Point and Lifetime Prevalence of Sexually Transmitted Diseases Based on the Definitions of the Iranian Syndrome Surveillance System: A Hospital-Based Survey

authors:

avatar Mohammad Fararouei ORCID 1 , avatar Mohammad Moein Derakhshan Barjoei ORCID 2 , avatar Reyhane Izadi ORCID 3 , avatar Parvin Afsar-kazerooni 4 , avatar Masoumeh Sadat Mousavi ORCID 5 , *

HIV/AIDs Research Center, Shiraz University of Medical Sciences, Shiraz, Iran
Student Research Committee, Shahid Sadoughi University of Medical Sciences, Yazd, Iran
Department of Health Care Managemant, School of Managemant and Information Sciences, Shiraz University Medical Sciences, Shiraz, Iran
Center for Communicable Disease Control, Ministry of Health and Medical Education, Tehran, Iran
Department of Epidemiology and Biostatistics, School of Public Health, Shahrekord University of Medical Sciences, Shahrekord, Iran

how to cite: Fararouei M, Derakhshan Barjoei M M, Izadi R, Afsar-kazerooni P , Mousavi M S. Point and Lifetime Prevalence of Sexually Transmitted Diseases Based on the Definitions of the Iranian Syndrome Surveillance System: A Hospital-Based Survey. Arch Clin Infect Dis. 2023;18(1):e132178. https://doi.org/10.5812/archcid-132178.

Abstract

Background:

Sexually transmitted infections (STIs) are among the most common infectious diseases and a globally concerning public health issue, especially in developing countries.

Objectives:

This study aimed to evaluate the syndrome-based point and lifetime prevalence of sexually transmitted infections in a big Iranian city.

Methods:

This cross-sectional study was conducted in 2019 on a hospital-based random sample of 2107 people (men and women aged 15 - 50) at Marvdasht Central Hospital (Iran).

Results:

The lifetime prevalence of Sexually Transmitted Diseases (STDs) was significantly higher in women than in men (81.56% vs. 33.60%, P-value < 0.0001). Also, about 20.7% of men and 48.26% of women had at least one of the STIs-associated syndromes at the time of the interview (instantaneous prevalence) (P-value = 0.001).

Conclusions:

The estimated prevalence of syndromes associated with sexually transmitted infections is alarmingly high. The results emphasize the need for further studies on effective health care and health promotion services to reduce STIs (including early detection and treatment of infections and public education).

1. Background

Sexually transmitted infections (STIs) are a group of infections that can be contracted through sexual contact and can cause sexually transmitted diseases (STDs). Sexually transmitted infections are the most common acute complications worldwide and can lead to severe and long-term complications (1, 2). Surveillance in the health system is defined as collecting, analyzing, interpreting, and publishing timely, continuous, and regular data related to health events to plan necessary interventions in a health system (3). Surveillance of diseases, especially when it comes to infectious ones, always faces different types of problems, including underreporting cases (3, 4).

In Iran, the "infectious diseases surveillance system" has been integrated into the country's primary health care network. The list of diseases with mandatory reporting (under surveillance) is reviewed every few years based on the latest circumstances (5). The purpose of establishing a sexually transmitted infection surveillance system is to provide reliable estimations of the incidence and prevalence of sexually transmitted infections and their trends over time (6). Hereby, the control of sexually transmitted infections can be improved, and recording and reporting cases can act as an effective warning system in areas where information about STIs is scarce or outdated. The STIs surveillance system is part of the second-generation HIV/AIDS care system (7). One essential component of the STIs surveillance system is monitoring the incidence and prevalence of STIs. However, despite the importance of monitoring STIs, in most parts of the world, including Iran, the STIs surveillance system remains unreliable (1, 8).

A sexually transmitted disease surveillance system can be designed on an etiologic or syndromic basis (8, 9). Etiologic-based case-reporting systems require laboratory diagnosis and advanced and costly laboratory support for routine STD surveillance systems. However, in most developing countries, limited or no laboratory services for etiological diagnosis of infections exist, and syndromic case reporting is the only available option for the surveillance of STIs (10). The syndromic registration and reporting system is designed to register and report cases with pre-defined signs and symptoms. This type of surveillance system can be easily set up in all countries. This is because, with minimal costs, the syndromic approach is based merely on the presence of pre-defined syndromes and can provide the necessary information for further actions to monitor and control STIs (8).

Currently, there are only two sources of information regarding the epidemiology of sexually transmitted infections in Iran: (1) individual studies conducted in different parts of the Iranian population (2, 11); and (2) the Iranian syndrome-based surveillance system for STIs. Only a few studies have been conducted on the prevalence of STIs in Iran, and most of them used specific populations with non-random sampling approaches (2, 11-13). Also, due to the variety of centers providing STI treatment services, collecting information for surveillance systems, especially from the private sector, and monitoring the actual trend of STIs is difficult (14, 15). This is partly due to the insufficient cooperation of the private sector in reporting diagnosed cases and also the fact that due to social stigma, many patients, especially men, self-treat themselves or refer to private physicians and pharmacies to hide their condition (15, 16). Moreover, in Iran, the laboratory capacities for diagnosing gonococcal infections (culture and testing of antimicrobial resistance), chlamydia infection (using a serological test instead of Nucleic Acid Amplification), and herpes virus type 2 (lack of a serological test for typing the virus) are limited and expensive. Also, many laboratories do not fully cooperate with the surveillance system and report no cases to surveillance centers (15).

2. Objectives

Based on the Iranian syndrome-based STI surveillance system, this study was performed to estimate the point and lifetime prevalence of sexually transmitted infections in the general population of Marvdasht, a large multicultural city in Iran.

3. Methods

3.1. Type of Study

This is a cross-sectional study of a representative population of sexually active age (aged 15 - 50 years) at Marvdasht Central Hospital, Iran, visitors.

3.2. Setting

Marvdasht is the second largest and most populated county in Fars province. The city is located 45 km north of Shiraz and has an altitude of 1620 meters above sea level; fertile lands and factories around the city were cultivated to make Marvdasht the major center of agricultural and industrial activities. As a result, Marvdasht has a multicultural and multi-ethnicity population making it a good sample of Iranian cultural and social characteristics (17).

3.3. Sampling

The required sample size (n = 2000) was calculated based on the results of a pilot study of 200 participants. Sampling was performed all days of the week during the busy hours of the morning and evening shifts (8 am to 2 pm) among men and women aged 15 - 50 years who entered the hospital as visitors. Time-based randomization sampling was performed so that every 12 minutes, one eligible participant was referred to the interview room.

3.4. Data Collection

Two interviewers (one female and one male) randomly selected same-sex visitors within the defined age range at the hospital entrance. The study process and its aims were explained to the participants, and because a significant number of the participants were illiterate, verbal consent was obtained if they were ready to participate. The eligible participants were then referred to the hospital outpatient clinic to complete an interview-administered questionnaire via a face-to-face interview in a private and comfortable room. The interviews were conducted by a midwife (for interviewing women participants) and a male nurse (for interviewing men participants).

3.5. Inclusion Criteria

All people referred to the hospital were aged 15 - 50.

3.6. Exclusion Criteria

People who do not want to participate in the study after being explained fully.

3.7. Data Analysis

Descriptive statistics (mean, median, and percentage) were used to summarize the data. Chi-square and t-test were used to compare quantitative and qualitative variables distribution among the comparing groups. STATA v.13.1 was used for data analysis. The difference is considered statistically significant if P < 0.05.

4. Results

A total of 2107 participants (1191 males and 916 females) with an average age of 33.11 ± 72 years participated in the study. Table 1 shows the demographic characteristics of all participants in the study.

Table 1.

Demographic Characteristics of the Participants in the Study

VariablesMale (%)Female (%)
Marital status
Single386 (32.5)176 (19.2)
Married793 (66.9)702 (76.4)
Widowed/divorced7 (0.6)41 (4.5)
Age
< 2087 (9.8)101 (11)
21 - 30304 (34.2)254 (27.7)
31 - 40337 (37.9)374 (40.7)
41 - 50162 (18.2)189 (20.6)
Having sex964 (81.1)871 (97.4)
Having urinary tract infections119 (10.1)336 (38.5)

Overall, the lifetime prevalence of STDs was significantly higher in women than in men (81.56% vs. 33.60%, P-value < 0.0001). Also, 20.7% of men and 48.26% of women had at least one of the STI-related symptoms at the time of the interview (instantaneous prevalence) (P-value = 0.001) (Table 2).

Table 2.

Prevalence of Sexually Transmitted Infections (Stis) in the Male and Female Participants

SymptomsMale PointMale Lifetime
No. (%)(%95 CI)No. (%)(%95 CI)
Dysuria67 (5.6)(0.0446 - 0.0709)196 (16.5)(0.1447 - 0.1868)
Frequency urination (urination more often than normal during the day)37 (3.1)(0.0226 - 0.0311)54 (4.5)0.035 - 0.0588)
Any sores in the genital area a23 (02.)(0.0129 - 0.0288)42 (3.5)(0.0262 - 0.0474)
Abnormal discharge from the genital area23 (1.9)(0.0129 - 0.0288)76(6.4)(0.0514 - 0.0792)
Bleeding or non-bloody discharge from the anus10 (0.8)(0.0046 - 0.0154)37 (3.1)(0.0226 - 0.0426)
Testicular pain and swelling18(1.5)(0.0096 - 0.0238)112 (9.4)(0.0788 - 0.112)
Swelling and redness in the scrotum120 (10.1)(0.085 - 0.1192)2 (0.2)(0.05 - 0.61)
Dyspareunia 6 (0.6)(0.23 - 01,09)
Pain after intercourse (after ejaculation)20 (2.1)(1.09 - 2.58)
Total symptoms246 (20.7)(18.47 - 23.06)400 (33.6)(30.98 - 36.34)
P-value b0.001< 0.0001
SymptomsFemale PointFemale Lifetime
No. (%)(%95 CI)No. (%)(%95 CI)
Mild abdominal pain (except menstrual pain)221 (23.9)(21.33 - 26.83)452 (49)(45.8 - 52.24)
Dysuria178 (19.3)(16.89 - 21.98)348 (37.7)(34.67 - 40.91)
Frequency urination81 (8.8)(7.13 - 10.79)125 (13.5)(11.5 - 15.92)
Abnormal genital338 (36.6)(33.61 - 39.82)534 (57.9)(54.71 - 61.07)
Genital sores a8 (0.9)(0.44 - 01.71)70 (7.9)(5.58 - 8.75)
Abnormal discharge from the anus10 (1.1)(0.5 - 1.98)22 (2.4)(1.5 - 4.0)
Any sores on the skin of the anal area2 (0.2)(0.06 - 0.79)1 (0.1)(0.02 - 0.61)
Itching on the inside or outside of the genital area194 (21)(18.53 - 23.79)338 (36.6)(33.56 - 39.87)
Dyspareunia 264 (38.71)(33.13 - 42.42)--
Pain after intercourse142 (20.82)(17.94 - 24.03)--
Bleeding after intercourse22 (3.3)(2.14 - 4.84)--
Total symptoms445 (38.26)(45.05 - 51.49)752 (81.56)78.93 - 83.93

Men with a history of the defined syndromes were, on average older than men without the syndromes (P-value = 0.0003). However, in women, there was no significant age difference between those with and without syndromes in the past (Tables 3 and 4).

Table 3.

Presence of the Defined Syndromes by Age

VariablesNowPast
Mean ± SDP-ValueMean ± SDP-Value
Male0.500.003
Symptoms reported31.79 ± 8.7033.63 ± 8.57
Symptoms reported32.34 ± 8.6731.72 ± 8.70
Mean difference-0.55 ± 0.111.91 ± 0.50
Female0.0030.59
Symptoms reported34.55 ± 6.7532.94 ± 8.82
No symptoms reported31.28 ± 9.7232.53 ± 9.24
Mean difference3.27 ± 2.150.41 ± 0.71
Table 4.

Demographic Status of People with and Without the Defined Syndromes

VariablesPoint Prevalence; No. (%)Lifetime Prevalence; No. (%)
No SymptomsHaving SymptomsP-ValueNo SymptomsHaving SymptomsP-Value
Male (marital status)0.5610.192
Single 308 (78.4)85 (21.6)271 (69)122 (31)
Married632 (79.7)161 (20.3)517 (65.2)276 (34.8)
Age0.9320.031
< 2072 (82.8)15 (17.2)67 (77)20 (23)
21 - 30259 (85.2)45 (14.8)234 (77)70 (23)
31 - 40286 (84.9)51 (15.1)232 (68.8)105 (31.2)
41 - 50139 (85.8)23 (14.2)108 (66.7)54 (33.3)
Female (marital status)< 0.00010.334
Single182 (83.9)35 (16.1)45 (20.7)172 (79.3)
Married293 (41.7)409 (58.3125 (17.8)577 (82.2)
Age< 0.00010.391
< 2087 (86.1)14 (13.9)24 (23.8)77 (76.2)
21 - 30133 (52.4)121 (47.6)45 (17.7)209 (82.3)
31 - 40161 (43.0)213 (57.0)63 (16.8)311 (83.2)
41 - 5094 (49.7)95 (50.3)38 (20.1)151 (79.9)

5. Discussion

The results of our study suggested that more than one-third of male and more than 80% of female participants have experienced at least one of the symptoms associated with sexually transmitted infections during their sexually active life. Also, more than 20 % of men and one-third of women currently suffer from at least one defined symptom. A study conducted in Guntur to measure the prevalence of sexually transmitted infections in women of childbearing ages showed that the lifetime prevalence of the syndrome was 32.69%, which was generally close to what was reported in our study (18). Also, a study by Nasiriyan et al. (14) in Kerman (another city in Iran) suggested that 16.66% of men and 33% of adult women in Iran had at least one of the symptoms of sexually transmitted infections at the time that they were interviewed. Again, the results are close to the results of our study. In addition, a study by Mousavi et al. on urban and rural general populations showed that one-third of men and more than two-thirds of women in the general population had experienced at least one of the symptoms associated with sexually transmitted infections since the age of 15. Moreover, 20.7% of men and more than a quarter of women currently suffer from the syndromes associated with sexually transmitted infections (18).

The point prevalence and lifetime prevalence of syndromes were significantly higher in women than in men. This issue may be because women care more about their health, pay more attention to symptoms, and remember and report them better (19). And on the other hand, this issue may be due to the low sensitivity and specificity of some symptoms related to sexually transmitted infections, especially in women. Some symptoms are also found in other diseases; having that symptom does not mean 100% having sexually transmitted infections (20-22).

The results of the current study showed that 36.6% of women were suffering from abnormal discharge from their genital organs, 0.9% had ulcers in the genital area, and 23.9% had pain in the lower abdomen. In a study conducted in Guntur, 27.88% of women had abnormal vaginal discharge, 1.34% had genital sores, and 3.46% had mild abdominal pain (23). In the current study, about 3.5% of men were suffering from genital sores, and about 58% of women have experienced abnormal vaginal discharge since the age of 15.

These results are close to a study conducted in Iran in 1390, which showed that 4.9% of men and 40% of women had experienced genital ulcers and abnormal vaginal discharge during their lifetime, respectively (12). In the present study, women reported more STI syndromes among the study participants. One possible justification for such a pattern is that women care more about their health, pay more attention to symptoms, and better remember and report their past health experiences. On the other hand, the difference between men and women may be due to the low sensitivity and specificity of some symptoms related to sexually transmitted infections, especially in women. This is because some symptoms are also found in other non-STI diseases. As a result, having symptoms does not necessarily mean the individual has a sexually transmitted infection (20-22).

In this study, individuals with the symptoms were older than those without the symptoms (in both men and women), and the highest prevalence in both lifetime and point prevalence was in the age group 30 - 40. Regarding the currently presented syndromes, the average age of women was 34.60 (43.71 - 25.49). Again, the prevalence of symptoms associated with sexually transmitted infections varies between different age groups. The prevalence of sexually transmitted infections seems higher in younger participants who are more sexually active (24). However, some symptoms associated with sexually transmitted infections are less specific and are more commonly reported in older individuals without STI infection (i.e., these symptoms may appear due to other illnesses than STIs) (25).

This study suggested that symptoms are more common in married women than in single individuals. One of the possible reasons for this finding is the social stigma, which is more imposed on single individuals by society in Iranian Muslim society; extramarital sex is not socially acceptable, and single people with sexually transmitted infections are more ashamed to express their illness and symptoms (26, 27). As a result, they may refuse to express these symptoms, and the prevalence of these symptoms in the population is underestimated.

5.1. Limitations

One of the most important challenges of studying STIs and their related behaviors is being highly sensitive, and the cultural and social stigma leads to a lower participation rate and underreporting in such studies. Depending on the importance and severity of each symptom, different degrees of reporting and recall bias may occur in the study.

Although some sexually transmitted infections are asymptomatic, syndromic surveillance has low sensitivity and specificity due to non-syndromic infections. However, such a surveillance approach is believed to be valid enough to monitor the trend and distribution of STIs in most communities (10).

5.2. Conclusions

The present study's estimated point and lifetime prevalence of the selected syndromes associated with sexually transmitted infections were alarmingly high. The results emphasize the need for widely available and effective STI-related health and medical services to reduce current infections and prevent new ones in the Iranian population.

Acknowledgements

References

  • 1.

    Newman L, Rowley J, Vander Hoorn S, Wijesooriya NS, Unemo M, Low N, et al. Global Estimates of the Prevalence and Incidence of Four Curable Sexually Transmitted Infections in 2012 Based on Systematic Review and Global Reporting. PLoS One. 2015;10(12). e0143304. [PubMed ID: 26646541]. [PubMed Central ID: PMC4672879]. https://doi.org/10.1371/journal.pone.0143304.

  • 2.

    Afsar Kazerooni P, Mousavi M, Khazaei Z, Esfahani MV, Mohseni S, Nejat M, et al. The prevalence of HIV among female head of household in Shiraz in 2015. Immunopathol Persa. 2018;4(2). e29.

  • 3.

    Afsar Kazerooni P, Fararouei M, Nejat M, Akbarpoor M, Sedaghat Z. Under-ascertainment, under-reporting and timeliness of Iranian communicable disease surveillance system for zoonotic diseases. Public Health. 2018;154:130-5. [PubMed ID: 29241098]. https://doi.org/10.1016/j.puhe.2017.10.029.

  • 4.

    Abouchadi S, Shahabuddin A, Zhang WH, Firoz T, Englert Y, Nejjari C, et al. Existing Models of Maternal Death Surveillance Systems: Protocol for a Scoping Review. JMIR Res Protoc. 2016;5(4). e197. [PubMed ID: 27729305]. [PubMed Central ID: PMC5080526]. https://doi.org/10.2196/resprot.5758.

  • 5.

    Tabatabaei S, Zahraei M, Ahmadnia H, Ghotbi M, Rahimi F. [Principles of disease prevention and surveillance]. Tehran, Iran: Roohe Ghalam Publishers; 2007. Persian.

  • 6.

    Underwood JM, Brener N, Thornton J, Harris WA, Bryan LN, Shanklin SL, et al. Overview and Methods for the Youth Risk Behavior Surveillance System - United States, 2019. MMWR Suppl. 2020;69(1):1-10. [PubMed ID: 32817611]. [PubMed Central ID: PMC7440204]. https://doi.org/10.15585/mmwr.su6901a1.

  • 7.

    Satterwhite CL, Torrone E, Meites E, Dunne EF, Mahajan R, Ocfemia MC, et al. Sexually transmitted infections among US women and men: prevalence and incidence estimates, 2008. Sex Transm Dis. 2013;40(3):187-93. [PubMed ID: 23403598]. https://doi.org/10.1097/OLQ.0b013e318286bb53.

  • 8.

    World Health Organization. Global health sector strategy on sexually transmitted infections 2016-2021: toward ending STIs. Geneva, Switzerland: World Health Organization; 2016, [cited 2022]. Available from: https://apps.who.int/iris/handle/10665/246296.

  • 9.

    Jardim Santos C, Gomes B, Ribeiro AI. Mapping Geographical Patterns and High Rate Areas for Sexually Transmitted Infections in Portugal: A Retrospective Study Based on the National Epidemiological Surveillance System. Sex Transm Dis. 2020;47(4):261-8. [PubMed ID: 31876867]. https://doi.org/10.1097/OLQ.0000000000001122.

  • 10.

    World Health Organization. Guidelines for surveillance of sexually transmitted diseases. Geneva, Switzerland: WHO Regional Office for South-East Asia; 2000, [cited 2022]. Available from: https://apps.who.int/iris/handle/10665/205170.

  • 11.

    Afsar Kazeroni P, Khazaei Z, Mousavi M, Khazaei S, Sohrabivafa M, Dehghani SL, et al. Prevalence of human immunodeficiency virus and tuberculosis among homeless individuals. Immunopathol Persa. 2018;4(1). e06.

  • 12.

    Nasirian M, Karamouzian M, Kamali K, Nabipour AR, Maghsoodi A, Nikaeen R, et al. Care Seeking Patterns of STIs-Associated Symptoms in Iran: Findings of a Population-Based Survey. Int J Health Policy Manag. 2015;5(1):5-11. [PubMed ID: 26673644]. [PubMed Central ID: PMC4676971]. https://doi.org/10.15171/ijhpm.2015.146.

  • 13.

    Shahesmaeili A, Shokoohi M, Tavakoli F, Rabiee MH, Kamali K, Haghdoost AA, et al. Prevalence of Symptom-based Sexually Transmitted Infections and Related Factors among Incarcerated Men in Iran, 2013. Med J Islam Repub Iran. 2021;35:185. [PubMed ID: 36042833]. [PubMed Central ID: PMC9391771]. https://doi.org/10.47176/mjiri.35.185.

  • 14.

    Nasirian M, Baneshi MR, Kamali K, Haghdoost AA. Estimation of Prevalence and Incidence of Sexually Transmitted Infections in Iran; A model-based approach. J Res Health Sci. 2015;15(3):168-74. [PubMed ID: 26411663].

  • 15.

    Bahrami N, Simbar M, Soleimani M. [Sexual health challenges of adolescents in Iran: a review article]. Scientific Journal of School of Public Health and Institute of Public Health Research. 2013;10(4):1-16. Persian.

  • 16.

    Vakilian K, Mousavi SA, Keramat A. Estimation of sexual behavior in the 18-to-24-years-old Iranian youth based on a crosswise model study. BMC Research Notes. 2014;7(1):1-4.

  • 17.

    Mousavi M, Fararooei M, Afsar Kazerooni P, Nasirian M, Ghaem H. Careseeking Pattern in the General Iranian Population with Sexually Transmitted Infection Syndromes: A Population-Based Survey. J Occup Health Epidemiol. 2022;11(4):275-80.

  • 18.

    Mousavi M, Fararouei M, Kazerooni PA, Nasirian M, Ghaem H. Population based estimation of point and period prevalence of sexully transmitted infections based the iranian symptoms surveillance system. Amazonia Investiga. 2019;8(1):29-42.

  • 19.

    Mousavi M, Fararooei M, Afsar Kazerooni P, Nasirian M, Ghaem H. Evaluation of Conducting Phone Interviews on Sexual Behavior: An Iranian Population-Based Study. Shiraz E-Med J. 2022;23(6).

  • 20.

    George R, Thomas K, Thyagarajan SP, Jeyaseelan L, Peedicayil A, Jeyaseelan V, et al. Genital syndromes and syndromic management of vaginal discharge in a community setting. Int J Std Aids. 2004;15(6):367-70. [PubMed ID: 15186579]. https://doi.org/10.1258/095646204774195191.

  • 21.

    Mlisana K, Naicker N, Werner L, Roberts L, van Loggerenberg F, Baxter C, et al. Symptomatic vaginal discharge is a poor predictor of sexually transmitted infections and genital tract inflammation in high-risk women in South Africa. J Infect Dis. 2012;206(1):6-14. [PubMed ID: 22517910]. [PubMed Central ID: PMC3490689]. https://doi.org/10.1093/infdis/jis298.

  • 22.

    Pourreza A, Khabiri R, Rahimi Foroushani A, Akbari Sari A, Arab M, Kavosi Z. Health care-seeking behavior in Tehran, Islamic Republic of Iran. World Appl Sci J. 2011;14(8):1190-7.

  • 23.

    Kokiwar PR, Reddy KS, Pragnya P, Akshay P, Srija R, Shravya G, et al. Prevalence of sexually transmitted diseases in an urban slum area. J Cli Sci Res. 2021;10(1):15-8.

  • 24.

    Sharma S, Gupta B. The prevalence of reproductive tract infections and sexually transmitted diseases among married women in the reproductive age group in a rural area. Indian J Community Med. 2009;34(1):62-4. [PubMed ID: 19876459]. [PubMed Central ID: PMC2763657]. https://doi.org/10.4103/0970-0218.45376.

  • 25.

    Nasirian M, Doroudi F, Gooya MM, Sedaghat A, Haghdoost AA. Modeling of human immunodeficiency virus modes of transmission in Iran. J Res Health Sci. 2012;12(2):81-7. [PubMed ID: 23241516].

  • 26.

    Zarei N, Joulaei H, Darabi E, Fararouei M. Stigmatized Attitude of Healthcare Providers: A Barrier for Delivering Health Services to HIV Positive Patients. Int J Community Based Nurs Midwifery. 2015;3(4):292-300. [PubMed ID: 26448956]. [PubMed Central ID: PMC4591575].

  • 27.

    Mousavi MS, Dehghani SL, Behzad B, Pourrezaei S, Ata'Ali M. Study of the Epidemiology and Use of Condoms in Vulnerable Women Referring to Damage Reduction Centers in Shiraz During 2015-2016. Int J Epidemiol Res. 2021;8(4):175-81.