Abstract
Background
Neisseria gonorrhoeae (N. gonorrhoeae) infections have increased among men who have sex with men and are high among transgender women. Presumptive treatment guidelines may lead to inaccurate treatments and possible antibiotic resistance. Using patient data from AIDS Healthcare Foundation sexually transmitted infection (STI) testing clinics in California and Florida, we identified clinical factors associated with accurate presumptive N. gonorrhoeae treatment.
Methods
Multivariable logistic regression analyses were conducted using patient visit data from 2013 to 2017. A sample of 42 050 patient encounters were analyzed. The primary outcome variable included accurate versus inaccurate presumptive treatment. Risk ratios were generated for particular symptoms, high-risk sexual behavior, and history of N. gonorrhoeae.
Results
Twelve percent (5051/42 050) of patients received presumptive N. gonorrhoeae treatment, and 46% (2329/5051) of presumptively treated patients tested positive for N. gonorrhoeae infection. Patients presenting with discharge or patients presenting with dysuria were more likely to receive accurate presumptive treatment.
Conclusions
Providers should continue to follow the Centers for Disease Control and Prevention guidelines and consider presumptive N. gonorrhoeae treatment based on specific symptoms. As the STI epidemic continues to rise in the United States, along with increased antibiotic resistance, it is imperative to accurately test, diagnose, and treat populations at risk for N. gonorrhoeae and other STIs.
Keywords: Neisseria gonorrhoeae, gonorrhea, men who have sex with men, presumptive treatment, sexually transmitted infections
Antibiotic-resistant Neisseria gonorrhoeae is a growing public health concern. Presumptive treatment may lead to inaccurate treatments and contribute to antibiotic resistance. We identified clinical factors associated with accurate presumptive treatment in effort to inform clinical decision making.
Neisseria gonorrhoeae (N. gonorrhoeae) infection is the second most common bacterial sexually transmitted infection (STI) in the United States, after Chlamydia trachomatis, contributes to serious health complications including epididymitis and increases the risk of human immunodeficiency virus (HIV) transmission particularly among gay, bisexual, and other men who have sex with men (collectively referred to as MSM) if left untreated [1,2].
The estimated N. gonorrhoeae case rate among MSM in the United States increased 375.5% between 2010 and 2018 [1]. Although trends are difficult to assess among transgender women due to lack of surveillance data inclusive of gender identity, recent studies demonstrate alarmingly high rates of N. gonorrhoeae infection among transgender women [3, 4]. The Centers for Disease Control and Prevention (CDC) guidelines recommend presumptive antibiotic treatment prior to a finalized laboratory result for patients with objective clinical evidence of N. gonorrhoeae infection, a known exposure, or those who are symptomatic and unlikely to follow up for treatment [5]. These guidelines are based on the fact that presumptive N. gonorrhoeae treatment reduces the need for a patient to return at a later date for treatment, hastens symptom resolution, and prevents further transmission [6]. Unfortunately, presumptive treatment faces growing concerns over antibiotic resistance. According to the CDC, more than half of all N. gonorrhoeae infections in 2018 were estimated to be resistant to at least one antibiotic [1]. Overtreating uninfected patients may promote antibiotic resistance [7].
It is well established that antibiotic resistance is a growing public health threat and that research and policies aimed at optimizing antibiotic treatment are needed [8]. This study aims to provide data on presumptive N. gonorrhoeae treatment practices by identifying clinical factors associated with accurate presumptive treatment of N. gonorrhoeae among MSM and transgender women in STI testing clinics in California and Florida, 2 states that reported the highest and fourth-highest number of N. gonorrhoeae cases in 2018, respectively [1].
METHODS
AIDS Healthcare Foundation (AHF) provides free walk-in STI testing, diagnosis, and treatment for MSM and other patients at its Wellness Centers. Using a cross-sectional study design, de-identified patient data from existing Wellness Center electronic medical records in California and Florida between 1 January 2013 and 31 December 2017 were analyzed. N. gonorrhoeae testing data were extracted from cisgender MSM and transgender women patients who self-report their gender and sexual identity. MSM and transgender women who received pharyngeal, rectal, and/or urine site-specific nucleic acid amplification tests (NAATs) for N. gonorrhoeae were included in the initial data set.
N. gonorrhoeae testing was ordered for 43 881 clinical encounters among MSM and transgender women during this time frame. In total, 1780 encounters were dropped due to lack of testing results or equivocal test results due to inadequate sample or lab error. Among those clinical encounters that involved N. gonorrhoeae testing, treatment data were extracted for individuals receiving intramuscular ceftriaxone and either oral azithromycin or oral doxycycline per 2010 and 2015 CDC guidelines [5, 9]. Clinical encounters that included non-guideline-based presumptive treatment with ceftriaxone alone (36 clinic encounters) or ceftriaxone, azithromycin, and doxycycline (15 clinical encounters) were dropped from the data set. A total of 42 050 patient encounters were analyzed (Figure 1).
Figure 1.
Patient encounters.
The outcome of interest was accurate presumptive N. gonorrhoeae treatment. This was defined as clinical encounters that involved same-day N. gonorrhoeae testing and CDC guideline-based presumptive N. gonorrhoeae treatment plus a positive N. gonorrhoeae laboratory test result. In order to create this outcome variable, an initial presumptive treatment variable was created. Presumptive treatment was defined as clinical encounters that involved CDC guideline-based treatment on the same day of N. gonorrhoeae testing. Laboratory testing for N. gonorrhoeae typically takes at least 24 hours to result into the electronic medical records database; therefore, same-day treatment was assumed to be presumptive because there was not enough time for results to be confirmed. Presumptive treatment was coded as a binary variable where 0 = no same day treatment and 1 = same day (and therefore presumptive) treatment. Next, a test result variable was created and coded as a binary variable where 0 = negative N. gonorrhoeae test result and 1 = positive N. gonorrhoeae test result. These variables were then multiplied to create the outcome variable, accurate presumptive treatment: 1 = same day presumptive treatment and positive N. gonorrhoeae test result; 0 = any other combination that does not result in same day (presumptive) treatment and positive N. gonorrhoeae test result. In other words, 0 represents all other outcomes that are not defined as accurate presumptive treatment.
Therefore, accurate presumptive treatment occurred among patients who received a positive N. gonorrhoeae test result on any laboratory sample (urine, pharyngeal swab, and/or rectal swab) collected on the same day of presumptive treatment. For example, if patients were treated for N. gonorrhoeae on the same day of sample collection and received a positive N. gonorrhoeae laboratory result the following day, then they were categorized as accurate presumptive N. gonorrhoeae treatment.
Correlates thought to be associated with accurate presumptive treatment were identified in an a priori manner via literature review and clinician judgement. Correlates included specific N. gonorrhoeae symptoms (eg, discharge, urogenital inflammation, dysuria, and acute pharyngitis), as well as high-risk sexual behavior and history of N. gonorrhoeae infection.
The symptom variables were extracted via key-word searches of clinician notes and/or ICD-9/10 codes. Discharge was defined as penile or anal discharge. Urogenital inflammation was defined as penile inflammation, urethritis, rectal inflammation, or proctitis. Dysuria was defined as dysuria or as burning, pain, or discomfort with urination. High-risk sexual behavior was defined as condomless anal sex within the last 12 months based on patient self-report. History of N. gonorrhoeae was defined as any prior history of N. gonorrhoeae infection based on patient self-report. All clinical encounters at AHF Wellness Centers included standardized questions regarding high-risk sexual behavior and history of N. gonorrhoeae.
Bivariate analysis was performed to determine unadjusted risk ratios (RRs) with the outcome variable. Correlates were further examined in multivariable logistic regression models. Covariates for multivariable logistic regression models were determined in an a priori manner based on literature review and directional acyclic graphing (Figures 2–4). All multivariable analyses adjusted for covariates: age, race, gender, and HIV status. Based on the current literature, each of the above-mentioned covariates is associated with N. gonorrhoeae infection and high-risk sexual behavior [1, 10–19]. Therefore, we ascertained that these covariates would influence the correlate variables (symptoms, history of N. gonorrhoeae, and high-risk sexual behavior) as well as the primary outcome variable (accurate presumptive treatment) and must be controlled for as potential confounders. Additionally, all multivariable analyses adjusted for region (California vs Florida). It was assumed in an a priori manner that there would be regional differences in N. gonorrhoeae rates, high-risk sexual behavior, and presumptive treatment practices. History of N. gonorrhoeae and high-risk sexual behavior variables were also controlled for in each respective model where the respective variables were not the primary correlate of interest. All statistical models were generated in accordance with directional acyclic graphing models (Figures 2–4). The assumptions of multivariable logistic regression were verified for each adjusted model. Hosmer-Lemeshow’s test was used to determine goodness of fit. Multi-collinearity was assessed by computing tolerance and the Variance Inflation Factor statistic.
Figure 2.
Covariates for multivariable logistic regression model: symptom. Abbreviation: HIV, human immunodeficiency virus.
Figure 3.
Covariates for multivariable logistic regression model: history of N. gonorrhoeae. Abbreviation: HIV, human immunodeficiency virus.
Figure 4.
Covariates for multivariable logistic regression model: high-risk sexual behavior. Abbreviation: HIV, human immunodeficiency virus.
Multivariable logistic regression was used to generate adjusted risk ratios to test the association between correlates (presence of symptoms, history of N. gonorrhoeae, and sexual behavior) and accurate presumptive N. gonorrhoeae treatment. Adjusted risk ratios (aRRs) are presented with 95% confidence intervals (CIs) and considers P < .05 as statistically significant. All analyses were performed using Stata v.14.2 (Stata Corp, College Station, Texas).
This study was deemed as non-humans subject research by the Boston University Institutional Review Board and therefore was considered as IRB exempt.
RESULTS
A total of N = 42 050 patient encounters resulted in N. gonorrhoeae testing. The vast majority of these encounters (n = 41 894; 99.6%) involved cis-gender men (Table 1). Twelve percent (n = 5051) received presumptive N. gonorrhoeae treatment. Among the 5051 patient encounters that led to presumptive treatment for N. gonorrhoeae, 46.1% (n = 2329) tested positive for N. gonorrhoeae infection and therefore received accurate presumptive treatment. Among the 53.9% (n = 2722) of patient encounters that resulted in inaccurate presumptive N. gonorrhoeae treatment, 14.8% (n = 404) received a positive Chlamydia trachomatis result.
Table 1.
Demographic and Risk Behavior Characteristics of Patients Seeking N. gonorrhoeae Testing at AIDS Healthcare Foundation Wellness Centers in California and Florida—2013–2017 (N = 42 050)
| Variable | n | % |
|---|---|---|
| Age group (Years) | ||
| 18–24 | 13 584 | 32.3 |
| 25–29 | 4780 | 11.4 |
| 30–34 | 6965 | 16.6 |
| 35–39 | 9817 | 23.4 |
| 40+ | 6904 | 16.4 |
| Gender | ||
| Male | 41 894 | 99.6 |
| Transgender male to female | 156 | 0.4 |
| Sexual orientation | ||
| Gay male | 35 242 | 83.8 |
| Bisexual | 6334 | 15.1 |
| Other | 474 | 1.1 |
| Race | ||
| White | 30 624 | 72.8 |
| Black | 6979 | 16.6 |
| Asian or Asian American | 2067 | 4.9 |
| Native American, Alaska Native, or American Indian | 119 | 0.3 |
| Native Hawaiian or Pacific Islander | 106 | 0.3 |
| Other | 2155 | 5.1 |
| Region | ||
| California | 15 288 | 36.4 |
| Florida | 26 762 | 63.6 |
| Presumptive treatment year | ||
| 2013 | 3041 | 7.2 |
| 2014 | 6879 | 16.4 |
| 2015 | 10 201 | 24.3 |
| 2016 | 10 750 | 25.6 |
| 2017 | 11 179 | 26.6 |
| HIV status | ||
| Negative | 32 809 | 78.0 |
| Positive | 4845 | 11.5 |
| Unknown | 4396 | 10.5 |
| Sexual behavior | ||
| No condomless anal sex in the past 12 months | 23 704 | 56.4 |
| Condomless anal sex in the past 12 months | 18 346 | 43.6 |
| History of prior NG infection | ||
| No | 37 039 | 88.1 |
| Yes | 5011 | 11.9 |
| Discharge | ||
| Not present | 35 313 | 84.0 |
| Present | 6737 | 16.0 |
| Urogenital Inflammation | ||
| Not present | 37 684 | 89.6 |
| Present | 4366 | 10.4 |
| Dysuria | ||
| Not present | 36 211 | 86.1 |
| Present | 5839 | 13.9 |
| Acute Pharyngitis | ||
| Not present | 36 421 | 86.6 |
| Present | 5629 | 13.4 |
Abbreviations: HIV, human immunodeficiency virus; NG, N. gonorrhoeae.
Among the symptom correlate models, only discharge and dysuria were significantly associated with accurate presumptive treatment. Patients presenting to AHF Wellness Centers with discharge were 4.5 times more likely to receive accurate presumptive treatment compared to patients not presenting with discharge (aRR: 4.51; 95% CI: 4.12–4.88), and patients presenting with dysuria were 2.5 times more likely to receive accurate presumptive treatment compared to patients presenting without dysuria (aRR: 2.52; 95% CI: 2.31–2.75). Conversely, patients presenting with acute pharyngitis were 1.3 times less likely to receive accurate presumptive treatment compared with patients presenting without acute pharyngitis (aRR: .67; 95% CI: .58–.76) (Table 2).
Table 2.
Symptoms Associated With Accurate Presumptive N. gonorrhoeae Treatment Among Patients Seeking N. gonorrhoeae Testing at AIDS Healthcare Foundation Wellness Centers in California and Florida—2013–2017
| Correlate | RR | (95% CI) | aRR | (95% CI) |
|---|---|---|---|---|
| Discharge (present vs not) | 4.91 | (4.54, 5.30) | 4.51a | (4.12, 4.88)a |
| Urogenital inflammation (present vs not) | 1.06 | (.94, 1.21) | 0.97a | (.85, 1.10)a |
| Dysuria (present vs not) | 2.71 | (2.49, 2.95) | 2.52a | (2.31, 2.75)a |
| Acute pharyngitis (present vs not) | 0.73 | (.64, .84) | 0.67a | (.58, .76)a |
Abbreviations: aRR, adjusted risk ratio; CI, confidence interval; RR, risk ratio.
aAdjusted for age, race, gender, region, high-risk sexual behavior, history of N.gonorrhoeae, and human immunodeficiency virus (HIV) status.
Additionally, individuals with a history of N. gonorrhoeae infection were 1.7 times more likely to receive accurate presumptive treatment compared to individuals without a prior history (aRR: 1.71; 95% CI: 1.55–1.88). Finally, individuals who had engaged in high-risk sexual behavior prior to their visit to AHF Wellness Centers were 1.2 times more likely to receive accurate presumptive treatment compared to individuals who did not report engaging in high-risk sexual behavior (aRR: 1.20; 95% CI: 1.11–1.30) (Table 3).
Table 3.
Clinical Correlates Associated With Accurate Presumptive N. gonorrhoeae Treatment Patients Seeking N. gonorrhoeae Testing at AIDS Healthcare Foundation Wellness Centers in California and Florida—2013–2017 (N = 42 050)
| Clinical Correlate | RR | (95% CI) | aRR | (95% CI) |
|---|---|---|---|---|
| History of Gonorrhea (yes vs. no) | 1.82 | (1.66, 2.02) | 1.71b | (1.55, 1.88)b |
| High-risk sexual behavior (yes vs. no) | 1.25 | (1.15, 1.35) | 1.20c | (1.11, 1.30)c |
Abbreviations: aRR, adjusted risk ratio; CI, confidence interval; RR, risk ratio.
bAdjusted for age, race, gender, region, high-risk sexual behavior and human immunodeficiency virus (HIV) status.
cAdjusted for age, race, gender, region, history of N. gonorrhoeae and HIV status.
There was no statistically significant difference in accurate presumptive treatment rates between cis-gender MSM and transgender women.
DISCUSSION
This study includes N. gonorrhoeae testing and treatment data from AHF Wellness Centers that provide standardized, free, and walk-in STI testing services in California and Florida. Nearly half (46.1%) of presumptively treated patients in this analysis were accurately treated for N. gonorrhoeae. In a similar study of patients in Los Angeles County, California, nearly one-third of patients presumptively treated for N. gonorrhoeae were accurately treated [20]. Based on the aRRs, patients with reported discharge or dysuria were more likely to be accurately presumptively treated for N. gonorrhoeae compared to presumptively treated patients who did not report these symptoms.
This study had several key limitations. The CDC recommends that individuals with a known exposure or contacts of persons with N. gonorrhoeae presenting for evaluation are presumptively treated. In this analysis the electronic medical records database did not include contact exposure from patients seeking testing. Second, patient symptom data were entered manually by clinical staff into the electronic medical records database using open-ended notes, which can lead to data entry errors. Third, symptoms may have been caused by other bacterial or viral agents not tested at AHF Wellness Centers, such as Mycoplasma genitalium. Furthermore, presumptive treatment cases were defined as cases that included N. gonorrhoeae testing and N. gonorrhoeae treatment during the same visit (prior to a diagnostic test result); it is possible that some patients received presumptive treatment and did not follow-through with laboratory testing due to unreported reasons.
Finally, given that this study is based on clinic data in metropolitan areas in California and Florida, there may limitations in generalizability to other parts of the United States, particularly rural areas and parts of the country where stigma towards gender identity and sexual orientation may prevent high-risk individuals from seeking STI clinic services. However, clinics that specifically cater its STI services toward MSM and transgender women may be able to adjust its presumptive treatment guidelines based on the findings of this large study.
Ultimately, the greatest hindrance in accurate treatment for N. gonorrhoeae and other STIs is the length of time from test to diagnosis. Although rapid point-of-care testing is the next evolution in STI testing technology, there is only one instrument currently approved by the Food and Drug Administration that can offer point-of-care N. gonorrhoeae urine test results in 30 minutes [21]. Alternatively, setting up in-house, certified laboratories to run STI specimens same-day using current STI testing technology may be too cost-prohibitive for STI clinics. Until STI clinics can provide rapid, point-of-care test results similar to HIV antibody testing, providers will continue to rely on patient-reported symptoms, exam findings, and clinical judgement regarding presumptive treatment.
Therefore, the results of this study suggest the need to improve presumptive N. gonorrhoeae treatment where same-day diagnoses are not available. Providers should continue to follow CDC guidelines and consider presumptive N. gonorrhoeae treatment based on specific symptoms. However, additional research is needed to better elucidate how presumptive treatment practices may affect antibiotic resistance, especially as the CDC suggests few antibiotic options remain for N. gonorrhoeae that are highly effective and well studied [1]. As the STI epidemic continues to rise in the United States, along with increased antibiotic resistance for N. gonorrhoeae, it is imperative to accurately test, diagnose, and treat patients at risk for N. gonorrhoeae and other STIs.
Glossary
Abbreviations
- AHF
AIDS Healthcare Foundation
- aRR
adjusted risk ratio
- CA
California
- CDC
The Centers for Disease Control and Prevention
- CI
confidence interval
- DAG
directional acyclic graph
- FL
Florida
- HIV
human immunodeficiency virus
- IRB
Institutional Review Board
- MSM
men who have sex with men
- NAAT
nucleic acid amplification test
- N. gonorrhoeae
Neisseria gonorrhoeae
- STI
sexually transmitted infection
Notes
Acknowledgments. The authors acknowledge Michael Hancock, Senior Database Developer at AIDS Healthcare Foundation, for extracting the data.
Potential conflicts of interest. The authors: No reported conflicts of interest. All authors have submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. Conflicts that the editors consider relevant to the content of the manuscript have been disclosed.
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