Persistent infection with oncogenic types of human papillomavirus (HPV) causes cervical intraepithelial neoplasia (CIN) and invasive cancer.1 Recently, the Food and Drug Administration (FDA) approved a sensitive and specific test for oncogenic HPV genotypes (Hybrid Capture 2, Digene Diagnostics, Gaithersburg, MD),2 and several organizations released guidelines about its use.3–10 In 1999, FDA approved this test to guide the management of the nearly 3 million American women each year with the borderline abnormal cervical cytology result, atypical squamous cells of undetermined significance (ASC-US).3 Clinicians can order HPV tests before and contingent upon an ASC-US result using residual cervical cells from liquid-based cytology media, a separate HPV specimen collected along with conventional cytology (“reflex testing”), or by recalling patients. By 2003, the American College of Obstetricians and Gynecologists (ACOG) and other organizations3–5 had endorsed HPV testing as one option to identify HPV-infected women with ASC-US results who were at highest risk of developing CIN and merited prompt colposcopy (Fig. 1). The FDA did not approve HPV testing to guide colposcopy triage of women with abnormalities of higher grade than ASC-US.2 Because most of these women are infected with oncogenic HPV, testing adds little to stratifying risk for prevalent high-grade CIN and might delay colposcopy, diagnosis, and treatment.3,5
In March 2003, FDA approved this HPV test as an adjunct to cytology for screening women aged 30 years and older (DNAwithPap test, Digene Diagnostics, Gaithersburg, MD).2 By 2004, several national organizations had endorsed this indication as an acceptable option,5–7 although one did not.10 Because HPV testing can distinguish persistently HPV-infected women at high risk of CIN from HPV-uninfected women at low risk of CIN, guidelines advise that women with normal cytology and positive HPV tests have repeat cytology within 6–12 months to determine whether HPV infection is transient, whereas women with normal cytology and negative HPV tests should be screened less frequently (eg, every 3 years) (Fig. 1).6 The test is not approved to replace cytology or as an adjunct to cytology for women under the age of 302 in whom most HPV infection is transient and benign.11 In mid-2004, we conducted the first national survey of clinician practices since the release of these guidelines.
MATERIALS AND METHODS
We sampled nonfederal, nonmilitary clinicians in specialties that often offer Pap screening: physicians who were office-based, spent most of their time in direct patient care, and practiced family, general, internal, or adolescent medicine or obstetrics-gynecology; certified nurse midwives; nurse practitioners practicing family, adult, or women's health; and physician assistants practicing primary care. We used the most complete U.S. clinician databases, all of which include members and nonmembers of these registry organizations: the American Medical Association Physician Masterfile, the American Association of Physicians' Assistant Masterfile, and databases of the American College of Nurse Midwives and the American Association of Nurse Practitioners. Because we expected specialty-specific data would vary and inform interventions, we used disproportionate sampling. Random samples of 760 of all specialties (except the universe of adolescent medicine physicians, 826) were selected to yield 1) 80% power to detect differences between specialties of point estimates at the middle of the binomial distribution (eg, 40–60%) assuming an adjusted response rate of 80% or more and α of 0.05 and 2) 95% confidence intervals within ±10 units of point estimates for main analyses.
Final survey content and format were developed and validated based on detailed input and piloting of several survey drafts by experts in HPV, cervical cancer, survey psychometrics, and 150 clinicians, including ones in all sampled specialties. The survey addressed clinicians' demographic, patient, and practice characteristics; HPV-related knowledge; screening; abnormal cytology management; HPV testing and test consent, counseling practices; and information sources used to guide screening and abnormal cytology management. We asked clinicians to assume women were immunocompetent, aged 65 years or less, and had intact cervices, low-average cervical cancer risk, and no past abnormal cytology. We assessed knowledge by agreement to true or false statements and used 5-point scales to assess opinions (from “strongly agree” to “strongly disagree”) and practice frequency (“never” to “always”).
The Centers for Disease Control and Prevention (CDC), the federal Office of Management and Budget, and Battelle approved survey and human subjects' protection procedures. In May 2004, we express-mailed surveys with $50 cash and a CDC cover letter stating that results would inform new materials for clinician training and decision support and patient education. Clinicians or office managers could note ineligibility due to death, retirement, or relocation on reply postcards. We mailed reminders from 2–15 weeks after the first mailing. Contact information was unlinked from data entry identification numbers and destroyed.
We double-entered and cleaned data received by September 30, 2004. Clinicians were eligible for the survey if they worked 8 or more hours per week in outpatient settings, provided routine checkups, and reported at least 20% of their patients were aged 13–65 years. To adjust for disproportionate sampling by specialty and nonresponse bias, we assigned each respondent a final case weight, the product of their base specialty weight (the reciprocal of the clinician's probability of selection) and their nonresponse weight. We computed nonresponse weights using demographic and practice data on nonrespondents and respondents available in the sampling databases. Because response rates varied appreciably only by specialty and years in practice, we devised nonresponse adjustment classes using specialty and 5-year intervals of years in practice (or age for midwives because years-in-practice data were not available) within each specialty. We computed means, percentages, 95% confidence intervals, t tests, and χ2 tests for between-group and within-group comparisons after accounting for weighting (SUDAAN 9.0 [Research Triangle Institute, Research Triangle Park, NC]; StataCorp 9 [StateCorp, College Station, TX]). A two-tailed P < .05 was considered statistically significant.
Of the 5,386 surveys mailed, 548 were undeliverable. Seventeen clinicians were deceased, 746 refused to or did not respond, and 736 were ineligible. After adjusting for ineligibility, the overall response rate was 82% (family physicians 68%, internists 59%, adolescent medicine physicians 79%, obstetrician-gynecologists 81%, nurse practitioners 96%, nurse midwives 95%, physician assistants 86%). We restricted further analyses to 2,980 (89%) clinicians who offered Pap tests: all obstetrician-gynecologists and midwives, 93% of nurse practitioners, 91% of family physicians, 90% of physicians assistants, 74% of internists, and 66% of adolescent medicine physicians.
Most clinicians practiced in groups (71%), private offices (74%), and settings supported primarily by the private sector (83%). Most clinicians reported that most patients were older than 17 years (except for adolescent medicine physicians), female, and white. About half of patients used private insurance as their primary payment method (Table 1).
Most were aware of some current HPV-related information, but only about half were aware that most HPV infections clear without medical intervention and that HPV genotypes associated with anogenital warts and cervical dysplasia usually differ (Table 1). Obstetrician-gynecologists and nurse-midwives were most knowledgeable. Most clinicians were aware of HPV DNA tests (91%) and HPV-related knowledge of test users was more accurate than that of nonusers (data not shown). More than one half of clinicians rated the materials or guidelines of their specialty organization (78%), ACOG (74%), CDC (63%), and the American Cancer Society (ACS) (59%) as valuable (as opposed to being not valuable, not aware of, or not using) for guiding screening and abnormal cytology management. Users of the HPV test were significantly more likely than non-users of the test to value information of ACOG, CDC, and ACS, which had issued HPV testing guidelines (data not shown).
During routine check-ups of patients believed to be sexually active, most clinicians routinely educated female patients about cervical cancer screening (85%), but fewer clinicians routinely educated patients about HPV infection or HPV-related conditions (52%) (Table 1). Fewer than 12% delegated such education to staff members or offered written materials. Clinicians who reported HPV testing as an adjunct to cytology or for abnormal cytology management were significantly more likely than clinicians who did not report such use to educate patients about HPV infection, HPV-related conditions, or general sexually transmitted disease (STD) prevention (data not shown). Most reported that some patients had requested information on prevention of cancer or HPV infection (Table 1).
A total of 66% of clinicians had used HPV tests for some reason, and test use was most common among obstetrician-gynecologists and midwives (Table 1). Many (58%) had ordered HPV tests because patients wanted to know their infection status. Of the 609 clinicians who did not use HPV tests, 60% declined to use it because they had timely access to colposcopy (60%); fewer than 20% reported that the test was not reimbursed for most patients, not recommended by their health system, or not offered by their laboratory; fewer than 5% wished to avoid discussing cancer screening in an STD context or noted that counseling HPV-positive patients would make patients feel uncomfortable, upset or angry, or take too much time.
Most clinicians used liquid cytology (78%), provided many Pap tests, and had many patients with abnormal cytology. Less than half offered on-site colposcopy (Table 2). Most usually assessed STD risk behaviors or discussed STD prevention methods when collecting Pap tests. Less than half usually discussed methods to prevent cervical cancer or HPV acquisition or noted that HPV was a cervical cancer risk factor (Table 2). Clinicians who used HPV tests as a Pap test adjunct or for managing abnormal cytology were significantly more likely than clinicians who had not to usually note that HPV is a cancer risk factor (48% versus 34%); to describe methods to prevent cervical cancer (51% versus 44%) or HPV infection (46% versus 37%); or to assess STD risk behaviors (99% versus 96%).
Only 647 (21%) clinicians used HPV tests as an adjunct to cytology, ie, ordering or collecting tests regardless of cytology results (Table 2). Clinicians who reported such testing were significantly more likely than clinicians who did not to be obstetrician-gynecologists and female, to practice in single specialty groups (versus solo or in multiple-specialty groups), to see a high proportion of female and privately insured patients, to use liquid cytology, to report more than 400 cytologic tests and more than 60 patients with abnormal cytology in the last year, and to offer on-site colposcopy (data not shown). In all specialties except obstetrics-gynecology, HPV testing of women under 30 years of age (not recommended by guidelines) was more commonly reported that testing for women 30 of age or older (recommended by guidelines) (Table 3). Most clinicians told patients they were ordering the test, explained the purpose of HPV tests in relation to Pap tests, or noted that HPV tests detect a STD. A minority usually sought test consent (Table 3).
To assess how HPV test results might influence counseling, we analyzed 489 clinicians who had seen women with normal cytology and positive HPV tests, as well as women with normal cytology and negative HPV tests. If HPV tests were positive, clinicians were significantly more likely to share the HPV test results (98% versus 67%); to explain that HPV is a cancer risk factor (99% versus 62%); to address methods to prevent cervical cancer (94% versus 55%) or HPV acquisition (89% versus 58%); and tell patients to get tested for other STDs (85% versus 45%) or inform sex partners of HPV test results (80% versus 39%).
Most clinicians (63%) ordered HPV tests for borderline or abnormal cytology results (Table 2), of whom 88% used reflex testing and 64% recalled patients. Clinicians who reported testing such patients were significantly more likely than clinicians who had not to be obstetrician-gynecologists and female and part of single specialty groups (versus solo practice or multiple specialty groups), to see a high proportion of female or privately insured patients, to use liquid cytology, to report more than 400 cytology tests and more than 60 patients with abnormal cytology in the last year, and to provide on-site colposcopy (not all data shown). Many clinicians reporting such testing told patients that they were ordering the test or that it detects a sexually transmitted infection. Only 28% sought test consent (Table 4). Most clinicians ordering HPV tests for borderline or abnormal cytology results usually ordered them for ASC-US, as guidelines recommend for colposcopy triage. Such testing was significantly more common among obstetrician-gynecologists and midwives. However, more than 60% of clinicians usually ordered HPV tests for higher-grade cytology results that guidelines do not endorse for colposcopy triage. Obstetrician-gynecologists were least likely to report such testing (Table 4).
To estimate how HPV test results influenced management of ASC-US results, we analyzed 1,782 clinicians who had seen patients with ASC-US results and positive HPV tests, as well as patients with ASC-US results and negative HPV tests. If HPV test results were positive, clinicians were significantly more likely to usually recommend colposcopy (95% versus 27%) and slightly less likely to recommend repeat cytology within 6–12 months (84% versus 91%). If tests were positive, clinicians were also significantly more likely to share the test result (100% versus 89%); to explain that HPV infection may be a possible cause of the Pap result (99% versus 73%) and is a risk factor for cervical cancer (99% versus 84%); to address methods to prevent cervical cancer (90% versus 73%); to describe ways to prevent HPV acquisition (91% versus 73%); and to advise patients get tested for other STDs (73% versus 47%) or inform sex partners of test results (74% versus 40%). By contrast, of the 856 clinicians who did not use HPV tests for ASC-US results, 66% usually recommended colposcopy and 93% usually recommended repeat cytology within 4–6 months (the recommended interval if not using HPV tests3) for ASC-US results. Less than three fourths told patients that HPV infection might have caused the ASC-US Pap result (67%) or is a risk factor for cervical cancer (70%); addressed cervical cancer prevention methods (66%); or advised testing for other STDs (52%) or informing sex partners of the HPV test results (46%).
A total of 2,561 clinicians had seen patients with cytology results of unspecified grade that were likely due to HPV infection or patients with a positive HPV test (regardless of test indication) (Table 5). Nearly all usually told such patients that their Pap test result was probably caused by a common sexually transmitted virus, that the patient may have been infected months or years earlier, and that the patient could transmit the virus to current or future sex partners. Most usually explained that not much is known about how long the infection will last, with or without treatment; that if their sex partners were also HPV-infected, unprotected sex may increase risk of future abnormal cytology; and that patients can prevent HPV transmission through monogamy, minimizing sexual partner number, or by using condoms. Only 41% usually explained that abstinence can prevent transmission, although adolescent medicine physicians reported this more often (63%). Many clinicians reported that addressing HPV would increase the likelihood that patients would return for repeat cytology (87%), would assure patients of receiving full information (83%), and would encourage patients to tell sex partners to see a clinician (62%), but few reported that addressing HPV would change sexual behaviors to prevent transmission (42%). Many indicated that addressing HPV could raise patients' concerns about partner fidelity (68%) or make patients feel uncomfortable, upset, or angry (32%). Many noted problematic issues: providing definitive answers about when or from whom infection was acquired (85%); dealing with patients' emotional, psychological, and relationship issues (73%); motivating patients to adopt measures to prevent HPV transmission (69%) or adhere to clinical follow-up advice (58%); finding sufficient time (54%) or reimbursement (74%) for counseling; or explaining HPV so patients can understand (44%).
This national survey demonstrates that the introduction of HPV tests and testing guidelines have transformed screening, abnormal cytology management, and counseling in the United States. Our findings allow clinicians to compare their practices with national patterns and can inform clinician, patient, and public education priorities; health care planning, reimbursement, and policy; and models of how HPV testing and HPV vaccines might influence cancer incidence and health care costs.
The large sample size, high response rate, adjustment for nonresponse, and inclusion of midlevel providers who provide a great deal of screening but are often overlooked in surveys make our data nationally representative of seven specialties that commonly offer screening. We enhanced survey validity by using established clinician survey metrics and extensive expert review and piloting. To discourage clinicians from reporting practices that were consistent with guidelines but not typical of their practice, the cover letter did not detail plans to compare reported practices with guidelines.
Most clinicians were aware that HPV infection causes cervical neoplasia and that HPV tests are available, but many were unaware of information useful for counseling; eg, most HPV infections clear spontaneously11 and wart- and cancer-related HPV genotypes usually differ.1 Most clinicians valued materials from organizations that issued recommendations about HPV testing, as other studies show.12–14 As expected, knowledge of obstetrician-gynecologists and nurse-midwives, who reported the highest cytology volume and most HPV test use, was most up-to-date. This knowledge will increase patient confidence in counseling15 and help answer patient questions raised by public education campaigns,16 HPV test consumer marketing,17 and news about HPV vaccines.18
Liquid cytology was the dominant cytology method used in all specialties, as surveys of gynecologists and family physicians have shown.12,13,19 Although this method facilitates HPV testing, only 21% of clinicians used HPV tests as an adjunct to cytologic screening. Limited use may reflect the 14-month interval between FDA approval of this indication and the survey, the interim nature of current guidelines related to uncertainty about the effect on outcomes and cost,5–8,10 and limited reimbursement. It may also reflect concerns about how to counsel up to 13% of women with normal cytology and positive HPV tests20 or extending screening intervals of women with normal cytology and negative HPV tests. Guidelines advise longer intervals in these “double negative” patients because this test combination has a high-negative predictive value for incident CIN.6,7 Although longer intervals may use medical resources more efficiently, reduce patient anxiety and follow-up, and free clinicians to focus on underscreened patients, they may also preclude interim visits for other care, reduce revenue from visits linked to screening, and be unacceptable to patients.6,7,12,21 Therefore, ACOG and ACS stressed regular gynecologic care when issuing their guidelines,5,7 and FDA approved this indication contingent on development of patient education materials.2 In one health plan, introducing HPV testing extended cytology intervals in HPV-negative women, increased CIN 2 detection, proved acceptable to patients, and overcame early clinician objections (Walter Kinney, written communication, December 6, 2004). Similar evaluations are needed in other health settings.
In all specialties except obstetrics-gynecology, HPV testing as an adjunct to cytology was more commonly used for women under 30 years of age (not recommended) than for older women (recommended).5–8 Misuse may stem from lack of awareness that most infections in young women are transient and benign11 and that testing may lead to unnecessary distress, colposcopy, invasive procedures, or costs5,7,8,22; liberal reimbursement; or test demand fueled by mass media or consumer marketing.16,17
Many clinicians in our survey, like less-representative ones,13,23 ordered HPV tests for ASC-US results, largely using reflex testing on liquid cytology specimens, and used test results for colposcopy triage. Solid clinical and cost evidence supports interest in this indication: HPV testing may speed the diagnosis or ruling out of CIN, reduce losses for follow-up cytology, prevent unnecessary visits, procedures, and treatment, and lower costs.3 Women can be spared the anxiety of delayed repeat cytology alternatives, and HPV-negative women can be returned to routine screening with confidence that they do not harbor high-grade CIN.3 The consensus of multiple guidelines, cost pressure to reduce colposcopy, test reimbursement by large public and commercial insurers, widespread use of liquid cytology, and standing orders or routine check boxes for reflex HPV testing3,24 may also foster test use. Although HPV testing for ASC-US results is now a mainstream practice in gynecologists, testing was least common among clinicians serving many patients without private insurance or on-site colposcopy access whose cancer risk may be elevated owing to irregular screening or poor colposcopic follow-up.7 Moreover, nearly 20% of clinicians noted that test reimbursement was problematic. Programs to expand access to this test indication would benefit medically underserved women if they improve colposcopy triage, outcomes, and patient satisfaction or reduce overtreatment and costs. In fact, our data on widespread HPV testing for ASC-US results supported continued federal funding of this indication for low-income women (Mona Saraiya, written communication, November 4, 2005).
Although HPV testing is not recommended to guide colposcopy triage of abnormalities of higher grade than ACS-US, many clinicians, including obstetrician-gynecologists, reported such use. We may have overestimated inappropriate use if respondents confused HPV testing to guide initial colposcopy after screening with another recommended HPV test use, ie, secondary triage of patients with low- or high-grade squamous intraepithelial lesions after colposcopy, treatment, or an accelerated cytology program.3,5,8,9 However, this misclassification was probably minor because the survey posed all HPV testing questions in the screening section and did not cover posttreatment or postcolposcopy management and most clinicians who used HPV tests for higher-grade abnormalities practiced specialties that rarely treat these lesions. Moreover, a survey of obstetrician-gynecologists found similar patterns.13 Test misuse may reflect confusion about newly marketed tests, liberal reimbursement, or patient demand for new technology prompted by consumer marketing; 58% of clinicians ordered tests at least partly on patient request. To enhance clinician knowledge about HPV and appropriate HPV testing, ACOG, CDC, and other organizations have developed training curricula, guideline summaries, and HPV test algorithms (see the box, “Materials for the Public, Patients, and Clinicians”).2,8,9 Attention should first focus on physicians in family, adolescent, or internal medicine and physician assistants who screen many women but often reported inappropriate testing. Laboratory quality improvement organizations, health plans, insurers, and health care purchasers should also discourage reimbursement for reasons not approved by the FDA.
When clinicians ordered HPV tests, less than two thirds of clinicians notified patients of HPV testing, sought consent for HPV testing, or explained that the HPV test detects a sexually transmitted infection. Clinicians should consider that STD testing without consent may raise ethical and billing dilemmas; cause anger, discomfort, or stigma for patients; prolong counseling; or discourage needed follow-up or later screening, even if HPV test results are negative.25 Being notified of a sexually transmitted infection linked with cancer can be alarming, regardless of the cytology result, and can magnify the stress associated with abnormal cytology.26 Accordingly, some clinics have successfully introduced routine informed consent procedures for reflex HPV testing for ASC-US (Thomas Cox, oral communication, April 20, 2004) or cytology notification letters that explain HPV (Walter Kinney, oral communication, December 6, 2004). Others are considering “shared decision making,” where clinicians and patients consider HPV testing along with other screening or ASC-US management options.25
We found that, during checkups, screening, and notification of patients about abnormal cytology, the use of HPV tests has reinforced the message that a STD causes cervical cancer. Most clinicians noted that addressing HPV would encourage follow-up and not detract attention from cancer prevention. It may also provide entrées to discussing STD and human immunodeficiency virus (HIV) prevention, screening, vaccines, or barrier contraception. However, many clinicians noted that discussing HPV raises concerns about partner fidelity and causes patient distress, anger, or shame, as other studies show.15,25–27 Public knowledge about HPV is limited and fraught with misunderstanding.25 Many patients find it hard to grasp that most infections are transient, asymptomatic, and do not result in cancer and that HPV tests can be positive when cytology is normal. Even after counseling, patients may misinterpret test results, overestimate their cancer risk, or be unsure about follow-up.25,26 Effective counseling therefore takes skill, comfort, and time. Clinicians must balance positive and negative aspects of patient anxiety: motivation to adhere to follow-up advice versus difficulty in processing complex, sensitive information.
Written educational materials about HPV and abnormal cytology can reinforce counseling messages and reduce distress of patients who can digest information over time,28 but few clinicians in our survey used such materials. Fortunately, many counseling and education materials and hotlines have been recently developed in English and Spanish for all literacy levels (see the box, “Materials for the Public, Patients, and Clinicians”). Many cover topics that might pre-empt anxiety, shame, and blaming: the high prevalence of benign HPV infection, the low absolute cancer risk of HPV-infected women, the value of regular cytologic screening, the likelihood that long-standing partners of HPV-infected women are already infected, and uncertainty about the timing of HPV acquisition. Studies of how these materials affect women's understanding and reactions, screening and follow-up, and sexual habits are especially important in high-risk, low-literacy women.
Many experts predict that HPV testing according to current guidelines will enhance the efficiency and cost-effectiveness of screening and follow-up of low-risk, regularly screened women. These are laudable goals, given that cytology is one of the nation's most costly screening programs and many women are overscreened.24 However, some experts caution that the current HPV test indications may not substantially reduce the bulk of U.S. cancer cases that are diagnosed in never or rarely screened women,29 most of whom are uninsured, rural, minority, or foreign-born,7 or that possibility of testing for HPV, a potentially stigmatized STD, may make such women less willing to seek screening.27 To meet the ultimate test of a new technology—to reduce cancer morbidity and mortality—HPV testing must be integrated into programs that enhance regular cytologic screening of underscreened women and ensure that STD-related stigma does not reduce screening participation.
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