Persistent high-risk human papillomavirus (HPV) infections are recognized as the cause of cervical cancer.1 A high-risk HPV DNA test to detect infection with oncogenic or high-risk HPV types has been available since the early 2000s and is most commonly used to screen or manage women with abnormal Pap test results.2,3 Recent surveys report that approximately one-third of health care providers use HPV tests as part of routine cervical cancer screening.4,5 As a screening test, the high-risk HPV test can be used as a cotest along with cervical cytology screening in women aged 30 years old and older. The most common use of HPV tests is as a management test, which involves HPV DNA testing after an atypical squamous cells of undetermined significance (ASC-US) Pap test result, a practice also known as reflex testing.4,5 A low-risk HPV DNA test, which detects five nononcogenic HPV types including HPV 6 and HPV 11, the most common types found in genital warts, is commercially available although there are no clinical indications nor recommendations by any organizations for its use.2,3,6
Few studies have examined health care provider use of HPV DNA tests, but inconsistencies have been shown between recommended uses of HPV DNA tests and health care provider-reported practices.4,7 Although the benefits of HPV testing include greater sensitivity in detecting precancerous lesions as well as a high negative predictive value when used with the Pap test, use of nonrecommended HPV testing potentially increases health care costs and unnecessary work-up of patients who test positive without adding clinical value. In an effort to reduce nonrecommended HPV DNA testing, a statement on recommended uses of HPV DNA tests was published in 2009, which was endorsed by various professional organizations, including the American Cancer Society and American Society for Colposcopy and Cervical Pathology, and included an outline of when high-risk HPV DNA testing is generally not recommended (Box 1). The purpose of our study is to assess reported HPV testing practices among U.S. health care providers who perform Pap tests—including low-risk HPV testing, which has not been examined previously—using a nationally representative survey of office-based health care providers and hospital outpatient clinics.
MATERIALS AND METHODS
We used data from the 2006 Cervical Cancer Screening Supplement, a self-administered survey commissioned by the Centers for Disease Control and Prevention, Division of Cancer Prevention and Control. The data were collected as a supplement to the Centers for Disease Control and Prevention, National Center for Health Statistics' National Ambulatory Medical Care Survey, and National Hospital Ambulatory Medical Care Survey to obtain information on physicians' practices and beliefs related to cervical cancer screening. The National Ambulatory Medical Care Survey collects visits, practice, and health care provider-level data annually from office-based physicians and community health centers. The sampling frame for the National Ambulatory Medical Care Survey is derived from American Medical Association and American Osteopathic Association lists of “office-based physicians” providing patient care. Excluded are federally employed physicians or those specializing in anesthesiology, radiology, or pathology, The sampling frame for the National Ambulatory Medical Care Survey community health center health care providers is developed using data from the Health Resources and Services Administration Bureau of Primary Health Care Uniform Data System and the Indian Health Service who received a list of physicians and midlevel health care providers available during a predetermined 1-week reporting period. In 2006, 3,500 physicians and 104 community health centers were sampled. National Center for Health Statistics' National Ambulatory Medical Care Survey collects information on visits and clinic data from general and short-stay hospitals with emergency or outpatient departments in all 50 states and the District of Columbia excluding Federal hospitals. In 2006, 480 hospitals were sampled. Additional information about both surveys can be found at www.cdc.gov/nchs/ahcd.htm.
Health care providers eligible for the Cervical Cancer Screening Supplement among sampled National Center for Health Statistics' National Ambulatory Medical Care Survey health care providers were restricted to the following specialties: general or family practice, internal medicine, or obstetrics and gynecology; midlevel health care providers in community health centers were also eligible. Among National Hospital Ambulatory Medical Care Survey clinics, only those specializing in general medicine or obstetrics and gynecology were eligible; emergency departments were not eligible. Health care providers from both surveys were further restricted to only those performing cervical cancer screening. Eligible health care providers and clinics had the option of completing the Cervical Cancer Screening Supplement survey as a paper survey or online. A total of 387 National Ambulatory Medical Care Survey health care providers (response rate 61.1%) and 216 National Hospital Ambulatory Medical Care Survey clinics (response rate 84.7%) responded. Eleven National Ambulatory Medical Care Survey respondents were not in eligible specialties and were excluded from our analysis. The Research Ethics Review Board of the Centers for Disease Control and Prevention's National Center for Health Statistics approved the National Ambulatory Medical Care Survey and National Hospital Ambulatory Medical Care Survey protocols.
The 2006 Cervical Cancer Screening Supplement contained nine multipart questions that examined cervical cancer screening practices, including screening methods; whether the practice performed colposcopy; HPV DNA test use, including types of HPV DNA tests used, HPV testing as a screening test, and HPV testing for management of abnormal Pap test results; and screening intervals. Health care provider demographics and practice characteristics collected from the National Ambulatory Medical Care Survey and used in our study included the health care provider's age, sex, specialty, board certification status, practice size, practice type, geographic region, and participation in the National Breast and Cervical Cancer Early Detection Program. The variables from the National Hospital Ambulatory Medical Care Survey used in our analysis included clinic characteristics such as clinic specialty and geographic region but not health care provider-specific demographics, which are not collected.
Four items assessed HPV testing practices, beginning with whether the practice ever ordered or collected the HPV DNA test. Health care providers who responded yes were asked to select the different types of HPV DNA tests ordered or collected in their practice from the following choices: “high-risk HPV DNA test,” “low-risk HPV DNA test,” “not aware there was a high-risk or low-risk HPV DNA test,” or “unknown.” Responses were categorized first into responses that indicated the total amount of low-risk HPV use, but in bivariate analyses, responses were categorized into mutually exclusive practices of high-risk HPV DNA test use only, both high-risk and low-risk HPV DNA test use, low-risk HPV DNA test use only, and not aware or unknown. HPV testing for management of an abnormal Pap test result was assessed in two items: “If the patient's screening Papanicolaou test result is borderline or abnormal, does your practice routinely order an HPV DNA test to be performed on that sample (commonly called reflex HPV DNA testing)?” and “Does your practice routinely recall patients to come back for a second sample for an HPV DNA test if their screening Papanicolaou test is abnormal or borderline (recall testing)?” Health care providers who routinely performed either reflex or recall testing were asked for which types of abnormal Pap test results would the HPV DNA test be ordered: ASC-US, atypical squamous cells, cannot exclude high-grade squamous intraepithelial lesions (ASC-H), low-grade squamous intraepithelial lesions (LSIL), high-grade squamous intraepithelial lesions (HSIL), or atypical glandular cells. Responses for reflex and recall HPV testing for management of abnormal Pap test results were combined and are referred to as reflex testing in the remainder of the article. HPV cotesting was assessed by a two-part item: “Does your practice routinely order or collect an HPV DNA test at the same time as the Papanicolaou test as part of routine cervical cancer screening (sometimes called adjunct HPV testing or cotesting)?” Health care providers who responded yes were asked, “For which patients does your practice routinely order or collect an HPV DNA test along with the Papanicolaou test?” Response options were nonexclusive and included: “women younger than 30 years old,” “women 30 years old and older,” “women who request the test for cervical cancer screening,” “women who request the test to check their HPV infection status,” or “other—specify [fill-in].”
We used guidelines from American Cancer Society, the American College of Obstetricians and Gynecologists, and the American Society for Colposcopy and Cervical Pathology as the basis for inappropriate HPV testing practices, as illustrated in Box 1.2,3,8 Only the high-risk HPV test, which tests for oncogenic HPV types, is recommended for clinical use. For our analysis, we defined the following testing practices, which were consistently not recommended (or actively discouraged) in any guidelines, as nonrecommended HPV testing: low-risk HPV testing; HPV cotesting in women younger than age 30 years; HPV testing after Pap test results of ASC-H; and HPV testing after Pap test results of HSIL. Although we asked about HPV testing after other Pap test results such as atypical glandular cells and LSIL, we did not include them as inappropriate practices because there are special situations in which HPV testing is considered acceptable within the guidelines.
We used χ2 statistics to compare various HPV testing practices by health care provider or clinic specialty for each sample of health care providers who responded to the Cervical Cancer Screening Supplement. Sampling weights provided by the National Center for Health Statistics were used to adjust for nonresponse and to provide nationally representative patterns of practice. We considered an estimate unstable if the relative standard error, calculated as (standard error/estimated percentage)×100, was more than 30% and, thus, should be interpreted cautiously. All statistical analyses were done using SAS 9.2 with SUDAAN 10.
The distribution of demographic and practice characteristics of both health care providers and clinics is shown in Table 1. Among National Ambulatory Medical Care Survey respondents, most were physicians (96.7%) and were more likely to be male, board-certified, practice in a solo or a single specialty practice, and work in a private setting. The majority of National Hospital Ambulatory Medical Care Survey clinics were general medicine clinics (76.0%).
Overall, 75.5% (95% confidence interval [CI] 68.7–81.2%) of health care providers and 77.2% (95% CI 60.3–88.3%) of clinics reported ever ordering or collecting the HPV DNA test. Obstetricians–gynecologists were significantly more likely to report using the HPV DNA test than family physicians and internists (98.9% compared with 76.8% and 44.7%, respectively) (P<.001). Of health care providers who collected the HPV test, 46.6% (95% CI 38.2–55.2%) used it with the Pap test for routine cervical cancer screening (HPV cotesting), whereas 88.5% (95% CI 83.3–92.3%) used it for managing an abnormal Pap test result (reflex or recall testing). Similarly, clinics were more likely to perform reflex or recall HPV testing than HPV cotesting (Table 2). There were differences in the use of HPV cotesting by geographic region of the country with the highest reported in the Northeast region (72.6%, 95% CI 59.1–82.9%) and the lowest in the Midwest (35.9%, 95% CI 23.1–51.1%).
Overall, 31.4% of office health care providers and 25% of hospital clinics reported using low-risk HPV testing with variation by specialty regardless of whether it was in an outpatient setting (obstetricians–gynecologists: 41.5%; midlevel: 36.7%; family physicians: 25.6%; internal medicine: 23.9% [the estimate for internal medicine should be interpreted with caution because its relative standard error is greater than 0.3]) or in clinics (obstetricians–gynecologists: 45.8%; general medicine: 17.7%). Using mutually exclusive categories, reported high-risk and low-risk HPV testing is shown in Figure 1. The majority of health care providers (56.4%, 95% CI 47.8–64.6%) reported using high-risk HPV tests only, 28.5% (95% CI 21.6–36.6) of health care providers reported using both high-risk and low-risk HPV tests in their practice, and 12.9% (95% CI 8.5–12.1%) did not know or were unaware there was a high-risk or low-risk HPV test. Approximately 2% reported performing low-risk HPV only (data not shown). Obstetricians–gynecologists (39.0%) had the highest reported percentage of both high-risk and low-risk HPV testing followed by midlevel health care providers (34.8%), family physicians (23.7%), and internists (16.6%), although no significant differences among specialties were detected. Among clinics, 56.1% (95% CI 43.5–68%) reported using high-risk HPV tests only, and 25% (95% CI 17.1–35%) used both high-risk and low-risk HPV tests. An estimated 18.7% of clinics were unaware there was a high-risk or low-risk HPV test. The pattern of testing in general medicine clinics was similar to that of family practitioners.
The majority of family physicians, obstetricians–gynecologists, and hospital clinics that routinely performed HPV cotesting reported testing women 30 years and older, the only age group for which cotesting is recommended (Table 2). Cotesting in women younger than 30 years old was also reported by 59.6% (95% CI 48.5–69.7%) of all health care providers and 66.0% (95% CI 48.0–80.3%) of clinics. Cotesting after patient request was also reported; overall, 43.8% (95% CI 33.4–54.7%) of health care providers performed cotesting in women who requested the test for cervical cancer screening and 40.8% (95% CI 30.7–51.7%) for women who requested the test to check their HPV infection status.
Health care providers' and clinics' use of HPV testing after an abnormal Pap test result is shown in Table 2. Among those that routinely performed reflex HPV testing, most reported testing after an ASC-US Pap test result, a use that is consistent with guideline recommendations. A high percentage of health care providers and clinics performed reflex HPV testing after Pap test results of ASC-H (71.4%, 95% CI 63.5–78.3% and 62.8%, 95% CI 49.0–74.9%, respectively) or HSIL (50.7%, 95% CI 42.4–58.9% and 49.0%, 95% CI 33.1–65.2%, respectively), results for which HPV testing is not recommended. For an LSIL Pap test result, in which reflex HPV testing is an acceptable option for postmenopausal women, 54.2% (95% CI 45.7–62.5%) of health care providers and 56.4% (95% CI 40.6–70.9%) of clinics used reflex HPV testing. Reflex HPV testing after an atypical glandular cell Pap test result was reported by 37.5% (95% CI 28.9–47.0%) of health care providers and 30.1% (95% CI 19.6–43.1%) of clinics. Reflex HPV testing in women younger than 30 years old was reported by 56.1% (95% CI 47.8–64.1%) of health care providers and 54.5% (95% CI 42.6–65.9%) of clinics, whereas 53.7% (95% CI 45.2–62.0%) of health care providers and 44.8% (95% CI 33.5–56.6%) of clinics reported using reflex HPV testing in women 30 years and older.
In this national survey of Pap test providers, we found HPV DNA test use to be widespread among various specialties that offer routine cervical cancer screening. Although many health care providers reported guideline-consistent HPV testing, a large number also reported inappropriate HPV testing such as low-risk HPV test use by nearly one-third of health care providers and HPV cotesting in women younger than age 30 years by 60% of health care providers. These findings suggest that although HPV testing has become a routine part of cervical cancer screening, many health care providers are not following guideline recommendations, which may increase medical costs and lead to unnecessary follow-up for women with positive test results.
Our findings of low-risk HPV testing by 31% of health care providers and 25% of clinics that perform HPV testing, a practice that has not been assessed previously, is surprising. The low-risk HPV DNA test screens for infection with nononcogenic HPV types and thus serves no purpose in the context of cervical cancer screening.2,3 In addition, although low-risk HPV types such as HPV 6 and HPV 11 cause 90% of genital warts, low-risk HPV testing should not be performed for genital warts screening or management because most HPV infections are asymptomatic and will clear on their own. Further information on the management of genital warts is available from the CDC at http://www.cdc.gov/std/treatment/2010/genital-warts.htm.9,10 A positive low-risk HPV test may prompt further follow-up testing or procedures by health care providers, outcomes that we were unable to assess in this survey. Although a positive low-risk HPV test may not be clinically significant, whether there is disclosure to patients of test results and the psychosocial effect of diagnosis with low-risk HPV are unclear.
The continued use of low-risk HPV testing by health care providers in the United States may be driven by a combination of financial gain, test marketing, and health care provider confusion on the difference between the low-risk and high-risk tests.4,7,11,12 Eliminating the availability of the low-risk HPV test, which has no clinical indications, should be considered regardless of the test's current level of penetration because such testing adds cost to the medical system without adding value to patient care. When HPV testing first became available, the early generations of Digene's Hybrid Capture HPV DNA tests included both high-risk and low-risk HPV types.11 Since then, HPV DNA tests that screen only for high-risk types have become available, yet the combined low-risk and high-risk HPV tests remains in active use.13 It is unknown how laboratories influence the amount of low-risk HPV testing that occurs, but a study in 2007 found 45% of pathology laboratories reported offering the low-risk HPV test with the widespread availability attributed mainly to reimbursement and physician demand.13 We examined laboratory requisition forms from several U.S. laboratories, some of which had the combined high-risk and low-risk HPV test available as a checkbox option, illustrating the ease with which health care providers can perform low-risk testing as part of routine cervical cancer screening.
When ordered together, the low-risk HPV DNA test is billed at the rate of the high-risk HPV DNA test using the same Current Procedural Terminology code, which doubles the cost of HPV testing. Because most health care providers (91%) in our study were in private practice, liberal test reimbursement by private insurance may be an important factor behind this practice.
More than half of health care providers and clinics that perform HPV cotesting reported doing so in women younger than 30 years old, in which a positive HPV test more likely signifies a transient HPV infection that will resolve spontaneously without needing further intervention.9,10 Because of the high prevalence of HPV infection in women in their 20s,14 a large number of women in this age group would subsequently be referred to colposcopy and follow-up testing after HPV cotesting. Compared with a study of health care providers conducted in 2004,4 our study found the percentage of health care providers who reported cotesting women younger than age 30 years old has doubled. Avoiding unnecessary workup or treatment of transient HPV infections in younger women is an important goal in cervical cancer screening because studies have found associations between certain procedures used to treat cervical dysplasia and adverse birth outcomes.15,16
Another common reason reported by health care providers for HPV cotesting was a request from patients to check HPV infection status. In a study of direct-to-consumer advertising and its effect on HPV testing, direct-to-consumer advertising was associated with significant increases in HPV test use by health care providers.17 Because HPV is the most common sexually transmitted infection in the United States and most HPV infections are asymptomatic and transient, screening for HPV infection status outside the context of cervical cancer screening should not be performed.18 Several studies found women who receive positive HPV test results can experience negative psychosocial effects and health care providers should consider discussing with patients whether HPV testing is clinically recommended for them if patients request to be tested.19–21
As a management test, most health care providers used reflex HPV testing after an ASC-US Pap test result, a recommended use in patients aged 21 years and older. However, health care providers and clinics also reported using HPV testing after higher-grade Pap test result abnormalities such as ASC-H and HSIL. We were unable to assess for nuances in HPV testing recommendations for certain Pap test result abnormalities in our study such as newer guidelines that recommend against reflex HPV testing for patients younger than age 21 years2; however, excluding those special circumstances, there are limited data on the use of HPV testing for higher grade abnormalities. Additionally, guidelines recommend that patients with such Pap test results be referred to immediate colposcopy (or excisional treatment for HSIL) as the next management step instead.2
Our findings of nonrecommended HPV DNA testing among Pap test providers indicate a need for developing and testing interventions, especially ones tied directly to reimbursement, to encourage guideline-consistent test use. The continued use of low-risk HPV testing by health care providers warrants special consideration. Based on our knowledge of the natural history of HPV and the association of high-risk types with cervical cancer, there is simply no role for low-risk HPV testing in cervical cancer screening nor any other clinical scenarios to justify its use. Although health care providers have now had the option of performing only high-risk HPV testing for a number of years, our findings indicate that stronger measures such as engaging laboratories to stop the availability of the low-risk HPV test and limiting reimbursement from insurance companies to high-risk testing only may be needed. Health care providers also have an ethical obligation to inform patients, who are ultimately responsible for the cost either directly or indirectly, when ordering this test that has no clinical value. Finally, providing evidence that low-risk HPV tests can result in unnecessary and even harmful follow-up procedures and tests may be the armamentarium needed to take the low-risk test off the market.
Convincing health care providers and patients that more testing does not equal better medical care is a challenging task with medicolegal concerns and patient demand cited as some of the barriers.22,23 Formative research is needed to clarify the issues surrounding health care providers' use of HPV tests and the factors influencing guideline adherence. Educational materials for the general public on HPV and HPV DNA tests can help patients understand when testing may or may not be needed.24 Health care provider education on recommended uses of HPV testing should reinforce the benefits of testing as well as potential harms of overtesting such as unnecessary follow-up or overtreatment of transient HPV infections. Changing laboratory requisition forms to clearly reflect guideline-consistent HPV testing and point-of-care decision support algorithms designed to generate patient-specific recommendations in clinical care have been effective in improving health care provider performance in other areas and should be further investigated for this purpose.25,26
Our study had several limitations. The small sample size limited our ability to describe certain HPV testing practices for internists and midlevel health care providers and caused some estimates to be unstable. It also limited our power to detect differences among specialties and perform multivariate analysis of demographic and practice characteristics associated with nonrecommended HPV testing. Also, information on the insurance distribution of the patient population in a practice was unavailable on an individual health care provider level and we were unable to assess for correlation between testing practices and the patient population served. With additional years of data and a larger sample, further analysis may identify associated health care provider or practice factors. Although our respondents were similar to nonrespondents in certain demographic characteristics such as geographic region and board certification, nonrespondents were more likely to be older males, and our results may not be representative of that group.
In our survey, health care providers were asked to identify patients for whom they would perform HPV testing based on age group, an abnormal Pap test result, or other short descriptive characteristic. The questions did not take into account other factors such as patient sexual history or previous Pap test results, which may influence health care providers' actual practices. Finally, our data were self-reported and not validated by data of actual laboratory tests ordered by health care providers.
In conclusion, many Pap test providers are using HPV DNA tests in ways inconsistent with guideline recommendations, most notably, the use of low-risk HPV testing. Our findings indicate the need for wide-reaching interventions such as limiting test reimbursement to facilitate recommended uses of HPV DNA tests and eliminate low-risk HPV testing. Educational materials for patients and health care providers to address patient demand for HPV testing may also help to increase guideline consistent HPV test use. Further research is needed to identify interventions that effectively promote health care provider adherence to guideline recommendations, especially for newer technologies.
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