Gonorrhea testing,morbidity,and reporting using an integrated sexually transmitted disease registry in Indiana: 2004

Abstract

Surveillance of gonorrhea (GC), the second most common notifiable disease in the United States, depends on case reports. Population-level data that contain the number of individuals tested in addition to morbidity are lacking. We performed a cross-sectional analysis of data obtained from individuals tested for GC recorded in a sexually transmitted disease (STD) registry in the state of Indiana. Descriptive statistics were performed, and a Poisson generalized linear model was used to evaluate the number of individuals tested for GC and the positivity rate. GC cases from a subset of the registry were compared to CDC counts to determine the completeness of the registry. A total of 1,870,811 GC tests were linked to 627,870 unique individuals. Individuals tested for GC increased from 54,334 in 2004 to 269,701 in 2016; likewise, GC cases increased from 2,039 to 5,997. However, positivity rate decreased from 3.75% in 2004 to 2.22% in 2016. The difference in the number of GC cases captured by the registry and those reported to the CDC was not statistically significant (P = 0.0665). Population-level data from an STD registry combining electronic medical records and public health case data may inform STD control efforts. In Indiana, increased testing rates appeared to correlate with increased GC morbidity.

Keywords

Gonorrhea screening epidemiology diagnosis,electronic health records,population healths

Introduction

Gonorrhea (GC) is the second most common notifiable disease in the United States (U.S.) with 583,405 cases reported to the U.S. Centers for Disease Control and Prevention (CDC) in 2018 at a rate of 179.1 cases per 100,000 population.¹ GC infection can result in pelvic inflammatory disease, infertility, chronic pelvic pain, disseminated infection, and ectopic pregnancy.² The economic and health burden of this disease is substantial, making the need for accurate ascertainment of GC morbidity imperative.²,³ However, reports underestimate the actual number of GC infections for reasons that include dependence on physicians and laboratory systems of reporting.^4–6 The CDC estimates that only half of GC infections are diagnosed, resulting in cases going undetected as well as incomplete case reporting.¹ Currently, GC disease burden in the U.S. is tracked by monitoring the number of cases reported to public health agencies, commonly referred to as morbidity. Screening rates, testing of multiple anatomic sites, completeness of reporting, and test characteristics influence case detection as well as the number of cases.

The numbers of GC infections appear to be increasing over time.¹ The CDC surveillance report has also noted that the rates of GC have increased over time among men who have sex with men (MSM) and heterosexual males and females in sexually transmitted disease (STD) clinics.¹ However, these STD clinics might not represent STD positivity rates at a population-level. Nationally, the proportion of GC cases that were identified in STD clinics was about 10% for males and about 6% for females.¹ However, in a recent study in central Indiana, the STD program diagnosed 50% of GC cases among 13- to 44-years-old males.⁷ A second study, conducted by CDC, found that emergency departments, GC diagnoses increased by 39% from 2008 to 2013.⁸ In addition, the number of GC infections reported by laboratories and physicians is likely an underestimation of the true burden of the disease.⁹ These observations emphasize the importance of looking at GC cases at a population level.

Gonorrhea occurs at a high rate in Indianapolis, Indiana. Compared to other U.S. Metropolitan Statistical Areas (MSAs), Indianapolis is ranked 7th in the nation with 241.6 cases per 100,000 population in 2018.¹ From 2014 to 2018, the number of reported GC cases increased by 30% and the rate by 27%.¹ Beginning in 2017, high levels of azithromycin resistance, N. gonorrhoeae isolates with a minimum inhibitory concentration (MIC) ≥256 µg/mL, were noted in Indianapolis.¹⁰ These factors necessitated enhanced resistance surveillance and a better understanding of the true burden of the disease in order to develop interventions to mitigate the potential spread of antibiotic-resistant gonorrhea.

The specific aim of this study is to investigate the trends in GC, examining both testing and morbidity, from 2004 to 2016 in the state of Indiana focusing on those at highest risk, individuals 13 to 44 years of age, at a population level using an integrated statewide STD registry. This study further aims to compare the number of GC cases from the Indianapolis metropolitan region in the STD registry to that reported to the CDC for the same geographic location in order to determine whether the registry captures a similar number of cases to the current official reporting system.

Materials and methods

We performed a retrospective cross-sectional analysis of data obtained from individuals tested for GC in Indiana using a de-identified statewide integrated STD registry described previously.⁷,^11–13 The STD registry integrates clinical, laboratory, and demographic data on individuals tested for GC, chlamydia (CT) or syphilis between January 1, 2004, and December 31, 2016, from the Indiana Network for Patient Care (INPC) and the Marion County Public Health Department (MCPHD) STD clinic. The MCPHD STD clinic provides medical services through a variety of affiliated outreach programs, such as jail screening, bars, bathhouses, street outreach, secondary schools, higher education institutions, and a sex worker project. This clinic and affiliated programs are referred to as the “STD Program”. The INPC is a statewide health information exchange network of electronic medical records that includes almost all major hospitals, laboratories, and many outpatient clinics in Indiana.¹²,¹³ Although data from other Indiana public STD programs were not available for inclusion in the statewide STD registry, the MCPHD STD Program captures data across a large geographic area known as District 5, which represents the largest proportion of Indiana morbidity.¹⁴

Since over 90% of GC cases occur in individuals under the age of 45 years, we focused our study on individuals aged 13 to 44 years who tested for GC.¹ For the purposes of describing the population tested, age was defined as the age of the individual at the first time they were tested for GC during the study period. Hispanic origin was recorded as race in the INPC, and as ethnicity in the MCPHD data, with race usually designated as “Other” as described previously.⁷ According to the U.S. Census, only 3.9% of Indianapolis residents are not White, Black, or Hispanic.¹⁵ Therefore “Other” race in the MCPHD data includes those who are Hispanic, American Indian, Alaska Native, Asian, Multiracial, Native Hawaiian, and Other Pacific Islander, but is comprised predominantly of Hispanic individuals. Thus, in this study, Hispanic and Other were combined as “Other”, missing and unknown race were combined as “Unknown”.

Testing data were restricted to include only positive and negative test results; we excluded indeterminate results (0.63%). Using CDC criteria, we classified an individual as positive for GC if they had at least one positive pharyngeal, rectal, or urethral infection within a 30-day period. Individuals with multiple positive tests within a 30-day period were counted as a single GC case. However, it is possible for an individual to be counted multiple times as a GC case in a year, if subsequent infections occur red outside previous infections’ 30-day window. Similarly, individuals whose tests were all negative were counted once as a negative case within a 30-day period, regardless of the anatomic site tested or the number of tests performed. The positivity rate was defined as the number of non-unique individuals positive for GC divided by the number of non-unique individuals with positive or negative tests in a year. Whereas the number of individuals from the STD Program included in the STD registry was relatively constant over time, the INPC, which contains health care systems across the state, increased substantially because health care systems joined the INPC at various points during the study period. Therefore, to compare the number of GC cases in the STD Registry to those reported to CDC, we used a subset comprised of records from the STD Program where providers had participated most consistently in the INPC during the study period using zip codes, prior to de-identification, to identify the geographic region. The geographic area served by the STD Program includes Marion County in which Indianapolis is located and all contiguous counties, specifically Hamilton, Boone, Hendricks, Hancock, Morgan, Johnson, and Shelby.¹⁴ A comparison of CDC data to this subset was performed to examine whether the registry captured a similar number of cases to the current reporting system.

Statistical method

Descriptive statistics were performed to determine the characteristics of the study population. Comparisons of continuous variables (age) were performed using ANOVA for continuous variables and Pearson $χ^{2}$ test for categorical variables (gender, race, individuals tested for GC, individuals positive for GC). A Poisson generalized linear model with log link function was used to evaluate the rate of individuals tested for GC, i.e., the number of individuals tested for GC per total INPC population, over time. Similarly, the positivity rate, that is, the number of individuals with a positive GC test, over time was also evaluated using a Poisson generalized linear model with log link function, adjusting for the number of individuals tested for GC. The distinct patient effect over time was accounted for in the model. Results were stratified by gender and race. The number of GC cases (morbidity) reported by the STD Program and those in the registry were compared using a general linear model.

The statistical software SAS, version 9.4, (SAS Institute Cary, NC) was used for all analyses, and an alpha of 0.05 was used for the level of significance. The study received approval by the Institutional Review Board at Indiana University (Study No. 1311659626).

Results

Study population

We identified a total of 627,870 unique individuals with a total of 1,870,811 GC tests during the study period in the registry. 77.8% were females, 22.2% males and less than 1% were of unknown gender. With respect to race, 45.5% were White, 20.3% were Black, 12.5% were Other, and 21.6% were of Unknown or missing race (Table 1). The mean age of individuals tested for GC was 26 years old, which remained constant over time (not shown). The annual number of unique individuals in the INPC (ages 13 to 44 years) when compared to the number of unique individuals tested for GC in the STD registry increased.

Table 1.

Demographics of individuals tested for gonorrhea in Indiana using a statewide STD Registry, 2004–2016 (N = 627,870).

Gender*	White	Black	Other	Unknown	Total
Female	232,421 (47.6%)	82,609 (16.9%)	63,408 (13.0%)	109,675 (22.5%)	488,113
Male	53,239 (38.2%)	44,680 (32.1%)	15,299 (11.0%)	26,140 (18.8%)	139,358
Total	285,660	127,289	78,707	135,815	627,471

Source: Indiana Network for Patient Care, Marion County Public Health Department STD Program.

*Gender was not available on 399 individuals. Gender identity was not captured reliably in the registry.

Table 2.

Annual number of individuals tested, positive for GC, and positivity rates for Indiana using an integrated STD registry, 2004–2016, stratified by gender and race.

	2004	2005	2006	2007	2008	2009	2010	2011	2012	2013	2014	2015	2016	Total
Gender*
Total** Females	50,165	57,287	59,570	66,238	88,661	113,333	129,629	155,207	137,562	145,159	156,374	206,845	226,184	1,592,214
Positive GC Females	1,366	2,317	3,645	2,610	3,327	2,582	1,898	1,875	1,774	1,981	1,894	2,581	3,028	30,878
Positivity Rate^§ Females	2.72%	4.04%	6.12%	3.94%	3.75%	2.28%	1.46%	1.21%	1.29%	1.36%	1.21%	1.25%	1.34%	1.94%
Total Males	4,160	10,294	13,384	12,975	14,623	18,132	21,521	25,232	23,977	26,444	28,051	35,885	43,467	278,145
Positive GC Males	673	1,616	2,102	1,813	1,703	1,663	1,470	1,501	1,483	1,726	1,948	2,349	2,969	23,016
Positivity Rate Males	16.18%	15.70%	15.71%	13.97%	11.65%	9.17%	6.83%	5.95%	6.19%	6.53%	6.94%	6.55%	6.83%	8.27%
Race
Total White	19,180	22,827	24,835	29,173	39,633	51,386	61,850	75,224	79,184	80,288	92,272	120,004	110,343	806,199
Positive GC White	435	819	1,518	998	1,160	871	688	764	885	1,115	1,157	1,733	1,860	14,003
Positivity Rate White	2.27%	3.59%	6.11%	3.42%	2.93%	1.70%	1.11%	1.02%	1.12%	1.39%	1.25%	1.44%	1.69%	1.74%
Total Black	26,907	33,965	36,477	37,281	45,551	52,061	56,812	60,946	58,713	57,893	59,125	67,181	65,648	658,560
Positive GC Black	1,442	2,836	3,664	3,171	3,442	3,006	2,384	2,220	2,172	2,212	2,338	2,483	2,599	33,969
Positivity Rate Black	5.36%	8.35%	10.04%	8.51%	7.56%	5.77%	4.20%	3.64%	3.70%	3.82%	3.95%	3.70%	3.96%	5.16%
Total Other	5,225	6,970	7,457	8,452	11,234	12,712	12,862	14,103	14,907	25,136	26,432	35,652	26,379	207,521
Positive GC Other	86	118	208	140	203	145	90	94	117	253	259	371	330	2,414
Positivity Rate Other	1.65%	1.69%	2.79%	1.66%	1.81%	1.14%	0.70%	0.67%	0.78%	1.01%	0.98%	1.04%	1.25%	1.16%
Total Unknown	3,022	3,841	4,207	4,330	6,897	15,425	19,673	30,249	8,742	8,296	6,606	19,912	67,331	198,531
Positive GC Unknown	76	162	359	116	225	223	206	298	83	127	89	343	1,208	3,515
Positivity Rate Unknown	2.51%	4.22%	8.53%	2.68%	3.26%	1.45%	1.05%	0.99%	0.95%	1.53%	1.35%	1.72%	1.79%	1.77%
Total Individuals Tested	54,334	67,603	72,976	79,236	103,315	131,584	151,197	180,522	161,546	171,613	184,435	242,749	269,701	1,870,811
Total Individuals Positive	2,039	3,935	5,749	4,425	5,030	4,245	3,368	3,376	3,257	3,707	3,843	4,930	5,997	53,901
Overall Positivity Rate	3.75%	5.82%	7.88%	5.58%	4.87%	3.23%	2.23%	1.87%	2.02%	2.16%	2.08%	2.03%	2.22%	2.88%
Total Unique Population
Individuals in the Statewide STD^§§ Registry	31,970	41,071	45,730	48,034	57,739	77,101	92,269	113,960	94,495	104,538	117,449	156,719	175,959	627,870
Individuals in the INPC^§§§ (aged 13-44)	384,397	806,879	826,764	1,118,301	1,402,301	1,443,073	1,485,711	1,585,514	1,664,974	1,599,999	1,150,777	1,319,795	1,339,671	5,269,149
Percent STD Tested	8.3%	5.1%	5.5%	4.3%	4.1%	5.3%	6.2%	7.2%	5.7%	6.5%	10.2%	11.9%	13.1%	11.9%

Source: Indiana Network for Patient Care, Marion County Public Health Department STD Program.

*Gender was not available on 452 individuals. Gender identity was not captured reliably in the Registry.

Individuals with multiple tests in 30 days were counted once.

STD = Sexually Transmitted Diseases.

§§

INPC = Indiana Network of Patient Care.

Individuals tested for gonorrhea, morbidity and positivity rates

Figures 1 and 2 depict individuals tested for GC, GC cases, and positivity rates over time stratified by gender and race, respectively. The number of individuals (non-unique) tested for GC increased from 54,334 in 2004 to 269,701 in 2016 as shown in Table 2. The number of unique individuals in the INPC (aged 13 to 44 years) increased from 384,397 in 2004 to 1,339,671 in 2016. To account for the INPC increase, we divided the number of individuals tested in the registry by the number of individuals available to test in the INPC. The percent tested rose from 8.3% in 2004 to 13.1% in 2016. More females and White individuals were tested compared to males and Black individuals throughout the study period.

Figure 1.

Annual gonorrhea testing data, morbidity, and positivity rate for Indiana by gender, 2004–2016 (N = 1,870,811 tests). Source: Indiana Network for Patient Care, Marion County Public Health Department STD Program.

Figure 2.

Annual gonorrhea testing data, morbidity, and positivity rate for Indiana by race, 2004–2016 (N = 1,870,811 tests). Source: Indiana Network for Patient Care, Marion County Public Health Department STD Program.

Both the number of GC cases and the amount of GC testing in the registry increased over the study period. There were 53,901 individuals positive for GC (GC cases) in the STD registry from 2004 to 2016. While the number of GC cases fluctuated from 2004 through 2009, it increased significantly from 2010 to 2016 (r = 0.8739, P = 0.0101). In contrast, the positivity rate decreased from 2004 through 2009 and 2010 through 2016 (r = −0.759, P = 0.0026). Positivity rates of GC were highest in the years 2005, 2006, and 2007. The number of male GC cases increased significantly over time (r = 0.6410, P = 0.0182) whereas the number of female GC cases did not (r = −0.0453, P = 0.8831). In contrast, the positivity rate decreased significantly for both males (r = −0.8943, P= <0.0001) and females (r = −0.7618, P = 0.0025). The positivity rate was higher in males than in females (Table 2). Racially, Black individuals had the highest number of GC cases compared to any other races (Table 2). The number of GC cases in White individuals decreased significantly over time (r = 0.5863, P = 0.0352) whereas the number of GC cases in Black individuals did not (r = −0.2254, P = 0.4591). GC positivity rate decreased significantly for Whites (r = −0.6458, P = 0.0173), Blacks (r = −0.7569, P = 0.0027), and Other races (r = −0.6291, P = 0.0212). However, the highest rate of GC positivity was observed among Black individuals (Table 2).

To determine whether the morbidity, that is, the number of GC cases, found in the STD registry was comparable to CDC reported morbidity, we compared a subset of the registry that had consistently participated in the INPC throughout the study period and for which public health data were available, specifically the district, which includes Indianapolis (District 5) (Figure 3). The difference between the number of GC cases from District 5 in the registry and the number of cases reported to the CDC over time was not statistically significant (P = 0.0665).

Figure 3.

Total number of Indiana's District 5 gonorrhea cases documented in a STD registry compared to official gonorrhea cases reported to the CDC, 2004–2016. Source: Indiana Network for Patient Care, Marion County Public Health Department STD Program, CDC.

Discussion

This study examined GC testing and morbidity at a population level using an integrated STD registry. We found that although GC cases increased, the positivity rate decreased. This is important because it demonstrates that understanding the disease burden depends on factors other than just the number of cases. Additionally, the increasingly higher positivity rates observed among males and Black individuals compared to females and White individuals informs the need for targeted screening and redirection of resources to address health disparities.

Although public health departments typically receive only reports of GC cases, the de-identified STD registry enabled examination of the number of individuals tested for GC as well as morbidity for the population in Indiana. Even though morbidity increased over time, a trend observed nationally¹, positivity decreased as more individuals were tested. The registry was able to capture morbidity and it compared favorably to CDC reports. Additional study comparing CDC reports with the STD registry might reveal ways to improve case capturing. One possibility would include individually examining the cases missed by either system.

Our study was not designed to investigate the causes of the observed increase in testing over time. We speculate that it may be due to compliance with the healthcare effectiveness data and information set (HEDIS) measure for CT testing since in our data, virtually all GC tests were associated with CT tests.¹⁶ In addition, Indiana, like many Midwest US regions, experienced increased opioid use late in the study period. Perhaps the increase in 2015 and 2016 was influenced by provider awareness of the outbreak.¹⁷ Furthermore, during this period, STD programs promoted increased testing in all settings in association with a syphilis outbreak in Indianapolis in 2008.¹⁸ The increase in testing does not appear to be the result of population increases in Indiana since, during this same period, the estimated population of the state and Indianapolis MSA increased only by 7% and 6%, respectively.¹⁵ It is also important to note that because we examined individuals tested rather than the number of tests performed, the increase would not reflect an increase in testing additional anatomic sites unless partner notification increased as a result of higher morbidity. Our analysis accounted for the increase in the number of unique individuals included in the INPC over time. Therefore, it appears that GC morbidity increased, at least in part, as a result of increased testing of individuals for GC. The reason individuals were tested was not included in the data available for the study but may reflect increased screening of those who were symptomatic for other STDs. The significance of the increase in testing warrants further study.

As expected, women were tested more frequently than men. This is likely due to routine screening. Assays for CT also contain GC, which are both part of primary care screening and the HEDIS measure, which calls for CT screening in women 16–24 years of age.¹⁶,¹⁹ It is worth noting that almost all individuals in the STD registry who at the time tested for CT also received a GC test (data not shown).

The increase in individuals tested by race is more challenging to interpret. It appears that the number of White individuals tested increased 10-fold (19,180 in 2004 to 110,143 in 2016) while that of Black individuals doubled (26,907 in 2004 to 65,648 in 2016). We were not able to examine the race of individuals in the INPC over time in the available data, but it is possible that differences in the racial components of the population changed during the study period. As stated previously, we do not attribute this increase to population growth. Nevertheless, positivity rates did decrease in most races until 2012. Although disparities still exist with the positivity rate, among Black individuals, the rate doubled compared to any other races.

There are several limitations to this study. The first limitation is missing data or differently coded data on demographics such as race, ethnicity, and gender in the dataset. In addition, data in the INPC were merged from different sources; thus, unique variable coding might have been used, affecting the completeness of the data used in the analysis. For example, we found that 5 out of the 68 institutions in the registry accounted for 73% of individuals with unknown or missing race. Data did not include the reason an individual was tested. This limited our ability to interpret the observation of increased testing. Lastly, the study was designed to look at testing and morbidity of individuals in the STD Registry, but an interpretation of increases in the number of individuals tested requires data from the entire unique INPC population that were only partially available.

To conclude, this study demonstrates a decrease in GC positivity rate despite the observed increase in the number of GC cases in our study population, suggesting the importance of tracking negative as well as positive tests in STD control and prevention. This was particularly evident when comparing the positivity rates by gender and race, which revealed the need to increase testing among certain high-risk demographics and redirect public health resources, as necessary. As public health workers face the prospect of resistant GC and cases appear to be increasing nationwide, an optimized healthcare system could aid in obtaining the most accurate ascertainment of GC cases and positivity rates. An integrated STD registry like the one used in this study could be used to develop better STD information systems and targeted interventions to reduce STD burden. Combining electronic health record data with STD program data may offer additional information regarding GC disease burden to inform public health interventions. At the very least, the availability of denominator data, which includes both positive and negative GC test results, may provide a more accurate assessment of GC incidence and control.

Footnotes

Acknowledgements

The authors wish to thank the following individuals for their valuable contributions to this manuscript: Ashley Wiensch, MPH, and Andrea Broyles, MPH, of the Regenstrief Institute for their help in developing and accessing the STD registry; and Yenling Ho, MPH, Nate Apathy, PhD, and Kevin Wiley, BS, of the IU Fairbanks School of Public Health for their assistance in analyzing the data and feedback on preliminary results.

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 work was supported by a contract from the U.S. Centers for Disease Control and Prevention [Contract number: 00HCVJDD-2019-32017] and a grant from the U.S. National Library of Medicine [Grant number: T15LM012502]. The views expressed in this publication are those of the authors and do not necessarily reflect the position or policy of the Centers for Disease Control and Prevention, National Library of Medicine, or the United States government.

ORCID iDs

Opeyemi C Ojo

Guoyu Tao

Brian E Dixon

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Gonorrhea testing,morbidity,and reporting using an integrated sexually transmitted disease registry in Indiana: 2004–2016

Abstract

Keywords

Introduction

Materials and methods

Statistical method

Results

Study population

Individuals tested for gonorrhea, morbidity and positivity rates

Discussion

Footnotes

Acknowledgements

Declaration of conflicting interests

Funding

ORCID iDs

References