Based on the central role that persistent carcinogenic human papillomavirus (HPV) plays in the development of cervical cancer, HPV testing has been added to cervical cancer screening practices. HPV testing with the Papanicolaou (Pap) test (called co-testing) for women age 30–65 years is a recommended option for cervical cancer screening by all national organizations.^1–4 From 2003 to 2012, most guidelines recommended extending the screening interval to 3 years for women with negative co-test results (normal Pap and negative HPV) because of the low risk of cervical precancer and cancer. In 2012, guidelines were revised to recommend extending the interval to 5 years for women age 30–65 years. Cost-effectiveness studies have demonstrated that the increased screening interval for women with negative co-tests (estimated to be about 90% of those screened) offsets the additional cost of the DNA test.^5–7 However, annual screening, regardless of screening strategy, remains the common practice throughout the United States and across provider specialty.^8–10 Studies in managed care settings examining the acceptability of the co-test strategy for screening found that both providers and women were amenable to the longer intervals once they understood the role of HPV in the development of cervical cancer.^11,12

To date, no studies have examined provider and patient acceptance of co-testing with longer screening intervals in a low income population. The Centers for Disease Control and Prevention (CDC) launched the CDC Cervical Cancer (Cx3) Study—a multi-component educational intervention to identify facilitators and barriers to guideline-consistent use of the co-test in an underserved population. The primary objective of this study was to determine whether an educational intervention would lead to increased willingness of providers and patients to extend the cervical cancer screening interval for women with negative co-tests and decrease cervical cancer screening visits to clinic sites for average risk women. This is contrary to most social marketing campaigns and patient education interventions that advocate annual Pap tests.

The purpose of this article is to give a detailed overview of the Cx3 Study and lessons learned once implemented in the field.

Of the 2,246 patients who had both HPV and Pap tests, 2,002 (89.1%) had a normal Pap test and a negative HPV test.¹⁸ These women will have a chart review at 40 months to determine if well-woman exams were performed and what screening tests occurred. The HPV test was positive in 162 (7.2%) women. (Data not shown.)

At the time of the baseline survey, HPV test use varied among providers at the study clinics. Most of the providers were using the HPV test for management after an abnormal Pap test (ASC-US) (91%) and fewer were using HPV for co-testing (39%).¹⁶ Most of the clinics (66%) had at least one provider who could conduct colposcopies on site. In the case of abnormal test results, most clinics relied on a combination of systems for follow-up including verbal prompts, mail and telephone reminders. Only one clinic did not have any reminder system in place. (Data not shown.)

A sample of the provider and patient characteristics are provided in Table 3. The average age of the providers was 41.3 years at the time of study initiation. Almost 70% of the providers were from the Chicago area. Approximately three-quarters of the providers were female and the majority were non-Hispanic (94%). With respect to race, 55% reported that they were white, 20% reported that they were black, and 25% reported that they were Asian. The average age of the patient sample at the time of recruitment was 45.0 years. Nearly one-third of the patient sample reported that they were Hispanic, and 26% that they were African American. Nearly one-third of those surveyed (31%) were born outside of the U.S, 26% were born in Mexico, and 28% reported that they normally speak Spanish in the home.

This study was developed to identify barriers to appropriate use of the co-test, and to implement an educational intervention to promote evidence-based screening practices. This article provides a detailed overview of the study including the multi-component intervention and brief participant characteristics. Additional information on the lessons learned is also an important contribution to the literature in conducting this type of study in the field. The lack of a physician recommendation for cancer screenings is one rea son why women report not being screened.¹⁹ One interventional strategy to disseminate evidence-based, provider-oriented interventions (provider assessment and feedback and provider reminders)²⁰ is academic detailing.²¹ Multiple studies in the literature have used these techniques to improve recruitment for screening but very few interventions have been introduced to address how to screen at the appropriate intervals (in this case, to decrease screening when not recommended). This study provided multiple evidence-based strategies to encourage providers to follow recommendations, including placing current screening guidelines in charts, discussing reimbursement codes, offering current literature on co-testing, and office-based materials (small media, examples of client reminders, discussions regarding system interventions). Additionally, podcasts were developed by professional experts in their communities covering recommended follow-up. Despite these efforts, the practice of annual screening may be difficult to change even after newer guidelines have recommended less frequent screening.

The impetus for this study was to understand the barriers with co-test use and the extension of the interval between screenings in the underserved population. To improve cervical cancer screening among medically underserved women, Congress authorized the CDC to develop the National Breast and Cervical Cancer Early Detection Program (nBCCEDP) in 1991.¹³ The NBCCEDP is a comprehensive public health program that helps low-income, under- and un-insured women gain access to breast and cervical screening services. Before the 2012 revision to the USPSTF screening guidelines, ²² the NBCCEDP reimbursed for the HPV test for management of cervical cancer, but not as a co-test²³. Therefore, this pilot study was also designed to provide feedback to the national program on facilitators and barriers to appropriate use of the co-test including screening intervals. This information is now even more useful, as the NBCCEDP began reimbursing for the co-test in July 2012 and will be using the outcomes of this study and the materials developed to help providers and patients adopt new recommendations.

This study had many strengths including enrolling over 2,000 low-income, un- and under- insured patients in the setting of FQHCs across a diverse population of urban and rural clinics in Illinois. Research among FQHC patients and providers allows for understanding the access and barriers to care among the underserved. These facilities and their staff provide care regardless of a person's insurance status, income, or ability to pay, and they are a large, essential component of the U.S. healthcare safety net for people who otherwise have limited options to access essential care.²⁴ Additionally, the multi-level assessment of the clinics, providers and patients provides details to understand how practices, attitudes and beliefs will change over time including the increase in the 3- to 5-year screening interval. This study also has the capacity to follow women with positive test results since they will have medical chart review through the 40 months. Additionally, the educational intervention that was developed gives the rationale for using all of the strategies for cervical cancer screening including longer intervals regardless of the method to screen.

As a demonstration study in one state, our results may not be generalizable to all. However, when we examined the racial and ethnic distribution of this study population in Illinois, it was very similar to the NBCCEDP racial and ethnic distribution. Since most of the clinics in our study did not have research experience, we faced challenges such as longer-than-expected patient enrollment, no data collection on the women who refused to participate (which does not allow us to calculate a response rate for patients), and limited staff time at one of the health centers to conduct the survey portion of the study.

While many studies are aimed at introducing new technology, very few are focused on introducing new technology coupled with evidence-based strategies that emphasize less but more-efficient screening. When complete, the Cx3 Study will provide a wealth of information on current trends in screening and effective approaches for encouraging guideline-adherent cervical cancer screening. These findings on practices and attitudes regarding HPV testing and screening interval extension are very timely with all national organizations recommending co-testing and extended screening intervals. Additionally, the management guidelines are being updated with a focus on triaging women with specific high-risk HPV types²³; thus, as the science advances, conveying this information to providers and patients will be essential to encouraging the most effective patient care. The information on the harms of over-testing—which may lead to over-diagnosis and overtreatment—is only useful to the extent that it is understood and accepted by providers and patients. CDC has produced several materials to educate providers and patients on the appropriate use of the co-test, and these materials may be adapted over time to meet the changing needs of the population and the latest science.