 1 was removed because of faults in her specimens. For the remaining 99 FSWs, mean (standard deviation [SD]) of age was 34.9 (8.6). All FSWs lived in urban areas. Although 49.5% of the participants were married at the time of the interview, 96.8% of them had been married at least once. About 8.1% of participants were university graduates, 80.4% had diploma or were under diploma, and 11.5% were illiterate (Table 1).

Table 1.

Comparison Prevalence of N gonorrhoeae and HPV among FSWs Based on Demographic Characteristic and Risk Behaviors.^a

Characteristics	Total Participants, N = 99)	N gonorrhoeae			HPV
Characteristics	Total Participants, N = 99)	Negative Group	Positive Group	P Value	Negative Group	Positive Group	P Value
Age, mean (SD)	34.9 (8.6)	34.9 (8.8)	34.4 (5.8)	.92	34.9 (8.8)	34.5 (5.9)	.86
Marital status
Ever married	96 (96.8)	87 (90.6)	9 (9.4)	.31	89 (92.7)	7 (7.3)	.23
Never married	3 (3.2)	3 (100)	0 (0)	.31	3 (100)	0 (0)	.23
Education
Illiterate	10 (11.5)	8 (80)	2 (20)	.34	10 (100)	0 (0)	.52
Under diploma/diploma	82 (80.4)	75 (91.5)	7 (8.5)		76 (92.7)	6 (7.3)
Graduated	7 (8.1)	7 (100)	0 (0)		6 (85.7)	1 (14.3)
Number of sexual partner
≤2	51 (51.5)	46 (90.2)	5 (9.8)	.79	48 (94.1)	3 (5.9)	.63
>2	48 (48.5)	44 (91.7)	4 (8.3)	.79	44 (91.7)	4 (8.3)	.63
Length of prostitution, year
≤3	41 (41.4)	34 (82.93)	7 (17.0)	.02	35 (85.4)	6 (14.6)	.01
>3	58 (58.6)	56 (96.5)	2 (3.5)	.02	57 (98.3)	1 (1.7)	.01
Alcohol consumption
No	50 (50.5)	46 (92.0)	4 (8.0)	.70	47 (94)	3 (6)	.68
Yes	49 (49.5)	44 (89.8)	5 (10.2)	.70	45 (91.8)	4 (8.2)	.68
Drug use
No	39 (39.4)	34 (87.2)	5 (12.8)	.29	38 (97.4)	1 (2.56)	.16
Yes	60 (60.6)	56 (93.3)	4 (6.7)	.29	54 (90)	6 (10)	.16
Imprisonment history
No	81 (83.5)	75 (92.6)	6 (7.4)	.15	75 (92.6)	6 (7.4)	.87
Yes	16 (16.5)	13 (81.2)	3 (17.8)	.15	15 (93.6)	7 (7.2)	.87
Condom use
No	38 (38.4)	30 (78.9)	8 (21.1)	.001	33 (86.8)	5 (13.2)	.02
Yes	61 (61.6)	60 (98.4)	1 (1.7)	.001	60 (98.3)	1 (1.6)	.02

Abbreviations: FSWs, female sex workers; HPV, human papilloma virus; N gonorrhoeae, Neisseria gonorrhoeae; SD, standard deviation.

^aData are original.

Sexual Behaviors and Condom Usage

The duration of prostitution varied from 2 months to 15 years, with a median of 3 years (average 3.73 ± 3.3 years). The last sexual intercourse extended from 1 to 120 past days and the median was 7 days. The number of sexual partners in a week ranged from 1 to 30, with the median of 2 persons. About 57% of FSWs had vaginal intercourse, 21.5% experienced vaginal and oral sex, and 7.1% had vaginal and anal intercourse. Condom usage among FSWs was about 67%; and of those who used condoms, 78% used male condom, 6.8% used female condom, and 15% used both types of condoms (Table 1).

Drug Abuse and Alcohol Consumption

Approximately 60.6% of FSWs abused drugs. They used various drugs including opium (40.4%), crystal methamphetamine (26.3%), opium resin (19.2%), cannabis/marijuana (1.01%), methadone (2.02%), crack cocaine (10.10%), and heroin (19.2%). The median duration of drug abuse was 5 years. About 3.1% of the FSWs injected the drugs. Almost half of the FSWs used only alcohol. However, 37% used both alcohol and drug. The median duration of alcohol abuse was 5 years (Table 1).

Imprisonment History

Approximately 16.5% of FSWs had imprisonment history. The number of captivities ranged between 1 and 4 times, with a median of 1 time. The median duration of imprisonment was 2 months (Table 1).

Factors Affecting STIs

There was a significant association between the duration of prostitution and the risk of HPV and gonorrhea infections (P _HPV = .012 and P _gonorrhea = .028). Each year of prostitution increased the risk of HPV and gonorrhea infections by 1 percent (OR_HPV = 1.009 [95% confidence interval, CI: 1.004-1.01]; OR_gonorrhea = 1.01 [95% CI: 1.00-1.01]). Results indicate that there was a significant association between condom usage and gonorrhea and HPV infection risk (P _gonorrhea = .003 and P _HPV = .045). Condom usage reduces the risk of HPV (by 96%) and gonorrhea (by 90%) infections (OR_HPV = 0.11 [95% CI: 0.012-0.98]; OR_gonorrhea = 0.04 [95% CI: 0.005-0.33]; Table 1).

Signs and Symptoms of STIs

Almost 84.9% of the participants had the STI symptoms. The lower abdominal pain was present in 61.6% of the FSWs. In all, 59.6% had abnormal vaginal discharge, 26.3% had genital pain and burning, 25.3% had pruritus, 24.2% had frequent urination, and 15.3% had dysuria. Genital ulcer was found in 4.04% of the FSWs during the clinical examination (Table 2). Cervicitis was not found in any of the FSWs.

Table 2.

Sensitivity, Specificity, Positive Predictive Value of STI Signs and Symptoms for Detection of N gonorrhoeae and HPV.^a

STI Symptoms	Number of Positive Test (%)				PCR for Vaginal Specimen
	n	N gonorrhoeae	HPV	HPV & N gonorrhoeae	Gonorrhea				HPV
	n	N gonorrhoeae	HPV	HPV & N gonorrhoeae	Sen (%)	Spe (%)	PPV (%)	NPV (%)	Sen (%)	Spe (%)	PPV (%)	NPV (%)
Asymptomatic	11	2 (18.2)	2 (18.2)	1 (9.1)	-
Symptomatic
Lower abdominal pain	61	2 (3.3)	3 (4.9)	1 (1.6)	18.2	34.4	3.3	81.6	42.8	37.0	4.9	89.5
Vaginal discharge	59	6 (10.2)	4 (6.8)	2 (3.4)	66.7	41.1	10.2	92.5	57.1	40.2	6.8	92.5
Genital burning	26	2 (7.7)	1 (3.8)	1 (3.8)	22.2	73.3	7.7	90.4	14.3	72.8	3.8	91.8
Pruritus	25	1 (4.0)	0	0	11.1	73.3	4.0	89.2	0	72.8	0	90.5
Frequent urination	24	1 (4.17)	1 (4.2)	1 (4.2)	11.1	74.4	4.2	95.8	14.3	75	4.2	92.0
Dysuria	15	2 (13.3)	2 (13.3)	2 (13.3)	22.2	85.4	13.3	86.7	0	92.8	13.3	93.9
Genital ulcer	4	0	0	0	0	95.5	0	90.5	0	95.7	0	92.6
At least 1 symptom	88	7 (8.0)	5 (5.7)	3 (3.4)	77.7	10.0	8.0	81.8	71.4	9.8	5.9	81.8

Abbreviations: HPV, human papilloma virus; N gonorrhoeae, Neisseria gonorrhoeae; NPV, negative predictive value; PCR, polymerase chain reaction; PPV, positive predictive value; Sen, sensitivity; Spe, specificity; STI, sexually transmitted infection.

^aData are original.

Prevalence of N gonorrhoeae, HPV, and T vaginalis

About 12.1% of the FSWs had at least 1 of the mentioned STIs. Among those who had at least 1 of the STI symptoms, 10.2% were truly infected with 1 of the mentioned STIs. All urine samples of FSWs, with or without symptoms, were negative for N gonorrhoeae. Urine and vaginal samples did not show any T vaginalis. Among all participants, the overall prevalence rates of N gonorrhoeae and HPV were 9.1% and 7.1%, respectively. In FSWs with STI symptoms, HPV and gonorrhea had the prevalence rates of 5.7% and 8%, respectively. Test results showed that 2.3% of the FSWs with STI symptoms just had HPV and 4.5% of them were just infected by N gonorrhoeae. Approximately 3.4% were simultaneously infected with HPV and N gonorrhoeae. Two of the FSWs with no symptoms were positive for N gonorrhoeae and 2 were positive for HPV (Table 2).

Sensitivity, Specificity, and Predictive Values of the STI-Associated Symptoms

Among diagnosed STI-associated symptoms, abnormal vaginal secretion had the highest sensitivity for clinical diagnosis of gonorrhea and HPV (66.7% and 57.1%). However, the specificity of this symptom was about 40%. The PPV of dysuria was higher than other symptoms for clinical diagnosis of gonorrhea and HPV (Table 2). There was a significant association between lower abdominal pain and STI risk (P = .032).

Discussion

In the current study, signs and symptoms of STI were found in 90% of FSWs throughout the clinical examination, whereas the prevalence of N gonorrhoeae, HPV, and T vaginalis among them was about 12%. Only 10% of those with at least 1 STI-associated symptom were actually infected with an STI. Neisseria gonorrhoeae was not detected in any of the urine samples. Trichomonas vaginalis was not found in urine or vaginal samples. Laboratory tests on vaginal samples revealed N gonorrhoeae and HPV among FSWs with STI-associated symptoms. Coinfection with both microorganisms occurred among a few of FSWs.

Studies indicate that HIV, syphilis, N gonorrhoeae, chlamydia, and T vaginalis infections are prevalent in Iranian FSWs.^8,15 A survey in 2015 revealed that the national prevalence rates of mentioned infections are 2.1%, 0.4%, 1.3%, 6.0%, and 11.9%, respectively (Shokoohi et al, 2016).¹⁶ Other studies reported the prevalence of HPV (5.5%),¹⁷ herpes simplex type-2 (9.7%),⁸ and HBV (13.13%)1 in Iran.

More than two-third of our participants declared condom use. In a study on 190 FSWs in Sari, Iran, it was found that 39% of FSWs were regular condom users.¹² A biobehavioral survey in 2015 indicated that 79.2% of a subgroup of FSWs used condom consistently with their partners.¹⁸ These significant proportions of condom use among FSWs, who attended FHRCs, illustrate their understanding of condom use as a protection against STIs. In a study in Tehran, Iran, 68.3% of FSWs acknowledged that appropriate condom use can prevent STIs.¹⁹ A national survey of FSWs in Iran indicated that frequent HIV testing is associated with receiving free condoms.²⁰ A prospective study of 402 prostitutes proved that it is possible to have a large number of clients and remain STI free, if only condoms are used consistently.²¹ Our study proved that using condom during sex reduces the risk of the HPV and gonorrhea infections. Female sex workers who do not use condoms consistently are at a 5-fold higher STI risk than those who use them.³ Condom use can decline HIV incidents in FSWs.²² Our results showed that FSWs who use condom have fewer sexual partners than those who do not use condoms. Even though consistent condom use with clients is high among FSWs, it is relatively low with regular partners.^6,11 To lower the prevalence of STIs in Isfahan, consistent condom use need to be emphasized. Additionally, it must be noted that sometimes FSWs use condoms consistently after getting infected to reduce the transmission risk. This leads to an unpredicted insignificant relationship between condom use and lower STI/HIV risk among FSWs, in studies.⁵

Our results indicated a significant association between the duration of prostitution and the risk for HPV and gonorrhea infections. The relationship between the years of prostitution and STIs varies in different studies. As the same for HIV antibody, duration of prostitution is an independent risk factor for STIs.²³ Conversely to our findings, Venegas et al concluded that the frequencies of gonorrhea and chlamydia infections are higher in those with a shorter period of prostitution.²⁴ Kreiss et al proclaimed that cervical HPV DNA is significantly associated with fewer years of prostitution.²⁵ This is likewise for C trachomatis as Brunham et al supported that the duration of prostitution is inversely related to the risk of C trachomatis infection.²⁶ Taghizadeh et al found an association between last sexual contact condom use and sex work duration.¹² Further studies are recommended to confirm appropriate associations between these variables.

Although in our study vaginal secretions had the highest sensitivity for clinical diagnosis of gonorrhea and HPV, the sensitivity of this symptom was much lower (12.3%)²⁷ in the high-risk South African women. Some studies proved that vaginal discharge is a poor predictor of STIs.^27,28 However, the specificity of this symptom was lower in the current study and higher in the mentioned study (93.8%).²⁶In another study on 598 women with genital complaints, the presence of abnormal vaginal discharge as a predictor of endocervical gonorrhea and chlamydia had both a poor sensitivity (30%) and a poor PPV (17%).²⁸ In the current study, the PPV of dysuria was higher than other symptoms. In a community-based study on the resource-limited population of sub-Saharan Africa, there was no significant association between the STI syndromic-based diagnosis and laboratory-confirmed STIs tests; the sensitivity and specificity of combined STI symptoms were poor (33%) and moderate (73%), respectively.²⁹ It is proven that diagnosis of vaginitis by a syndromic approach has a higher sensitivity than that based on the vaginal discharge type.³⁰ Symptoms are sometimes of higher prediction value as for bacterial vaginosis, as there is a high sensitivity (92%), a moderate specificity (77%), and a PPV of 80% for syndromic diagnosis.²⁸ A study in the Republic of Benin illustrated that in syndromic approach for STI diagnosis, higher sensitivity would be achieved if the duration of prostitution was taken into account in the scoring system.³¹ We believe that when there are adequate facilities and no limits, the best approach is a combination of syndromic and laboratory tests for STI diagnosis.

One of our limitations is the low number of participants, which weakens statistical power. Second, Iranian FSWs are categorized into different classes such as street FSWs, Internet FSWs, and unclassified covert FSWs. We only had access to those who attended the FHRCs. Another limitation is that FSWs were not tested for HIV, which limits the design of intervention programs. Moreover, face-to-face interview for such a sensitive issue considering the setting may not allow the participants give reliable information. However, FSW recruitment was performed in FHRCs and participants were apprised of the study’s objectives and were assured of confidentiality and anonymity of their data. In addition, participants trusted the FHRC personnel and responded to the questions in a stress-free setting. Interviews were performed by a social worker who had been trained on how to appropriately communicate with FSWs. Yet, because of the possibility of underreporting in surveys, bias corrections may be needed. Finally, since we did not evaluate all STIs, we cannot conclude that those with STI-associated symptoms, who were negative in HPV, N gonorrhoeae, and/or T vaginalis, are free from other STIs. Further studies are required to evaluate the prevalence of STIs in Iran. Notwithstanding the limitations, this study’s outcomes can be used in developing intervention programs to control and prevent STIs in Isfahan FSWs.

Conclusion

Neisseria gonorrhoeae, HPV, and T vaginalis were found in one-tenth of FSWs with an STI-related symptom. This outcome suggests that a symptomatic approach for STI diagnosis is unsuccessful. Hence, for an accurate diagnosis, it is best to use all the available resources. The STI prevalence in Isfahan FSWs can be controlled with efficient intervention programs, including consistent condom use and STI treatment programs.

Footnotes

Acknowledgments

The authors appreciate all those who assisted them in the conductance of this study, particularly Isfahan University of Medical Sciences that funded this study.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by the Isfahan University of Medical Sciences (projects number: 291198-202).

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