Abstract
Gonococcal urethritis (GU) is the second most common sexually transmitted infection (STI). Epidemiologic studies of the situation of GU reinfection and its related risk factors among patients with a history of GU in Thailand remain somewhat limited. A hospital-based retrospective cohort study was conducted between January 1, 2010 and December 31, 2020 to determine the incidence and risk factors of GU reinfection among male patients visiting in Royal Thai Army (RTA) Hospitals. A total of 2,465 male patients presenting a history of GU was included in this study. In all, 147 (6.0%; 95% CI 5.1–6.9) male patients presented GU reinfection, representing an incidence rate of 1.3 (95% CI 1.1–1.5) per 100 person-years. The independent risk factors for GU reinfection were age < 30 years (AHR 1.7; 95% CI 1.0–2.8), number of sexual partners equal to 2 (AHR 3.4; 95% CI 1.0–11.2), \(\ge\) 3 (AHR 5.6; 95% CI 2.7–11.6), and participants residing in the north (AHR 4.1; 95% CI 2.3–7.5) and northeast regions (AHR 2.1; 95% CI 1.1–3.9). Incidence of GU reinfection among male patients visiting RTA Hospitals was significantly high among younger aged patients, especially in the north and northeast regions. Multiple sex partners played a major role in GU reinfection. Effective STI prevention programs should be provided to alleviate reinfection and its complications.
Similar content being viewed by others
Introduction
Gonococcal urethritis (GU) is the second most common sexually transmitted infection (STI) and has been increasing both among males and females, affecting public health and economics worldwide1. Gonorrhea is caused by Neisseria gonorrhoeae infection; a columnar-type epithelial infection at the genital organs among both males and females2,3. When the disease is untreated, the infection would invade adjacent organs causing prostatitis, or posterior urethritis leading to infertility2,4,5.
Globally in 2018, the World Health Organization reported that the estimated cases of GU involved 87 million patients and about 27 million were in the Asia Pacific6. In Thailand, the data for the population aged 15–24 years demonstrated that Neisseria gonorrhoeae infection increased from 38.7 per 100,000 population in 2014 to 68.1 in 20177. A related population-based study in the US reported that the cumulative incidence of GU reinfection was 5%8; additionally, a wide range of incidence rates was found for reinfection from 2.3 to 4.3 per 100 person years9,10. Sexual behaviors including having multiple sexual partners remain risk factors for GU infection11,12. Moreover, a related study reported that GU reinfection was more common in young male populations8. Additionally, GU infection also related to other STIs including non-gonococcal infection and HIV13,14.
The related evidence demonstrated that the prevalence of gonococcal transmission in Thailand has been rising continuously. However, the essential information of GU reinfection and its related risk factors among patients with a history of GU in Thailand remain somewhat limited. Furthermore, a recent study reported that a history of gonococcal infection was an independent risk for antimicrobial-resistant Neisseria gonorrhoeae15. Essential information is required to focus disease prevention and control strategies. Attenuating the risk for gonococcal infection will help to reduce the transmission and to alleviate its complications. Therefore, the investigators aimed to determine the incidence and risk factors for GU reinfection among men visiting military hospitals in all regions of Thailand.
Methods
Study designs and subjects
A hospital-based retrospective cohort study was conducted between January 1, 2010 and December 31, 2020 to determine the incidence and risk factors of gonococcal urethritis reinfection among male patients visiting in the Royal Thai Army (RTA) Hospitals. In Thailand, 37 RTA Hospitals are located nationwide in five regions, i.e., central, north, northeast, south and Bangkok. Each RTA Hospital provides medical care for both military personnel and civilians. As a tertiary (standard/advanced) hospital, the RTA Hospitals, selected to be the study sites, were located in five provinces of five regions including Phramongkutklao Hospital in Bangkok, Anandamahidol Hospital in Lop Buri (central), Fort Somdej Phra Naresuan Hospital in Phitsanulok (north), Fort Suranaree Hospital in Nakhon Ratchasima (northeast), and Fort Wachirawut Hospital in Nakhon Si Thammarat (south). The eligible criteria of participants comprised male patients aged at least 20 years presenting a history of GU. GU was determined according to the International Classification of Diseases, Tenth Revision codes (ICD-10) in A540, A541, A548 or A549, presented in medical records16. At each RTA Hospital, the internist would be available at the STI clinic to provide care. Typically, male patients with suspected GU infection would access care at STI clinics. History taking and physical examination would be performed by the internist. Patients presenting gram-negative intracellular diplococci on microscopic examination of a smear of mucopurulent urethral exudate received a diagnosis of GU.
Data collection
Patient information was retrieved from the database of STI clinics. In all, 2,465 male patients in five hospitals were included in this study. A standardized case report form (CRF) was used to collect data of patients from medical records, including demographic characteristics, age, residential area, occupation, marital status, number of lifetime sexual partners, history of GU diagnosis, history of other STIs and sexual behaviors. The data in the medical records of patients were retrieved and filled in the CRF by trained registered nurses in five hospitals and sent to the data management unit at Phramongkutklao College of Medicine in Bangkok.
Ethics consideration
The study was reviewed and approved by the Institutional Review Board, Royal Thai Army Medical Department in compliance with international guidelines such as the Declaration of Helsinki, the Belmont Report, CIOMS Guidelines and the International Conference on Harmonization of Technical Requirements for Registration of Pharmaceuticals for Human Use—Good Clinical Practice (ICH-GCP) (Approval number R126h/62). Due to the retrospective cohort study design, a waiver of documentation of consent was used; the waiver for consent was granted by the Institutional Review Board, Royal Thai Army Medical Department.
Statistical analysis
All analyses were conducted using StataCorp, 2021, Stata Statistical Software: Release 17, College Station, TX, USA: StataCorp LLC. Demographic characteristics were analyzed using descriptive statistics. Continuous data were presented as mean and standard deviation while percentage was used for categorical data. The incidence rates per 100 person-years of observation for GU reinfection was presented. Reinfection was defined as the first episode of GU diagnosed at least 14 days after a previously recorded infection for patients during the study period10. The person-times of observation of the participants were calculated as the duration between a previously treated GU and the next reinfection at the end of the study period, whichever occurred first.
Patients having no record of reinfection were assumed to be free of subsequent infection throughout the follow-up period. Participants’ follow-up was right censored December 31, 2020. Multivariate cox regression analysis was performed to obtain the adjusted hazard ratio (AHR) and 95% confidence interval (95% CI) of the risk factors related to the first episode of GU reinfection during the study period. A p-value less than 0.05 was considered statistically significant.
Results
Characteristics of study participants
A total of 2,465 male patients, presenting a history of GU from five regions of Thailand, was included in this study. All the subjects were males aged 27.2 ± 7.9 years. The majority of patients were from a hospital in Bangkok (37.9%). In terms of occupation, 42.0% of participants comprised government officers. The median number of lifetime sexual partners was 1.0. Participants with a history of consistent condom use among participants was 6.2%. A history of other STIs and sexual behaviors is presented in Table 1.
Incidence and risk factors of GU reinfection among male patients visiting RTA hospitals
A total of 147 (6.0%; 95% CI 5.1–6.9) male patients presented GU reinfection, representing an incidence rate of 1.3 (95% CI 1.1–1.5) per 100 person-years. The univariate and multivariate cox regression analysis identifying risk factors for GU reinfection are shown in Table 2. The independent risk factors for GU reinfection were age < 30 years (AHR 1.7; 95%CI 1.0–2.8), number of lifetime sexual partners equal to 2 (AHR 3.4; 95%CI 1.0–11.2), ≥ 3 (AHR 5.6; 95%CI 2.7–11.6), and participants residing in the north (AHR 4.1; 95%CI 2.3–7.5) and northeast regions (AHR 2.1; 95%CI 1.1–3.9), adjusting for age, occupations, regions and number of lifetime sexual partner.
Discussion
Our data demonstrated that the incidence rate of GU reinfection among male patients visiting RTA Hospitals between 2010 and 2020 was 1.3 per 100 person-years. GU reinfection was significantly related to personal characteristics and a history of multiple sexual partners. Estimates of the incidence of GU remain limited in Southeast Asia, including Thailand. To our knowledge, this constitutes the first report on the incidence of GU reinfection among Thai men visiting hospitals located in all regions.
The cumulative incidence of GU reinfection among men in this study accounting for 6.0% and may be comparable to the cumulative incidence of those among men in a population-based study in California, USA. (5%)8. However, longitudinal studies conducted in public STI clinics in Baltimore, USA, and in Alberta, Canada indicated incidence was 4.3 and 2.3 reinfections per 100 person years, respectively, indicating the incidence rate of reinfection in the present study was relatively low9. The reported GU reinfection in the present study was based on medical records in hospitals; thus, only male patients with GU visiting the hospitals would be recorded while others visiting STI clinics were excluded from this study. According to this reason, the incidence of GU reinfection in the present study may have been underestimated.
We found that younger age male patients (< 30 years old) were highly related to GU reinfection. Similarly, related reports conducted in the USA and Canada showed that patients aged less than 25 years were independently at risk of increased reinfection9,10. Furthermore, one related study in the New Zealand health care setting demonstrated that patients aged less than 20 years were more likely to have a potential risk for Neisseria gonorrhoeae reinfection17. This finding may be explained by younger sexually active males using condoms inconsistently18, leading to STIs including GU, nonGU and HIV12,19,20. Regarding one related report among young Thai men from 2008 to 200912, male patients having multiple sexual partners indicated a risk behavior for STIs and tended to be a risk for GU reinfection. The finding was consistent with related studies of Rangsin et al. revealing young males having multiple sexual partners ≥ 4 were more likely to have STIs12,13. In terms of occupation, our finding reported no significant evidence of any association between occupation and GU reinfection. However, a related study in Thailand demonstrated that unemployed young men were associated with STIs such as Chlamydia trachomatis infection12.
In terms of geographic region of the participants, the results of the study participants may not represent the incidence rate of GU reinfection among all male patients in these regions, especially in Bangkok where several clinics and hospitals are available. Male patients with GU may not receive care at the same hospital. Therefore, the results reflected the situation of those among male patients vising RTA Hospitals located in each region of Thailand. The incidence rate of GU reinfection among participants was significantly high in the north (2.6 per 100 person-years) and northeast (1.2 per 100 person-years). These regions also experienced the highest epidemic of HIV/AIDS and other STIs such as Chlamydia trachomatis and Hepatitis C7,20. Likewise, related studies in Thailand demonstrated a high prevalence of STIs among young Thai men residing in north12 and northeast regions20. One of the explanations for this finding is that GU reinfection may be a proxy indicator for other STIs in these regions. Furthermore, the knowledge of STIs such as gonococcal infection may be limited; some people did not know the mode of transmission or prevention for gonococcal infection21,22.
We found that male patients vising RTA Hospitals reporting a history of consistent condom use was 6.3%. Our data suggested that effective interventions such as 100% condom use should be implemented among young Thai men, especially in the north and the northeast, to alleviate the transmission of Neisseria gonorrhoeae, Chlamydia trachomatis and HIV, and its complications including periurethral abscesses, postinflammatory urethral strictures and pelvic inflammatory diseases23,24. In addition, modifiable risk behaviors such as having multiple sexual partners should be diminished. Furthermore, the system for active STIs case detection, STIs education, motivation to seek diagnosis and treatment in youth and general populations should be established7.
Limitations involving these data must be considered. First, this constituted a hospital-based retrospective cohort study; thus, we were unable to obtain confirmation by cultures of the reported Neisseria gonorrhoeae infection. However, we attempted to define GU according to the ICD-10 appearing in medical records. Although this was a hospital-based study, the results of the present study corresponded to those of the report by the Department of Disease Control, Ministry of Public Health demonstrating a continuous increase in GC infection cases in the north and northeast regions7. Second, we intended to determine the situation of GU reinfection; unfortunately, the data of the other sites of gonococcal infection, including rectum and throat, were not collected in this study. Therefore, the rates for gonococcal reinfection in these other sites were unreported. Third, male patients presenting a history of GU may not revisit the same hospital; they may visit STI clinics located at the provincial public health office. Hence, the incidence of GU reinfection may have been underestimated. This issue may be associated with the loss to follow-up and might have introduced selection bias. However, in Thailand, the universal health coverage scheme was implemented since 200225; therefore, the Thai population could access care at registered hospitals. RTA Hospitals are under the government administration and provide care for military personnel and civilians residing in the area. Because of their health scheme attached to the specific hospital, most patients would receive care at the same RTA Hospital. Since this comprised a retrospective cohort study, we lacked the opportunity to explore risk behaviors including history of sex in exchange for gifts/money and history of sex with a female sex worker among these subjects; only data available in medical records were analyzed. However, the case report form was completed by well-trained registered nurses using a standard protocol. Finally, a small number in some variable categories was included; thus, the association between well-known risk factors such as history of other STIs, history of consistent condom use, sexual behaviors and outcome could not be presented.
Conclusion
In conclusion, the incidence of GU reinfection among male patients visiting RTA Hospitals was significantly high among younger aged patients vising the five hospitals, especially in the north and northeast. Multiple sex partners played a major role in GU reinfection in this population. Effective STI prevention programs should be implemented to attenuate reinfection and its complications.
Data availability
The datasets generated during and/or analyzed during the current study are not publicly available because the data set contains sensitive identifying information; thus, ethical restrictions are required concerning the data set. However, the data set are available from the corresponding author on reasonable request.
Abbreviations
- GU:
-
Gonococcal urethritis
- STI:
-
Sexually transmitted infection
- HIV:
-
Human immunodeficiency virus
- ICD-10:
-
The International Classification of Diseases, tenth revision codes
- HR:
-
Hazard ratio
- AHR:
-
Adjusted hazard ratio
- 95%CI:
-
95% Confidence interval
References
Handsfield HH. Color Atlas & Synopsis of sexually transmitted diseases. (McGraw Hill Professional, 2011).
Centers for Disease Control and Prevention. Sexually Transmitted Disease Surveillance 2019. https://www.cdc.gov/std/statistics/2019/default.htm (2019).
Buder, S. et al. Bacterial sexually transmitted infections. JDDG J. German Soc. Dermatol. 17, 287–315 (2019).
Ness, R. B. et al. Douching, pelvic inflammatory disease, and incident gonococcal and chlamydial genital infection in a cohort of high-risk women. Am. J. Epidemiol. 161, 186–195 (2005).
Robertson, J. N., Ward, M. E., Conway, D. & Caul, E. O. Chlamydial and gonococcal antibodies in sera of infertile women with tubal obstruction. J. Clin. Pathol. 40, 377–383 (1987).
World Health Organization. Baseline report on global sexually transmitted infection surveillance 2012. (World Health Organization, 2013).
Ministry of Public Health (Thailand). Progress Report for Thailand Ending AIDS 2018. http://azp.ddc.moph.go.th/report.php. (2018).
Gunn, R. A., Maroufi, A., Fox, K. K. & Berman, S. M. Surveillance for repeat gonorrhea infection, San Diego, California, 1995–2001: establishing definitions and methods. Sexually Transm. Dis. 31, 373–379 (2004).
Mehta, S. D., Erbelding, E. J., Zenilman, J. M. & Rompalo, A. M. Gonorrhoea reinfection in heterosexual STD clinic attendees: longitudinal analysis of risks for first reinfection. Sexually Transm. Infect. 79, 124–128 (2003).
De, P., Singh, A. E., Wong, T. & Kaida, A. Predictors of gonorrhea reinfection in a cohort of sexually transmitted disease patients in Alberta, Canada, 1991–2003. Sexually Transm. Dis. 34, 30–36 (2007).
Dela, H. et al. Risk factors associated with gonorrhea and chlamydia transmission in selected health facilities in Ghana. BMC Infect. Dis. 19, 1–8 (2019).
Jatapai, A. et al. Prevalence and risk factors for chlamydia trachomatis infection among young Thai men in 2008–2009. Sexually Transm. Dis. 40, 241–246 (2013).
Rangsin, R. et al. Risk Factors for HIV Infection among Young Thai Men during 2005–2009. PLoS ONE 10, e0136555 (2015).
Bernstein, K. T., Marcus, J. L., Nieri, G., Philip, S. S. & Klausner, J. D. Rectal gonorrhea and chlamydia reinfection is associated with increased risk of HIV seroconversion. J. Acquired Immune Deficiency Syndromes 53, 537–543 (2010).
Fuertes de Vega, I. et al. Risk factors for antimicrobial-resistant Neisseria gonorrhoeae and characteristics of patients infected with gonorrhea. Enferm. Infecc. Microbiol. Clin. 36, 165–168 (2018).
World Health Organization. International Statistical Classification of Diseases and Related Health Problems 10th Revision. https://icd.who.int/browse10/2010/en (2010).
Rose, S. B., Garrett, S. M., Stanley, J. & Pullon, S. R. H. Chlamydia trachomatis and Neisseria gonorrhoeae retesting and reinfection rates in New Zealand Health care settings: implications for sexually transmitted infection control. Sexually Transm. Dis. 47, 151–157 (2020).
Celentano, D. D. et al. Epidemiologic risk factors for incident sexually transmitted diseases in young Thai men. Sexually Transm. Dis. 23, 198–205 (1996).
Jose, J. E. et al. Prevalence of HIV infection and related risk factors among young Thai men between 2010 and 2011. PLoS ONE 15, e0237649 (2020).
Jose, J. E., Sakboonyarat, B., Mungthin, M., Nelson, K. E. & Rangsin, R. Rising prevalence of HIV infection and associated risk factors among young Thai Men in 2018. Sci. Rep. 11, 1–10 (2021).
Svensson, Linn, S. W. Knowledge of and attitudes to sexually transmitted diseases among Thai university students. Caring Sci. 41, 10–18 (2013).
Paz-Bailey, G. et al. Risk factors for sexually transmitted diseases in Northern Thai adolescents: an audio-computer-assisted self-interview with noninvasive specimen collection. Sexually Transm. Dis. 30, 320–326 (2003).
Bachmann, L. H. et al. Advances in the Understanding and Treatment of Male Urethritis. Clin. Infect. Dis. 61, S763–S769 (2015).
Scholes, D. et al. Prevention of pelvic inflammatory disease by screening for cervical chlamydial infection. New Engl. J. Med. 334, 1362–1366 (1996).
Sumriddetchkajorn, K. et al. Universal health coverage and primary care, Thailand. Bull. World Health Organ. 97, 415 (2019).
Acknowledgements
The authors express their grateful thanks to Col. Prof. Dr. Ram Rangsin for his support to complete the study. The authors are exceedingly grateful to all those involved in the successful field operations in the study, including staff of Phramongkutklao Hospital, Ananda Mahidol Hospital, Fort Somdej Phra Naresuan Hospital, Fort Suranaree Hospital and Fort Wachirawut Hospital. The authors thank all the staff members of the Department of Medicine, Phramongkutklao College of Medicine, for their support in completing this study.
Funding
The present study was supported by (1) Phramongkutklao College of Medicine Foundation and (2) Department of Medicine, Phramongkutklao Hospital.
Author information
Authors and Affiliations
Contributions
The concept for study was developed by MM, BS and ST. MM and BS collected the data. BS analyzed the data. MM, BS and ST wrote the first draft. All authors contributed and approved the final version.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Meesaeng, M., Sakboonyarat, B. & Thaiwat, S. Incidence and risk factors of gonococcal urethritis reinfection among Thai male patients in a multicenter, retrospective cohort study. Sci Rep 11, 22992 (2021). https://doi.org/10.1038/s41598-021-02398-6
Received:
Accepted:
Published:
DOI: https://doi.org/10.1038/s41598-021-02398-6
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.