Comparing Cervical Cancer Screening Strategies in an Incarcerated Population

Abstract

Objective:

To describe the prevalence of cervical intraepithelial neoplasia (CIN), high-risk human papillomavirus (hrHPV) infection, and cervical cancer in a high-risk, underscreened incarcerated population and to evaluate the performance of current cervical cancer screening options to detect cervical precancer (CIN 2/3) in this population.

Study Design:

Deidentified data were obtained from all cytological, hrHPV DNA, and histopathological testing of cervical biopsies performed on people incarcerated at the North Carolina Correctional Institute for Women between January 1, 2013, and December 31, 2020. These were linked to corresponding demographic data. The proportions of histopathological diagnoses of CIN2+ and CIN3+ immediately preceded by abnormal cytology testing or hrHPV testing were determined, and prevalence differences and 95% confidence intervals were calculated.

Results:

A total of 15,319 individuals incarcerated at the North Carolina Correctional Institute for Women had at least one cytology result during 2013–2020. Of these, 2,829 (18%) had abnormal cervical cytology, and 3,724 (24.3%) had positive hrHPV testing. The detection of CIN2+ was 95.9% by preceding abnormal cervical cytology, 89.9% by preceding positive hrHPV testing (p = 0.03), and 96.5% by preceding positive co-testing. The detection rate of CIN3+ was 96.6% by preceding abnormal cervical cytology, 90.8% by preceding positive hrHPV testing (p = 0.12), and 96.6% by positive co-testing.

Conclusion:

In our sample, primary cytology and co-testing detected CIN2+ at higher rates when compared with primary hrHPV testing. This reinforces that incarcerated populations do not fall into average-risk populations for which current cervical cancer screening options are designed, which should be considered when performing screening in this population.

Introduction

In the United States, it is estimated that there will be 13,960 new invasive cervical cancer cases with as many as 4,310 deaths in 2023.¹ A 2019 international systematic review reported that the incidence of cervical cancer and abnormal cervical cytology was consistently higher in incarcerated populations when compared with the general population.² In the United States, even after adjusting for factors such as age, race, education level, employment status, and alcohol use, the odds of having cervical cancer have been estimated to be up to four times higher in incarcerated individuals compared with the general population.³ Known factors associated with cervical cancer include early age at first intercourse, multiple sexual partners, tobacco use, low education levels, low income, and history of other sexually transmitted infections, such as chlamydia, human herpes simplex virus-2 (HSV2), and human immunodeficiency virus (HIV).^4

–8 These risk factors are known to be concentrated among women experiencing incarceration, supporting the documented higher rates of human papillomavirus (HPV) infection, abnormal cytology, and cervical cancer in this population.^2,9,10 In addition, several barriers to appropriate cervical cancer screening and treatment may uniquely exist in this population, including higher distrust of the medical system, hesitation to participate in a pelvic exam due to history of trauma, and highly variable sentence times that may preclude the ability to follow-up on an abnormal result.^11
–13

As our understanding of the etiology of and risk factors for cervical cancer has evolved, so too have the screening guidelines. Current cervical cancer screening guidelines were updated in 2019 by the American Society for Colposcopy and Cervical Pathology (ASCCP) to reflect risk-based algorithms and endorse primary high-risk HPV (hrHPV) testing as a preferred method of testing in individuals at average risk (those without special management considerations including pregnant individuals, those younger than 25 or older than 65 years of age, immunosuppressed individuals, those without a uterus, or those at high risk for cervical cancer).¹⁴ There is paucity of data to support these guidelines for high-risk or underscreened populations.^15,16

The incarcerated population presents a unique opportunity to study cervical cancer screening in high-risk and underscreened individuals since many who are involved with the criminal legal system have experienced significant barriers to healthcare access before incarceration.^12,17,18 Although most incarcerated individuals accept, and even request, preventative health services (including cervical cancer screening) while they are incarcerated, they enter facilities as a high-risk and underscreened population.¹⁹ A systematic review demonstrated that in the United States, 66–84% of women have self-reported being up to date on cervical cancer screening, with 66–77% reporting they have had screening within the prior 3 years.¹² The strongest predictor of being up to date on screening was receiving screening during incarceration, with one study demonstrating that of the 67% of women surveyed in prison who reported cervical cancer screening within the past year, 58% reported having had screening during incarceration.²⁰ In comparison, an analysis of the 2015 National Health Interview Survey demonstrated that 81.1% of eligible women reported undergoing cervical cancer screening within the prior 3 years.²¹

The goals of this study were to evaluate the performance of current cervical cancer screening methods in people incarcerated at the North Carolina Correctional Institution for Women (NCCIW) in order to compare the proportion of cervical intraepithelial neoplasia (CIN) 2+ and CIN3+ detected by cytology-based screening, primary hrHPV screening, and combination hrHPV and cytology (co-testing) in this population.; We hypothesized that the prevalence of abnormal cytology, hrHPV, and CIN 2+/3+ is higher in the incarcerated population than in the general population.

Materials and Methods

Data source

All people over the age of 18 years who had at least one cervical cancer screening test performed during the study period were included in this analysis. Deidentified data were obtained from all cytology, hrHPV testing, and histopathology records from any cervical biopsies or excisional procedures performed on people incarcerated at the NCCIW between January 1, 2013, and December 31, 2020. People aged 18–21 years were included because screening protocols at NCCIW during the study period included performing co-testing on all entrants to the facility, irrespective of age. At the NCCIW, the protocol for the duration of the study period has been to obtain both ThinPrep liquid-based cytology and Aptima hrHPV (Hologic, Massachusetts) testing on all individuals undergoing cervical cancer screening. Pathology results were obtained from the NCCIW medical record system by the North Carolina Department of Adult Corrections (DAC), linked to corresponding demographic data including age, race, ethnicity, and county of conviction, and provided to our study team. This study was approved by the University of North Carolina Institutional Review Board and the North Carolina DAC.

Categorization of pap and biopsy results

All cytology results were reviewed by a board-certified OB/Gyn (A.C.C.) and categorized as one of the following cytology results as per current ASCCP guidelines¹⁴: normal, atypical squamous cells of undetermined significance (ASC-US), low-grade squamous intraepithelial lesion (LSIL), atypical squamous cells, cannot rule out high-grade lesion (ASC-H), LSIL, cannot rule out high-grade lesion (LSIL-H), atypical glandular cells (AGC), high-grade squamous intraepithelial lesion (HSIL), carcinoma in situ (CIS), or adenocarcinoma. Cytology results of “unsatisfactory” or “epithelial cell abnormality” without further comment were excluded from the analysis. A team of board-certified OB/Gyns (A.K.K. and A.C.C.) reviewed the results and determined the ranking of cytology result severity as follows, from least to most severe: normal, ASC-US, LSIL, ASC-H/LSIL-H, HSIL, and CIS/adenocarcinoma. We included any result of AGC as HSIL. Given the high rate of re-entry into the prison system, many subjects in our cohort had more than one cervical cancer screening result available. For this analysis, only one result was included per subject to avoid artificial overestimation of abnormal results. For any subject with an abnormal result, only the result with the highest graded severity was included. Strain-specific hrHPV testing was not consistently performed throughout the study period. Therefore, all results of hrHPV testing were collapsed into one binary (yes/no) indicator of any hrHPV-positive result. Finally, a binary indicator was created to distinguish any abnormal co-test; we categorized any Pap test with a result of normal cytology combined with negative hrHPV as “not abnormal,” whereas all other results were labeled “abnormal.”

The DAC guidelines during the study period referred any abnormal cervical cancer screening test result for further evaluation and consideration for colposcopy and/or excisional procedure during the period of incarceration. All pathology results were reviewed separately. A board-certified OB/Gyn (A.C.C.) categorized each biopsy result as one of the following: normal, CIN1, CIN 2, CIN3, and carcinoma in situ (CIS)/adenocarcinoma in situ (ACIS)/cancer. For any individual who had more than one biopsy result during the study period, only the most severe result was included in the descriptive analyses. For the purposes of analysis, we created binary indicator variables of high-grade intraepithelial lesions (CIN2+ and CIN3+). We categorized those with a biopsy diagnosis of CIN3 or cancer as CIN3+, and those with biopsy diagnoses of CIN2, CIN3, or cancer as CIN2+, consistent with other similar analyses.^15,22

Statistical analysis

Sociodemographic characteristics of our sample, including age, race, and ethnicity, as well as the results of cytology and hrHPV testing, and the proportion of included patients who had a biopsy completed during the study period were analyzed with descriptive statistics. For the remainder of our analysis, we restricted our sample to only those who had both a cervical cancer screening test result (cytology and/or hrHPV) and a biopsy performed during the study period. Due to small sample sizes, subjects of all age groups were analyzed together. Among anyone who had more than one cytology or hrHPV test during the study period, we identified the result most immediately preceding the available biopsy. Among individuals with histopathology results categorized as CIN2+ and CIN3+, we calculated the proportion of cytology, hrHPV, and co-testing results that were normal to determine the proportion of false negatives. We also calculated the proportion of abnormal cytology and positive hrHPV tests among those with biopsy diagnoses of CIN2+ and CIN3+, which we consider to be the true prevalence proportion. We determined prevalence differences (PDs) and 95% confidence intervals (CIs) by comparing the proportion of true positives (i.e., number of abnormal screening results with abnormal biopsy results) and false negatives (i.e., number of normal screening results with abnormal biopsy results) for cytology versus hrHPV results. We conducted a sensitivity analysis of our results by repeating the above analysis excluding results of AGC and adenocarcinoma. All analyses were performed using SAS 9.4 (SAS Institute, Inc., Cary, NC).

The proportion of abnormal co-test results was mapped by county of conviction in North Carolina. The incidence of any CIN2+ was also mapped by county of conviction. The map of abnormal co-test proportions and CIN2+ was created using Arc GIS Pro (ArcGIS Pro, Redlands, CA). We also conducted a post hoc exploratory analysis of any association between the North Carolina Department of commerce ranking by economic well-being²³ and the county-specific prevalence of abnormal cervical cancer screening.

Results

Study population characteristics

There were a total of 24,992 cervical cancer screening tests performed on 15,319 unique individuals incarcerated at the NCCIW from 2013 to 2021 (Table 1). Of these, 371 (2.4%) had an inconclusive result and were excluded from the analytic sample. Sociodemographic characteristics are shown in Table 1. The median age of people included in our population was 33 years old (interquartile range 27,41; full range 18, 92). Most individuals in our sample were White (69.0%) and non-Hispanic (94.1%). Individuals represented in the dataset had been convicted in each of the 100 counties in North Carolina.

Table 1.

Sociodemographic Characteristics of 15,319 Individuals Who Underwent Cytology and High-Risk HPV Testing at the North Carolina Correctional Institute for Women between 2013 and 2021

	n = 15,319 N (%)
Age (Median [IQR])	33 [27, 41]
Race
American Indian or Alaskan Native	257 (1.7)
Asian	65 (0.4)
Black	3,736 (24.4)
White	10,562 (69.0)
Other	279 (1.8)
Missing	463 (3.0)
Ethnicity
Hispanic	273 (1.8)
Non-Hispanic	14,414 (94.1)
Missing	632 (4.1)
Cytology result
Normal	12,119 (79.1)
ASC-US	1,392 (9.1)
LSIL	910 (5.9)
ASC-H or LSIL-H	219 (1.4)
AGC	56 (0.4)
HSIL	225 (1.5)
CIS	26 (0.2)
Adenocarcinoma	1 (0.0)
Missing^a	371 (2.4)
HPV testing
Positive	3,724 (24.3)
Negative	10,177 (66.4)
Missing	1,418 (9.3)
Biopsy completed during study period^b	829 (5.4)

Includes cytology results of “unsatisfactory” or “epithelial cell abnormality” without other diagnosis.

Includes 7 “insufficient” biopsy results and 18 biopsies completed without preceding Pap test in the system.

AGC, atypical glandular cells; ASC-H, atypical squamous cells, cannot rule out high-grade lesion; ASC-US, atypical squamous cells of undetermined significance; CIN, cervical intraepithelial neoplasia; CIS, carcinoma in situ; HPV, human papillomavirus; HSIL, high-grade squamous intraepithelial lesion; LSIL, low-grade squamous intraepithelial lesion; LSIL-H, low-grade squamous intraepithelial lesion, cannot rule out high-grade lesion.

Cytology and hrHPV testing results

The most common cytology result in our sample was “normal” (79.1%) (Table 1). The second most common cytology result was ASC-US (9.1%), followed by LSIL (5.9%), HSIL (1.5%), ASC-H or LSIL-H (1.4%), AGC (0.4%), CIS (0.2%), and adenocarcinoma (0%). Just under a quarter of individuals had positive hrHPV testing (24.3%), though hrHPV test results were missing for 9.3% of the individuals.

Cervical biopsy results

Of our sample, 829 (5.4%) had a histopathological specimen obtained via colposcopy and/or excisional procedure performed during the study period (Table 1). Of these, seven had “unsatisfactory” results, and 18 had no preceding cervical cancer screening test in the system. Therefore, 804 biopsies were included in our analysis of CIN2+ and CIN3+ detection. The most common biopsy result was benign (61.2%), followed by CIN1 (17.2%), CIN2 (10.3%), CIN3 (10.6%), and cancer (0.7%).

Detection of CIN2+ and CIN3+ by cervical cancer screening methods

Given that our dataset contained both preceding cytology and hrHPV testing for almost all individuals who underwent cervical biopsy or excisional procedure, we were able to determine the approximate detection of CIN2+ and CIN3+ by each individual method (Table 2). Of CIN2+ diagnoses, 95.9% were preceded by abnormal cytology results and 89.9% by positive hrHPV testing (PD 5.92, 95% CI 0.48, 11.36; p = 0.03) (Table 3). An abnormal co-test preceded a diagnosis of CIN2+ 96.5% of the time (n = 163/169). Separating the components of the preceding co-testing, the proportion of those with CIN2+ with negative preceding testing (false negatives) was 4.1% for cytology testing compared with 10.1% for hrHPV. Of those with CIN3+ results on biopsy, 96.6% had abnormal cytology results on prior Pap testing and 90.8% had positive hrHPV testing (PD 5.75, 95% CI −1.43, 12.93; p = 0.12). Of CIN3+ diagnoses, 96.6% were preceded by an abnormal co-test (n = 84/87). The false-negative rate for each component of the co-testing for CIN3+ was 3.5% for cytology testing and 9.2% for hrHPV testing. It is also interesting to note that there was a discrepant normal result in more than 1/3 of HSIL or CIS cytology results (Table 2). Direction and magnitude of effect, as well as statistical significance, were preserved when sensitivity analysis was performed excluding AGC and adenocarcinoma (data not shown).

Table 2.

Cytology and HPV Results from 804 Individuals Who Underwent Cervical Biopsies and/or Excisional Procedures among Whom Preceding Pap Test Data Was Available, Stratified by Biopsy Diagnosis of CIN2+

	<CIN2 n = 633	CIN2+ n = 171	CIN3+ n = 91	Total n = 804
	n (row %)	n (row %)	n (row %)	n
Cytology result^a
Normal	152 (95.6)	7 (4.4)	3 (1.9)	159
ASC-US	121 (89.6)	14 (10.4)	6 (4.4)	135
LSIL	253 (86.4)	40 (13.7)	11 (3.8)	293
ASC-H or LSIL-H	50 (64.9)	27 (35.1)	13 (16.9)	77
AGC	11 (55.0)	9 (45.0)	8 (40.0)	20
HSIL	41 (38.7)	65 (61.3)	40 (37.7)	106
CIS	5 (35.7)	9 (64.3)	7 (50.0)	14
HPV result^b
Positive	411 (72.9)	153 (27.1)	80 (14.2)	564
Negative	200 (91.7)	18 (8.3)	9 (4.1)	218

Missing cytology diagnosis from 3 people with CIN3+.

Missing HPV results for 22 people with a <CIN2 biopsy and 23 people with a <CIN3 biopsy.

Table 3.

False-Negative and True-Positive Rate of Cytology Testing versus High-Risk HPV Testing among Individuals with Biopsy-Proven CIN2+ and CIN3+^a

	CIN2+ n = 169	CIN3+ n = 87
	False Negatives n (%)
Normal cytology	7 (4.1)	3 (3.5)
Negative HPV testing	17 (10.1)	8 (9.2)
Prevalence difference (95% confidence interval)	−5.92 (−11.36,−0.48)	−5.75 (−12.93, 1.43)
p value	0.03	0.12
	True positives n (%)
Abnormal cytology	162 (95.9)	84 (96.6)
Positive HPV testing	152 (89.9)	79 (90.8)
Prevalence difference (95% confidence interval)	5.92 (0.48, 11.36)	5.75 (−1.43, 12.93)
p value	0.03	0.12

^aTable contains only those who have both cytology and HPV results on the Pap test immediately preceding biopsy or excisional procedure.

HPV, human papillomavirus.

Geographic distribution

The proportion of abnormal cervical cancer screening by co-testing, mapped by county of conviction of our study population, is shown in Figure 1. Abnormal co-testing was most prevalent in Cherokee (34.15%), Franklin (33.33%), and Davie (32.56%) counties and was least prevalent in Clay (0%), Richmond (1.65%), and Transylvania (4.76%) counties. The incidence of any case of CIN2+ mapped by county of conviction is also shown in Figure 1. Cross-tabulation of cases of CIN2+ by county was unable to be reported because of the risk of deductive disclosure. A diagnosis of CIN2+ was noted in 64 of 100 counties. There was no relationship between the North Carolina Department of Commerce ranking and the county-specific prevalence of abnormal cervical cancer screening (data not shown).

FIG. 1.

Proportion of abnormal co-tests by county of conviction of 15,391 individuals with cervical cancer screening results and incidence of any case of CIN2+ of 822 individuals with cervical pathology results from the North Carolina Correctional Institute for Women from 2013 to 2021.

Discussion

In our sample of people incarcerated at NCCIW from 2013 to 2021, we identified a high prevalence of both hrHPV infection and abnormal cytology. In this setting, the rate of detection of cervical pre-cancer (CIN2+) was significantly higher with cytology testing rather than primary hrHPV testing. Detection of both CIN2+ and CIN3+ by co-testing was higher than by cytology or hrHPV testing.

The prevalence of genital hrHPV among women in the United States aged 18–59 years was 20.4% based on data collected from the National Health and Nutrition Examination Survey from 2011 to 2014.²⁴ In our sample, the prevalence of hrHPV was 24.3%, consistent with prior studies reporting a higher prevalence of hrHPV infection in incarcerated populations.² In addition, in our sample, the prevalence of abnormal cytology results was 18.5%. Prior studies report the prevalence of abnormal cervical cytology in the general population to be substantially lower than this, at just 6.3% in the United States and ranging from 1.5% to 8% internationally.^25,26 Taken together, these findings provide updated evidence demonstrating higher risk of abnormal screening and hrHPV infection in an incarcerated population.

These data also indicate that incarcerated populations do not fall into the “average-risk” groups for which the cervical cancer screening guidelines were developed. A meta-analysis evaluating cervical cancer screening techniques found that individuals undergoing primary hrHPV screening had significantly higher CIN3+ detection rates than screening with cytology alone and comparable with screening with co-testing.¹⁵ Individuals who had negative hrHPV testing, regardless of cytology, had an exceptionally low risk of developing cervical cancer at 3 years (0.085%) and 5 years (0.114%) after testing.¹⁵ Of the 32 studies included in this meta-analysis, only one study was in an underscreened population, and studies in high-risk populations were excluded.¹⁵

In our study, the first of which we are aware of exploring the performance of cytology and hrHPV testing in detecting CIN 2/3 in a high-risk, underscreened, incarcerated population, cytology detected CIN2+ at a significantly increased rate when compared with hrHPV testing alone. Although the detection rate of CIN3+ by cytology was higher than with hrHPV testing, this difference was not statistically significant. These suggest that co-testing may continue to outperform primary hrHPV testing in high-risk, underscreened populations, and additional research may be needed before implementing guidelines for the general population in this setting.

Geographic disparities in cervical cancer screening, cervical dysplasia, and cancer diagnosis and mortality have been previously documented.^27,28 Several factors have been identified that may be contributing to these disparities including lower rates of HPV vaccination, decreased access to care due to lower provider or healthcare facility density, and increased rates of uninsurance.^29

–32 In North Carolina, 80 of the 100 state counties are designated as “rural” based on the North Carolina Rural Center’s analysis of county population density.³³ Of these 80 counties, 63 are designated as health professional shortage areas, and 26 do not have a gynecologist.³³ In our study, although two of the three counties with the highest prevalence of abnormal cervical cytology by county of conviction were designated as rural counties, the same was true of the three counties with the lowest prevalences. Additionally, the North Carolina Department of Commerce ranking by economic well-being²³ was not associated with the county-specific prevalence of abnormal cervical cancer screening. Although intersections between access to screening and vaccination with individual travel patterns and setting of conviction may be contributing to these findings, our data do not support that rurality or economic distress is associated with the prevalence of abnormal cervical cancer screening among people experiencing incarceration. This suggests that this population may be underscreened for a variety of reasons and may warrant special intervention. However, limitations in our dataset and study methodology meant that we could not further test for associations of geographic patterns of cervical dysplasia in North Carolina.

Our study has several strengths. To our knowledge, our data represent one of the largest single-site analyses of cervical cancer screening results among underscreened individuals in the United States. Additionally, the availability of both cytology and hrHPV testing in the majority of our population allows for head-to-head comparison of CIN 2/3 detection in an underscreened population. Finally, all cytology, hrHPV testing, and histopathological specimens included in the study were performed by a single lab (LabCorp, Burlington, NC) providing testing consistency across the duration of the study.

This analysis should be interpreted within the confines of its limitations. Owing to the nature of incarceration, including sentence time limitations and high rates of re-entry, as well as the current screening protocol indicating a co-test on every consenting person at time of entry, many individuals had several co-tests performed over the course of the study period, often more frequently or at younger ages than medically indicated. This may have affected the overall prevalence and detection rates of cervical dysplasia and hrHPV infection in this study. Although we do not have access to the rate of screening acceptance within the prison system, it is very likely that those individuals least likely to seek screening in the community would be among those to decline screening in the prison setting. Although attempting to calculate the rate of screening is outside the scope of the data used for this article, published estimates of screening acceptance of 71–94% support that the majority of individuals entering prison are likely to accept screening.^19,20,34 In addition, referral criteria for colposcopy in the prison system have varied over the course of the study. To account for this, we included the most severe cytological and pathological results for each individual to capture the prevalence of CIN 2+. Although this study represents a large sample of individuals in this population, the small number of false-negative tests in each group resulted in relatively wide CIs for the calculated PDs. Our data were obtained from the NCCIW and compiled by the NC DAC for the purpose of this study, and therefore does not represent an externally validated dataset.

We did not find statistical significance between the detection of CIN3+ by cytology versus hrHPV, although the gross detection rates approximated those of CIN2+. Given that the overall sample size in this group was approximately half of the CIN2+ group, this lack of statistical significance may represent a lack of power to detect this difference. We were also unable to conduct meaningful analyses by race and ethnicity, as it was unclear whether these classifications were assigned by staff rather than allowing individuals to self-assign. Finally, true sensitivity cannot be described from this study as only patients who had positive screening tests received biopsy evaluations and therefore any false-negative screening tests could not be identified. However, our method of evaluating CIN2+ and CIN3+ detection by hrHPV and cytology screening provides a real-world approximation of the sensitivity of these two methods and is consistent with prior studies comparing method-specific detection rates.^22,35

Conclusions

The ASCCP updated guidelines in 2019 to reflect risk-based screening strategies for cervical cancer detection. These guidelines endorse primary hrHPV testing as a reasonable alternative to traditional cytology or co-testing and were driven by data gathered from screening results in an average-risk population. Our study comparing hrHPV testing with cytology testing in the detection of advanced cervical dysplasia in a high-risk, underscreened population suggests that primary hrHPV testing may underperform when used alone in this population. As a result, policy changes regarding screening regimens in carceral facilities may be best informed by local data in the absence of national data about this population. Our findings highlight the need for continued evaluation of optimal cervical cancer screening in populations that are both high risk and substantially underscreened.

Footnotes

Data Access Statement

Research data supporting this publication are not publicly available due to the sensitive nature of this research in a protected population.

Authors’ Contributions

A.C.C.: Conceptualization, methodology, investigation, data curation, writing—original draft, writing—review and editing, and visualization; B.W.B.: conceptualization, methodology, formal analysis, data curation, writing—original draft, writing—review and editing, and visualization; C.P.: writing—original draft, and writing—review and editing; L.R.: conceptualization, methodology, writing—review and editing, and supervision, A.K.K.: conceptualization, methodology, investigation, data curation, writing—review and editing, and supervision.

Author Disclosure Statement

The authors report no conflict of interest.

Funding Information

No funding directly supported this study; however, Dr. Rahangdale received support from the National Cancer Institute (NCI) (R01 CA250850) and the Department of Health and Human Services HHSN2612012000311, and Dr. Knittel was supported by the National Institute of Child Health and Human Development (NICHD) under the University of North Carolina at Chapel Hill Women’s Reproductive Health Research Career Development Program (K12 HD103085). Ms. Bullington’s contribution was supported by a National Research Service Award (T32HD052468) and an infrastructure grant for population research (P2C HD050924) to the Carolina Population Center at the University of North Carolina at Chapel Hill.

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