Clinical Analysis of Gonorrhea Coinfection With Ureaplasma urealyticum,Chlamydia trachomatis,and Mycoplasma hominis in Southern China

Abstract

This retrospective study investigated coinfection with Ureaplasma urealyticum (UU), Chlamydia trachomatis (CT), and Mycoplasma hominis (MH) among patients with Neisseria gonorrhoeae (NG) in southern China to support clinical diagnosis and treatment. A total of 1,138 specimens from patients with gonorrhea were tested for UU, CT, MH, and other pathogens using culture methods, electrochemiluminescence, and fluorescence quantitative PCR. Among the 1,138 patients with NG, 526 (46.2%) were coinfected with at least one additional pathogen. The most frequent coinfection patterns involving UU, CT, or MH were NG+UU (235, 20.7%), NG+CT (173, 15.2%), and NG+MH (90, 7.9%). Coinfections with two or more additional pathogens occurred in 171 patients (15.0%): NG+UU+MH (82, 7.2%), NG+UU+CT (53, 4.7%), NG+MH+CT (21, 1.8%), and NG+UU+MH+CT (15, 1.3%). The distribution of coinfections differed by age group for NG+UU (χ² = 12.23, df = 5, p = .032) and NG+CT (χ² = 29.05, df = 5, p < .001), and women showed a higher rate of NG+UU coinfection than men (χ² = 24.30, df = 1, p < .001). Overall, mixed infections involving UU, CT, and MH were common among patients with NG, supporting comprehensive sexually transmitted infections screening to reduce missed diagnoses, treatment delays, and transmission.

Keywords

Mycoplasma non-gonococcal urethritis antimicrobial resistance surveillance

Introduction

Sexually transmitted infections (STIs) have a high global incidence and disease burden. According to the World Health Organization (WHO), more than 1 million new infections occur daily worldwide as of 2023 (Liblik et al., 2023). Gonorrhea, caused by Neisseria gonorrhoeae (NG), leads to infections of the genital tract, rectum, pharynx, and eyes, resulting in severe complications such as epididymitis, salpingitis, infertility, and other long-term sequelae. Gonorrhea accounts for approximately 87 million new cases annually among the global adult population (Ball et al., 2024; Belcher et al., 2023; Unemo et al., 2019).

Chlamydia trachomatis (CT), one of the most prevalent bacterial STIs in humans, accounts for an estimated 131 million cases globally each year (Jury et al., 2023). Chlamydia trachomatis can cause serious health conditions such as pelvic inflammatory disease, pelvic fibrosis, and tubal infertility (Sturd & Rucks, 2023). Ureaplasma urealyticum (UU), one of the smallest prokaryotes, occupying an intermediate position between bacteria and viruses, primarily resides in the human urogenital tract. Ureaplasma urealyticum not only causes infections of the vagina and cervix but is also closely associated with miscarriage, infertility, and intrauterine growth restriction (T. Liu et al., 2022).

Patients with NG infections typically present with acute onset and prominent clinical symptoms, enabling timely diagnosis and treatment, whereas infections caused by UU, CT, or Mycoplasma hominis (MH) often exhibit mild or asymptomatic presentations (T. Liu et al., 2022; Martins et al., 2022). When patients with gonorrhea have concurrent infections with UU, CT, or MH, copathogen testing may be overlooked, and treatment for non-gonococcal pathogens may be delayed. This NG–non-gonococcal urethritis (NGU) mixed-infection pattern increases the complexity of clinical management and poses new challenges for public health control.

When comparing the detection methods employed in this study, culture-based techniques for UU and MH detection present distinct limitations relative to nucleic acid amplification tests (NAATs). Culture methods, which depend on the growth of viable pathogens, exhibit reduced sensitivity in identifying asymptomatic infections, particularly among patients with a history of antibiotic use. NAATs demonstrate high sensitivity in detecting non-viable or low-load infections, but their availability and implementation may be constrained in resource-scarce clinical environments. Coinfections involving UU, CT, and MH not only intensify inflammatory processes within the urogenital tract but also foster the emergence of antimicrobial resistance through synergistic interactions between pathogens. For example, mucosal damage caused by NG can facilitate the adhesion and immune evasion of CT, whereas UU infection can increase the production of pro-inflammatory cytokines such as interleukin 6 (IL-6), thereby accelerating tissue damage and treatment failure. Such interaction mechanisms underscore the imperative for comprehensive STI screening in patients with NG to avoid treatment delays and the dissemination of resistance.

Despite extensive global research on NG coinfections with NGU, studies specifically focusing on southern China remain scarce. Given the well-established role of UU and MH as primary causative agents of NGU in this region, as indicated by their high prevalence in local STI cohorts (T. Liu et al., 2022), UU and MH are prioritized in this investigation. The availability of standardized culture-based diagnostic kits for routine clinical screening has enabled a systematic retrospective analysis. This study retrospectively analyses NG coinfections with CT, MH, and UU among patients in Zhuhai, China (2018–2023) and systematically evaluates NG antimicrobial resistance patterns to support clinical diagnosis and treatment.

Materials and Methods

General Information

Strain Sources

Between 2018 and 2023, a total of 1,138 unique NG strains were isolated from patients at sexually transmitted disease (STD) surveillance sites in Zhuhai, China. These strains were cultured on Thayer–Martin (TM) NG agar for 24–48 h. All strains were identified using the VITEK MS microbial mass spectrometry analysis system and the VITEK 2 Compact automated microbial identification system. After purification, the strains were stored in fetal bovine serum at −80 °C for further use.

Reference Strains

Three reference strains, WHO G, WHO P and WHO K, were provided by the STD Control Center of the Chinese Center for Disease Control and Prevention (CDC). Each batch of experiments conducted between 2018 and 2023 participated in the inter-laboratory quality control assessment for gonococcal resistance monitoring organized by the Chinese CDC, and all returned quality evaluation results met the required standards.

Reagents and Main Instruments

The VITEK MS microbial mass spectrometry analysis system, the VITEK 2 Compact automated microbial identification system, and the VITEK 2 NH Test Card (bioMérieux, Marcy-l’Étoile, France) were used for microbial identification.

Gonococcal minimum inhibitory concentration (MIC) test plates (Zhuhai Gold Standard Medical Laboratory Technology Co., Ltd., Zhuhai, China) were used.

Mycoplasma hominis and UU culture and antimicrobial susceptibility test kits (Zhuhai Livzon Diagnostics Inc., Zhuhai, China) were purchased.

Chlamydia trachomatis nucleic acid detection kits (PCR fluorescence probe method; Da An Gene Co., Ltd. of Sun Yat-sen University, Guangzhou, China) were used. Amplification was performed using a LightCycler 480 II system (Roche Diagnostics, Mannheim, Germany).

Neisseria gonorrhoeae culture media consisted of TM agar (Guangzhou Dijie, Guangzhou, China).

Preparation of Bacterial Suspensions

Experimental and reference strains were incubated on selective media in a 5% CO₂ incubator for 18–24 h and then adjusted to bacterial suspensions at a concentration of 1.5 × 10⁸ CFU/mL using physiological saline.

Minimum inhibitory concentration determination and sensitivity criteria: MICs were determined using the agar dilution method, with results interpreted according to the guidelines outlined in the 31st edition of the Clinical and Laboratory Standards Institute document M100 (Humphries et al., 2021). WHO reference strains were used as quality control strains in each test batch, and MIC₅₀ and MIC₉₀ were calculated. High-level tetracycline-resistant NG (TRNG) was defined as having a tetracycline MIC ≥16 mg/L. Penicillinase-producing NG (PPNG) was identified using the acidometric disk method.

Inclusion and Exclusion Criteria

Patients with NG exhibiting typical symptoms of gonorrhea, such as urethral pain, increased urinary frequency and urgency, dysuria, redness and swelling of the urethral meatus, and purulent discharge, were included if they met the following criteria: detection of Gram-negative diplococci in urethral or cervical secretions, a positive NAAT result, or a positive NG culture. Secretions were directly inoculated onto TM agar for culture and identification (Barbee & St. Cyr, 2022).

Patients with UU and MH presenting with typical symptoms of ureaplasma or mycoplasma infection, such as urethral itching, burning sensations, or increased secretions, as well as asymptomatic individuals (i.e., those without urethral or cervical symptoms at the time of sampling), were included if urethral or cervical secretions yielded positive results. Cultures were performed using specific identification panels at 35°C–37°C for 24–48 h, with a color change from yellow to red in liquid medium indicating a positive result for UU (World Health Organization [WHO], 2024d).

Chlamydia trachomatis

Inclusion criteria required that urethral or cervical secretions be suspended in 1 mL of sterile physiological saline, followed by DNA extraction according to the instructions of the CT DNA detection kit (Daan Gene). Amplification was performed using the LightCycler 480 II, with a Ct value <27 considered positive, confirming CT infection (Rodrigues et al., 2022).

Statistical Analysis Methods

Statistical analyses were performed using SPSS version 29.0. Categorical data were expressed as counts and percentages (n [%]). Chi-square (χ²) tests were used to compare group proportions where applicable, and results were reported as χ² (df) with corresponding P-values. When the expected frequency in any cell was <5, Fisher’s exact test was applied. The level of statistical significance was set at p < .05.

Results

General Sociodemographic Characteristics of Patients

Between 2018 and 2023, a total of 1,138 NG isolates were collected, including 1,037 isolates from male urethral secretions and 101 from female cervical secretions. The male-to-female ratio of the study population was 10.3:1 (1,037:101), reflecting a high number of sampled male cases in this surveillance cohort. Patients’ ages ranged from 15 to 72 years, with 90.61% aged between 18 and 59 years. The peak age of infection for both sexes was 18–29 years (Figure 1).

Figure 1.

The Peak Infection Age for Both Genders.

Coinfection With Other Pathogens in Patients With Gonorrhea

Among the 1,138 gonorrhea cases, 526 (46.2%) were coinfected with at least one other pathogen. The most frequent coinfection patterns were NG+UU (235, 20.7%), NG+CT (173, 15.2%), and NG+MH (90, 7.9%). Coinfection with two or more additional pathogens occurred in 171 cases (15.0%), mainly NG+UU+MH (82, 7.2%), NG+UU+CT (53, 4.7%), NG+MH+CT (21, 1.8%), and NG+UU+MH+CT (15, 1.3%).

Women showed higher rates than men for NG+UU (39.6% vs 18.8%; χ² = 24.30, df = 1, p < .001), NG+UU+MH (12.9% vs 6.7%; χ² = 5.32, df = 1, p = .021), NG+UU+CT (11.9% vs 4.0%; Fisher’s exact test, p = .002), NG+MH+CT (5.0% vs 1.5%; Fisher’s exact test, p = .032), and NG+UU+MH+CT (4.0% vs 1.1%; Fisher’s exact test, p = .037). No sex differences were observed for NG+MH (χ² =2.40, df = 1, p = .121) or NG+CT (χ² = 0.01, df = 1, p = .918; Table 1).

Table 1.

Mixed Infection Rates of CT, UU, and MH in Neisseria gonorrhoeae Patients [n (%)].

Gender	n	NG+UU	NG+MH	NG+CT	NG+UU+MH	NG+UU+CT	NG+MH+CT	NG+UU+MH+CT
Males	1,037	195 (18.8%)	78 (7.5%)	158 (15.2%)	69 (6.7%)	41 (4.0%)	16 (1.5%)	11 (1.1%)
Females	101	40 (39.6%)	12 (11.9%)	15 (14.9%)	13 (12.9%)	12 (11.9%)	5 (5.0%)	4 (4.0%)
Total	1,138	235 (20.7%)	90 (7.9%)	173 (15.2%)	82 (7.2%)	53 (4.7%)	21 (1.8%)	15 (1.3%)

Comparison of Coinfections Across Different Age Groups

Dual coinfections involving UU, MH, or CT were most frequently observed in terms of case counts in patients aged 18–39 years (Table 2). Age-group distributions differed for NG+UU (χ² = 12.22, df = 5, p = .032) and NG+CT (χ² = 29.05, df = 5, p < .001), whereas NG+MH showed no significant variation by age group (χ² = 10.15, df = 5, p = .071). Although the <18 group showed relatively high proportions of NG+UU (9/29, 31.0%) and NG+CT (11/29, 37.9%), post hoc Fisher’s exact tests comparing the <18 group with the combined 18–39 group demonstrated a significantly higher rate of NG+CT in those aged <18 (37.9% vs 13.6%, p = .0013), whereas the difference in NG+UU was not statistically significant (31.0% vs 20.8%, p = .244; Table 2). These findings suggest a high burden of NG+CT coinfection among adolescents, supporting combined CT screening in this subgroup.

Table 2.

Mixed Infection Status of UU, MH, CT, and UU Control Group in Gonorrhea Patients of Different Age Groups [n (%)].

Age Group	n	NG+UU	NG+MH	NG+CT	UU+MH	UU+CT
<18	29	9 (31.0%)	1 (3.4%)	11 (37.9%)	8 (27.6%)	8 (27.6%)
18–29	537	97 (18.1%)	32 (6.0%)	76 (14.2%)	85 (15.8%)	77 (14.3%)
30–39	330	83 (25.2%)	35 (10.6%)	42 (12.7%)	56 (17.0%)	33 (10.0%)
40–49	146	25 (17.1%)	15 (10.3%)	34 (23.3%)	33 (22.6%)	8 (5.5%)
50–59	74	19 (25.7%)	7 (9.5%)	4 (5.4%)	14 (18.9%)	6 (8.1%)
≥60	22	2 (9.1%)	0 (0.0%)	6 (27.3%)	6 (27.3%)	1 (4.5%)
Total	1,138	235 (20.7%)	90 (7.9%)	173 (15.2%)	202 (17.8%)	133 (11.7%)

Analysis of PPNG and TRNG

Between 2018 and 2023, 504 PPNG strains (44.29%) and 442 high-level TRNG strains (38.84%) were identified. The annual PPNG positivity rate ranged from 23.44% to 62.65%, showing a significant upward trend that peaked at 62.65% in 2023 (p < .05). In contrast, the annual TRNG positivity rate fluctuated between 29.90% and 52.44% without a clear monotonic trend (Figure 2).

Figure 2.

The Annual TRNG Positivity Rate Fluctuated.

Antimicrobial Susceptibility Results of Neisseria gonorrhoeae Strains

Penicillin resistance increased significantly from 36.4% in 2018 to 69.2% in 2023 (p < .05; Supplementary Table 1). Correspondingly, MIC₅₀ values (2021–2023) and MIC₉₀ values (2018–2023) were ≥2 mg/L, exceeding the resistance threshold. Tetracycline resistance decreased from 93.6% in 2018 to 56.3% in 2019 and then gradually increased to 68.5% in 2023; MIC₅₀ and MIC₉₀ values remained ≥2 mg/L throughout, indicating sustained high-level resistance.

Ciprofloxacin resistance remained consistently high (93.7%–100%), with MIC50 4–8 mg/L and MIC90 16 mg/L. In contrast, azithromycin non-susceptibility decreased from 8.6% in 2018 to 2.1% in 2023, with MIC₅₀ and MIC₉₀ values ≤1 mg/L. Ceftriaxone non-susceptibility increased from 0.0% in 2018 to 2.1% in 2023, whereas MIC₅₀ and MIC₉₀ values remained ≤0.25 mg/L. Cefixime non-susceptibility rose from 1.4% in 2018 to 11.2% in 2023, accompanied by increases in MIC₅₀ (0.03 mg/L in 2018–2019 to 0.06 mg/L in 2020–2023) and MIC₉₀ (0.025 mg/L in 2018 to 0.5 mg/L). Spectinomycin intermediate susceptibility was observed in three cases (2.1%) in 2022 and two cases (1.4%) in 2023, with MIC₅₀ and MIC₉₀ values of 8–16 mg/L (Supplementary Table 1).

Discussion

STIs are a major global reproductive health issue (Hufstetler et al., 2024). According to the WHO, over one million new STI cases occur daily worldwide, with many being asymptomatic, thereby exacerbating the urgency of the problem (Liblik et al., 2023). The burden of STIs is particularly heavy in low- and middle-income countries, largely due to inadequate diagnostic capabilities and the high cost of testing services where available (WHO, 2024b). Beyond physiological harm, STIs severely affect patients’ psychological, social, and economic well-being, considerably reducing their quality of life (WHO, 2024c). Gonorrhoea, a widespread STI, poses a substantial threat to public health (Williams et al., 2024). In 2022, 96,313 cases of gonorrhoea were reported in China, making it the fourth most prevalent notifiable infectious disease in the country after viral hepatitis, tuberculosis, and syphilis (Zhu et al., 2024).

This study retrospectively analyzed gonorrhea cases with concurrent infections of other STIs in southern China between 2018 and 2023, aiming to provide updated insights for clinical diagnosis, treatment, and STI control. Among 1,138 gonorrhea cases, coinfections with pathogens such as UU, MH, and CT were observed. Single-pathogen coinfection was identified in 526 cases (46.2%), with NG+UU being the most common pattern (235/1,138, 20.7%), exceeding the prevalence reported in central China (S. Liu et al., 2024). Furthermore, NG+CT coinfection accounted for 173 cases (15.2%), which was lower than that reported in Taiwan (Wu et al., 2024). Coinfections with two or more additional pathogens were observed in 171 cases (15.0%). This study emphasizes that coinfections increase the severity and complexity of infections (Saldanha, 2020). Clinically, screening for other STIs in patients with gonorrhea may facilitate early detection and management of coinfections, thereby improving treatment outcomes and reducing the risk of complications. Population-based prevalence data for UU, CT, and MH in asymptomatic individuals in southern China remain limited; this evidence gap makes it difficult to distinguish pathogenic infection from commensal colonization, particularly for UU and MH (T. Liu et al., 2022).

Gender differences in dual and multiple NG coinfections with UU, MH, and CT were evident. Men were more frequently diagnosed, likely because more pronounced symptoms such as dysuria and urethral discharge prompt earlier health care seeking (Yonke et al., 2022). However, women exhibited higher NG+UU coinfection rates than men (40/101, 39.6% vs 195/1,037, 18.8%; χ² = 24.30, df = 1, p < .001; Table 1), possibly due to anatomical factors facilitating pathogen entry and milder symptoms leading to delayed diagnosis and treatment (Li et al., 2023). The 19–39 age group accounted for the majority of NG+NGU coinfections (867/1,138, 76.2%), which may be associated with high sexual activity, multiple partners, and insufficient awareness of safe sex practices and gonorrhea prevention (Cannovo et al., 2024; Liddon et al., 2022; Lovett & Duncan, 2019). Age-group differences were observed for NG+CT (χ² = 29.05, df = 5, p < .001) and NG+UU (χ² = 12.22, df = 5, p = .032; Table 2).

In our cohort, NG+MH coinfection (90, 7.9%) was less common than NG+UU (235, 20.7%) and NG+CT (173, 15.2%). Coinfections involving UU and MH were also frequent (e.g., NG+UU+MH: 82, 7.2%). The lower NG+MH rate may be attributable to the biological and ecological similarities between UU and MH, which often coexist and adhere effectively to epithelial cells, thereby exacerbating epithelial damage (Oh et al., 2024; Wasnik et al., 2022). The observed frequency of NG+CT coinfection highlights a clinically important combination, consistent with evidence that NG-induced mucosal damage can facilitate CT adherence and immune evasion, particularly among sexually active young individuals (Darville, 2021; Zhai et al., 2021).

Patients with gonorrhea and concurrent NGU often present with acute gonorrhea symptoms, which may lead to the oversight of other pathogens during diagnosis (T. Liu et al., 2022). Residual pathogens following treatment may cause NGU or cervicitis (Moi et al., 2015; Niforatos & Rothman, 2022). Ureaplasma infections can induce cytokine secretion, such as IL-6, through Toll-like receptor 2 activation, resulting in tissue damage. Neisseria gonorrhoeae infection involves host cell adhesion and invasion and can trigger oxidative stress, whereas concurrent NGU pathogens may further amplify mucosal inflammation and prolong symptoms if non-gonococcal pathogens are not treated (Sell et al., 2022). Coinfections may reduce antibiotic efficacy, necessitating tailored antimicrobial regimens (Lu et al., 2023; Maueia et al., 2024). Screening for NGU pathogens in patients with acute gonorrhea may therefore enable targeted treatment and improve clinical outcomes.

Analysis of gonococcal antibiotic resistance showed notable year-to-year changes over 2018–2023. Penicillin resistance increased from 51/140 (36.3%) in 2018 to 99/143 (69.5%) in 2023, although this rate remained lower than that reported in Indonesia (97.1%; Indriatmi et al., 2020). The PPNG positivity rate rose to 62.7% by 2023 (p < .05), exceeding rates reported in Sweden and Norway (Speers et al., 2014). Furthermore, TRNG positivity exhibited a fluctuating trend, reaching 52.4% in 2023 (p < .05). Ciprofloxacin resistance remained consistently high (93.9%–100%), far exceeding the rate reported in Spain (56.2%; Salmerón et al., 2021). The WHO recommends discontinuing antibiotics with resistance rates above 5% (WHO, 2015). Under this threshold-based approach, penicillin, tetracycline, and ciprofloxacin are not appropriate monotherapies for gonorrhea in this setting. Tetracycline resistance initially declined from 93.8% in 2018 to 56.3% in 2019 before increasing again to 68.3% in 2023. This initial decline (2018–2019) followed by a rebound (2020–2023) may reflect changes in antibiotic stewardship associated with China’s antimicrobial resistance action plan and subsequent variability in enforcement. Azithromycin resistance remained below the WHO 5% threshold for empirical treatment, suggesting its potential suitability as a future first-line option (WHO, 2024e). Ceftriaxone resistance increased from 0.0% in 2018 to 2.4% in 2023, whereas cefixime resistance reached 11.0% by 2023, exceeding the rate reported in Vietnam (3.2%; Adamson et al., 2020). Spectinomycin, a first-line alternative for cephalosporin-resistant strains, maintained susceptibility above 97.6% through 2023, consistent with findings from Zhejiang, China (Zhang et al., 2023). Potential drivers of gonococcal resistance in this setting include unrestricted antimicrobial use, inappropriate antibiotic selection, and genetic mutations. Extragenital infections, particularly in men who have sex with men, play a critical role in fostering resistant strains through pathogen interaction and gene exchange (WHO, 2024a). Enhanced global resistance monitoring is therefore imperative to curb the spread of multidrug-resistant pathogens.

To address gonorrhea and STI coinfections, a multifaceted approach is essential. Clinicians should screen for all relevant STI pathogens in patients with gonorrhea to ensure comprehensive care. Public health efforts must prioritize sexual health education and encourage routine STI testing among high-risk groups. Governments and organizations should strengthen oversight in high-risk areas, provide free screening, and raise public awareness. Personalized treatment regimens and regular post-treatment follow-up are crucial. International collaboration is vital to address the global STI challenge; collectively, these clinical and public health actions can safeguard sexual health and mitigate STI transmission.

This study’s strengths lie in its comprehensive analysis of 1,138 gonorrhea cases, incorporating coinfections with pathogens such as UU, MH, CT, HPV, TP-Ab, HIV, and HSV. Detailed data analysis provided insights into prevalence, variations in positivity rates, and infection patterns, offering valuable guidance for clinical management. The high prevalence of single-pathogen coinfections underscores the importance of addressing dual infections in clinical practice. The study also explored the implications of coinfections for gonorrhea management and proposed robust prevention strategies.

Limitations of this single-region retrospective surveillance analysis include limited Generalizability, incomplete exploration of pathogen interaction mechanisms, and potential measurement variability related to detection methods and sample handling. Future studies should broaden sample diversity and investigate underlying mechanisms to refine STI prevention strategies.

Conclusion

Given the high coinfection rates among patients with gonorrhea, simultaneous testing for UU, MH, and CT is recommended. Managing coinfections with combination therapies may reduce treatment duration and transmission risk. Continued monitoring of antibiotic resistance at local and global levels, together with research into resistance mechanisms, is essential for effective gonorrhea prevention, control, and treatment.

Supplemental Material

sj-docx-1-jmh-10.1177_15579883261418251 – Supplemental material for Clinical Analysis of Gonorrhea Coinfection With Ureaplasma urealyticum, Chlamydia trachomatis, and Mycoplasma hominis in Southern China

Supplemental material, sj-docx-1-jmh-10.1177_15579883261418251 for Clinical Analysis of Gonorrhea Coinfection With Ureaplasma urealyticum, Chlamydia trachomatis, and Mycoplasma hominis in Southern China by Bo Zheng, Hongyan Ma, Zixin Liu, Zhenzhen Du, Jianhong Xie and Hongfu Li in American Journal of Men's Health

Footnotes

ORCID iD

Hongfu Li

Ethical Considerations

This study was conducted in accordance with the Declaration of Helsinki and was approved by the ethics committee of The Third People’s Hospital of Zhuhai. The study adhered to ethical guidelines to ensure the protection of participants’ rights, privacy, and safety throughout the research process.

Informed Consent

Informed consent was obtained from all participants prior to their participation in the study. For participants under the age of 16, informed consent was obtained from their legal guardians. This process ensured that all participants were fully informed about the study’s purpose, methods, potential risks, and possible benefits, and participated voluntarily.

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

Declaration of Conflicting Interests

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

Data Availability Statement

The datasets used and analyzed during the current study are available from the corresponding author on reasonable request.

Supplemental Material

Supplemental material for this article is available online.

References

Adamson

P. C.

Van Le

H. H. L.

G. M.

Nguyen

T. V.

Klausner

J. D

. (2020). Trends in antimicrobial resistance in Neisseria gonorrhoeae in Hanoi, Vietnam, 2017-2019. BMC Infectious Disease, 20(1), 809. https://doi.org/10.1186/s12879-020-05532-3

Ball

L. M.

Bronstein

Liechti

G. W.

Maurelli

A. T.

(2024). Neisseria gonorrhoeae drives Chlamydia trachomatis into a persistence-like state during in vitro co-infection. Infection and Immunity, 92(1), e0017923. https://doi.org/10.1128/iai.00179-23

Barbee

L. A.

St. Cyr

S. B.

(2022). Management of Neisseria gonorrhoeae in the United States: Summary of evidence from the development of the 2020 Gonorrhea treatment recommendations and the 2021 centers for disease control and prevention sexually transmitted infection treatment guidelines. Clinical Infectious Disease, 74(Suppl_2), S95–S111. https://doi.org/10.1093/cid/ciac043

Belcher

Rollier

C. S.

Dold

Ross

J. D. C.

MacLennan

C. A.

(2023). Immune responses to Neisseria gonorrhoeae and implications for vaccine development. Frontiers in Immunology, 14, 1248613. https://doi.org/10.3389/fimmu.2023.1248613

Cannovo

Bianchini

Gironacci

Garbati

Di Prospero

Cingolani

Scendoni

Fedeli

(2024). Sexually transmitted infections in adolescents and young adults: A cross section of public health. International Journal of Environmental Research and Public Health, 21(4), 501. https://doi.org/10.3390/ijerph21040501

Darville

(2021). Pelvic inflammatory disease due to Neisseria gonorrhoeae and Chlamydia trachomatis: Immune evasion mechanisms and pathogenic disease pathways. Journal of Infectious Disease, 224(12 Suppl. 2), S39–S46. https://doi.org/10.1093/infdis/jiab031

Hufstetler

Llata

Miele

Quilter

L. A. S.

(2024). Clinical updates in sexually transmitted infections, 2024. Journal of Women’s Health, 33(6), 827–837. https://doi.org/10.1089/jwh.2024.0367

Humphries

Bobenchik

A. M.

Hindler

J. A.

Schuetz

A. N.

(2021). Overview of changes to the clinical and laboratory standards institute performance standards for antimicrobial susceptibility testing, M100, 31st edition. Journal of Clinical Microbiology, 59(12), e0021321. https://doi.org/10.1128/JCM.00213-21

Indriatmi

Prayogo

R. L.

Nilasari

Suseno

L. S.

(2020). Antimicrobial resistance of Neisseria gonorrhoeae in Jakarta, Indonesia: A cross-sectional study. Sexual Health, 17(1), 9–14. https://doi.org/10.1071/SH19140

10.

Jury

Fleming

Huston

W. M.

Luu

L. D. W.

(2023). Corrigendum: Molecular pathogenesis of Chlamydia trachomatis. Frontiers in Cellular and Infection Microbiology, 13, 1358553. https://doi.org/10.3389/fcimb.2023.1358553

11.

You

Lee

Yaesoubi

Hsu

Gift

T. L.

Chesson

H. W.

Berruti

A. A.

Salomon

J. A.

Rönn

M. M.

(2023). The estimated lifetime quality-adjusted life-years lost due to Chlamydia, Gonorrhea, and Trichomoniasis in the United States in 2018. Journal of Infectious Disease, 227(8), 1007–1018. https://doi.org/10.1093/infdis/jiad047

12.

Liblik

Lam

Pham

Byun

Farina

J. M.

Baranchuk

(2023). Sexually transmitted infections & the heart. Current Problems in Cardiology, 48(5), 101629. https://doi.org/10.1016/j.cpcardiol.2023.101629

13.

Liddon

Pampati

Dunville

Kilmer

Steiner

R. J.

(2022). Annual STI testing among sexually active adolescents. Pediatrics, 149(5), e2021051893. https://doi.org/10.1542/peds.2021-051893

14.

Liu

Ouyang

Tang

Mei

(2024). Prevalence of Neisseria gonorrhoeae, Chlamydia trachomatis, Ureaplasma urealyticum among outpatients in central China: A retrospective study. Diagnostic Microbiology and Infectious Disease, 110(1), 116394. https://doi.org/10.1016/j.diagmicrobio.2024.116394

15.

Liu

Lai

S. Y.

Zhou

Liu

Y. L.

Chen

S. S.

Jiang

Y. M.

(2022). Analysis of Ureaplasma urealyticum, Chlamydia trachomatis, Mycoplasma genitalium and Neisseria gonorrhoeae infections among obstetrics and gynecological outpatients in southwest China: A retrospective study. BMC Infectious Disease, 22(1), 283. https://doi.org/10.1186/s12879-021-06966-z

16.

Lovett

Duncan

J. A.

(2019). Human immune responses and the natural history of Neisseria gonorrhoeae infection. Frontiers in Immunology, 9, 3187. https://doi.org/10.3389/fimmu.2018.03187

17.

Zhao

Xiao

(2023). Analyses of human papillomavirus, Chlamydia trachomatis, Ureaplasma urealyticum, Neisseria gonorrhoeae, and co-infections in a gynecology outpatient clinic in Haikou area, China. BMC Women’s Health, 23(1), 117. https://doi.org/10.1186/s12905-023-02259-6

18.

Martins

J. L. R.

Pinto

E. M. H.

Oliveira

S. A.

Gomes

F. A. C.

Silva

O. N.

(2022). Treatment of sexually transmitted infections (STIs) caused by Neisseria Gonorrhoeae and the global shortage of antibiotics. Venereology, 1(3), 235–244.

19.

Maueia

Murahwa

Manjate

Sacarlal

Kenga

Unemo

Andersson

Mussá

Williamson

A. L.

(2024). The relationship between selected sexually transmitted pathogens, HPV and HIV infection status in women presenting with gynaecological symptoms in Maputo City, Mozambique. PLOS ONE, 19(9), e0307781. https://doi.org/10.1371/journal.pone.0307781

20.

Moi

Blee

Horner

P. J.

(2015). Management of non-gonococcal urethritis. BMC Infectious Disease, 15, 294. https://doi.org/10.1186/s12879-015-1043-4

21.

Niforatos

J. D.

Rothman

R. E.

(2022). Sexually transmitted infections treatment guidelines, 2021. Annals of Emergency Medicine, 80(1), 68–70.

22.

K. Y.

Lee

Park

M. H.

Jeong

J. H.

Yang

J. B.

Lim

C. K.

J. G.

Yang

Y. S.

(2024). Vaginal microbiota of pregnant women with Ureaplasma urealyticum and Mycoplasma hominis infections. Frontiers in Cellular and Infection Microbiology, 14, 1445300. https://doi.org/10.3389/fcimb.2024.1445300

23.

Rodrigues

Marques

Vieira-Baptista

Sousa

Vale

(2022). Therapeutic options for Chlamydia trachomatis infection: Present and future. Antibiotics (Basel), 11(11), 1634. https://doi.org/10.3390/antibiotics11111634

24.

Saldanha

(2020). STIs in adolescents: Chlamydia, gonorrhea, mycoplasma genitalium, and HPV. Current Problems in Pediatric and Adolescent Health Care, 50(7), 100835. https://doi.org/10.1016/j.cppeds.2020.100835

25.

Salmerón

Viñado

Arando

Alcoceba

Romero

Menéndez

Bernal

Idigoras

Colomina

Martin-Saco

Leal-Negredo

Á.

Torreblanca

Martínez

Serra-Pladevall

(2021). Neisseria gonorrhoeae antimicrobial resistance in Spain: A prospective multicentre study. Journal of Antimicrobial Chemotherapy, 76(6), 1523–1531. https://doi.org/10.1093/jac/dkab037

26.

Sell

Nasir

Courchesne

(2022). Erratum: Urethritis: Rapid evidence review. American Family Physician, 105(1), 8.

27.

Speers

D. J.

Fisk

R. E.

Goire

Mak

D. B.

(2014). Non-culture Neisseria gonorrhoeae molecular penicillinase production surveillance demonstrates the long-term success of empirical dual therapy and informs gonorrhoea management guidelines in a highly endemic setting. Journal of Antimicrobial Chemotherapy, 69(5), 1243–1247. https://doi.org/10.1093/jac/dkt501

28.

Sturd

Rucks

E. A.

(2023). Chlamydia trachomatis. Trends in Microbiology, 31(5), 535–536. https://doi.org/10.1016/j.tim.2022.11.002

29.

Unemo

Seifert

H. S.

Hook

E. W.

3rd Hawkes

Ndowa

Dillon

J. R.

(2019). Gonorrhoea. Nature Reviews, Disease Primers, 5(1), 79. https://doi.org/10.1038/s41572-019-0128-6

30.

Wasnik

Mittal

Ghope

Sonkar

S. C.

Arora

Saluja

(2022). Multiple sexually transmitted co-infections are associated with adverse reproductive outcomes in asymptomatic adolescent pregnant women; A prospective cohort study. Frontiers in Medicine, 9, 1046233. https://doi.org/10.3389/fmed.2022.1046233

31.

Williams

Seib

K. L.

Fairley

C. K.

Pollock

G. L.

Hocking

J. S.

McCarthy

J. S.

Williamson

D. A.

(2024). Neisseria gonorrhoeae vaccines: A contemporary overview. Clinical Microbiology Reviews, 37(1), e0009423. https://doi.org/10.1128/cmr.00094-23

32.

World Health Organization. (2015). Global action plan on antimicrobial resistance.

33.

World Health Organization. (2024a). Global health sector strategies on, respectively, HIV, viral hepatitis and sexually transmitted infections for the period 2022-2030.

34.

World Health Organization. (2024b). Global hepatitis report 2024: Action for access in low- and middle-income countries.

35.

World Health Organization. (2024c). HIV and viral hepatitis diagnostic tests in low-and middle-income countries: Forecasts of global and regional demand for 2022-2026.

36.

World Health Organization. (2024d). Recommendations for the treatment of Trichomonas vaginalis, Mycoplasma genitalium, Candida albicans, bacterial vaginosis and human papillomavirus (anogenital warts): Executive summary [Internet]. https://www.ncbi.nlm.nih.gov/books/NBK605750/

37.

World Health Organization. (2024e). Updated recommendations for the treatment of Neisseria gonorrhoeae, Chlamydia trachomatis and Treponema pallidum (syphilis), and new recommendations on syphilis testing and partner services.

38.

T. Y.

Lin

K. Y.

L. H.

Sun

H. Y.

Huang

Y. S.

Liu

W. D.

Liu

W. C.

Chang

L. H.

Chang

S. Y.

Hung

C. C.

(2024). Sexually transmitted coinfections among at-risk HIV-positive MSM: Implications for optimal preemptive treatment. Frontiers in Medicine, 11, 1328589. https://doi.org/10.3389/fmed.2024.1328589

39.

Yonke

Aragón

Phillips

J. K.

(2022). Chlamydial and gonococcal infections: Screening, diagnosis, and treatment. American Family Physician, 105(4), 388–396.

40.

Zhai

Wang

Qiao

Zhao

Wang

(2021). Correction: Detection of Neisseria gonorrhoeae and Chlamydia trachomatis infections in pregnant women by multiplex recombinase polymerase amplification. PLOS ONE, 17(7), e70271836. https://doi.org/10.1371/journal.pone.0271836

41.

Zhang

L. H.

Huang

M. Q.

Zeng

F. R.

Chen

S. C.

(2023). Evaluation of Neisseria gonorrhoeae isolates susceptibility to antibiotics in Zhejiang Province Since 2007. Infection and Drug Resistance, 16, 1441–1448. https://doi.org/10.2147/IDR.S396793

42.

Zhu

Gong

Chen

(2024). Ceftriaxone-resistant Gonorrhea—China, 2022. Morbidity and Mortality Weekly Report, 73(12), 255–259. https://doi.org/10.15585/mmwr.mm7312a2

Supplementary Material

Please find the following supplemental material available below.

For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.

For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.

0.00 MB

0.02 MB