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Third-Trimester Prenatal Syphilis Screening

A Cost-Effectiveness Analysis

Albright, Catherine M. MD; Emerson, Jenna B. MD; Werner, Erika F. MD; Hughes, Brenna L. MD

doi: 10.1097/AOG.0000000000000997
Original Research
Free

OBJECTIVE: To estimate the cost to prevent one case of congenital syphilis or fetal or neonatal death with universal third-trimester syphilis rescreening in the United States and to estimate the incidence of syphilis seroconversion at which rescreening becomes cost-effective.

METHODS: We created a decision model comparing universal third-trimester syphilis rescreening in women who screened negative in the first trimester with no rescreening. The assumed base case incidence of seroconversion was 0.012%. The primary outcome was the cost to prevent one case of congenital syphilis. Secondary outcomes included the cost to prevent one fetal or neonatal death and the number needed to rescreen to prevent one adverse outcome. A strategy was considered cost-effective if it cost less than $285,000 to prevent one case of congenital syphilis (the estimated long-term care cost).

RESULTS: Under our assumptions, universal third-trimester rescreening would cost an additional $419,842 for each case of congenital syphilis prevented and $3,621,144 and $6,052,534, respectively, for each fetal and neonatal death prevented. Rescreening 4,000,000 women would prevent 60 cases of congenital syphilis and seven fetal and four neonatal deaths. Prevention of one case of congenital syphilis would require 65,790 women be rescreened. Seroconversion incidence of 0.017% would make third-trimester rescreening cost-effective.

CONCLUSION: Universal third-trimester syphilis rescreening requires a large number of women be rescreened at a high health care cost to prevent one adverse outcome from maternal syphilis. Seroconversion incidence must be 19-fold higher than the national average of primary and secondary syphilis in women for universal third-trimester rescreening to be cost-effective.

Third-trimester syphilis rescreening is not cost-effective, except in high-risk populations with a seroconversion rate of greater than 0.017%.

Division of Maternal Fetal Medicine, Department of Obstetrics and Gynecology, Women and Infants Hospital, Alpert Medical School of Brown University, Providence, Rhode Island.

Corresponding author: Catherine M. Albright, MD, 101 Dudley Street, Providence, RI 02905; e-mail: calbright@wihri.org.

Presented at the Annual Meeting of the Infectious Disease Society of Obstetrics and Gynecology, August 7–9, 2014, Stowe, Vermont.

Financial Disclosure The authors did not report any potential conflicts of interest.

The combined rate of primary and secondary syphilis in the United States declined by almost 90% in the 1990s and by 2000 was the lowest ever recorded, at a rate of 2.1 per 100,000. There has been a continued decline in the combined rate of primary and secondary syphilis in women from 1.7 per 100,000 in 2000 to 0.9 per 100,000 in 2013; unfortunately, since 2000, the overall rate has increased to 5.3 per 100,000 in 2013 as a result of increasing rates of syphilis in men.1 Although this is mostly attributed to the population of men who have sex with men, as was seen in the human immunodeficiency virus epidemic, eventual crossover to female partners is likely.

Antepartum syphilis is a maternal bacterial infection that is associated with a highly curable fetal infection in which a single intramuscular dose of penicillin can prevent neonatal infection in 98% of cases of primary, secondary, or early latent syphilis.2 Congenital syphilis occurs when the spirochete Treponema pallidum is transmitted from a pregnant woman with syphilis to her fetus. Untreated maternal syphilis can lead to intrauterine fetal demise, neonatal death, and long-term sequelae among survivors such as deafness, neurologic impairment, and bone deformities. The rate of congenital syphilis is closely related to the rate of primary and secondary syphilis in women and has remained low and generally stable since the early 2000s.1

To prevent congenital syphilis, the Centers for Disease Control and Prevention (CDC) recommends that all pregnant women be screened for syphilis at the first prenatal visit.3 This intervention has been shown to be cost-effective in multiple studies.4–84–84–84–84–8 Also, since the early 1990s, the CDC has recommended repeat screening in the third trimester in areas or communities of high syphilis prevalence.3 The rationale behind this recommendation was likely based on identifying every case of maternal syphilis and not based on cost and was clearly influenced by the high rates of syphilis in the United States in the 1990s. It is unclear, however, how reported national prevalence estimates relate to this recommendation because those estimates may not accurately reflect local incidence rates in pregnancy.

Given this uncertainty, we sought to estimate the incidence at which this testing would become cost-effective by assessing the cost to prevent one case of congenital syphilis, intrauterine fetal demise, or neonatal death with third-trimester screening in addition to first-trimester screening and the number of women who would need to be rescreened to prevent one case of congenital syphilis, intrauterine fetal demise, or neonatal death.

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MATERIALS AND METHODS

We developed a decision model to evaluate the costs and benefits of two syphilis screening strategies (universal syphilis rescreening in the third trimester or no rescreening) in a theoretical cohort of pregnant women in the United States between 28 and 32 weeks of gestation who had negative syphilis screening at their initial prenatal visit (Appendix 1, available online at http://links.lww.com/AOG/A668). The analysis was performed from a health care perspective to estimate the total direct expenditures related to syphilis screening and treatment.

To obtain base case probability point estimates and confidence intervals (CIs), we conducted an English language search of PubMed in July 2014 to identify relevant publications. The MeSH search term syphilis and the MeSH descriptor cost were used initially and then expanded to find the necessary data for the model. The final search terms included: syphilis, congenital syphilis, syphilis screening, syphilis treatment, pregnancy, rapid plasma reagin, RPR, fluorescent treponemal antibody, FTA, and Jarisch-Herxheimer reaction. The search was not limited by publication date or country of origin. All identified documents were examined and those that were relevant were retrieved. Reference lists of retrieved documents were manually reviewed to identify additional publications. To assign the base case value, randomized controlled trials and U.S. population-level data were used when possible, but when not available, the largest prospective, or if needed, retrospective, data were used. The remaining studies were used for the minimum and maximum values. If there was not one study that was clearly superior, we calculated base case point estimates as the unweighted mean or median of the available data based on their distributions (Tables 1 and 2). In calculating preterm delivery rates and morbidity and mortality of a preterm neonate, only births after 28 weeks of gestation were considered given the timing of rescreening. There was no assumed gestational age at delivery for women with syphilis because there is no known average gestational age of delivery in this population. For that reason, the general incidence of preterm birth and the corresponding neonatal morbidity and mortality data between 28 and 36 weeks of gestation in the United States was used. However, because it seemed reasonable that antepartum syphilis would increase the risk of preterm delivery, we allowed antenatal syphilis to double the rate of preterm delivery in our sensitivity analyses.

Table 1

Table 1

Table 2

Table 2

We derived cost estimates in a similar fashion to the probability estimates, but additionally queried local and national hospital and insurance data (Table 3). Of note, to calculate the cost of a preterm delivery, we used a weighted average based on the distribution of timing of preterm delivery in the United States. We adjusted all costs to reflect 2014 U.S. dollars. The costs accounted for in the model included the cost of testing, maternal follow-up and treatment, penicillin desensitization, maternal delivery, and neonatal care. In this model, we did not include long-term care costs.

Table 3

Table 3

Data regarding syphilis seroconversion during pregnancy are limited to two studies. These studies reported incidence of syphilis seroconversion between 0% and 0.17%.9,109,10 Shiber et al identified an average incidence over a 17-year period (1993–2009) of 0.029%. In the first year of the study, there was an incidence of seroconversion of 0.17%. However, in the 16,423 women who delivered from 2005 to 2009, no seroconversions were noted. In the only other study evaluating seroconversion in pregnancy, there were no seroconversions in the 1,377 women rescreened in the third trimester between 2004 and 2006.9 To assign a base case, we used the final 9-year period evaluated by Shiber et al (2000–2009), which demonstrated an incidence of syphilis seroconversion in pregnancy of 0.012%.10 This is likely higher than is found in the U.S. population in general, but by using this base case, we intentionally biased our decision analysis toward a best case scenario for screening.

Our other major assumptions included all women are screened for syphilis early in pregnancy, therefore assuming 100% compliance with the screening recommendations. All women who rescreened positive received adequate and timely treatment (more than 4 weeks before delivery) with one dose of 2.4 million units of benzathine penicillin G.11,1211,12 Because all syphilis infections detected in women by this antenatal syphilis screening program received adequate and timely treatment, their neonates required only serologic follow-up.13 All women were identified as having syphilis in the third trimester, and therefore had a fetus beyond the threshold of viability and were treated and then monitored in the hospital to assess for Jarisch-Herxheimer reaction, but not necessarily admitted. In practice, treatment failure is more likely when ultrasound abnormalities are present, but the exact risk is imprecise.11,1411,14 Therefore, all treatments were assumed to be successful, but in sensitivity analysis, this was allowed to vary to 50% treatment failure in the setting of an abnormal ultrasound finding. A Jarisch-Herxheimer reaction was assumed to result in a 24-hour maternal hospitalization but to have no effect on preterm delivery or intrauterine fetal demise.11,1411,14 The effect of a Jarisch-Herxheimer reaction on preterm delivery and intrauterine fetal demise is also unclear, so this risk was also initially assumed to be negligible but varied in a sensitivity analysis to up to doubling the probabilities of both preterm delivery and intrauterine fetal demise. We assumed that all women with an anaphylactic allergy to penicillin were appropriately identified. We did not account for a risk for anaphylaxis given its rarity (1/5,000–10,000 courses of penicillin therapy)15–1815–1815–1815–18 but accounted for the cost of penicillin desensitization in the women with a reported allergy to penicillin who received penicillin for treatment of syphilis.

The primary outcome was the cost to prevent one case of congenital syphilis. Secondary outcomes included the cost to prevent one intrauterine fetal demise or neonatal death, the number of women who would need to be rescreened in the third trimester to prevent one of these adverse outcomes, and the likelihood that screening would be cost-effective under the plausible probabilities included in the model. We assumed that screening was cost-effective if it cost less than $285,000 to prevent one case of congenital syphilis. We chose this cost-effectiveness threshold because the average lifetime direct medical cost (accounting for 5% discounting) to care for an individual with a severe disability, like congenital syphilis, is approximately $285,000,19 thus making the cost to prevent the disease equivalent to the expenditures to care for a child born with the disease. Because we did not directly include long-term care costs in the model, this allowed us to relate the outcome of the model to overall health care costs. In sensitivity analysis, we allowed the cost-effectiveness threshold to vary up to $1,000,000 because this may better account for the direct and indirect costs as well as differences in discounting of long-term care of a severe disability.19,2019,20

In addition to the base case analysis, we performed one-way and two-way sensitivity analyses. In particular, this allowed for an investigation into how the incidence of seroconversion affected the outcomes of interest. Monte Carlo simulation (a computational algorithm that relies on repeated random sampling of all variables across their CIs based on their distributions) was also used. The distributions used in the Monte Carlo simulation for the probabilities were triangular or normal as appropriate based on available data. Gamma distributions were used for all cost variables. Given the plausible variation in all of the probabilities and cost estimates included in the model, no variable was excluded from the Monte Carlo analysis. Ten thousand simulations were run to estimate the percentage of time that universal third-trimester rescreening would be cost-effective as compared with no rescreening. This number of simulations was chosen because it is our routine practice when performing these analysis. We performed all analyses using TreeAge Pro 2013 Suite. The study did not involve human participants and was exempt from institutional review board approval.

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RESULTS

The results of the base case model are presented in Table 4. The base case model demonstrated that at a rate of syphilis seroconversion of 0.012%, the cost to prevent one case of congenital syphilis with universal third-trimester syphilis rescreening was $419,842. Prevention of one intrauterine fetal demise cost $3,621,144 and one neonatal death cost $6,052,534. Under the base case assumptions, by rescreening 4,000,000 pregnant women (the annual pregnant population in the United States) in the third trimester, 60 cases of congenital syphilis, seven intrauterine fetal demises, and four neonatal deaths would be prevented. Finally, to prevent one case of congenital syphilis, 65,790 women would need to be rescreened. Similarly, 568,182 would need to be rescreened to prevent one intrauterine fetal demise and 952,381 to prevent one neonatal death resulting from maternal syphilis.

Table 4

Table 4

In one-way sensitivity analyses, the model was most sensitive to the incidence of syphilis seroconversion (Table 5). If the incidence of seroconversion was greater than 0.017%, universal third-trimester screening became cost-effective. If the incidence of seroconversion was greater than 0.2%, universal third-trimester screening became cost-saving. However, if the incidence was low (ie, 0.001%), it would cost more than $5 million to prevent one case of congenital syphilis. Additionally, the model was highly sensitive to the neonatal cost of preterm delivery and the probability of congenital syphilis given untreated maternal syphilis. If the cost of preterm delivery reached $75,000 on average (or approximately the cost of a 31- to 32-week neonate21), universal third-trimester rescreening became cost-effective. However, when delivered near term, at a cost of $3,328, the overall cost to prevent one case of congenital syphilis became $443,077. Similarly, at the highest probability of congenital syphilis without treatment, 29%, prevention of one case of congenital syphilis would cost $218,528 and would therefore be cost-effective. However, at any probability less than 22.5%, rescreening would not be cost-effective. The model was relatively refractory to changes in other variables. For example, at a relative risk of preterm delivery given untreated maternal syphilis of 9.09, the cost to prevent one case of congenital syphilis would be $391,135.

Table 5

Table 5

Two-way sensitivity analysis was then performed to evaluate the interaction between the two most influential variables, the incidence of syphilis seroconversion and the neonatal cost of a preterm delivery (Fig. 1). As the incidence of seroconversion approached 0.017%, universal screening became cost-effective at a lower overall preterm delivery cost (practically speaking, a greater gestational age at birth).

Fig. 1

Fig. 1

Using Monte Carlo Simulation, rescreening is cost-saving in only 3% of simulations (Fig. 2). However, in an additional 84.7% of simulations, rescreening costs less than $285,000 to prevent one case of congenital syphilis. At a minimum cost-effectiveness threshold of $100,000 to prevent one case of congenital syphilis, only 7.6% of simulations would be cost-effective or cost-saving. However, at a maximum threshold of $1,000,000, which at least partially accounts for the indirect costs of caring for a child with multiple comorbidities, 99.9% of simulations would be cost-effective or cost-saving (Appendix 2, available online at http://links.lww.com/AOG/A669).

Fig. 2

Fig. 2

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DISCUSSION

This model shows that in the United States, universal syphilis rescreening in the third trimester in women who screen negative at their initial prenatal visit requires a large number of women be screened at a high health care cost to prevent one adverse outcome from maternal syphilis. Unfortunately, data regarding syphilis seroconversion during pregnancy are limited to the two aforementioned studies.

An alternative to using the limited information regarding seroconversion during pregnancy is using the overall rate of primary and secondary syphilis in women in the United States as reported by the CDC. This incidence ranged from zero to 5.7 cases per 100,000 by state or area (0–0.0057%) in 2013.1 Notably, the national prevalence for women was reported to be 0.9 per 100,000 in 2013 (Table 6).1 If policy were then to be based on state-level prevalence estimates, even the highest risk states or areas would require a very large number of women be screened at a high health care cost (Table 6). If we assume that most communities fall near the national average of primary and secondary syphilis rates in women (0.0009%), this is 19 times lower than the incidence of seroconversion that would make universal third-trimester screening cost-effective, costing more than $5,000,000 per case of congenital syphilis prevented. Therefore, given that the majority of the country has an incidence at or below 0.0009% (because it is reasonable to assume that pregnant women represent only a small portion of these prevalence estimates, and therefore would have a lower incidence), universal third-trimester screening should not be recommended. However, it remains reasonable for individual high-risk cities and communities to evaluate the incidence in their population on an ongoing basis and implement a program of routine syphilis rescreening with a sufficiently high incidence of seroconversion.

Table 6

Table 6

Strengths of this study are the ability to evaluate large ranges of costs and probabilities. Additionally, a unique characteristic of this study is that we were able to evaluate the CDC recommendation for third-trimester screening from a cost perspective.

The major limitation of all cost analyses is that the evaluation is only as good as the available data. In this model in particular, we made use of data from outside of the United States and extrapolated them to our population. Additionally, there is currently clinical uncertainty regarding the optimal treatment regimen for syphilis in pregnancy12 and the actual relative risks of different clinical scenarios on both the probability of preterm delivery and the probability of a neonate having congenital syphilis. We did vary these relative risks in our sensitivity analyses to account for this clinical uncertainty. We did not directly account for lifetime costs within the model. However, we set the cost-effectiveness threshold to lifetime costs so that screening would be a net-neutral health care expenditure. Finally, we did not account for indirect costs such as loss of work.

Even with a recommendation for universal syphilis screening in the first and possibly third trimesters in the United States, only 52% of mothers of neonates with congenital syphilis reported having at least one prenatal visit.22 Our analysis therefore assumes a best-case scenario regarding compliance with initial screening, and, although universal syphilis rescreening would prevent a small number of cases of congenital syphilis, interventions to improve access to health care may have a greater effect on reduction of the rate of congenital syphilis in the United States.

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