Abstract
Background
Standard-of-care nucleic acid amplification tests (routine NAAT) for Neisseria gonorrhoeae (GC) and Chlamydia trachomatis (CT) can take several days to result and therefore delay treatment. Rapid point-of-care GC/CT NAAT (rapid NAAT) could reduce the time to treatment and therefore onward transmission. This study evaluated the incremental cost per infectious day averted and overall cost of implementation associated with rapid compared to routine NAAT.
Methods
Prospective sexually transmitted infection (STI) treatment data from MSM and TGW in San Diego who received rapid NAAT between 11/2018 and 02/2021 were evaluated. Historical time from testing to treatment for routine NAAT were abstracted from the literature. Costs per test for rapid and routine NAAT were calculated using a micro-costing approach. The incremental cost per infectious day averted comparing rapid to routine NAAT and the costs of rapid GC/CT NAAT implementation in San Diego Public Health STI clinics were calculated.
Results
Overall, 2,333 individuals underwent rapid NAAT with a median time from sample collection to treatment of two days, compared to 7–14 days for routine NAAT equating to a reduction of 5–12 days. The cost of rapid and routine GC/CT NAAT was $57.86 and $18.38 per test respectively with a cost-effectiveness of between $2.43 and $5.82 per infectious day averted. The incremental cost of rapid NAAT improved when at least 2000 tests were performed annually.
Conclusions
While rapid GC/CT NAAT is more expensive than routine testing, the reduction of infectious days between testing and treatment may reduce transmission and provide improved STI treatment services to patients.
Keywords: Neisseria gonorrhoeae, Chlamydia trachomatis, rapid testing, cost-effectiveness
Short Summary
Rapid gonorrhea and chlamydia testing is associated with a reduced time to treatment and infectious days averted. The cost per infectious day averted is estimated at $2.43 to $5.82.
Introduction
Rates of bacterial sexually transmitted infections (STIs) in the United States (U.S.) among sexual and gender minorities such as cisgender men who have sex with men (MSM) and transgender women (TGW) have been steadily increasing since the mid-1990s (1–3). In addition, between 2015–2019 the rates of Neisseria gonorrhoeae (GC) and Chlamydia trachomatis (CT) diagnoses among all men, including cis-gender men who have sex with women, have gone up by 60.6% and 32.1%, respectively (4). The observed changes in rates of both GC and CT are likely to be multifactorial and may be partly attributable to increased screening among MSM at extra-genital sites, more frequent screening (e.g., for MSM who take HIV pre-exposure prophylaxis (PrEP)), and greater sensitivity of diagnostic tests, though increased transmission is likely to contribute (4).
The current standard for diagnosing GC/CT infection uses nucleic acid amplification testing (NAAT) which offers increased sensitivity compared to bacterial culture and can be performed more rapidly (5). Routine bacterial STI NAAT typically takes three to five days to result with reported sensitivity of over 90% and specificity of 98% (Routine NAAT) (3, 6–8). The time taken to receive results of GC/CT testing directly impacts the time between testing and treatment (9). The average time to treatment for GC or CT using routine NAAT modalities varies in the literature, ranging from seven to 30 days (10–12). Minimizing the time to treatment is important as approximately 50% of patients with positive GC/CT test results, even if symptomatic, continue to have sex in the interval between diagnosis and treatment (11, 13). While empiric treatment pending STI test results is an option, two inner-city emergency departments showed that this approach resulted in both over-treatment of more than 45% of participants without infection and undertreatment of participants with infection (14, 15). Any increase in time delay between testing and treatment is highly undesirable for several reasons including a risk for loss to follow-up, secondary STI transmission, complications of untreated infection, and increased risk of acquiring or transmitting other infections such as HIV (16, 17).
The polymerase chain reaction Cepheid GeneXpert (Sunnyvale, CA) test provides rapid diagnosis and differentiation between GC and CT resulting within 90 minutes, making same-day diagnosis and treatment possible (Rapid NAAT) (18). Studies evaluating cost-effectiveness of and implementation strategies for rapid NAAT testing in a US public health system are lacking (19). Rapid NAAT STI testing has been shown to be cost-effective when taking into consideration cost of sequelae of untreated infections, decrease in inappropriate treatment, and transmissions prevented in studies conducted in the United Kingdom that included persons regardless of sex assigned at birth, gender identity, and sexual orientation (9, 20–22). It remains unclear, however, if this strategy would be cost-effective if implemented in the U.S. among MSM and TGW.
We evaluated the impact on time to treatment of rapid NAAT compared to routine NAAT (10–12). We also evaluated the incremental cost per infectious day averted of rapid NAAT testing compared to routine NAAT and the total cost of implementing this new modality at scale at the public STI clinics of the County of San Diego Health and Human Services Agency (SD-HHSA).
Materials and Methods
Time to treatment
Time to treatment estimates for rapid NAAT were abstracted from data collected as part of the NIH-funded Primary Infection Resource Consortium (PIRC) study. Briefly, between November 2018 and February 2021, adult MSM and TGW in San Diego, California were screened with the “Total Test” for bacterial (GC, CT, and syphilis) and viral (HIV, Hepatitis B Virus, and Hepatitis C Virus) STIs in a community-based sexual health clinic. Study participants provided self-collected samples from three anatomical sites (urethral, oropharyngeal, and rectal), and underwent phlebotomy for syphilis testing.
Rapid NAAT for GC/CT was performed using Cepheid GeneXpert (Sunnyvale, CA). Participants who tested positive for GC/CT at any anatomic site were notified by text message or email within 90 minutes to 2 hours following STI testing with instructions to call and schedule an appointment immediately (ideally the same day) for treatment. Participants who did not respond within 24 hours were contacted by the study team to arrange treatment follow-up. Treatment was provided according to Centers for Disease Control and Prevention (CDC) guidelines at the primary research facility located two miles from the community-based sexual health clinic (1). A questionnaire was completed at the time of treatment to assess site-specific symptoms consistent with bacterial STIs. Individuals were classified as symptomatic for urethral GC/CT if they reported abnormal urethral discharge, bleeding, pain during intercourse, pain or burning with urination, or discharge from penis; and symptomatic for rectal GC/CT if they reported anorectal pain, discharge, or bleeding. Some with site-specific GC/CT infections reported vague and non-localizing symptoms that were not site-specific, so these data were not included in the final analysis. Individuals who received STI treatment at another facility or were lost to follow-up were excluded from the study analysis. Among those included in the treatment analysis, the median time from sample collection to treatment delivery was calculated.
As a comparator, estimates of historical time to treatment using routine NAAT among a broad population of cis-gender men and women, TGW, and MSM were abstracted from the literature (10–12).
Cost Analysis
Cost of Rapid GC/CT Testing
The total unit cost per test for rapid NAAT was calculated using an ingredients-based micro-costing approach (23). Cost data were classified as recurrent (i.e., personnel and non-personnel) and non-recurrent (capital). Equipment and lab test costs were obtained from the manufacturer and the remaining costs were collected from financial records. Capital costs consisted of price of the rapid GC/CT instrument. Recurrent non-personnel costs included costs of building space, supplies, utilities, and services such as maintenance and security. Recurrent personnel costs included lab technicians and housekeeping. To calculate the time used to perform rapid GC/CT testing, three sexual health clinic lab technicians were given time logs to document the time spent doing GC/CT testing duties over a period of nine days.
Cost of equipment was divided by the expected lifespan of the instrument provided by the supplier and divided by number of tests per year to calculate unit cost per test. We multiplied lab technician hourly wages by the average time in hours spent performing a GC/CT test. As the clinic was devoted to other activities in addition to rapid GC/CT testing, we attributed a fraction of the yearly cost for cleaning, rent, utilities, security, Wi-Fi, and phone to the rapid testing by multiplying these total costs by the proportion of clinic space occupied by the rapid GC/CT equipment, and then divided by the total GC/CT tests run per year to determine the per test cost.
Cost of Routine GC/CT NAAT Using the Aptima Combo-2 Assay at the County of San Diego HHSA
Unit costs per routine GC/CT NAAT were provided by HHSA for the fiscal year 2019 (at each of the four STI clinics) to provide cost data prior to patient testing restrictions associated with the global COVID-19 pandemic. Unit costs were obtained from HHSA and included recurrent personnel and non-personnel costs. Recurrent personnel costs included lab technicians and staff. Recurrent non-personnel included cost of equipment, supplies, and overhead.
We did not include the purchase price of the Aptima machine itself as it is used to perform a variety of tests and is not used solely for GC/CT NAAT. We assumed equivalent time spent for individual education and sample collection for rapid and routine NAAT.
Cost Effectiveness Analysis
We performed a cost effectiveness analysis (CEA) comparing rapid GC/CT NAAT to routine NAAT. Costs were identified in monetary terms and the effect in number of infectious days averted described in an incremental cost effectiveness ratio (ICER) expressed by the equation:
where C1 and E1 are the cost (2019 US dollars, $) and effect (time from sample collection to treatment) of rapid GC/CT NAAT, and C2 and E2 are the cost and effect of routine GC/CT NAAT.
Cost of Scale-up of Rapid NAAT across the County of San Diego HHSA STI Clinics
We estimated the cost of scale-up of rapid NAAT across the county of San Diego HHSA STI Clinics. Scale-up costs of rapid GC/CT NAAT at HHSA STI clinics included the costs of GeneXpert equipment purchase for each of the four clinics. The size and therefore the cost of rapid testing equipment (C. Meyrath, personal communication [Cepheid]) used at each of the four STI clinics was selected based on the average number of tests per day performed at each site. The annual recurrent costs after implementation of the rapid testing program were based on our estimate of cost of rapid testing supplies as well as costs provided by HHSA including cost for personnel required to perform testing at each clinic, maintenance, and overhead. We replaced supply costs for routine testing with supply costs specific for rapid NAAT to calculate a total unit cost per test.
Results
Between 26th November 2018 and 28th February 2021, a total of 2,333 individuals received 3,761 rapid NAAT results for GC or CT reported as positive, negative, or invalid with 49 results missing or unknown (Figure 1). Most participants were white, non-Hispanic (43.2%) and assigned male sex at birth (98.2%) (Table 1). A total of 158 individuals were excluded from the analysis; 119 were referred to an outside facility for STI treatment, and 39 (1.7%) were lost to follow-up, or had unknown treatment status.
Figure 1.
Study Design. Total Test (TT) visits were from 11/26/2018–02/28/2021 and were included in the analysis. 15.8% of those with STI results had at least one positive test. Time to treatment data only included participants who were treated at the study site. Participants who were exclusively referred out were excluded from time to treatment calculations.
Figure 1 abbreviations: TT – total test, STI – sexually transmitted infection, PrEP – HIV pre-exposure prophylaxis, LTFU – lost to follow-up
Table 1.
Demographics of Participants undergoing rapid NAAT for Neisseria gonorrhoeae and Chlamydia trachomatis
| Sex at birth | N (%) |
|---|---|
| Male | 2291 (98.2%) |
| Female | 41 (1.8%) |
| Unknown | 1 (0.04%) |
| Race/ethnicity | N (%) |
| White, non-Hispanic | 1009 (43.3%) |
| Black, non-Hispanic | 150 (6.4%) |
| Hispanic | 813 (34.9%) |
| Asian/PI (non-Hispanic) | 245 (10.5%) |
| Native American/Alaskan Native (non-Hispanic) | 4 (0.2%) |
| Other (includes multi-racial) | 93 (4.0%) |
| Unknown | 19 (0.8%) |
| Risk Factors Among those treated on-site | N (%) |
| Condomless, penetrative anal intercourse | 364 (85.4%) |
| Condomless, receptive anal intercourse | 248 (58.2%) |
Of the individuals with GC/CT results included in the analysis, there were 205 positive tests for GC from 152 individuals (6.6% of all tests) and 256 positive tests for CT from 225 individuals (9.8% of all tests). A breakdown of testing site outcomes is shown in Table 2. Among individuals with a positive GC/CT result, 85.4% reported condomless penetrative anal intercourse in the past three months, 25.1% were taking HIV PrEP, and the median number of sexual partners in the past three months was 4 (range 0–58).
Table 2.
GC/CT NAAT results by anatomical site
| (+) for STI | Symptomatic | Asymptomatic | Symptoms Unknown | |
|---|---|---|---|---|
| Rectal GC | 84 (41.0%) | -- | -- | -- |
| Pharyngeal GC | 96 (46.8%) | -- | -- | -- |
| Urethral GC | 25 (12.2%) | -- | -- | -- |
| Any GC * | 152 | 122 (80.3%) | 0 (0%) | 30 (19.7%) |
| Rectal CT | 159 (62.1%) | -- | -- | -- |
| Pharyngeal CT | 30 (11.7%) | -- | -- | -- |
| Urethral CT | 67 (26.2%) | -- | -- | -- |
| Any CT * | 225 | 176 (78.2%) | 0 (0%) | 49 (21.8%) |
Represents any positive result among entire tested population at any anatomical site.
The median time from specimen collection to STI treatment for rapid GC/CT NAAT was two days (range 0–16 days), and the time to treatment for routine GC/CT NAAT using conservative estimates from literature review was 7–14 days (10–12). Use of rapid NAAT therefore resulted in a reduction in post-testing transmission risk duration of approximately 5–12 days compared to routine NAAT strategies.
Rapid and Routine GC/CT NAAT Unit Cost per Test
The total unit cost of rapid GC/CT NAAT was $57.86 compared to $18.38 (Table 3) for routine GC/CT NAAT. For rapid NAAT, recurrent non-personnel costs represented the most substantial component with individual cartridges costing $38.00 per test. Purchase of the rapid NAAT (GeneXpert) instrument represented the largest start-up cost to a rapid GC/CT testing program and contributes to the high unit cost per test. At the sexual health study clinic, the 16-cartridge GeneXpert instrument had a cost of $174,000 with an average lifespan of 10 years. Recurrent non-personnel costs were the biggest contributor to cost of routine GC/CT NAAT as well, but the total unit cost per test was cheaper compared to rapid GC/CT NAAT.
Table 3.
Cost per test per year for rapid and routine GC/CT NAAT
| Rapid GC/CT NAAT | |
|---|---|
| Fixed Cost (Capitol) | $6.68 |
| Recurrent Costs (Personnel) | $3.54 |
| Recurrent Costs (non-personnel) | $47.64 |
| Total Unit Cost per Test | $57.86 |
| Routine GC/CT NAAT | |
| Labor and supply costs per test | $17.71 |
| Services costs per test | $ 0.67 |
| Total Unit Cost per Test | $ 18.38 |
Cost Effectiveness Analysis: Incremental Cost per Infectious Days Averted
The median number of infectious days was reduced by 5–12 days using rapid GC/CT NAAT compared to routine NAAT, though it was costlier. The ICER for rapid GC/CT NAAT ranged from $5.12 to $12.30 per infectious day averted when 1,000 tests were run per year. Rapid NAAT became more cost-effective by increasing the number of tests run per year with the ICER ranging from $2.43 to $5.82 per infectious day averted when running 10,000 tests per year (Figure 2). Based on 10 minutes required to prepare, load, and unload a specimen and 90 minutes for a test to run, the total capacity of a 16-chamber instrument during a five-day work week is 384 tests or over 19,000 tests per year.
Figure 2.
Incremental Cost per Infectious Days Averted
Replacing Routine NAAT with Rapid GC/CT NAAT at the County of San Diego HHSA
Implementing and scaling up rapid GC/CT testing in the HHSA of San Diego County would eliminate the need for specimens to be sent to the central public health lab by allowing each clinic to perform tests on-site. The personnel needed to perform rapid GC/CT NAAT at each testing site is already available, so hiring new testers is not required. Of the four STI clinics in HHSA, the Rosecrans clinic performed the greatest mean daily tests (N=29) and would require the largest rapid GC/CT testing equipment. The other STI clinics averaged between one and four tests per day and would need the smallest rapid testing machine to function (See supplementary data). Purchasing rapid GC/CT NAAT for all four county STI clinics in San Diego would cost $307,600 with annual recurrent costs estimated to be $621,204 across all sites (Table 4).
Table 4.
Cost of implementing and maintaining rapid GC/CT NAAT at public health service centers
| Public Health STI Clinic | Cost of Rapid GC/CT Testing Equipment | Annual Recurrent Cost |
|---|---|---|
| Central Region PH Center | $44,400 | $73,841.28 |
| North Coastal PH Center | $44,400 | $50,687.98 |
| Rosecrans STD | $174,400 | $476,468.03 |
| South Region PH Center | $44,400 | $20,206.34 |
| Combined Centers | $307,600 | $621,203.63 |
Discussion
Our study demonstrated that implementing a rapid NAAT testing strategy can reduce the time lag between testing and treatment for GC and CT STIs by up to 12 days compared to routine NAAT standard of care. If testing volumes were increased to 10,000 tests per year in San Diego County, we estimated the cost per infectious day averted could be in the range from $2.40 to $5.80. To implement this strategy across 4 public health testing sites in San Diego would cost approximately $307,600 in initial outlay with $621,204 in recurrent costs each year.
Previous work has estimated that direct medical costs of treatment for CT and GC are around $151 and $85 respectively (2016 dollars) in addition to productivity loss from individuals presenting for testing and/or treatment (24). When combined with our results indicating that individuals were at ongoing high risk for STI transmission and previous data suggesting most persons continue to have sex between testing and treatment, it is likely that the costs of each infectious day averted might be partially or completely offset by infections averted (11, 13). These potential cost benefits of rapid NAAT testing are in addition to providing a faster and more convenient STI health service.
Sexual health clinics such as the Dean Street Express clinic in the United Kingdom have reported similar findings regarding decreased time to treatment with rapid GC/CT NAAT from over a week to just a few hours (20). They also demonstrated a substantial decrease in partner attendance and decreases in GC and/or CT transmissions (20). In a similar fashion, the New York City public health department reduced the time to treatment from eight days to two days after replacing routine NAAT with rapid GC/CT NAAT (GeneXpert) (10).
As with many new technologies, our study shows that rapid GC/CT NAAT is more costly than routine NAAT but reduces infectious days. As the volume of tests increased, the cost per infectious day averted decreased. In the current healthcare model, many healthcare systems with multiple clinics send GC/CT lab specimens to a central lab and can run tests in batches. Rapid GC/CT NAAT supports immediate on-site testing. The issue then becomes whether a clinic runs enough tests to justify the cost as even the smallest GeneXpert instrument requires a substantial investment. A pilot study for rapid GC/CT testing and same day treatment among MSM found that most participants felt positive about receiving test results quickly, which may lead to more diagnostic testing and treatment thus potentially justifying the investment even in smaller clinics (25).
Other than cost alone, clinics should consider other factors when deciding whether to implement this testing modality. The convenience of offering self-collected three-site GC/CT NAAT, combined with the ability to receive same-day results, likely would be preferred by patients and potentially increase access to care allowing greater treatment of GC/CT. A clinic in Los Angeles, CA offered rapid GC/CT NAAT and immediate treatment to patients and found an increase in same-day treatment for positive test results from 3.6% to 21.1% (26). Rapid NAAT has the potential to increase provision of GC/CT treatment and provide the immediate infrastructure for additional prevention services to interrupt transmission of GC/CT that could also impact transmission and acquisition of HIV.
One of the main limitations of our analysis was a lack of data to inform more robust modeling of downstream transmission pathways. This limitation prevented us from formally evaluating cost-effectiveness against thresholds which use quality-adjusted life years (QALYs) or disability adjusted life years (DALYs) as metrics (27). More sophisticated analyses informed by data on transmission risk prior to and after diagnosis could inform more detailed modeling on the number of infections averted and formal economic evaluation.
This study supports the implementation of rapid GC/CT NAAT in clinics serving a large proportion of MSM and TGW patients. This testing modality is more expensive than routine GC/CT NAAT; however, the benefit of increased infectious days averted and probable reduction in onward transmission combined with likely improved healthcare service quality for patients argue a strong case for implementation.
Supplementary Material
Acknowledgements
The Study authors would like to acknowledge the input from San Diego HHSA in provision of costing data for this study.
Sources of Support:
This work was supported by the National Institutes of Health (NIH) awards AI106039, MH100974, 5T32AI007384 and Gilead contract IN-US-292-4217, and the James Pendleton Charitable Trust.
Footnotes
Conflict of Interest Statement: SJL has received funding from Gilead Sciences paid to her institution and donation of medications from Gilead Sciences. EW, TM, NM, WT have no conflicts of interest to disclose.
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