Repeat symptomatic Neisseria gonorrhoeae infections among men who have sex with men in Bangkok,Thailand,2006

Abstract

We analyzed the incidence and predictors of symptomatic repeat Neisseria gonorrhoeae (NG) infection among men who have sex with men (MSM) enrolled in the Bangkok MSM Cohort Study. Thai MSM aged ≥18 years were enrolled during 2006–2010 and followed every four months. At baseline, participants were screened for rectal and urethral NG and Chlamydia trachomatis (CT) infections using nucleic acid amplification testing (NAAT), rectal and pharyngeal NG by culture, and pharyngeal CT by NAAT. During follow-up, symptomatic participants were tested for NG infection by NAAT and Gram stain of rectal or urethral specimens. Among 1464 participants without NG infection at the baseline visit and having at least one follow-up visit, 11.2% (164/1464) developed symptomatic NG infection, for a total of 251 infections. Symptomatic repeat NG infection occurred in 28.0% (46/164) of participants. The incidence rate was 3.9 cases per 100 person-years. Baseline predictors of repeat symptomatic NG were as follows: unknown human immunodeficiency virus (HIV) status despite history of HIV testing, previous sexually transmitted infection diagnosis by physician, insertive-only anal intercourse without a condom, amyl nitrate use at baseline, CT infection at baseline, age 18–24 years, and being a student; HIV infection at baseline or during the study period was also associated with repeat symptomatic NG infection.

Keywords

Asia homosexual men

Introduction

Infection with Neisseria gonorrhoeae (NG) may increase the risk of human immunodeficiency virus (HIV) transmission.^1,2 NG infection is concentrated in specific communities,^3,4 and subgroups of men who have sex with men (MSM) are at high risk for NG infection.⁵ Persons with repeat NG infection are considered core transmitters of NG⁶ and at even greater risk for HIV infection. A study in San Francisco, California, found that MSM with repeat NG or Chlamydia trachomatis (CT) infections in the past two years had almost a nine-fold increased risk of incident HIV infection.²

A systematic review demonstrated that repeat NG infection among men (median 7%, range: 0%–31%) occurred frequently and at rates similar to those among women.⁷ In the United Kingdom (UK), around 10% of MSM receiving care were diagnosed with a repeat NG infection within one year.⁸ Most repeat NG infections result from re-infection caused by lack of treatment of partners or the initiation of sexual activity with a new infected partner.⁴ However, repeat infections may also be a marker for persistent NG infection.

The U.S. Centers for Disease Control and Prevention (CDC) recommends re-screening men and women at three months after an initial NG diagnosis to identify re-infections.⁴ Thailand’s 2015 National Guidelines on Sexually Transmitted Infections also recommends re-screening persons diagnosed with NG by Gram stain and culture, and re-assessing sexually transmitted infection (STI) risk at seven days and three months after initial diagnosis.⁹ A study conducted from 2006 to 2010 among MSM in Bangkok, Thailand, demonstrated a prevalence of NG infection at 5%, with predominantly rectal site infections.¹⁰ A recent study conducted from 2015 to 2016 in Khon Kaen province reported 55% prevalence of NG infection in MSM.¹¹ However, there are few studies describing repeat NG infection in this population. Although most NG infections are asymptomatic, symptomatic NG infections are more likely to lead to presentation for care and treatment.⁴ To further understand the epidemiology of repeat symptomatic NG infection, we describe the incidence of NG infection and predictors of symptomatic repeat NG infection among MSM in Bangkok, Thailand.

Methods

We recruited participants into the Bangkok MSM Cohort Study (BMCS) from men attending Silom Community Clinic (SCC), a male sexual health clinic located in central Bangkok. A description of the BMCS has been previously published.^10,12,13 Eligibility criteria for inclusion in the BMCS included being a Thai national, male at birth, at least 18 years of age, resident of Bangkok or neighboring provinces (Patumthani, Nonthaburi, Samutprakarn, and Nakorn Prathom), and reporting penetrative oral or anal sex with another man in the six months preceding study entry, commitment to attend at least 36 months of follow-up visits at four-month intervals for a maximum of 60 months and being willing and able to provide written informed consent.

At the enrollment visit, participants underwent a physical examination and answered a computer-assisted self-interview (CASI) to report their socio-demographic and sexual behaviors during the previous four months. All CASI questions were originally adapted from the CDC’s Young Men’s Survey,¹⁴ which had been validated with MSM in Thailand.^15–18 At baseline, rectal and pharyngeal swabs and first-void urine were collected for CT and NG testing. Urine and rectal swabs were tested for CT and NG by nucleic acid amplification test (NAAT; Roche Amplicor®, Roche Diagnostics, Branchburg, NJ, USA).

At baseline and follow-up, all participants were tested for HIV infection using oral fluid and OraQuick® (OraSure Technologies Inc., Oregon, USA). If reactive, three other HIV rapid tests were performed on venous blood: (1) Determine™ HIV 1/2 (Abbott, Japan); (2) DoubleCheck™ II HIV 1&2 (Organics Ltd, Israel), replaced in February 2011 by SD-Bioline HIV1/2 3.0 (Standard Diagnostics, South-Korea), and replaced in January 2012 by Double Check Gold™ Ultra HIV 1&2 (Organics Ltd, Israel); and (3) Capillus™ HIV-1/HIV-2 (Trinity Biotech, Kansas City, USA), replaced in November 2008 by Core™ HIV-1/2 (Core Diagnostics, Birmingham, UK), and replaced in August 2013 by SD-Bioline HIV1/2 3.0. If all three rapid tests were reactive, HIV infection was confirmed and the participant was given post-test counseling, and referred for care and treatment according to Thai national guidelines. If rapid tests were inconclusive, anti-HIV testing (both rapid tests and enzyme immunoassay) was performed on a second sample taken 14 days after the initial blood draw.

At each follow-up visit, participants reported behaviors during the last four months via CASI and underwent HIV testing and counseling. Participants with signs or symptoms consistent with CT or NG infection (i.e. penile or anogenital pain, urethral discharge) had either urethral swab, urine, or rectal swab specimens tested for CT or NG by NAAT, and Gram stain (for NG only), depending on the site of symptoms. They were also advised to come to SCC at any time if they had signs or symptoms of STI and have an unscheduled visit for testing. We defined NG infection as positive test by NAAT and/or Gram stain. Participants who had NG infection were treated with ceftriaxone 250 mg intramuscular injection and azithromycin 1 g. If they had CT infection, they were treated with azithromycin 1 g oral dose. Participants with CT and NG infections were counseled about partner management and treatment and encouraged to bring partners to the clinic for treatment.

Statistical analyses

Analysis of incident and repeat infections during follow-up visits were limited to participants who did not have evidence of NG infection at baseline, as detected by NAAT, Gram stain, or culture.

The minimum duration between episodes of symptomatic NG infections in our sample was 80 days, suggesting reinfection was more likely rather than a treatment failure.^8,19 The incidence rate of symptomatic repeat NG infection was calculated using survival analysis, defined as first incident and any repeat infection(s), regardless of anatomical site, during follow-up. As a result, we used the Andersen-Gill extension of the Cox regression model for multiple failures²⁰ to evaluate and test predictors of symptomatic repeat NG infections. All predictors were measured at enrollment except HIV infection which was assessed at enrollment and follow-up visits. Variables associated with symptomatic repeat NG infection with a p ≤ 0.10 in bivariate analysis were included in multivariable analysis, with likelihood ratio test and manual backward elimination approach used to determine variables to include in the final model and adjusted for period of enrollment. Statistical significance was evaluated using a two-sided p<0.05. We performed all analyses using STATA^® (Version 12, 2011, Stata Corp., College Station, TX, USA).

Ethical review

We obtained written informed consent from all participants of the BMCS. The Ethical Review Committee for Research in Human Subjects of the Thailand Ministry of Public Health, and the CDC Institutional Review Board approved the protocol, informed consents, and supporting documents.

Results

Participant characteristics at enrollment

We enrolled 1744 Thai MSM during 2006–2008 (Period 1) and 2009–2010 (Period 2). Of the 1744, one (0.1%) participant declined to provide samples. Anatomic site-specific NG prevalence and risk factors for infection were described elsewhere.¹⁰ Briefly, the overall baseline prevalence of CT was 14.6% (255/1743) and NG was 6.9% (120/1743).¹⁰ Of 1743 participants with specimens at baseline, 165 (9.5%) were lost to follow-up (i.e. never retuned for any follow-up visit after enrollment by February 2016, observation period of this analysis). Among 120 participants with NG infection at baseline, 78 (65.0%) had at least one follow-up visit and, among those, 18 (23.1%: 95% confidence interval [CI] 14.3–34.0) had at least one symptomatic NG infection on a follow-up visit (Figure 1). Repeat infection occurred within six months of first infection among five (27.8%) participants.

Figure 1.

Participant flow diagram of Neisseria gonorrhoeae infection among Thai men who have sex with men from the Bangkok MSM Cohort Study, Bangkok, Thailand, 2006–2016. LTFU: lost to follow-up; NG: Neisseria gonorrhoeae.

Characteristics of symptomatic repeat NG infections

After excluding participants lost to follow-up as well as those with baseline NG infection (detected by NAAT, Gram stain, or culture), regardless of anatomic site, we included 1464 (83.9%) participants of 1744 initially enrolled for incident analysis of repeat symptomatic NG infection (Figure 1). Of these, 897 (61.3%) were aged >24 years and 1162 (79.4%) self-reported being homosexual (Table 1).

Table 1.

Characteristics of Thai men who have sex with men from the Bangkok MSM Cohort Study with repeat symptomatic Neisseria gonorrhoeae (NG) infection, Bangkok, Thailand, 2006–2016.

	Total	Repeat symptomatic NG infection
Characteristics	N	%	N	%
Overall	1464	100.0	164	100.0
Age (years)
18–24	567	38.7	83	50.6
≥25	897	61.3	81	49.4
Education
Less than secondary	29	2.0	4	2.4
Secondary/vocational	752	51.4	103	62.8
University or higher	683	46.6	57	34.8
Living situation
Live with partner	224	15.3	54	32.9
Live alone/roommate	651	44.5	92	56.1
Live with family	589	40.2	18	11.0
Employment
Unemployed	63	4.3	6	3.7
Full-time employed	877	59.9	82	51.0
Student	524	35.8	76	46.3
Enrollment period
Period 1 (2006–2008)	1077	73.6	132	80.5
Period 2 (2009–2010)	387	26.4	32	19.5
Sexual orientation
Homosexual	1162	79.4	130	79.3
Heterosexual	10	0.7	0	0.0
Bisexual	248	16.9	31	18.9
Transgender women	44	3.0	3	1.8

Among 1464 participants, 164 (11.2%) had at least one symptomatic NG infection detected by NAAT and/or Gram stain at either the rectum or urethra during follow-up (time at risk to the first episode was 6045 person-years [PY], median follow-up time two years [[Interquartile Range, IQR = 1, 4], for a total of 251 NG infections [time at risk for all episodes was 6436 PY]). Of these 164 men with symptomatic NG infections, 99 (60.3%) had urethral infections and 65 (39.6%) had rectal infections (Table 2).

Table 2.

Symptomatic Neisseria gonorrhoeae (NG) infection among Thai men who have sex with men from the Bangkok MSM Cohort Study, Bangkok, Thailand, 2006–2016.

	Total	Urethral infection (n, %)	Rectal infection (n, %)
Overall	164	99 (60.4)	65 (39.6)
Diagnosis
Positive by NAAT and Gram stain	96	88	8^a
Positive by NAAT only	61	8	53
Positive by Gram stain only	7	3^b	4^a
Number of infections during follow-up
1	118 (72.0)
>1	46 (28.0)
Same anatomic site	35 (76.1)	32	3
Different anatomic site	11 (23.9)
Repeat NG infection within six months	7 (15.2)

^aFrom 17 Gram stain tested.

^bNo nucleic acid amplification test (NAAT) specimens were available.

Among 164 participants with NG infection during follow-up, 118 (72.0%) had one infection only, 26 (15.8%) had two infections, and 20 (12.2%) had three or more infections (Figure 2). More than one infection (repeat symptomatic infection) occurred in 46 (28.0%, 95% CI 21.3–35.6) of 164 participants with NG infection. Among participants without NG infection during follow-up, 32.6% had current HIV infection (424/1300: 95% CI 30.1%–35.2%); among those with symptomatic NG infection during follow-up, 50.6% had current HIV infection (83/164: 95% CI 42.7%–58.5%; p < 0.05) (Figure 1).

Figure 2.

Number of Neisseria gonorrhoeae (NG) infections during follow-up from the Bangkok MSM Cohort Study, Bangkok, Thailand, 2006–2016 (n = 164).

Among 46 participants with repeat infection: 35 (76.1%) had repeat infection at the same anatomic site; the median time between infections (i.e. first and second infection) was 548 days (range: 80–1608 days); seven (15.2%) had repeat infections within six months (Table 2).

Factors associated with symptomatic repeat NG infections

In the final multivariable Cox regression model, factors significantly associated with symptomatic repeat NG infection were as follows: unknown HIV status despite history of HIV testing reported at enrollment (adjusted hazard ratio [AHR] 3.5, 95% CI 2.0–6.3); report of previous STI diagnosis by physician (AHR 2.4, 95% CI 1.1–2.3); insertive-only anal intercourse without a condom (AHR 2.2, 95% CI 1.4–3.6); report of amyl nitrate use at baseline (AHR 1.7, 95% CI 1.1–2.5); CT infection at baseline (AHR 1.6, 95% CI 1.1–2.4); age 18–24 years (AHR 1.6, 95% CI 1.1–2.3); being a student (AHR 1.6, 95% CI 1.1–2.1); and HIV infection at baseline or during the study (AHR 2.0, 95% CI 1.5–2.8) (Table 3). The incidence rate of repeat symptomatic NG infection overall was 3.9 infections per 100 PY (95% CI 3.4–4.4).

Table 3.

Multivariable model of characteristics associated with repeat symptomatic Neisseria gonorrhoeae (NG) infections among Thai men who have sex with men in the Bangkok MSM Cohort Study, Bangkok, Thailand, 2006–2016 (n = 1464).

Characteristics at enrollment	No. of infections, N (251/1464)	Person-years (PY)	Incidence rate per 100 PY	Repeat symptomatic NG infection^a,b
Characteristics at enrollment	No. of infections, N (251/1464)	Person-years (PY)	Incidence rate per 100 PY	HR, 95% CI		AHR^b, 95% CI
Age at entry (years)
18–24	126/567	2410	5.2	1.7, 1.3–2.2		1.6, 1.1–2.3
≥25	125/897	4026	3.1		1.0	1.0
Employment
Unemployed	9/63	282	3.2	1.0, 0.5–2.0		0.4, 0.1–1.4
Student	119/877	2240	5.3	1.7, 1.3–2.2		1.6, 1.1–2.1
Full-time employed	123/524	3914	3.1		1.0	1.0
Anal intercourse
Insertive and receptive without a condom	139/664	2947	4.7	1.7, 1.3–2.2		1.5, 1.01–2.1
Insertive only without a condom	31/145	625	5.0	1.8, 1.2–2.7		2.2, 1.4–3.6
Always use condom	81/653	2864	2.8		1.0	1.0
Amyl nitrate use
Yes	50/161	720	6.9	2.0, 1.5–2.7		1.7, 1.1–2.5
No	201/1300	5717	3.5		1.0	1.0
History of HIV testing reported at enrollment
Yes and do not know result	17/41	183	9.3	2.2, 1.3–3.7		3.5, 2.0–6.3
Yes and know result	112/732	3322	3.4	0.8, 0.6–1.0		0.9, 0.6–1.2
Never tested	122/687	2926	4.2	1.0		1.0
History of STI diagnosis by physician (self-report)
Yes	121/370	1628	7.4	2.7, 2.1–3.5		2.4, 1.1–2.3
No/no information	130/1091	4809	2.7	1.0		1.0
HIV infection
Prevalent/incident infection before NG infection	141/505	2296	6.1	2.3, 1.8–2.9		2.0, 1.5–2.8
No	110/959	4141	2.7	1.0		1.0
CT infection at enrollment
Prevalent infection	72/193	818	8.8	2.6, 2.0–3.4		1.6, 1.1–2.4
No	174/1159	5159	3.4	1.0		1.0

Note: Denominator may not sum to 100% due to missing value. AHR: adjusted hazard ratio; CT: Chlamydia trachomatis; HR: hazard ratio; STI: sexually transmitted infection.

^aDuring follow-up visits from enrollment to February 2016.

^bAdjusted for period of enrollment, lifetime history of sexual coercion (yes/no), existence of social support (yes/no), ever thought or attempted suicide (yes/no), ever had sex with a female in one’s lifetime (yes/no), age at first anal sex with a man (<18 years/≥18 years), history of HIV testing (yes/no), self-reported circumcision (yes/no), and comprehensive knowledge of HIV (agreement with four statements: know that a condom can protect against HIV transmission during vaginal sex, know that a condom can protect against HIV transmission during anal sex, know that a person living with HIV can look healthy, and know that HIV is common among MSM/otherwise). Behaviors during the past four months reported at the baseline visit were as follows: recreational drug use (yes/no), recreational drug use to enhance sex (yes/no), erectile dysfunction drug use (yes/no), location for casual sex encounters (school, work, hotel, pub or disco, department store toilet, other (yes/no), being paid for sex (yes/no), having a foreign partner (yes/no), binge drinking at least 2–3 times per week (yes/no), number of casual male partners in last four months (≥5 vs. 2–4 vs. 0–1), casual sex encounters where one lives/own home (yes/no or other place), casual sex encounters at a partner’s home (yes/no or other place), casual sex encounters at a sauna (yes/no or other place), casual sex encounters at a park (yes/no or other place).

Discussion

Our study found the incidence of symptomatic repeat NG infections in a cohort of sexually active MSM to be high, with approximately 4% of MSM diagnosed with symptomatic NG infection at the urethral or rectal site each year. Twenty-eight percent of participants diagnosed with symptomatic NG infection had a repeat symptomatic infection.

Repeat NG infection indicates ongoing risk for HIV and STI acquisition and, as previously described, those with repeat NG infection are core transmitters.⁶ Targeted prevention strategies for this group could potentially lower STI and HIV acquisition rates in a community more than broad prevention strategies alone.⁶ A systematic review of the prevalence of repeat (mostly asymptomatic) NG infections among men attending STI clinics or population-based studies in the United States, UK, and Denmark reported a range of 0–30%.⁷ In our cohort of MSM with high-risk behaviors, we found that 28% of participants initially diagnosed with NG infection had one or more repeat infections, and 15% of these had repeat infection within six months. Our observed incidence rate of 3.9 repeat symptomatic NG infections per 100 PY was among participants with baseline NG negative results during the observation period. This incidence is lower than the rate reported from a retrospective cohort study of MSM attending the Melbourne Sexual Health Center (6.2 per 100 PY, 95% CI 5.9–6.5). However, that study included both symptomatic and asymptomatic infections.²¹

We found that factors associated with repeat symptomatic NG infection were unknown HIV status despite history of HIV testing, report of previous STI diagnosis, insertive-only anal intercourse without a condom, report of amyl nitrate use, CT infection at baseline, young age, being a student, and HIV infection at baseline or during the study. Many of these risk factors were similar to those found for incident HIV infection; a previous analysis from BMCS found a significant association between HIV infection and amyl nitrate.¹³ Amyl nitrate, or poppers, have been commonly used among MSM attending sex parties, who also reported sexual intercourse with limited access to condoms and lubricant.²² Among participants in our cohort, consistent high-risk behaviors were found throughout the follow-up period (i.e. the enrollment visit and 36 months of follow-up visits): 2% reported anal sex without a condom, 1% reported recreational drug use, and 4% reported engaging with multiple sexual partners.¹³ Identifying persons with repeat NG infections to target STI and HIV prevention counseling and biomedical approaches such as pre-exposure prophylaxis (PrEP) may be a strategy to prioritize HIV prevention efforts.

Because this analysis includes only participants who had signs or symptoms of NG infection, which are more commonly associated with urethral infection, men reporting insertive-only anal intercourse without a condom were more likely to have repeat symptomatic NG infection compared to men who preferred a versatile sexual role (i.e. insertive and receptive anal sex) (Table 3). A prior study by Tongtoyai et al. found that 56% of MSM with urethral NG had symptoms, compared to 6% of MSM with rectal NG.¹⁰ van Liere et al. found that, in MSM, the sensitivity of NAAT testing for anorectal NG detection based on symptom and sexual history was 71%.²³ We were more likely to detect infection at the urethra, the location for over 60% of NG infections, using a syndromic approach.

Twenty-eight percent of participants diagnosed with symptomatic NG infection had repeat infection, with 15% of these having repeat infection within six months. CDC and Thai guidelines recommend re-screening at three months after an initial NG diagnosis^4,9; however, many men may not return for retesting. It is possible that active recall (i.e. postal, short message service, and phone call reminders) at the time of NG diagnosis can increase engagement in re-screening in high-risk populations such as MSM.²⁴ Re-screening also offers an opportunity for prevention counseling and biomedical prevention approaches.

Our study had several limitations. Only participants with symptoms were tested for NG infection during the follow-up visit, so the reported incidence and repeat infection rates are likely an underestimate, given that asymptomatic NG infection is common.^3,25,26 Our assessment only included participants with no NG at baseline; when we assessed repeat infection among participants with NG infection at enrollment, we found a similar high proportion of repeat infection similar to this assessment (23.1% and 28.0%, p = 0.41). Symptomatic pharyngeal NG infections were not assessed in the study because of the possibility of false-positive NAAT.²⁷ It is difficult to define if repeat infections were new infections or persistent infection; however, given that the time between first and second infections was more than 80 days, these are likely re-infections. Previous studies have used a variety of intervals to define repeat infection with durations of 30–90 days being standard.^19,22

In conclusion, our study demonstrated that repeat symptomatic NG infection was associated with a number of factors. HIV testing venues for MSM should provide routine STI screening and treatment, re-screening, and provision of HIV/STI prevention strategies, such as condoms and PrEP. Given growing concern for antimicrobial-resistant NG infection, enhanced surveillance for infection with NG in MSM and transgender women will allow programs to monitor for the emergence of antimicrobial resistance.

Repeat NG infection is a sentinel event, providing an opportunity for targeted HIV and STI prevention.

Footnotes

Acknowledgments

The authors kindly acknowledge and are thankful for the support of the Thailand Ministry of Public Health-U.S. Centers for Disease Control and Prevention Collaboration, the Silom Community Clinic (Silom Community Clinic @TropMed), the Department of Disease Control, Thailand Ministry of Public Health, the Rainbow Sky Association of Thailand, and the Service Workers in Group Foundation. The authors also wish to thank Dorothy L Southern for her assistance in scientific writing and critical review of this manuscript. We dedicate this work to the memory of Supaporn Chaikummao, RN, and Patrick J Flaherty who devoted their professional lives to the care of persons at risk of HIV infection. The findings and conclusions in this manuscript are those of the authors and do not necessarily represent the views of the U.S. Centers for Disease Control and Prevention.

Declaration of conflicting interests

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

Funding

The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This study was supported by the U.S. Centers for Disease Control and Prevention and funded by the Division of HIV/AIDS Prevention, CDC.

ORCID iDs

Sarika Pattanasin

Eileen F Dunne

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Repeat symptomatic Neisseria gonorrhoeae infections among men who have sex with men in Bangkok,Thailand,2006–2016

Abstract

Keywords

Introduction

Methods

Statistical analyses

Ethical review

Results

Participant characteristics at enrollment

Characteristics of symptomatic repeat NG infections

Factors associated with symptomatic repeat NG infections

Discussion

Footnotes

Acknowledgments

Declaration of conflicting interests

Funding

ORCID iDs

References