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Original Contribution  |   January 2018
Variations in Progression and Regression of Precancerous Lesions of the Uterine Cervix on Cytology Testing Among Women of Different Races
Author Notes
  • From the Department of Obstetrics and Gynecology at the New York University School of Medicine in New York (Drs D. Martingano and F.X. Martingano); the Department of Clinical Research and Statistics at the New York University Langone Hospital–Brooklyn in Brooklyn (Ms Renson); the Department of Psychology at The New School for Social Research in New York, New York (Ms Martingano); and the Department of Biomedical Informatics at Rutgers University School of Health Professions in Newark, New Jersey (Dr D. Martingano). 
  • Financial Disclosures: None reported. 
  • Support: None reported. 
  •  *Address correspondence to Daniel Martingano, DO, New York University Langone Hospital, 150 55th St, Brooklyn, NY 11220-2508. Email: daniel.martingano@nyumc.org
     
Article Information
Obstetrics and Gynecology
Original Contribution   |   January 2018
Variations in Progression and Regression of Precancerous Lesions of the Uterine Cervix on Cytology Testing Among Women of Different Races
The Journal of the American Osteopathic Association, January 2018, Vol. 118, 8-18. doi:10.7556/jaoa.2018.003
The Journal of the American Osteopathic Association, January 2018, Vol. 118, 8-18. doi:10.7556/jaoa.2018.003
Abstract

Background: Although not incorporated into current cervical cancer screening guidelines, racial differences are known to persist in both occurrence of and outcomes related to cervical cancer.

Objective: To compare the differences in progression and regression of precancerous lesions of the uterine cervix on cervical cytologic analysis among women of different races who adhered to cervical cancer screening recommendations and follow-up.

Methods: Retrospective cohort study comparing differences in precancerous lesion diagnoses for patients receiving adequate evaluation according to the American Society for Colposcopy and Cervical Pathology guidelines. The authors fit Markov multistate models to estimate self-reported race-specific expected wait times and hazard ratios for each possible regression and progression and compared a race model with an intercept-only model using a likelihood ratio test.

Results: The sample included 5472 women receiving a Papanicolaou test between January 2006 and September 2016, contributing a total of 24,316 person-years of follow-up. Of 21 hazard ratios tested for significance, the following 4 hazard ratios (95% CIs) were statistically significant: atypical squamous cells of undetermined significance (ASC-US) progression to low-grade squamous intraepithelial lesion (LSIL) for Hispanic patients (0.72; 95% CI, 0.54-0.96); LSIL regression to ASC-US for Hispanic patients (1.55; 95% CI, 1.04-2.31), LSIL regression to ASC-US for Asian patients (1.91; 95% CI, 1.08-3.36), and high-grade squamous intraepithelial lesion regression to LSIL for black patients (0.39; 95% CI, 0.16-0.96). There is an observed trend that all racial groups other than white had a slower rate of progression from ASC-US to LSIL, with Hispanics having demonstrated the slowest rate from ASC-US to LSIL. Hispanics also demonstrated the fastest rate from LSIL to HSIL when compared with all other race categories. In regressions, blacks had the slowest rate of regression from HSIL to LSIL, and Asians had the fastest rate from LSIL to ASC-US. The Hispanic group demonstrated the fastest expected progression (17.6 months; 95% CI, 11.5-25.5), as well as the fastest regression (27.6 months; 95% CI, 21.5-35.6), and the black group has the slowest expected times for both progression (28.1 months; 95% CI, 14.6-47.2) and regression (49 months; 95% CI, 29.1-86.2). The number of visits (1 vs ≥2) in the study was differentially distributed both by race (P=.033) and by last diagnosis (P<.001).

Conclusion: Variations in precancerous lesions of the uterine cervix are not uniform across races.

The American Cancer Society (ACS) estimates that 12,990 women will receive a diagnosis of invasive cervical cancer, and 4120 women will have died of the disease, in 2016 in the United States.1 Cervical cancer incidence and mortality rates have declined by more than 60% since the introduction of the Papanicolaou (Pap) test in the mid-20th century, and overall rates continue to decline with the refinement and revision of screening guidelines2 and widespread application by primary care physicians and obstetricians and gynecologists. 
In 2012, the ACS, the American Society for Colposcopy and Cervical Pathology (ASCCP), and the American Society for Clinical Pathology issued joint guidelines for cervical cancer screening.3 Similar recommendations were released in 2012 by the US Preventive Services Task Force.4 The screening guidelines recommend different surveillance strategies and options based on a woman's age, screening history, other risk factors, and the choice of screening tests. However, race is not currently included in these screening guidelines, and a paucity of studies consider the ways in which race may inform cervical cancer screening strategies in the United States. Studies that have considered race in cervical cancer screening have focused mainly on access to care and follow-up for treatment rather than the pathogenesis of precancerous lesions themselves.5-7 
Although not incorporated into current guidelines, racial differences are known to persist in both the occurrence of and outcomes related to cervical cancer. In 2016, black women had a 41% greater incidence and 2 times greater mortality rate compared with white women,1 with the gap in survival increasing during the past few decades.8 These differences have in part been attributed to social and institutional factors, such as differential access to high-volume hospital centers,9 disparities in research enrollment,10 inequalities in health insurance coverage,11 and lower rate of human papillomavirus (HPV) vaccination in blacks vs whites.12 The role of biological factors in progression and regression of precancerous lesions of the cervix before reaching the stage of invasive cervical cancer, however, is not well characterized. These potential biological factors include known regional distribution of types and intratype variants of HPV,13,14 as well as an association between race and HPV coinfection rates.15 
The goal of this study was to evaluate for potential differences in the rates of progression and regression of precancerous lesions of the uterine cervix on cervical cytologic analysis among women of different races/ethnicities who received adequate adherence to cervical cancer screening recommendations by the ASCCP and follow-up within our institution on the basis of race, lesion change (progression or regression), and time to change. 
Methods
Design
This investigation was a retrospective cohort study approved by the institutional review board at NYU Lutheran Medical Center. Medical records from all patients who received screening for cervical cancer from January 2006 through September 2016 were reviewed. The period was selected based on availability from the initiation of our institution's electronic medical record (EMR) system through the study's institutional review board approval date. The following International Classification of Diseases, Ninth Revision codes were used to identify patients through the EMR: “795.03: papanicolaou smear of cervix with low grade squamous intraepithelial lesion (LSIL),” “795.04: papanicolaou smear of cervix with high grade squamous intraepithelial lesion (HSIL),” “795.02: papanicolaou smear of cervix with atypical squamous cells cannot exclude high grade squamous intraepithelial lesion (ASC-H),” and “795.01: papanicolaou smear of cervix with atypical squamous cells of undetermined significance.” 
A diagnosis of cervical intraepithelial neoplasia was given and recorded in the EMR by a primary care physician (family medicine, internal medicine, obstetrics and gynecology) and was managed by the same physician according to the ASCCP guidelines. These guidelines were used respective to the time in which the diagnosis was given; namely, patients who received a diagnosis before the release of the 2012 guidelines16 were treated according to the 2006 guidelines.17 
Patients who elected to have their precancerous lesion monitored were included in the study. Patients who received an excisional procedure of any type were excluded from the study, as this procedure would confound true regression or progression of a precancerous lesion. Because dates for excisional procedures were inconsistently recorded in the EMR, patients who had excisional procedures were excluded regardless of the purported temporal order of transitions (time to progression or regression) and procedures. Data abstracted from the patient's medical record included the date and type of diagnosis, patient age, and self-reported race. 
Variables
The primary outcomes as measured from Pap test results were (1) the expected time to progression testshowing (a) ASC-US to LSIL; and (b) the expected time to progression from LSIL to HSIL; and (2) the time to regression test showing (a) HSIL to LSIL; and (b) LSIL to ASC-US. As secondary outcomes, we examined Pap test rests of (1) progression from “atypical squamous cells cannot exclude HSIL” (ASC-H) to HSIL, and (2) regression from HSIL to ASC-H. We considered the ASC-H/HSIL pathway separately because our first goal was to describe overall expected progression and regression curves, and ASC-H does not have a clear position between ASC-US and LSIL or between LSIL and HSIL. 
Self-reported race categories were combined based on the definitions detailed by the National Institutes of Health for race reporting,18 which contain 6 minimum categories: American Indian or Alaska Native, Asian, black or African American, Hispanic or Latino, Native Hawaiian or other Pacific Islander, and white. In the remainder of this article, we use the terms Native American, Asian, black, Hispanic, Pacific Islander, and white. 
Statistical Analysis
To model the multiple status changes per patient and allow for correlation between measurements, we used a multistate Markov model19 to estimate hazard ratios and predicted times to progression from ASC-US to LSIL, LSIL to HSIL and ASC-H to HSIL; and regression from LSIL to ASC-US, HSIL to LSIL, and HSIL to ASC-H. The main model included a term for race. Because of very low patient counts for Native American, Pacific Islander, and other (including multiracial) patients, these categories were dropped from the regression model. For each patient, we added an observation on the cutoff date for data collection (the date of study approval), in which the state was marked as censored, to allow patients whose lesions had not progressed or regressed to be included in the denominator of the hazard function. No additional covariates were included in the model, as this was primarily a descriptive study and not intended to control for confounding. 
The primary hypothesis was that rates of progression and regression differ by race overall. This hypothesis was tested using a χ2 likelihood ratio test for nested models to compare the model using race with an intercept-only model. Results from the multistate model are presented as hazard ratios, 95% CIs, and expected wait times for each transition by race, along with a P value for the global hypothesis test. 
Because of the varying rate of follow-up, it was plausible for selection bias to occur if race (the exposure) and rate of progression/regression (the outcome) were both associated with likelihood of continued follow-up. To assess this possibility, we examined both the association between race and the number of follow-up visits and between the last diagnosis recorded and the number of follow-up visits. Both associations were tested using a Pearson χ2 test. Statistical significance for all tests was determined at α<.05. All statistical analyses were conducted in R version 3.3.1 for Windows,20 and multistate models were fit using the msm package for R.21 
Results
We identified 8589 potentially eligible patients, from which 954 (11.1%) were excluded because they had an excision procedure. An additional 1333 patients (17.5%) were excluded because race was not recorded in their medical record, and 830 patients (10.9%) were excluded owing to unsatisfactory Pap test results. Therefore, the analytic sample included 5472 women receiving a Pap test between January 2006 and September 2016, contributing a total of 24,316 person-years of follow-up time. Descriptive statistics are presented in Table 1 and Table 2. The mean (SD) baseline age was 34.5 (12.1) years (range, 13-91 years) for those included in the sample. The sample was racially diverse, with 2019 (36.9%) self-reporting as Hispanic, 1160 (21.2%) as black, 389 (7.1%) as Asian, and 1878 (34.3%) as white. 
Table 1.
Descriptive Statistics of Women With Precancerous Lesions of the Uterine Cervix (N=5472)
Characteristic No. (%)a
Race
Hispanic 2019 (36.9)
Black 1160 (21.2)
Asian 389 (7.1)
White 1878 (34.3)
Other 26 (0.5)
Age Baseline, Mean (SD) 34.50 (12.13)
Age Change, Mean (SD) 0.73 (2.55)
No. of Changes per Category
1 3098 (56.6)
2 1332 (24.3)
3 529 (9.7)
 ≥4 513 (9.4)
Years Follow-up, Mean (SD) 4.44 (2.16)

a Data are given as No. (%) unless otherwise indicated.

Abbreviations: ASC-H, atypical squamous cells cannot exclude high grade squamous intraepithelial lesion; ASC-US, atypical squamous cells of undetermined significance; HSIL, high-grade squamous intraepithelial lesion; LGSIL, low-grade squamous intraepithelial lesion.

Table 1.
Descriptive Statistics of Women With Precancerous Lesions of the Uterine Cervix (N=5472)
Characteristic No. (%)a
Race
Hispanic 2019 (36.9)
Black 1160 (21.2)
Asian 389 (7.1)
White 1878 (34.3)
Other 26 (0.5)
Age Baseline, Mean (SD) 34.50 (12.13)
Age Change, Mean (SD) 0.73 (2.55)
No. of Changes per Category
1 3098 (56.6)
2 1332 (24.3)
3 529 (9.7)
 ≥4 513 (9.4)
Years Follow-up, Mean (SD) 4.44 (2.16)

a Data are given as No. (%) unless otherwise indicated.

Abbreviations: ASC-H, atypical squamous cells cannot exclude high grade squamous intraepithelial lesion; ASC-US, atypical squamous cells of undetermined significance; HSIL, high-grade squamous intraepithelial lesion; LGSIL, low-grade squamous intraepithelial lesion.

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Table 2.
Distribution of All Diagnoses of Precancerous Lesions of the Uterine Cervix by Race (N=5472)a
Distribution ASC-US ASC-H LSIL HSIL
Race
 Hispanic (n=2019) 1369 (67.8) 165 (8.2) 672 (33.3) 98 (4.9)
 Black (n=1160 758 (65.3) 199 (17.2) 320 (27.6) 54 (4.7)
 Asian (n=389) 227 (58.4) 48 (12.3) 136 (35.0) 34 (8.7)
 White (n=1878) 1050 (55.9) 237 (12.6) 745 (39.7) 103 (5.5)
 Other (n=26) 16 (61.5) 2 (7.7) 9 (34.6) 1 (3.8)
Total 3420 (62.5) 651 (11.9) 1882 (34.4) 290 (5.3)

a Data are reported as No. (%).

Abbreviations: ASC-H, atypical squamous cells cannot exclude high grade squamous intraepithelial lesion; ASC-US, atypical squamous cells of undetermined significance; HSIL, high-grade squamous intraepithelial lesion; LSIL, low-grade squamous intraepithelial lesion.

Table 2.
Distribution of All Diagnoses of Precancerous Lesions of the Uterine Cervix by Race (N=5472)a
Distribution ASC-US ASC-H LSIL HSIL
Race
 Hispanic (n=2019) 1369 (67.8) 165 (8.2) 672 (33.3) 98 (4.9)
 Black (n=1160 758 (65.3) 199 (17.2) 320 (27.6) 54 (4.7)
 Asian (n=389) 227 (58.4) 48 (12.3) 136 (35.0) 34 (8.7)
 White (n=1878) 1050 (55.9) 237 (12.6) 745 (39.7) 103 (5.5)
 Other (n=26) 16 (61.5) 2 (7.7) 9 (34.6) 1 (3.8)
Total 3420 (62.5) 651 (11.9) 1882 (34.4) 290 (5.3)

a Data are reported as No. (%).

Abbreviations: ASC-H, atypical squamous cells cannot exclude high grade squamous intraepithelial lesion; ASC-US, atypical squamous cells of undetermined significance; HSIL, high-grade squamous intraepithelial lesion; LSIL, low-grade squamous intraepithelial lesion.

×
The majority of patients (3420 [62.5%]) received a diagnosis of ASC-US during follow-up; 651 (11.9%) ever had a diagnosis of ASC-H; 1882 (34.4%) ever received an LSIL diagnosis; and 290 (5.3%) ever had a diagnosis of HSIL. A total of 2374 patients (43.4%) contributed 2 or more observations to the study, meaning that the majority of patients were censored on all progressions and regressions. The distributions of changed diagnoses and person-time contributed are shown in Figure 1. Table 3 presents average times to progression or regression to and from each of the abnormal Pap test results, along with the number of patients who contributed time to each wait time estimate. 
Figure 1.
Distributions of changed precancerous cervical lesion diagnoses and person-time contributed. Abbreviations: ASC-H, atypical squamous cells cannot exclude high-grade squamous intraepithelial lesion; ASC-US, atypical squamous cells of undetermined significance; HSIL, high-grade squamous intraepithelial lesion; LSIL, low-grade squamous intraepithelial lesion.
Figure 1.
Distributions of changed precancerous cervical lesion diagnoses and person-time contributed. Abbreviations: ASC-H, atypical squamous cells cannot exclude high-grade squamous intraepithelial lesion; ASC-US, atypical squamous cells of undetermined significance; HSIL, high-grade squamous intraepithelial lesion; LSIL, low-grade squamous intraepithelial lesion.
Table 3.
Progression and Regression Times of Precancerous Lesions of the Uterine Cervix in Women of Different Races (N=5472)a
ASC-US ASC-H LSIL HSIL
ASC-US 3.8 (63) 0.8 (241) 7.0 (32)
ASC-H 0.3 (109) 1.0 (37) 6.7 (7)
LSIL 0.6 (278) 3.0 (29) 6.2 (39)
HSIL 0.9 (31) 3.4 (8) 0.4 (25)

a Data are presented as mean y (No. of patients who contributed time). Means were calculated from the multistate Markov model including race. Red indicates progression; green, regression.

Abbreviations: ASC-H, atypical squamous cells cannot exclude high grade squamous intraepithelial lesion; ASC-US, atypical squamous cells of undetermined significance; HSIL, high-grade squamous intraepithelial lesion; LSIL, low-grade squamous intraepithelial lesion.

Table 3.
Progression and Regression Times of Precancerous Lesions of the Uterine Cervix in Women of Different Races (N=5472)a
ASC-US ASC-H LSIL HSIL
ASC-US 3.8 (63) 0.8 (241) 7.0 (32)
ASC-H 0.3 (109) 1.0 (37) 6.7 (7)
LSIL 0.6 (278) 3.0 (29) 6.2 (39)
HSIL 0.9 (31) 3.4 (8) 0.4 (25)

a Data are presented as mean y (No. of patients who contributed time). Means were calculated from the multistate Markov model including race. Red indicates progression; green, regression.

Abbreviations: ASC-H, atypical squamous cells cannot exclude high grade squamous intraepithelial lesion; ASC-US, atypical squamous cells of undetermined significance; HSIL, high-grade squamous intraepithelial lesion; LSIL, low-grade squamous intraepithelial lesion.

×
Table 4 shows results of the multistate model with race as a covariate. As stated in the Methods section, Native American (n=0), Pacific Islander (n=1), and other (including multiracial) (n=25) patients, these categories were dropped from the regression model because of the very low patient counts. We tested the global hypothesis that a model including race is more informative than an intercept-only model using a Pearson χ2 likelihood ratio test for nested models. This test resulted in statistical significance (P=.004), indicating that differences in wait times by race are not entirely due to chance. 
Hazard ratios and 95% CIs are presented in Table 4 and shown in Figure 2, representing the ratio of the rate of each transition for each race group compared with the rate for the same transition in the white group. Of 21 hazard ratios tested for significance, the following 4 hazard ratios (95% CIs) were statistically significant: ASC-US to LSIL for Hispanics (0.72; 95% CI, 0.54-0.96), LSIL to ASC-US for Hispanics (1.55; 95% CI, 1.04-2.31), LSIL to ASC-US for Asians (1.91; 95% CI, 1.08-3.36), and HSIL to LSIL for blacks (0.39; 95% CI, 0.16-0.96). A trend seemed to suggest that all racial groups other than whites had a longer rate of progression from ASC-US to LSIL, with Hispanics having the slowest rate, and a shorter rate of progression from LSIL to HSIL, with Hispanics having the fastest rate. With regard to regression, blacks had the slowest rate of regression from HSIL to LSIL, and Asians had the fastest rate from LSIL to ASC-US. 
Table 4.
Multistate Markov Model for Incidence of Changed Papanicolaou Test Diagnosis by Hispanic, Black, and Asian Patients (n=5446)a
Diagnosis Transition Hispanic (n=330) Black (n=193) Asian (n=73)
Progression
ASC-US→LSIL 0.72 (0.54-0.96) 0.95 (0.68-1.34) 0.96 (0.6-1.53)
LSIL→HSIL 1.67 (0.83-3.38) 0.98 (0.44-2.16) 1.21 (0.44-3.33)
ASC-H→HSIL 5.63 (0.59-53.78) 0.47 (0.02-14.07) 1.09 (0.04-33.06)
Regression
ASC-H→ASC-US 1.33 (0.74-2.36) 1.25 (0.7-2.2) 0.66 (0.32-1.35)
LSIL→ASC-US 1.55 (1.04-2.31) 1.12 (0.59-2.11) 1.91 (1.08-3.36)
LSIL→ASC-H 0.86 (0.47-1.58) 1.77 (0.94-3.31) 1.31 (0.61-2.83)
HSIL→LSIL 1.29 (0.7-2.39) 0.39 (0.16-0.96) 0.50 (0.17-1.51)

a Data are given as hazard ratio (95% CI). Likelihood ratio test: χ221=53.73, P<.001.

Abbreviations: ASC-H, atypical squamous cells cannot exclude high grade squamous intraepithelial lesion; ASC-US, atypical squamous cells of undetermined significance; HSIL, high-grade squamous intraepithelial lesion; LSIL, low-grade squamous intraepithelial lesion.

Table 4.
Multistate Markov Model for Incidence of Changed Papanicolaou Test Diagnosis by Hispanic, Black, and Asian Patients (n=5446)a
Diagnosis Transition Hispanic (n=330) Black (n=193) Asian (n=73)
Progression
ASC-US→LSIL 0.72 (0.54-0.96) 0.95 (0.68-1.34) 0.96 (0.6-1.53)
LSIL→HSIL 1.67 (0.83-3.38) 0.98 (0.44-2.16) 1.21 (0.44-3.33)
ASC-H→HSIL 5.63 (0.59-53.78) 0.47 (0.02-14.07) 1.09 (0.04-33.06)
Regression
ASC-H→ASC-US 1.33 (0.74-2.36) 1.25 (0.7-2.2) 0.66 (0.32-1.35)
LSIL→ASC-US 1.55 (1.04-2.31) 1.12 (0.59-2.11) 1.91 (1.08-3.36)
LSIL→ASC-H 0.86 (0.47-1.58) 1.77 (0.94-3.31) 1.31 (0.61-2.83)
HSIL→LSIL 1.29 (0.7-2.39) 0.39 (0.16-0.96) 0.50 (0.17-1.51)

a Data are given as hazard ratio (95% CI). Likelihood ratio test: χ221=53.73, P<.001.

Abbreviations: ASC-H, atypical squamous cells cannot exclude high grade squamous intraepithelial lesion; ASC-US, atypical squamous cells of undetermined significance; HSIL, high-grade squamous intraepithelial lesion; LSIL, low-grade squamous intraepithelial lesion.

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Figure 2.
Hazard ratios and 95% CIs for progression and regression of precancerous lesions of the uterine cervix in women of different races. Of 21 hazard ratios tested for significance, the following 4 hazard ratios were statistically significant: ASC-US to LSIL for Hispanics (0.72; 95% CI, 0.54-0.96), LSIL to ASC-US for Hispanics (1.55; 95% CI, 1.04-2.31), HSIL to LSIL for blacks (0.39; 95% CI, 0.16-0.96), and LSIL to ASC-US for Asians (1.91; 95% CI, 1.08-3.36). Abbreviations: ASC-US, atypical squamous cells of undetermined significance; HSIL, high-grade squamous intraepithelial lesion; LSIL, low-grade squamous intraepithelial lesion.
Figure 2.
Hazard ratios and 95% CIs for progression and regression of precancerous lesions of the uterine cervix in women of different races. Of 21 hazard ratios tested for significance, the following 4 hazard ratios were statistically significant: ASC-US to LSIL for Hispanics (0.72; 95% CI, 0.54-0.96), LSIL to ASC-US for Hispanics (1.55; 95% CI, 1.04-2.31), HSIL to LSIL for blacks (0.39; 95% CI, 0.16-0.96), and LSIL to ASC-US for Asians (1.91; 95% CI, 1.08-3.36). Abbreviations: ASC-US, atypical squamous cells of undetermined significance; HSIL, high-grade squamous intraepithelial lesion; LSIL, low-grade squamous intraepithelial lesion.
Figure 3 plots expected times to progression and regression by racial group, making it possible to interpret overall time from ASC-US to HSIL and vice versa. The Hispanic group demonstrated the fastest progression (expectation, 17.6 months; 95% CI, 11.5-25.5), as well as the fastest regression (expectation, 27.6 months; 95% CI, 21.5-35.6). The black group had the slowest expected times for both progression (expectation, 28.1 months; 95% CI, 14.6-47.2) and regression (expectation, 49 months; 95% CI, 29.1-86.2). 
Figure 3.
Expected times to (A) progression and (B) regression of precancerous cervical lesion diagnoses by racial group. The Hispanic group demonstrated the fastest expected progression (17.6 months; 95% CI, 11.5-25.5), as well as the fastest regression (27.6 months; 95% CI, 21.5-35.6), and the black group has the slowest expected times for both progression (28.1 months; 95% CI, 14.6-47.2) and regression (49 months; 95% CI, 29.1-86.2). Abbreviations: ASC-US, atypical squamous cells of undetermined significance; HSIL, high-grade squamous intraepithelial lesion; LSIL, low-grade squamous intraepithelial lesion.
Figure 3.
Expected times to (A) progression and (B) regression of precancerous cervical lesion diagnoses by racial group. The Hispanic group demonstrated the fastest expected progression (17.6 months; 95% CI, 11.5-25.5), as well as the fastest regression (27.6 months; 95% CI, 21.5-35.6), and the black group has the slowest expected times for both progression (28.1 months; 95% CI, 14.6-47.2) and regression (49 months; 95% CI, 29.1-86.2). Abbreviations: ASC-US, atypical squamous cells of undetermined significance; HSIL, high-grade squamous intraepithelial lesion; LSIL, low-grade squamous intraepithelial lesion.
In Table 5, results are presented for the assessment of selection bias. The number of visits (1 vs ≥2) contributed to the study was differentially distributed both by race (P=.033) and by last diagnosis (P<.001). Patients whose last diagnosis was ASC-H were much more likely to have contributed only 1 visit. Patients whose records lacked information on race (17.9% of the collected sample) were also more likely to have contributed only 1 visit than patients with other last diagnoses (70% vs 52%-60%). 
Table 5.
Distribution of Follow-up Visits by Race and Last Diagnosis
Follow-up Visits, No. (%)
Category 1 2 P Value
Race .019
Hispanic 1113 (55.1) 906 (44.9)
Black 658 (56.7) 502 (43.3)
Asian 201 (51.7) 188 (48.3)
White 1108 (59) 770 (41)
Other 18 (69.2) 8 (30.8)
Last Diagnosis <.001
ASC-US 1854 (58.6) 1309 (41.4)
ASC-H 369 (73.4) 134 (26.6)
LSIL 770 (48.8) 808 (51.2)
HSIL 105 (46.1) 123 (53.9)

Abbreviations: ASC-H, atypical squamous cells cannot exclude high grade squamous intraepithelial lesion; ASC-US, atypical squamous cells of undetermined significance; HSIL, high-grade squamous intraepithelial lesion; LSIL, low-grade squamous intraepithelial lesion.

Table 5.
Distribution of Follow-up Visits by Race and Last Diagnosis
Follow-up Visits, No. (%)
Category 1 2 P Value
Race .019
Hispanic 1113 (55.1) 906 (44.9)
Black 658 (56.7) 502 (43.3)
Asian 201 (51.7) 188 (48.3)
White 1108 (59) 770 (41)
Other 18 (69.2) 8 (30.8)
Last Diagnosis <.001
ASC-US 1854 (58.6) 1309 (41.4)
ASC-H 369 (73.4) 134 (26.6)
LSIL 770 (48.8) 808 (51.2)
HSIL 105 (46.1) 123 (53.9)

Abbreviations: ASC-H, atypical squamous cells cannot exclude high grade squamous intraepithelial lesion; ASC-US, atypical squamous cells of undetermined significance; HSIL, high-grade squamous intraepithelial lesion; LSIL, low-grade squamous intraepithelial lesion.

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Discussion
Although racial differences in cervical cancer and related mortality have been consistently observed, no study, to our knowledge, has examined the variation in progression and regression of precancerous lesions of the uterine cervix on cervical cytology testing among patients of different races who received consistent and adequate follow-up care according to current ASCCP guidelines. 
The current study found that in a 10-year sample of patients, the rates of progression and regression of precancerous lesions of the uterine cervix were not uniform across races. We also thoroughly reviewed the studies used to revise the 2006 ASCCP consensus guidelines and create the 2012 guidelines for the management of abnormal cervical cancer screening test results and cancer precursors.22-35 These studies included comments about the demographics of the populations studied; however, they did not evaluate specific differences in race. 
Invasive cervical carcinoma has been found to be nearly twice as common in blacks as in whites, with age-adjusted rates of 14.8 per 100,000 and 7.8 per 100,000, respectively.32 Studies that have examined racial differences in cervical cancer–related mortality have found that an appreciable portion of the difference can be attributed to factors related to access to health care.36 However, because the patients in the current study all had access to health care and adequate follow-up, our results suggest that differences in the incidence of invasive cervical carcinoma between blacks and whites cannot be solely due to health care disparities but instead may represent potential biological factors as the root of this observed variation. 
A possible biological explanation is the differences in the distribution of types and intratype variants of HPV. Yamada et al13 examined intratype HPV-16 sequence variation in tumor samples that were collected and analyzed in an international study of invasive cervical cancer that involved 22 countries in 5 continents. Based on E6 hybridization patterns, most of the variants from European and North American samples were phylogenetically classified as European prototype, and samples from Africa contained primarily African 1 or African 2 variants. The majority of Asian variants were observed in Southeast Asia, and almost all Hispanic variants were from Central and South America or Spain. Although this study13 did not report direct correlations to the behavior of precancerous lesions caused by these variants, it established a foundation for the existence of HPV variations that lead to cervical cancer and gives credence to the plausibility that HPV and resultant precancerous lesions of the uterine cervix may behave differently among various ethnicities. 
In addition to the type of HPV strain that leads to cervical intraepithelial neoplasia, an important risk factor for cervical cancer is coinfection with more than 1 type of HPV: an important association has been found between the number of viral types at the site of infection and the severity of the cervical intraepithelial neoplasia.37 Furthermore, Soto-De Leon et al15 demonstrated that race may be a factor in HPV coinfection: the authors examined cervical samples by Pap test and DNA PCR from 1810 women with diverse sociocultural backgrounds and showed that different ethnicities demonstrated higher multiple-strain HPV coinfection rates. 
Although the exact cause is not known, the lack of uniformity in precancerous lesion behavior across different races/ethnicities in the current study may affect how these groups should be respectively screened and treated. Such differences represent an important site of intervention and should be incorporated into screening guidelines to maximize the benefit over the risks of excisional procedures in the prevention of cervical cancer once further studies solidify these differences. Given that our results demonstrate, for example, that blacks have the slowest expected times for both progression and regression of precancerous lesions, it may be acceptable to choose observation or excision for persistent precancerous lesions in cases in which the decision for observation vs excision is equivocal. 
Limitations
This study had several limitations. Strengths of the current study include a racially diverse sample with sufficient power to detect relatively subtle differences across race, which is attributable to both a fairly large sample and extended follow-up time. Because of the varying rate of follow-up in the study, it was plausible that selection bias could have been responsible for the observed associations. We assessed this possibility by examining the associations of race and last diagnosis with number of visits contributed to the study (1 vs ≥2). We found that the number of visits was associated with both variables, indicating that selection bias could have influenced the observed association. 
Patients whose last diagnosis was ASC-H were much more likely to have only 1 visit, and treatment rather than observation is recommended in these cases. Patients whose medical record lacked lesion transition information were much more likely to have had only 1 visit than were patients with other diagnoses. This factor may indicate that patients with less information available were less likely to be involved in care and may have represented a higher-risk category that was therefore underrepresented in the study. Because we considered each patient to have person time from their first recorded Pap test result to the end of the study, it is possible that losses to follow-up representing higher-risk patients could have caused overestimates of the expected transition times that may have been patterned by race. Therefore, our results may not be generalizable to all patients and will need to be confirmed in prospective studies that can make specific efforts to reduce loss to follow-up. 
The current study included all diagnoses of ASC-US, both HPV+ and HPV−. Although ASC-US itself is not necessarily representative of a precancerous lesion of the cervix without concurrent HPV positivity, its addition was favored given that ASC-US is involved in the initial cervical cancer screening pathway designated by the most recent ASCCP guidelines.16 The guidelines state that ASC-US is the most common cytologic abnormality and carries the lowest risk of CIN 3+ given that one-third to two-thirds are not associated with HPV. Although a low risk is associated with ASC-US, it is still involved in the screening algorithm, HPV-associated or not, and thus its dynamics across races is of interest and of potential clinical utility. 
Conclusion
Our study findings indicate that the dynamics of precancerous intraepithelial lesions of the cervix are likely to be patterned by race. However, for these observations to be incorporated into clinical screening guidelines, higher-powered, prospective studies are needed to generate reliable and biologically meaningful race-specific estimates of progression and regression probabilities. More studies are required to make definitive claims about variations of these lesions among races, which ultimately will be incorporated into screening guidelines to ensure that women do not receive unnecessary excisional procedures or inadequate treatment leading to a diagnosis of invasive cervical cancer. 
Author Contributions
All authors provided substantial contributions to conception and design, acquisition of data, or analysis and interpretation of data; Dr D. Martingano and Ms Renson drafted the article or revised it critically for important intellectual content; all authors gave final approval of the version of the article to be published; and all authors agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. 
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Figure 1.
Distributions of changed precancerous cervical lesion diagnoses and person-time contributed. Abbreviations: ASC-H, atypical squamous cells cannot exclude high-grade squamous intraepithelial lesion; ASC-US, atypical squamous cells of undetermined significance; HSIL, high-grade squamous intraepithelial lesion; LSIL, low-grade squamous intraepithelial lesion.
Figure 1.
Distributions of changed precancerous cervical lesion diagnoses and person-time contributed. Abbreviations: ASC-H, atypical squamous cells cannot exclude high-grade squamous intraepithelial lesion; ASC-US, atypical squamous cells of undetermined significance; HSIL, high-grade squamous intraepithelial lesion; LSIL, low-grade squamous intraepithelial lesion.
Figure 2.
Hazard ratios and 95% CIs for progression and regression of precancerous lesions of the uterine cervix in women of different races. Of 21 hazard ratios tested for significance, the following 4 hazard ratios were statistically significant: ASC-US to LSIL for Hispanics (0.72; 95% CI, 0.54-0.96), LSIL to ASC-US for Hispanics (1.55; 95% CI, 1.04-2.31), HSIL to LSIL for blacks (0.39; 95% CI, 0.16-0.96), and LSIL to ASC-US for Asians (1.91; 95% CI, 1.08-3.36). Abbreviations: ASC-US, atypical squamous cells of undetermined significance; HSIL, high-grade squamous intraepithelial lesion; LSIL, low-grade squamous intraepithelial lesion.
Figure 2.
Hazard ratios and 95% CIs for progression and regression of precancerous lesions of the uterine cervix in women of different races. Of 21 hazard ratios tested for significance, the following 4 hazard ratios were statistically significant: ASC-US to LSIL for Hispanics (0.72; 95% CI, 0.54-0.96), LSIL to ASC-US for Hispanics (1.55; 95% CI, 1.04-2.31), HSIL to LSIL for blacks (0.39; 95% CI, 0.16-0.96), and LSIL to ASC-US for Asians (1.91; 95% CI, 1.08-3.36). Abbreviations: ASC-US, atypical squamous cells of undetermined significance; HSIL, high-grade squamous intraepithelial lesion; LSIL, low-grade squamous intraepithelial lesion.
Figure 3.
Expected times to (A) progression and (B) regression of precancerous cervical lesion diagnoses by racial group. The Hispanic group demonstrated the fastest expected progression (17.6 months; 95% CI, 11.5-25.5), as well as the fastest regression (27.6 months; 95% CI, 21.5-35.6), and the black group has the slowest expected times for both progression (28.1 months; 95% CI, 14.6-47.2) and regression (49 months; 95% CI, 29.1-86.2). Abbreviations: ASC-US, atypical squamous cells of undetermined significance; HSIL, high-grade squamous intraepithelial lesion; LSIL, low-grade squamous intraepithelial lesion.
Figure 3.
Expected times to (A) progression and (B) regression of precancerous cervical lesion diagnoses by racial group. The Hispanic group demonstrated the fastest expected progression (17.6 months; 95% CI, 11.5-25.5), as well as the fastest regression (27.6 months; 95% CI, 21.5-35.6), and the black group has the slowest expected times for both progression (28.1 months; 95% CI, 14.6-47.2) and regression (49 months; 95% CI, 29.1-86.2). Abbreviations: ASC-US, atypical squamous cells of undetermined significance; HSIL, high-grade squamous intraepithelial lesion; LSIL, low-grade squamous intraepithelial lesion.
Table 1.
Descriptive Statistics of Women With Precancerous Lesions of the Uterine Cervix (N=5472)
Characteristic No. (%)a
Race
Hispanic 2019 (36.9)
Black 1160 (21.2)
Asian 389 (7.1)
White 1878 (34.3)
Other 26 (0.5)
Age Baseline, Mean (SD) 34.50 (12.13)
Age Change, Mean (SD) 0.73 (2.55)
No. of Changes per Category
1 3098 (56.6)
2 1332 (24.3)
3 529 (9.7)
 ≥4 513 (9.4)
Years Follow-up, Mean (SD) 4.44 (2.16)

a Data are given as No. (%) unless otherwise indicated.

Abbreviations: ASC-H, atypical squamous cells cannot exclude high grade squamous intraepithelial lesion; ASC-US, atypical squamous cells of undetermined significance; HSIL, high-grade squamous intraepithelial lesion; LGSIL, low-grade squamous intraepithelial lesion.

Table 1.
Descriptive Statistics of Women With Precancerous Lesions of the Uterine Cervix (N=5472)
Characteristic No. (%)a
Race
Hispanic 2019 (36.9)
Black 1160 (21.2)
Asian 389 (7.1)
White 1878 (34.3)
Other 26 (0.5)
Age Baseline, Mean (SD) 34.50 (12.13)
Age Change, Mean (SD) 0.73 (2.55)
No. of Changes per Category
1 3098 (56.6)
2 1332 (24.3)
3 529 (9.7)
 ≥4 513 (9.4)
Years Follow-up, Mean (SD) 4.44 (2.16)

a Data are given as No. (%) unless otherwise indicated.

Abbreviations: ASC-H, atypical squamous cells cannot exclude high grade squamous intraepithelial lesion; ASC-US, atypical squamous cells of undetermined significance; HSIL, high-grade squamous intraepithelial lesion; LGSIL, low-grade squamous intraepithelial lesion.

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Table 2.
Distribution of All Diagnoses of Precancerous Lesions of the Uterine Cervix by Race (N=5472)a
Distribution ASC-US ASC-H LSIL HSIL
Race
 Hispanic (n=2019) 1369 (67.8) 165 (8.2) 672 (33.3) 98 (4.9)
 Black (n=1160 758 (65.3) 199 (17.2) 320 (27.6) 54 (4.7)
 Asian (n=389) 227 (58.4) 48 (12.3) 136 (35.0) 34 (8.7)
 White (n=1878) 1050 (55.9) 237 (12.6) 745 (39.7) 103 (5.5)
 Other (n=26) 16 (61.5) 2 (7.7) 9 (34.6) 1 (3.8)
Total 3420 (62.5) 651 (11.9) 1882 (34.4) 290 (5.3)

a Data are reported as No. (%).

Abbreviations: ASC-H, atypical squamous cells cannot exclude high grade squamous intraepithelial lesion; ASC-US, atypical squamous cells of undetermined significance; HSIL, high-grade squamous intraepithelial lesion; LSIL, low-grade squamous intraepithelial lesion.

Table 2.
Distribution of All Diagnoses of Precancerous Lesions of the Uterine Cervix by Race (N=5472)a
Distribution ASC-US ASC-H LSIL HSIL
Race
 Hispanic (n=2019) 1369 (67.8) 165 (8.2) 672 (33.3) 98 (4.9)
 Black (n=1160 758 (65.3) 199 (17.2) 320 (27.6) 54 (4.7)
 Asian (n=389) 227 (58.4) 48 (12.3) 136 (35.0) 34 (8.7)
 White (n=1878) 1050 (55.9) 237 (12.6) 745 (39.7) 103 (5.5)
 Other (n=26) 16 (61.5) 2 (7.7) 9 (34.6) 1 (3.8)
Total 3420 (62.5) 651 (11.9) 1882 (34.4) 290 (5.3)

a Data are reported as No. (%).

Abbreviations: ASC-H, atypical squamous cells cannot exclude high grade squamous intraepithelial lesion; ASC-US, atypical squamous cells of undetermined significance; HSIL, high-grade squamous intraepithelial lesion; LSIL, low-grade squamous intraepithelial lesion.

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Table 3.
Progression and Regression Times of Precancerous Lesions of the Uterine Cervix in Women of Different Races (N=5472)a
ASC-US ASC-H LSIL HSIL
ASC-US 3.8 (63) 0.8 (241) 7.0 (32)
ASC-H 0.3 (109) 1.0 (37) 6.7 (7)
LSIL 0.6 (278) 3.0 (29) 6.2 (39)
HSIL 0.9 (31) 3.4 (8) 0.4 (25)

a Data are presented as mean y (No. of patients who contributed time). Means were calculated from the multistate Markov model including race. Red indicates progression; green, regression.

Abbreviations: ASC-H, atypical squamous cells cannot exclude high grade squamous intraepithelial lesion; ASC-US, atypical squamous cells of undetermined significance; HSIL, high-grade squamous intraepithelial lesion; LSIL, low-grade squamous intraepithelial lesion.

Table 3.
Progression and Regression Times of Precancerous Lesions of the Uterine Cervix in Women of Different Races (N=5472)a
ASC-US ASC-H LSIL HSIL
ASC-US 3.8 (63) 0.8 (241) 7.0 (32)
ASC-H 0.3 (109) 1.0 (37) 6.7 (7)
LSIL 0.6 (278) 3.0 (29) 6.2 (39)
HSIL 0.9 (31) 3.4 (8) 0.4 (25)

a Data are presented as mean y (No. of patients who contributed time). Means were calculated from the multistate Markov model including race. Red indicates progression; green, regression.

Abbreviations: ASC-H, atypical squamous cells cannot exclude high grade squamous intraepithelial lesion; ASC-US, atypical squamous cells of undetermined significance; HSIL, high-grade squamous intraepithelial lesion; LSIL, low-grade squamous intraepithelial lesion.

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Table 4.
Multistate Markov Model for Incidence of Changed Papanicolaou Test Diagnosis by Hispanic, Black, and Asian Patients (n=5446)a
Diagnosis Transition Hispanic (n=330) Black (n=193) Asian (n=73)
Progression
ASC-US→LSIL 0.72 (0.54-0.96) 0.95 (0.68-1.34) 0.96 (0.6-1.53)
LSIL→HSIL 1.67 (0.83-3.38) 0.98 (0.44-2.16) 1.21 (0.44-3.33)
ASC-H→HSIL 5.63 (0.59-53.78) 0.47 (0.02-14.07) 1.09 (0.04-33.06)
Regression
ASC-H→ASC-US 1.33 (0.74-2.36) 1.25 (0.7-2.2) 0.66 (0.32-1.35)
LSIL→ASC-US 1.55 (1.04-2.31) 1.12 (0.59-2.11) 1.91 (1.08-3.36)
LSIL→ASC-H 0.86 (0.47-1.58) 1.77 (0.94-3.31) 1.31 (0.61-2.83)
HSIL→LSIL 1.29 (0.7-2.39) 0.39 (0.16-0.96) 0.50 (0.17-1.51)

a Data are given as hazard ratio (95% CI). Likelihood ratio test: χ221=53.73, P<.001.

Abbreviations: ASC-H, atypical squamous cells cannot exclude high grade squamous intraepithelial lesion; ASC-US, atypical squamous cells of undetermined significance; HSIL, high-grade squamous intraepithelial lesion; LSIL, low-grade squamous intraepithelial lesion.

Table 4.
Multistate Markov Model for Incidence of Changed Papanicolaou Test Diagnosis by Hispanic, Black, and Asian Patients (n=5446)a
Diagnosis Transition Hispanic (n=330) Black (n=193) Asian (n=73)
Progression
ASC-US→LSIL 0.72 (0.54-0.96) 0.95 (0.68-1.34) 0.96 (0.6-1.53)
LSIL→HSIL 1.67 (0.83-3.38) 0.98 (0.44-2.16) 1.21 (0.44-3.33)
ASC-H→HSIL 5.63 (0.59-53.78) 0.47 (0.02-14.07) 1.09 (0.04-33.06)
Regression
ASC-H→ASC-US 1.33 (0.74-2.36) 1.25 (0.7-2.2) 0.66 (0.32-1.35)
LSIL→ASC-US 1.55 (1.04-2.31) 1.12 (0.59-2.11) 1.91 (1.08-3.36)
LSIL→ASC-H 0.86 (0.47-1.58) 1.77 (0.94-3.31) 1.31 (0.61-2.83)
HSIL→LSIL 1.29 (0.7-2.39) 0.39 (0.16-0.96) 0.50 (0.17-1.51)

a Data are given as hazard ratio (95% CI). Likelihood ratio test: χ221=53.73, P<.001.

Abbreviations: ASC-H, atypical squamous cells cannot exclude high grade squamous intraepithelial lesion; ASC-US, atypical squamous cells of undetermined significance; HSIL, high-grade squamous intraepithelial lesion; LSIL, low-grade squamous intraepithelial lesion.

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Table 5.
Distribution of Follow-up Visits by Race and Last Diagnosis
Follow-up Visits, No. (%)
Category 1 2 P Value
Race .019
Hispanic 1113 (55.1) 906 (44.9)
Black 658 (56.7) 502 (43.3)
Asian 201 (51.7) 188 (48.3)
White 1108 (59) 770 (41)
Other 18 (69.2) 8 (30.8)
Last Diagnosis <.001
ASC-US 1854 (58.6) 1309 (41.4)
ASC-H 369 (73.4) 134 (26.6)
LSIL 770 (48.8) 808 (51.2)
HSIL 105 (46.1) 123 (53.9)

Abbreviations: ASC-H, atypical squamous cells cannot exclude high grade squamous intraepithelial lesion; ASC-US, atypical squamous cells of undetermined significance; HSIL, high-grade squamous intraepithelial lesion; LSIL, low-grade squamous intraepithelial lesion.

Table 5.
Distribution of Follow-up Visits by Race and Last Diagnosis
Follow-up Visits, No. (%)
Category 1 2 P Value
Race .019
Hispanic 1113 (55.1) 906 (44.9)
Black 658 (56.7) 502 (43.3)
Asian 201 (51.7) 188 (48.3)
White 1108 (59) 770 (41)
Other 18 (69.2) 8 (30.8)
Last Diagnosis <.001
ASC-US 1854 (58.6) 1309 (41.4)
ASC-H 369 (73.4) 134 (26.6)
LSIL 770 (48.8) 808 (51.2)
HSIL 105 (46.1) 123 (53.9)

Abbreviations: ASC-H, atypical squamous cells cannot exclude high grade squamous intraepithelial lesion; ASC-US, atypical squamous cells of undetermined significance; HSIL, high-grade squamous intraepithelial lesion; LSIL, low-grade squamous intraepithelial lesion.

×