Adherence to Sexually Transmitted Infection Screening in Pregnancy

Abstract

Objective:

Professional guidelines and state law require screening for sexually transmitted infections (STI) during pregnancy. Our objective was to evaluate adherence to these recommendations.

Methods:

This is a retrospective cohort study of patients initiating prenatal care before 20 weeks' gestation. Demographic characteristics and STI screening were abstracted from prenatal records. Tests of interest included initial syphilis, human immunodeficiency virus (HIV), hepatitis B, chlamydia, and gonorrhea tests, as well as repeat (third trimester) syphilis and HIV tests. All patients were eligible for initial screening. Patients were eligible for analysis of whether they received adherent repeat third trimester screening for syphilis (mandated by state law) and HIV (institutional protocol) if they delivered at or after 32 weeks' gestation. Adherent screening was defined as performance of all recommended screening.

Results:

Of 2370 patients, 1816 (76.6%) received adherent initial STI screening and 181 (7.8% of 2308 patients who delivered at or after 32 weeks' gestation) received adherent repeat third trimester STI screening. After adjusting for covariates, private insurance (adjusted odds ratio [aOR] 1.45, confidence interval [95% CI] 1.12–1.95) was associated with adherent initial screening, whereas being non-Hispanic Black or Hispanic were associated with lower odds of adherent initial screening. Factors associated with adherent repeat third trimester STI screening were younger age (aOR 0.93, 95% CI 0.90–0.97) and non-Hispanic Black race (aOR 3.24, 95% CI 1.94–5.42). Those with private insurance (aOR 0.10, 95% CI 0.06–0.15) were less likely to receive adherent repeat third trimester screening.

Conclusion:

STI screening rates remain suboptimal. Multiple disparities exist in performance both of initial and repeat third trimester screening.

Introduction

Sexually transmitted infections (STIs) can have adverse effects on maternal, fetal, and neonatal health in pregnancy, leading to complications including stillbirth, preterm birth, fetal growth restriction, and congenital anomalies.¹ The rates of STIs among patients of childbearing potential have increased in recent years.^2
–4 Screening and treating patients for STIs can reduce the risk of these complications, including perinatal transmission of infections that can have lifelong consequences for offspring, including the human immunodeficiency virus (HIV), syphilis, and hepatitis B.^5,6 In 2018, the most recent year for which complete data are available, one study estimated 2.4 million incident cases of chlamydia, 853,000 incident cases of gonorrhea, 25,000 incident cases of syphilis, 52,000 prevalent cases of hepatitis B, and 5,700 incident cases of HIV among patients of reproductive ages in the United States.²

The American College of Obstetricians and Gynecologists (ACOG) recommends universal screening of all pregnant patients for HIV, syphilis, hepatitis B, hepatitis C, chlamydia, and gonorrhea at the initial prenatal care visit.⁷ The CDC and ACOG both support repeated screening for HIV and syphilis in the third trimester for patients at high risk of infection based either on geographic prevalence or personal characteristics.^7
–9 In Illinois, providers are required by law to test patients in both the first and third trimester for syphilis¹⁰; Illinois is one of 44 states that legally mandates some form of syphilis testing in pregnancy.^11,12

Despite recommendations for STI screening, prior data have suggested STI screening performance remains suboptimal, even when state-mandated.¹² Our objective was to evaluate clinician adherence to STI screening during prenatal care, and to identify factors associated with adherent screening.

Methods

This is a retrospective cohort study of patients who received prenatal care and delivered at Northwestern Memorial Hospital between November 2011 and November 2015. Inclusion criteria were patients >18 years with singleton pregnancies who initiated prenatal care before 20 weeks' gestation within the academic practices of this institution. Individuals whose initial prenatal visits were conducted outside of this system and transferred to this institution were excluded, as their STI screening data may have had differential ascertainment. For patients who experienced more than one pregnancy during the study period, only data from the first pregnancy observed were used.

Information on STI screening and patient characteristics was abstracted from the electronic medical record. Tests of interest included initial screening for syphilis, HIV, hepatitis B, chlamydia, and gonorrhea as well as third trimester repeat screening for syphilis and HIV. All patients were eligible for initial screening. Patients were eligible for third trimester repeat screening (anytime at 27 weeks' gestational age or greater) for syphilis (mandated by state law) and HIV (institutional protocol at the time of the study) if they delivered at ≥32 weeks' gestation, to allow time for patients to have a prenatal visit in which they could have plausibly been screened after 27 weeks but before delivery. The primary outcome was adherent screening, defined as whether a patient received all screening tests during a specified period (initial vs. third trimester, which were analyzed separately).

We also examined several characteristics we believed were possibly correlated with STI screening based on prior literature,^12,13 including maternal age (years), self-identified maternal race/ethnicity (White non-Hispanic, Black non-Hispanic, Hispanic, Asian, and other), insurance status (private vs. other), nulliparity, tobacco use (defined as any current or prior use), body mass index (kg/m²), gestational age at first prenatal visit (in weeks), and total number of prenatal care visits.

Student's t-tests were used for continuous variables, and chi square tests and Fisher's exact tests were used for categorical variables, respectively, in bivariable analyses. Multivariable logistic regression was used to adjust for factors associated with STI screening at the p < 0.05 level in bivariable analyses. All hypothesis tests were two-tailed, and a probability value of 0.05 was used to determine statistical significance. All analyses were conducted in STATA (version 17.0; StataCorp, College Station, TX). This protocol was approved by the Northwestern University Institutional Review Board with a waiver of informed consent

Results

Our study sample included 2,370 patients, of whom 2,308 delivered after 32 weeks and were included in both analyses. Of the entire cohort, 76.6% (N = 1,816) of all patients received adherent initial screening. Patients who received appropriate initial screening were more likely to be older, non-Hispanic White, and more likely to initiate prenatal care earlier in pregnancy (Table 1). After adjusting for potential confounders, private insurance was associated with increased odds of adherent initial screening (adjusted odds ratio [aOR] 1.45, confidence interval [95% CI] 1.12–1.95), whereas non-White, non-Hispanic race/ethnicity were associated with decreased odds of initial adherent screening.

Table 1.

Factors Associated with Receipt of Initial Screening for Sexually Transmitted Infections

Variable	Nonadherent (N = 554)^a	Adherent (N = 1,816)	p ^b	Adjusted odds ratio ^c (95% confidence interval)
Age (years)	32.7 ± 5.8	33.2 ± 4.6	0.047	0.99 (0.97–1.01)
Race and ethnicity
White non-Hispanic	268 (48.4)	1,063 (58.5)	<0.001	Referent
Black non-Hispanic	101 (18.2)	202 (11.1)		0.61 (0.43–0.86)
Hispanic	87 (15.7)	205 (11.3)		0.71 (0.51–0.99)
Asian	47 (8.5)	147 (8.1)		0.73 (0.50–1.09)
Other	51 (9.2)	199 (11.0)		1.09 (0.75–1.58)
Private insurance	382 (69.2)	1,527 (84.2)	<0.001	1.45 (1.12–1.95)
Nulliparous	277 (52.0)	908 (52.1)	0.97
Tobacco use^d	118 (21.5)	294 (16.2)	0.004	0.61 (0.46–0.80)
Body mass index (kg/m²)	27.3 ± 6.8	26.0 ± 6.1	0.001	1.00 (0.99–1.02)
Gestational age at first prenatal care visit (weeks)	13.0 ± 4.2	9.5 ± 3.2	<0.001	0.80 (0.78–0.82)
No. of prenatal care visits	10.4 ± 4.8	12.1 ± 4.6	<0.001	1.00 (0.99–1.03)

Data presented as mean ± standard deviation for continuous variables, N (%) for categorical variables.

p Value for Student's t-test for continuous variables, chi square or Fisher's exact test for categorical variables.

Odds ratios adjusted for all variables listed (age, race, ethnicity, insurance status, tobacco use, nulliparity, body mass index, gestational age at first prenatal care visit, and number of prenatal care visits).

Tobacco use defined as any past or present tobacco use versus never use.

Of the 2,308 patients eligible for repeat third trimester screening, 7.6% (N = 181) received the appropriate screening. Factors associated with adherent repeat third trimester STI screening were younger age (aOR 0.93, 95% CI 0.90–0.97), non-Hispanic Black race (aOR 3.24, 95% CI 1.94–5.42), and maternal tobacco use (aOR 1.73, 95% CI 1.10–2.73). Private insurance (aOR 0.10, 95% CI 0.06–0.15) and nulliparity (aOR 0.64, 95% CI 0.43–0.95) were both associated with decreased likelihood of repeat third trimester screening (Table 2).

Table 2.

Factors Associated with Receipt of Repeat Screening for Sexually Transmitted Infections

Variable	Nonadherent (N = 2,127)^a	Adherent (N = 181)	p ^b	Adjusted odds ratio ^c (95% confidence interval)
Age (years)	33.4 ± 4.8	29.6 ± 5.4	<0.001	0.93 (0.90–0.97)
Race and ethnicity
White non-Hispanic	1,260 (59.0)	39 (21.6)	<0.001	Referent
Black non-Hispanic	212 (10.0)	76 (42.0)		3.24 (1.94–5.42)
Hispanic	246 (11.6)	41 (22.7)		1.86 (1.06–3.27)
Asian	173 (8.1)	17 (9.4)		3.41 (1.75–6.64)
Other	236 (11.1)	8 (4.4)		0.76 (0.33–1.74)
Private insurance	1,819 (85.7)	42 (23.2)	<0.001	0.10 (0.06–0.15)
Nulliparous	1,083 (53.1)	62 (35.4)	<0.001	0.64 (0.43–0.95)
Tobacco use^d	358 (16.9)	45 (24.9)	0.007	1.73 (1.10–2.73)
Body mass index (kg/m²)	26.0 ± 6.1	29.3 ± 7.6	<0.001	1.02 (0.99–1.03)
Gestational age at first prenatal care visit (weeks)	10.1 ± 3.7	12.4 ± 4.1	<0.001	1.05 (1.00–1.10)
No. of prenatal care visits	12.0 ± 4.6	9.5 ± 4.7	<0.001	0.93 (0.89–0.97)

Data presented as mean ± standard deviation for continuous variables, N (%) for categorical variables.

p Value for Student's t-test for continuous variables, chi square or Fisher's exact test for categorical variables.

Tobacco use defined as any present or past tobacco use versus never use.

Discussion

Despite recommendations and even state laws recommending screening all pregnant patients for STIs at the first prenatal visit, our results show that adequate screening is far from universal, with only 76.6% of patients receiving all recommended screening tests at initial presentation to antenatal care. Despite a state law requiring repeat screening for syphilis and a long-standing institutional protocol requiring repeat screening for HIV in the third trimester, <10% of eligible patients received both of these tests. We find that completing adequate screening is associated with nonclinical patient characteristics, including insurance status and maternal race/ethnicity.

Other previous studies have also indicated that adherence to screening guidelines is far from universal. Ojo et al. found, for instance, that although syphilis screening rates improved over time, they ranged from 71.7% to 86.6% of all live births.¹⁴ The authors also found that patients of Black race and with public insurance were more likely to be screened. A study from Montreal found only 85% of patients were screened for chlamydia and gonorrhea during pregnancy, with disparities evident by provider specialty.¹⁵ In a nationally representative study from the United States, ∼48% of recently pregnant patients reported being screened for chlamydia, whereas 54% reported being screened for something other than chlamydia. Again, non-Hispanic Black women were more likely to be screened in this study.¹³

One explanation for the disparities we see in STI screening by insurance status is that this may reflect differences in access to and uptake of prenatal care in general (not just STI screening). Differential access to care and timing of initiation of prenatal care based on insurance status may explain some of the disparities we see in initial adherent screening. Even if patients are eligible for public insurance during pregnancy, coverage gaps outside of pregnancy in this population is associated with decreased likelihood of initiating prenatal care in the first trimester.¹⁶

Yet, our study represents a population who had presented for antenatal care, as this was an inclusion criterion for analysis, and still these insurance-based disparities exist, suggesting other underlying biases and inequities. These inequities in perceived risk have been borne out in other studies. For example, other studies posit that there may be differences in screening based on provider perception that those insured through public insurance are at higher risk for STIs, particularly chlamydia.¹⁷ An alternate explanation could be that patients who presented for some prenatal care, but who did not attend all recommended visits, were less likely to be screened, although we found no association between number of visits and initial screening, and an inverse association between number of visits and repeat screening (i.e., more visits led to a lower likelihood of repeat screening). These nuances could be explored in future studies.

Previous literature supports the notion that patients may be screened differentially based on other personal characteristics besides insurance status that providers may consciously or subconsciously feel places them at “high risk” of STIs, regardless of whether this risk assessment is correct. Wiehe et al., for instance, find among nonpregnant female patients with symptoms, those of non-White race or Hispanic ethnicity and those with either public or no insurance are more likely to be tested for chlamydia.¹⁸ These disparities in screening persist even when accounting for whether an individual has been diagnosed previously with an STI.¹⁹ Others have found that screening patients based on assumptions regarding the underlying risk of their communities can lead to overscreening of some populations and underscreening of others.²⁰ These studies indicate that screening strategies based on provider discretion are flawed, and potentially prone to provider biases regarding who is most likely to have an STI.

The solution to suboptimal screening as well as screening disparities remains truly universal screening during pregnancy, which has benefits for both pregnant patients and neonates. In two different studies, universal prenatal screening for chlamydia in one institution substantially decreased the percentage of neonates with conjunctivitis due to Chlamydia trachomatis.^21,22 Antenatal screening has reduced perinatal transmission of syphilis,²³ HIV,²⁴ and hepatitis B⁶. Screening during pregnancy allows pregnant patients with HIV to receive antiretroviral therapy,²⁵ decreasing the risk of maternal opportunistic infections.

Universal screening for hepatitis C identified that >10% of infections occurred in patients with no known risk factors, allowing these patients to be identified and to receive postnatal treatment.²⁶ Clearly, a shift toward universal STI screening offers potential maternal and neonatal clinical benefits as well as a reduction in inequities that occur when clinician perception of risk is used for decision-making. Measures that may encourage universal screening may include addressing barriers to screening at prenatal visits such as availability of supplies, using electronic medical record reminders, and reminding patients about screening guidelines^.27 Universal screening could also be utilized as a quality measure.

Strengths of the study include a racially and ethnically diverse study population with detailed information on prenatal care visits, including STI screening. Objective test results were available, and thus, differences seen are not just differences in documentation of screening. There remain several limitations, however, that must be considered when interpreting these data. Patients may have been screened elsewhere before presenting to our facility for prenatal care in the first trimester, such as at the time of being diagnosed with pregnancy; however, if records were not transferred to the electronic medical record for research purposes, they were similarly not available for clinical use, and thus individuals should have undergone screening at this institution. Similarly, in the third trimester, they may have been screened elsewhere (such as at an emergency room facility) and these test results were not populated in our medical record.

We are also unable to determine whether screening was ordered at a visit, but not completed (for whatever reason). Selection bias may exist in which patients received prenatal care at our facility, and these data are not meant to be representative of the entire population of pregnant patients in the United States. Patients may have also declined screening (especially repeat screening) in ways that are not able to be captured in a retrospective study. There may be residual confounding, and these data are correlational only; causation cannot be implied. Finally, this study took place before the 2018 amendment to the Illinois Perinatal HIV Prevention Act that mandated third-trimester repeat HIV testing, and thus further study is needed to understand the effect of this legislation on subsequent repeat screening performance.

Conclusion

At our institution, screening for STIs during routine prenatal care remains suboptimal, and disparities exist in both initial screening and in repeat screening in the third trimester. This is true even in a state where initial and third trimester screening for syphilis is a state law. Our data show that patients with private insurance are more likely to receive initial screening, whereas those patients who are younger and of Black race are more likely to undergo repeat third trimester screening. The goal of implementing universal screening is to eliminate such disparities, and further study is needed to ensure all pregnant individuals receive appropriate universal STI screening.

Footnotes

Authors' Contributions

Conceptualization and writing—original draft by A.M.D. Conceptualization, investigation, and writing—review and editing by K.D. Conceptualization, supervision, and writing—review and editing by L.M.Y. Conceptualization, formal analysis, methodology, and writing—review and editing by N.B.

Disclaimer

The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Author Disclosure Statement

No competing financial interests exist.

Funding Information

Research reported in this publication was supported, in part, by the National Institutes of Health's National Center for Advancing Translational Sciences, Grant No. UL1TR001422. At the time of this study, L.M.Y. was supported by NICHD K12 HD050121. The NIH played no role in study design, collection or interpretation of data, and decision to publish the results.

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