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Sexually Transmitted Diseases:
doi: 10.1097/OLQ.0b013e318249cbaa
Original Study

Chlamydia trachomatis Infections Among Women Attending Prenatal Clinics: United States, 2004–2009

Satterwhite, Catherine Lindsey PhD, MSPH, MPH*; Gray, Alyson M. MPH; Berman, Stuart MD, ScM*; Weinstock, Hillard MD, MPH*; Kleinbaum, David MA, PhD; Howards, Penelope P. MS, PhD

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Author Information

From the *Centers for Disease Prevention and Control, Atlanta, GA; CDC Foundation, Atlanta, GA; and Department of Epidemiology, Emory University, Atlanta, GA

The authors thank Dr. James Buehler at the Centers for Disease Control and Prevention (CDC) for providing valuable insights in the early conceptualization of this analysis, and Rob Nelson at CDC for graphical assistance.

The findings and conclusions in this report have not been formally disseminated by the Centers for Disease Control and Prevention and should not be construed to represent any agency determination or policy.

Correspondence: Catherine Lindsey Satterwhite, PhD, MSPH, MPH, Department of Preventive Medicine and Public Health, University of Kansas School of Medicine, 3901 Rainbow Blvd, MS: 1008, Kansas City, KS 66160. E-mail: csatterwhite@kumc.edu.

Received for publication October 20, 2011, and accepted January 3, 2012.

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Abstract

Background: Chlamydia screening practices, positivity, and trends from 2004 to 2009 in publicly funded prenatal clinics have not been described.

Methods: A phone-based survey assessing chlamydia screening practices was conducted among a random sample of clinics providing prenatal services (prenatal, family planning, and integrated clinics: “prenatal clinics”) that reported data to the Infertility Prevention Project (IPP) in 2008. Using existing IPP data, chlamydia positivity and trends were assessed among women aged 15 to 24 years seeking care in any prenatal clinic reporting ≥3 years of data to IPP from 2004 to 2009. Linear trends of the effect of year (a continuous variable) on positivity were evaluated using a correlated modeling approach with a random intercept where the unit of analysis was the individual clinic performing chlamydia tests (clinic-based analysis). Covariates included race, age, test technology, and geography.

Results: Of 210 sampled clinics, 166 (79%) completed the survey. Of these, 163 (98.2%) had documented chlamydia screening criteria. Most clinics screened all women during their first trimester and reported 100% screening coverage. From 2004 to 2009, 267,416 tests among women aged 15 to 24 years were reported to IPP from eligible prenatal clinics. Overall chlamydia positivity was 8.3%. Controlling for all covariates, positivity decreased from 2004 to 2009 (odds ratio: 0.93 per year, 95% confidence interval: 0.92, 0.95, 35% decrease overall).

Conclusions: The substantial burden of chlamydia among young women tested in prenatal clinics reporting data to IPP suggests the continued need for routine screening. Decreasing trends from 2004 to 2009 in the IPP prenatal population correspond to findings of overall decreasing chlamydia prevalence in the United States.

It is estimated that 2.8 million chlamydial infections occur in the United States annually.1 Among women, chlamydia, a sexually transmitted disease, may cause pelvic inflammatory disease, ectopic pregnancy, infertility, or chronic pelvic pain. Among pregnant women, chlamydia can lead to premature rupture of membranes, low birth weight infants, and neonatal ophthalmia.25 In a US population-based survey conducted from 1999 to 2002, 2.0% of pregnant women aged 14 to 39 years had chlamydia.6

The Centers for Disease Control and Prevention (CDC) currently recommends that all pregnant women, regardless of age, be screened for chlamydia at their first prenatal visit.7 The United States Preventive Services Task Force recommends first trimester screening of pregnant women aged <25 years and older women at increased risk (e.g., new or multiple sexual partners or inconsistent condom use).8 Despite the risks of infection during pregnancy and established chlamydia screening recommendations, published reports on screening practices and coverage are not widely available. Screening coverage measures, such as those from commercial health plans and Medicaid, do not directly address pregnant women.

The Infertility Prevention Project (IPP) is a national screening program to detect and treat Chlamydia trachomatis and Neisseria gonorrhoeae infections among sexually active young women to prevent sequelae leading to infertility. Although the majority of clinics participating in IPP are designated as family planning clinics, prenatal clinics also report data to IPP. IPP data represent a unique opportunity to assess chlamydia screening and positivity in a large group of women seeking prenatal care in publicly funded clinics. This study had 2 primary goals. First, to better describe chlamydia screening policies and practices in publiclyfunded IPP prenatal clinics, a survey was conducted among prenatal clinics reporting data to IPP. Second, existing IPP data were used to describe chlamydia positivity and trends from 2004 to 2009 among women seeking prenatal services.

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METHODS

Using data submitted through IPP, clinics providing care to women seeking prenatal services were identified. Three types of publicly funded clinics were eligible for inclusion: prenatal clinics, family planning clinics providing prenatal services, and integrated clinics providing prenatal services. Prenatal clinics were defined as clinics whose primary mission is to provide health care and education to pregnant women. Family planning and integrated clinics offer multiple services; for these clinics, a visit type designated as “prenatal” was used to identify women eligible for inclusion. For simplicity, all 3 clinics are referred to as “prenatal clinics” (clinics providing prenatal services) for this analysis.

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Survey of Prenatal Clinics Reporting Data Through IPP

To address the first study goal, describing publicly funded IPP prenatal clinics, a survey was conducted among publicly funded prenatal clinics reporting data to IPP in 2008. The survey was administered from December 2009 to July 2010. Of the 559 eligible clinics, time and resources permitted a random sample of 210 (38%) clinics invited to participate in the survey. The objective was to describe chlamydia screening policies and practices. Questions addressed age criteria used, frequency of testing, timing of test (trimester), and whether women seeking a pregnancy test only are routinely screened for chlamydia. Survey questions also included clinic census information aggregated at the clinic level (number of women seeking care at the clinic and the number of those women tested for chlamydia) to assess chlamydia screening coverage. The survey was administered to clinic administrators via phone, with optional e-mail follow-up. No incentives were offered for participating in the survey, which typically took 10 to 15 minutes to complete. The survey was determined to not constitute human subjects research (CDC and Emory University Institutional Review Boards).

Survey responses to clinical chlamydia screening policies and practices were summarized and reported in a descriptive manner. Open-ended responses were reviewed to determine common responses and create summary data groupings.

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Analysis of Chlamydia Positivity and Trends

To address the second study goal, existing IPP data were used to describe chlamydia positivity and trends among women seeking prenatal services. Because data from the survey were not longitudinal, these data were not applicable to this goal. Using IPP data, the study population consisted of all prenatal clinics reporting at least 3 years of data to IPP from 2004 to 2009. Only individual test results from women aged 15 to 24 years were included. In order for a clinic to contribute data for a given calendar year, the clinic must have reported at least 25 tests designated as prenatal (positive and negative) during that year.

Where available, pregnancy status was included in analyses; however, pregnancy status is not part of the standard IPP dataset and not uniformly reported. It was thus not possible to determine whether the visit was made because a woman was already aware of her pregnancy, or whether the visit was made primarily to seek a pregnancy test. Women seeking a pregnancy test only are a high-risk group, with substantially higher chlamydia rates than other groups, particularly women seeking standard prenatal care.9

IPP data consist of chlamydia test results. No personal identifiers are available; therefore, women who had multiple test results over the course of a year contribute multiple observations to the dataset. Chlamydia positivity was calculated by dividing the total number of positive tests by the total number of positive and negative tests. Chlamydia positivity has been found to be a reasonable approximation of prevalence.10

To assess positivity trends from 2004 to 2009, a correlated, longitudinal analysis was conducted. The unit of analysis was the individual clinic performing chlamydia tests (clinic-based analysis), as opposed to an analysis based only on individual test results. Methodology using the clinic as the unit of analysis has been previously described and applied to IPP data; data summarized at the clinic level and treated as correlated likely minimize the influence of some unmeasured confounders.11 The outcome of interest was chlamydia positivity. An events/trials approach was used to allow for incorporation of clinic size (denominator) into the modeled outcome.

The primary independent exposure of interest was defined as calendar year, from 2004 to 2009. To determine whether year should be treated as ordinal or categorical, a linearity assessment was performed. Estimated logit plots, as well as parameter estimates from a generalized estimating equation model including categorical indicator variables representing year, suggested a general linear pattern. Therefore, year was included as an ordinal variable in the final model. To account for the variation in the underlying prenatal chlamydia positivity between clinics at baseline, a random intercept was included.

Five possible covariates were considered. The proportion of tests conducted using nucleic acid amplification test (NAAT) technology performed by a given clinic was likely an important covariate because NAATs demonstrate substantially increased sensitivity over prior generation tests.12 Two demographic covariates were also considered: the proportion of tests occurring among young women aged 15 to 19 years and the proportion of tests occurring among black women. The fourth covariate identified the region (Fig. 1) where the clinic was geographically located. All 2-way interaction terms (product of year with each of the 4 covariates) were assessed, in order to detect differences in trends over time in subgroups. The proportion of the tested population that was pregnant at the time of the test was also considered in the subset of clinics where this information was available.

Figure 1
Figure 1
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During trend ascertainment, data from 4 separate clinic scenarios were modeled (1): data from all prenatal clinics, (2) data from prenatal clinics where all reported tests were conducted on women known to be pregnant, (3) data from all prenatal clinics where pregnancy status was reported, and (4) data from clinics where pregnancy status was not reported. The second scenario attempted to capture the specific population with the lowest positivity. By selecting clinics that report chlamydia tests on pregnant women only, women not pregnant (and hypothetically only seeking a pregnancy test, a high-risk group) are excluded. The third scenario allowed for incorporation of pregnancy status into the model as a potential confounder. The fourth scenario was used to determine whether trends among clinics not reporting pregnancy status were consistent with the other scenarios.

All statistical analyses were performed using SAS version 9.2 (SAS Institute Inc., Cary, NC). Modeling was conducted using the SAS GLIMMIX procedure, with a σ02 (scalar) G-matrix and a σ12I5 R-matrix correlation structure (exchangeable, with random intercept).

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RESULTS

Survey

Of the 210 clinics invited to participate in the survey, 166 (79%) completed questions about clinic chlamydia screening policies and practices. The majority of clinics not completing the survey (29 of 44, 66%) were not able to be contacted despite multiple attempts; failure to contact was due primarily to unreturned messages or lack of a useful phone number.

Overall, clinics from 22 states, Puerto Rico, and the Virgin Islands completed at least part of the survey. Of the 166 clinics completing the survey, 163 (98.2%) reported that their clinic had documented chlamydia screening criteria for prenatal women (Table 1). The majority of clinics (>95%) did not have age-based screening criteria and screened pregnant women of all ages per CDC recommendations. Only 12.7% of clinics (21 of 166) reported that they screen women aged <25 years who come into the clinic only seeking a pregnancy test.

Table 1
Table 1
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Of the 106 clinics reporting information on clinic census, only about half reported consistently analyzable data (e.g., did not respond to questions with “don't know”). Among a subset of these clinics, median clinic-reported screening coverage among women aged <25 years who were seeking prenatal care was 100% (mean: 86.2%, interquartile range [IQR]: 77.6%–100%, 55 clinics). Clinic-reported median chlamydia positivity in this group of women was 5.7% (mean: 10.0%, IQR: 4.0%–10.6%, 40 clinics).

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Chlamydia Positivity and Trends

From 2004 to 2009, 267,416 chlamydia tests conducted among young women aged 15 to 24 years seeking prenatal care were reported to IPP. These tests were administered in 335 eligible prenatal clinics, located in 23 states, Puerto Rico, and the Virgin Islands, and representing 7 of 10 regions (Fig. 1). More than 98% (n = 329) of eligible clinics were defined as “prenatal clinics” (i.e., clinics whose primary mission is to provide health care and education to pregnant women); the remaining 6 clinics were integrated clinics that provided prenatal care. The mean number of tests reported per clinic per year was 180 (IQR: 61–227).

When examining mean clinic-specific proportions, 37.0% of tests were conducted among white women, and 62.1% were among women aged 20 to 24 years (Table 2). Although mean NAAT use increased over time, the median was 100.0% beginning in 2005, remaining at that level in subsequent years. All other covariates (race, age, region) were also stable over the 6-year analysis period (data not shown). Of the 335 prenatal clinics, 220 reported data on pregnancy status at the time of test administration (65.7%). The overwhelming majority of chlamydia tests conducted at these clinics were administered to pregnant women (mean: 94.4%).

Table 2
Table 2
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Overall chlamydia positivity was 8.3% (22,097/267,416). When examining prenatal clinics by whether pregnancy status at the time of a chlamydia test was reported, trends in crude chlamydia positivity from 2004 to 2009 were fairly consistent, with no meaningful changes over time (Fig. 2). Based on annual data from all prenatal clinics, positivity ranged from a minimum of 7.8% to a maximum of 8.7%. When assessing clinics where all chlamydia tests (100%) were reported as being conducted among pregnant women, the range over time was slightly lower, from 6.1% to 7.3%. Positivity in clinics reporting pregnancy status and clinics not reporting pregnancy status was similar.

Figure 2
Figure 2
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Contrary to crude positivity trends, trends assessed using a multivariable approach showed a decrease in chlamydia positivity from 2004 to 2009 among women aged 15 to 24 years tested in all prenatal clinics reporting at least 3 years of data to IPP during this time frame (Table 3). After controlling for age, race, test technology, and region, the odds ratio (OR) associated with a single-year change was 0.93 (95% confidence interval [CI]: 0.92, 0.95).

Table 3
Table 3
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Further sensitivity analyses varying the clinics included in analysis were consistent with these findings. Among the 33 prenatal clinics reporting that all tests were conducted on pregnant women, the OR associated with a single-year change was 0.94 (95% CI: 0.86, 1.01). Likewise, clinics that reported pregnancy status and clinics that did not report pregnancy status showed decreasing chlamydia positivity trends (data not shown). When the proportion of the population that was pregnant was entered as a covariate in the model, results did not change.

When data from each region were modeled separately, controlling for age, race, and test technology, some variations were observed in the effect of year on chlamydia positivity. Of the 7 regions included in the analysis, trends were relatively flat in 5 regions. In Region VII, the OR was 1.04 (95% CI: 1.01, 1.08). In Region IV, where the majority of eligible prenatal clinics were located, a decrease was detected (OR: 0.92; 95% CI: 0.91, 0.94). When population subgroups were independently modeled, adjusting for all covariates, decreases of varying magnitude were consistently demonstrated (Table 4). Although only 1462 tests among nonpregnant women were reported from 6 clinics (reporting at least 25 of these tests for 3 or more years from 2004 to 2009), a decreasing trend in chlamydia positivity was also observed in this population (OR: 0.92; 95% CI: 0.85, 0.99).

Table 4
Table 4
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DISCUSSION

The chlamydia burden among women aged 15 to 24 years seeking prenatal services in clinics reporting data to IPP is substantial. The overall chlamydia positivity estimate of 8.3% is higher than the population-based prevalence estimate of 2.0% in pregnant women.6 However, the latter estimate covers all women tested at all stages of pregnancy, including many women who were likely already screened and treated for chlamydia at prior prenatal visits; thus, this may be an underestimate of the actual burden among pregnant women initially screened for chlamydia. In addition, the population-based estimate represents women aged 14 to 39, thus including older women at lower risk for chlamydia. Positivity in publicly funded IPP prenatal clinics is likely an overestimate of the proportion of all pregnant women with chlamydia because it excludes pregnant women seeking care in the private sector (a lower risk group) and includes women who may have sought a pregnancy test only, a higher risk group, in addition to overrepresenting women of low socioeconomic status.

Although women seeking a pregnancy test perceive themselves to be at risk for pregnancy, they may also be at risk for a sexually transmitted disease. In a recent study, Geisler et al reported a chlamydia prevalence of 12% among women aged 16 to 45 years who were seeking a pregnancy test only (South Carolina family planning clinics).9 Importantly, prevalence did not vary based on whether a woman tested positive for pregnancy.

Survey findings suggested that most clinics screen all pregnant women for chlamydia at least once before delivery regardless of age. However, only 12.7% of clinics reported routinely screening women aged <25 years who were only seeking a pregnancy test, despite this group being covered by general chlamydia screening recommendations. Pregnancy tests are performed using urine; testing the same sample for chlamydia using a NAAT requires no additional effort on the part of the patient and little additional effort on the part of clinic staff. Although prenatal clinics report high screening coverage among pregnant women, not actively screening women seeking a pregnancy test may be a missed opportunity for prevention, even if relatively few women use prenatal clinics for this service.

The finding that chlamydia positivity decreased over the 6-year analysis timeframe corresponds to findings from previous analyses that reported decreases in chlamydia prevalence, both in general US population of men and women aged 14 to 39 years from 1999 to 200813 and in high-risk men and women aged 16 to 24 years from 2003 to 2007.14 These analyses run counter to reported trends in national chlamydia case report data; however, increasing screening coverage and improvements in test technology make interpretation of such data challenging.15 Although chlamydia case report rates have steadily increased over the past 20 years, these data likely do not represent true increases in disease incidence. Because of the limitations in case report data, examining chlamydia prevalence in specific populations, such as women in prenatal settings, is important in supplementing case report data.

Although 23 states, Puerto Rico, and the District of Columbia were represented in this analysis, 3 regions (I, VIII, IX) of the United States were not included due to the absence of IPP data from any clinics designated as providing prenatal services. Overall, the majority of prenatal clinics eligible for inclusion in this analysis were located in the eastern half of the United States, specifically in Region IV (southeastern states). Decreasing chlamydia positivity in Region IV contributed heavily to overall trend findings. Region IV has the highest positivity of any IPP region; therefore, it is possible that there was a greater opportunity to detect a change in positivity than in other regions. In addition, the population of women represented in this analysis may be somewhat different than women in standard prenatal care who are already aware of and committed to their pregnancy; women tested in IPP prenatal clinics may not be representative of all pregnant women being screened for chlamydia. Although it was neither possible to determine whether women knew their pregnancy status before their visit nor to differentiate women seeking a pregnancy test only, chlamydia positivity trends were similar across different prenatal settings, suggesting that trends were likely not affected by possible population differences. Only a limited number of covariates were available for analysis. In particular, IPP data lack behavioral risk data. Although use of data summarized at the clinic level likely minimized the influence of some unmeasured confounders, additional data to allow for further classification of women by pregnancy status and health care-seeking reason may have been useful.

Findings of high chlamydia positivity in this analysis support the need for continued screening in the population seeking prenatal care to prevent possible adverse outcomes of infection in both pregnant and nonpregnant women. The prenatal population may also be a reasonable sentinel population to monitor trends in chlamydia prevalence. Population-based estimates are neither easily or economically obtained at state and local levels nor are they reliable long-term national sources for chlamydia surveillance; if chlamydia prevalence continues to decline over time, standard errors will increase, limiting point estimate precision. The biases associated with service-based clinic prevalence are likely to be minimized when considering the prenatal population compared with other populations captured in national data (e.g., family planning clinics) because the prenatal population is likely to be a more stable population that is less affected by general health care-seeking behaviors.

In summary, survey findings suggested that the prenatal care population is being regularly screened for chlamydia. This analysis demonstrates a substantial burden of chlamydial infection in the population of women aged 15 to 24 years who received a chlamydia test during a prenatal care visit to a publicly funded clinic reporting data to IPP. Although positivity was high, modeled trends showed a decrease from 2004 to 2009, providing further evidence to suggest overall decreasing chlamydia prevalence in the United States.

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