In 2012, the American Society for Colposcopy and Cervical Pathology (ASCCP), American Society for Clinical Pathology, American Cancer Society, and the U.S. Preventive Services Task Force published unified cervical cancer screening guidelines that sought to minimize the harms of overscreening while maintaining adequate detection of treatable cervical cancer precursors.1,2 The guidelines recommended against screening in average-risk women younger than 21 years and older than 65 years of age provided adequate previous screening and no history of high-grade dysplasia in the past 20 years and posthysterectomy with the cervix removed and no history of high-grade dysplasia in the past 20 years. For women for whom screening is still recommended, the guidelines lengthened the screening interval for all age groups (Table 1). These guidelines were developed based on an extensive systematic evidence review and were endorsed by the American College of Obstetricians and Gynecologists3 with subsequent updates published by the American College of Obstetricians and Gynecologists in 2016.4
Although cervical cancer screening guidelines have recommended against screening in women posthysterectomy and age older than 65 years since 2003 and against screening in women younger than 21 years since 2009, survey studies have shown that a majority of women younger than age 21 years, older than age 65 years, and posthysterectomy continue to undergo cytology screening.5,6 Although these self-reported high rates of continued screening are concerning, health care provider and patient surveys are only a proxy for true practice patterns. This study was performed to obtain a more objective measure of the rates of nonindicated cervical cancer screening at the extremes of age and posthysterectomy. The primary objective of this study was to determine the guideline-nonindicated screening Pap test rates in women younger than age 21 years, older than age 65 years, or posthysterectomy in a single large health system. The secondary objectives of this study were to describe patient and health care provider characteristics associated with performance of a nonindicated Pap test in populations for whom the guidelines recommend against screening and to describe temporal trends during the study period.
MATERIALS AND METHODS
This retrospective cross-sectional study was approved by the University of Minnesota institutional review board. The electronic health record was queried using Current Procedural Terminology codes for all Pap tests performed between September 1, 2012 (6 months after publication of the ASCCP, American Society for Clinical Pathology, and American Cancer Society guidelines) and August 31, 2014, within University of Minnesota Physicians and Fairview Health Services, a large nonprofit health center in Minnesota, which partners with 2,500 physicians and has more than 40 primary care clinics.7 The health system includes academic and community clinics in urban, suburban, and rural locations. The data set included the following information: 1) patient demographics: patient age at the time of Pap test and patient race; 2) encounter information: clinic location and specialty; and 3) health care provider information: health care provider name and degree (medical doctor or doctor of osteopathy, nurse practitioner, physician assistant, certified nurse-midwife, other). The data set was then further queried to identify the three following groups of patients: 1) younger than 21 years of age; 2) older than 65 years of age; and 3) posthysterectomy. For patients undergoing more than one Pap test during the study period, only the first Pap test was included in the data analysis. A random number generator (www.randomizer.org/form.htm) was used to randomly select 30% of charts within each of the three screening groups for a manual chart review. For each group, if greater than 10% of reviewed Pap tests were categorized as indicated based on patient risk factors, previous Pap test results, or both, all charts in that group were manually reviewed.
For the manual chart reviews and encounter notes, previous Pap and human papillomavirus (HPV) test results and patient medical and surgical histories were reviewed to determine the indication for the Pap test. For the younger than 21 years group, indicated reasons for Pap testing included: 1) immunosuppression, including transplant clearance; 2) follow-up of a previous abnormal Pap test result; and 3) age 21 years within 6 months of the Pap test. Although screening women aged 20.5 years is not specifically indicated by the guidelines, we assumed that health care providers were providing necessary preventive health care as a result of worry that these women may not return to clinic for several years, and thus these Pap tests were analyzed as indicated. For the older than 65 years group, indicated reasons for screening included: 1) history of high-grade dysplasia within the past 20 years; 2) inadequate previous screening (adequate previous screening defined per the guidelines as at least three documented Pap tests with normal results or two cotests with normal results within the past 10 years, with at least one test within 5 years of age 65 years); 3) immunosuppression; 4) in utero diethylstilbestrol exposure; and 5) cancer surveillance (cervical, vulvar, vaginal, anal, endometrial, ovarian cancer surveillance). For the posthysterectomy group, indicated screening included: 1) supracervical hysterectomy (a supracervical hysterectomy was assumed unless removal of the cervix was documented in the surgical history, clinic, or operative notes or vaginal cytology was specified on the Pap test order); 2) a history of high-grade dysplasia within the past 20 years; 3) immunosuppression; 4) diethylstilbestrol exposure; and 5) cancer surveillance. Although vaginal cytology is no longer recommended for endometrial cancer surveillance, it was not removed from the National Comprehensive Cancer Network surveillance guidelines until 2015 and thus was categorized as indicated for the study period. During the study period, national cancer surveillance guidelines did not recommend vaginal cytology for ovarian cancer surveillance; however, because this was recommended by most of the local gynecologic oncologists during the study period, Pap tests performed for this reason were coded as indicated. For encounter notes detailing the reason for cervical cancer screening, the stated reason was used as the indication unless a more guideline-adherent reason also existed. For example, if the clinic note documented that screening was performed in a woman older than 65 years per patient request but review of her laboratory test results and previous clinic notes did not document three normal Pap test results within 10 years, inadequate previous screening was listed as the indication for screening. For women younger than 21 years of age who were presenting for prenatal care or their postpartum visit with no other indicated reason for Pap testing, “pregnancy” was listed as the reason for screening unless the patient was within 6 months of her 21st birthday. For charts in which the reason for Pap testing was not stated and an indicated reason was not discovered during chart review, “routine health maintenance” was assigned by the investigators as the indication for screening (Fig. 1).
Health care provider information, including gender and birth date to calculate age in 2012, was obtained from the Minnesota Board of Medical Practice for physicians and physician assistants and from the Minnesota Board of Nursing for nurse practitioners and certified nurse-midwives. The zip codes for the clinics were documented, and clinic locations were dichotomized as less than or greater than 60 miles from Minneapolis to serve as a surrogate for urban or suburban (less than 60 miles) or rural (greater than 60 miles) clinics.
The primary objective of the study was to determine the proportion of nonindicated screening Pap tests performed in women younger than 21 and older than 65 years of age and posthysterectomy. The secondary objectives were to describe patient and health care provider characteristics associated with screening in populations for whom the guidelines recommend against screening and to describe temporal trends during the study period. Point estimates and exact 95% confidence intervals (CIs) for the proportion of nonindicated Pap tests were calculated for each screening group. Differences in the proportion of nonindicated Pap tests were compared within each screening scenario by patient race and year of test using χ2 tests and age using Wilcoxon rank-sum tests. Descriptive statistics for health care provider-level data were calculated, and adherence to guidelines by health care provider-level characteristics, including age, gender, degree, specialty, clinic location, and frequency of Pap test orders (dichotomized as less than one Pap test per week or more than one Pap test per week), was compared using general estimating equation models to account for repeated measures for some health care providers assuming an exchangeable correlation structure. Multivariate models were considered for each screening group including both patient and health care provider-level characteristics identified as potentially relevant based on the univariate analyses, including variables with P<.10. Data were analyzed using SAS 9.4, and P<.05 was considered statistically significant.
Between September 1, 2012, and August 31, 2014, a total of 122,254 Pap tests were performed in 77,899 individual patients within the health system. Pap tests were performed in a total of 3,920 women younger than 21 years and older than 65 years and posthysterectomy (5% of the total population). During this time period, cotesting was not uniformly performed, but reflex HPV testing was performed as indicated per the ASCCP Management guidelines8; primary HPV testing was not performed during the study period. In the review of a random sample of 30% of the charts in each age group, 31% (n=62) in the younger than 21 years, 51% (n=207) in the older than 65 years, and 48% (n=506) in the posthysterectomy group were guideline-indicated Pap tests. Therefore, all charts within each group were manually reviewed.
A total of 509 women younger than age 21 years (1% of all patients) underwent at least one Pap test during the study period. Of those, 257 (50.5%; 95% CI 46.1–54.9%) of these Pap tests were not indicated per the 2012 guidelines; if patients within 6 months of their 21st birthdays had been coded as not indicated, 94% of Pap tests in this age group would have been nonindicated. The reasons for the nonindicated tests included routine health maintenance (66%), pregnancy (27%), and patient request (7%). A majority of indicated Pap tests were performed in women who were within 6 months of their 21st birthdays (89%), with a smaller number done to follow up abnormal results from Pap test performed before 2012 (8%), as a result of immunocompromised status or transplant clearance (3%), or as a requirement to enroll in the military (0.4%). There was a difference in median age between those for whom screening was indicated compared with those for whom screening was not indicated (P<.001), likely as a result of inclusion of all women within 6 months of their 21st birthdays as indicated (Table 2). Patients in this age group were seen by 219 health care providers; the median number of patients seen by each health care provider was one (range 1–19). Health care providers performing nonindicated Pap tests were more likely to be older (P=.01), male (P<.001), and to perform Pap tests less than once per week (P=.002). Compared with physicians, nurse practitioners (P=.05) and physician assistants (P=.003) were less likely to perform nonindicated Pap tests. However, in multivariate analysis, performing Pap tests only less than once per week remained significant (P=.003) (Table 2).
A total of 1,327 women older than age 65 years (2% of all patients) underwent at least one Pap test during the study period. Of these, 536 (40.4%; 95% CI 37.7–43.1%) were not indicated. The most common reason for nonindicated Pap tests was routine health maintenance (88%). Other reasons for nonindicated Pap tests were patient request (7%), follow-up of previous abnormal Pap test results for which the guidelines do not recommend follow-up (eg, follow-up of an atypical squamous cells, cannot excluded high-grade squamous intraepithelial lesions Pap test 10 years prior with subsequent normal Pap test results; 5%), and history of high-grade cervical dysplasia more than 20 years prior with subsequent normal screening result (0.6%). The most common reasons for indicated cervical cancer screening in this age group were inadequate previous screening (56%) followed by guideline-adherent follow-up of an abnormal cervical cancer screening test result (18%). Other reasons for indicated Pap testing were cancer surveillance (11%), evaluation of postmenopausal bleeding or abnormal examination findings (10%), high-grade dysplasia within the past 20 years (3%), immunocompromised state or transplant clearance (1%), diethylstilbestrol exposure (0.1%), and to meet a requirement for a research study (0.1%). In this group, white women were more likely to receive nonindicated screening (P=.007) (Table 3). Patients in this age group were seen by 317 health care providers; the median number of patients seen by each health care provider was two (range 1–52). Health care providers performing nonindicated Pap tests in this group were more likely to be older (P=.008), male (P=.02), in specialties other than gynecology (P=.04), and to work within 60 miles of Minneapolis (P=.002). In multivariate analysis, male gender (P=.01), specialty (P=.02), and clinic location (P=.001) remained significant (Table 3).
A total of 2,084 women had at least one Pap test posthysterectomy (3% of all patients). Of these, 605 (29.0%; 95% CI 27.1–31.0%) were not indicated per the guidelines. The most common reason for nonindicated Pap tests was routine health maintenance (87%) with a much smaller proportion performed for nonindicated follow-up of abnormal Pap test results in the distant past (6%), patient request (4%), history of high-grade dysplasia more than 20 years prior (3%), and cancer surveillance in cancers without a Pap test indication such as nongenital melanoma (0.7%). The most common reasons for indicated Pap tests were cancer surveillance (45%) and supracervical hysterectomy (37%). Other indications were a history of high-grade dysplasia within the past 20 years (11%), guideline-adherent follow-up of an abnormal Pap test result (3%), evaluation of vaginal bleeding or an abnormal examination finding (3%), and diethylstilbestrol exposure, immunocompromised state or transplant clearance, or patient request (each less than 1%). There were no differences patient characteristics between those who had indicated compared with nonindicated testing (Table 4). Patients in this group were seen by 362 health care providers; the median number of patients seen by each health care provider was three (range 1–122). Gynecologists were less likely than primary care health care providers to order nonindicated Pap tests (P=.003); no other health care provider characteristics were associated with the ordering of nonindicated tests (Table 4).
Between 2012 and 2014, the total number of Pap tests ordered per month decreased in all three groups. However, temporal trends in the proportion of nonindicated Pap tests ordered each year varied by group. In the younger than 21 years group, there was a decline in the proportion of nonindicated Pap tests over the study time period (P=.006). In contrast, there was an increase in the proportion of nonindicated tests ordered in the posthysterectomy group during the same time period (P=.04). The proportion of nonindicated Pap tests in the older than 65 years group remained relatively stable over time (P=.91).
Cervical cancer screening at the extremes of age and posthysterectomy was performed in 35% patients in our health system despite recommendations against screening for more than a decade. The proportion of nonindicated Pap tests appeared to increase in the posthysterectomy group despite a temporal decrease in the total number of Pap tests and a concomitant decrease in the proportion of nonindicated tests in the younger than 21 years age group. There were no common patient or health care provider characteristics associated with excess screening across all groups. Nonindicated screening is likely the result of confusion about the guidelines and patient and health care provider worry that omitting screening will increase the cervical cancer incidence.
Our results build on those of previous survey studies showing that women at low risk for developing cervical cancer continue to undergo screening. A claims database study showed that 57% of women younger than age 21 years had Pap tests performed,5 and a 2010 study using data from the National Health Interview Survey showed that 58.4% of women older than 65 years of age and 34.1% of women posthysterectomy continued Pap testing.6
Lack of knowledge of the guidelines is one reason for nonadherence.9 Unified guidelines were created in 2012,1–3 but the guidelines are complex and changed frequently before 201210,11 and will likely become even more complicated in the future as primary HPV testing12 and different guidelines for those vaccinated against HPV13 are incorporated. Our chart review showed that health care providers often did not differentiate between abnormal cytology and a histologic diagnosis of dysplasia. Furthermore, the coupling of Pap tests with prenatal care increased screening in women younger than 21 years of age.
Some health care providers distrust the guidelines. In a 2016 California survey, 35% of primary care and 59% of gynecologists did not feel that the current guidelines were clinically appropriate14; interestingly, gynecologists had lower rates of nonindicated screening in our study. Some respondents to the California survey felt that the guidelines were created to save money and that decreasing screening would result in an increased incidence of cervical cancer. Other health care providers continue screening to meet patient expectations during health maintenance visits, and many health care providers do not have adequate time to explain the guideline changes to patients.14 Lastly, some health care providers acknowledged financial incentive to continuing cervical cancer screening.14
In this study, the increase in the proportion of nonindicated Pap tests in the posthysterectomy group may be the result of a change in the total number of Pap tests performed rather than a true increase in the performance of nonindicated tests. During the study period, the total number of Pap tests performed in the posthysterectomy group declined by 56%, whereas the number of nonindicated Pap tests decreased by only 46%. This may reflect adoption of the guidelines by some, whereas those who intentionally disregarded the guidelines continued to screen.
The strengths of this study are the large number of patients from a large health system, which includes urban, suburban, and rural sites and both academic and community clinics. All charts were manually reviewed; an electronic health record query alone would have inaccurately doubled the number of nonindicated Pap tests in women younger than 21 years and older than 65 years old and tripled the number in posthysterectomy patients. Nonetheless, our study provides a conservative estimate of the number of nonindicated Pap tests, and the true number may be much higher. The primary limitation of our study is the fact that we could compare the number of nonindicated Pap tests only with the total number of Pap tests performed within each screening group; ideally, we would have compared the number of Pap tests performed with the total number of women seen within the health system in each group; however, we were unable to query the data in this way. This study was performed within a single health system, so our results may not be generalizable to other health systems. Other limitations of the study are those inherent to a retrospective chart review. Data collection was limited by the quality of documentation and we had access to records only within our electronic health record. It is possible that patients had a Pap testing history outside of our system, which likely resulted in an overestimate in the number of women older than 65 years of age who continued screening as a result of inadequate previous testing.
The 2012 guidelines seek to maintain the benefits of screening while limiting potential harms such as preterm delivery in future pregnancies after excisional procedures, increased risk of pelvic organ prolapse or urinary incontinence after hysterectomy, or vaginal stenosis after treatment of vaginal dysplasia.2 Continued screening in populations at low risk for cervical cancer limits the protections sought by the current guidelines.
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