ANOGENITAL WARTS ARE COMMON, affecting approximately 1% of the US population, with more than 500,000 new cases of anogenital warts believed to occur annually.1,2 Anogenital warts result in over 300,000 health care provider visits per year3; more than 70% of patients diagnosed with anogenital warts by a clinician are aged 20 to 39 years, and half to more than two-thirds of such patients are women.4 The most commonly consulted clinicians for anogenital warts in the United States include obstetrician/gynecologists, dermatologists, and urologists.4
Anogenital warts are caused by several genotypes of sexually transmitted human papillomavirus (HPV), especially Types 6 and 11. Other HPV genotypes, especially Types 16 and 18, are commonly associated with cervical intraepithelial neoplasia (CIN) and cervical cancer, in addition to other anogenital cancers.5,6 HPV DNA tests for genital HPV genotypes have been recently approved by the Food and Drug Administration (FDA), but none are currently approved for testing HPV infection status of patients with anogenital warts.7
The recurrent nature and sexual transmission of anogenital warts may prompt clinicians to counsel patients about the causes and prevention of transmission of warts, and the implications for anogenital cancer. Consequently, the US Centers for Disease Control and Prevention (CDC) and other national clinical organizations, such as the American Social Health Association and the American College of Obstetricians and Gynecologists, recommend specific counseling messages for patients with anogenital warts.8-10 For example, CDC currently recommends that patients with anogenital warts be counseled about watching for wart recurrences, that women with warts undergo cervical cancer screening with Pap tests at regular (and not increased) intervals, that examination of sex partners is not necessary, and that female sex partners of patients who have warts get routine Pap screening.10
Information about HPV natural history, clinical sequelae and transmission, and HPV test technology has evolved over the past 2 decades and has been actively disseminated to clinicians, patients, and the general public.11 Additionally, several studies indicate a great need and demand by patients with anogenital warts for counseling and education.12,13 No national-level data exist on clinicians' knowledge about anogenital warts and their relation to HPV or the counseling and clinical follow-up practices they provide to patients with anogenital warts. Therefore, in mid-2004 we surveyed US clinicians who care for patients with anogenital warts to assess their wart-related knowledge and practices and to determine clinician characteristics associated with gaps in knowledge and counseling practices that are inconsistent with current scientific evidence.
Methods
The survey methods have been detailed elsewhere14 but are summarized here.
Survey Sample
We selected a nationally representative sample of clinicians in 9 specialties that commonly diagnose anogenital warts. These include physicians in the specialties of family and general practice, general internal medicine, adolescent medicine, obstetrics and gynecology, dermatology, and urology, and midlevel providers, including nurse practitioners specializing in family, adult, or women's health; certified nurse midwives practicing in nonfederal, nonmilitary settings; and physician assistants practicing primary care. Clinicians were randomly sampled from the most comprehensive US clinician databases that include members and nonmembers of the American Medical Association (AMA), American Association of Physicians' Assistants, and databases of the American College of Nurse Midwives and the American Association of Nurse Practitioners. We selected samples of 760 clinicians per specialty (except all 826 adolescent medicine physicians in the AMA database) to (1) achieve 80% power to detect differences between specialties of percentages and means at the middle of the binomial distribution assuming an adjusted response rate of 80% and α of 0.05 and (2) to achieve 95% confidence intervals that were within ±10 units of point estimates for main analyses.
Survey Instrument
The final instrument was developed after several rounds of review and pilot testing by HPV and cancer experts and practicing clinicians.14 The survey addressed many topics, including respondents' demographic characteristics, characteristics of their primary practice site and patients, experience diagnosing warts and providing cervical cancer screening, anogenital wart knowledge, awareness and opinions of information sources used to manage patients with anogenital warts, counseling and patient education practices for patients with anogenital warts, barriers to counseling and education, and HPV testing practices for patients with anogenital warts. The survey took 20 to 40 minutes to complete. We estimated knowledge by assessing agreement (yes or no) to several statements that were and were not consistent with current scientific evidence, and we assessed opinions using a 5-point Likert scale (strongly agree to strongly disagree). Frequency of counseling, education, and testing practices was assessed using a 5-point Likert scale (never to always). To assess opinions about wart clinical information sources, we asked respondents if they were aware of materials or guidelines of a given organization, and if so, if they rated them as not, somewhat, or quite valuable. Respondents indicated if they addressed specific counseling issues, and if so, if they were not, somewhat, or quite problematic.
Data Collection Procedures
CDC, the Federal Office of Management and Budget, and Battelle Centers for Public Health Research and Evaluation approved survey and human subjects' protection procedures. In May 2004, we express mailed surveys to 6906 clinicians with a $50 cash incentive and a CDC cover letter indicating that survey findings would be used to update clinical training curricula, clinical decision support tools, and patient education materials. On a reply postcard, clinicians or their office managers could indicate ineligibility due to death, retirement, or relocation. Clinicians were eligible for the survey if they practiced at least 8 hours per week in an outpatient setting, they provided routine checkups, and at least 20% of their patients were aged 13 to 65 years. Additionally, primary care clinicians, obstetrician/gynecologists, and nurse midwives were eligible to complete the survey only if they provided routine checkups to patients. We mailed reminder postcards 10 days after the initial mailing and complete survey packets to nonrespondents approximately 5, 8, 11, and 15 weeks after the first mailing. To maintain confidentiality, identifying information used in mailings was unlinked from identification numbers used for data entry and analysis.
Data Analysis
We double-entered and cleaned data from surveys received by September 30, 2004, to resolve inconsistent responses. To adjust for disproportionate sampling by specialty and nonresponse bias, we assigned each respondent a final case weight that was the product of the respondent's base specialty weight and their nonresponse weight. Each clinician in a given specialty had the same base specialty weight, the reciprocal of the clinician's probability of selection. We computed nonresponse weights using information on nonrespondents and respondents from the databases used for sampling. Because response rates varied appreciably by specialty and years in practice, we created nonresponse adjustment classes using specialty and 5-year intervals of years in practice (or for nurse midwives, age, because data on years in practice were not available) within each specialty. All analyses were done using SAS Version 9 (SAS Institute, Cary NC),15 and Stata Version 9 (StataCorp, 2005),16 to account for this weighting and the stratified sampling design. Confidence intervals (95%) were calculated for all estimates presented in tables. Interval ranges were specified in the table endnotes.
χ2 tests and 95% confidence intervals around percentages were used to assess the relationship between selected clinician characteristics and (1) knowledge items in which <70% of respondents answered correctly (dichotomized as correct or incorrect) and (2) counseling practices in which <70% of respondents reported practices consistent with scientific evidence (dichotomized as usually/always combined vs. half the time/sometimes/never combined). These characteristics were specialty (each of 9 specialties) diagnostic experience (<5 vs. ≥5 patients with anogenital warts in the last year), gender, age (<45 years vs. ≥45 years), practice type (group vs. solo), practice location (urban vs. other), and practice region (Northeast, South, West, and Midwest). We also analyzed how selected knowledge topics varied by counseling practices, HPV testing of patients with genital warts (not approved by FDA), and Pap testing frequency recommendations for female patients with warts. A two-tailed probability of <0.05, and nonoverlapping 95% confidence intervals (CI) between comparison groups were considered statistically significant.
To supplement the univariate analyses, we simultaneously entered all the variables significantly associated with a given outcome in univariate analysis into logistic regression models. We then identified variables that remained significantly associated with that outcome after adjusting for the remaining variables. An adjusted odds ratio (AOR) in which 95% CI did not overlap 1.0 was considered statistically significant (data not included in tables). Reference categories for measures with 3 or more categories were assigned as follows: obstetrics and gynecology physicians for specialty and Midwest for region.
Results
Response Rate
Of the 6906 surveys mailed, 690 were undeliverable, and 25 were sent to deceased clinicians. There were 1005 clinicians who refused or did not respond, and 881 were ineligible. There were 4305 completed surveys, and after adjusting for ineligibility, deceased recipients, and undeliverable surveys the overall response rate was 81%. Response rates were higher for midlevel providers (nurse practitioners 96%, certified nurse midwives 95%, physicians' assistants 86%) than for physicians (obstetrics/gynecology 81%, dermatology 80%, adolescent medicine 79%, urology 78%, family medicine 68%, and general internal medicine 59%). We restricted all further analyses to the 89% of clinicians (n = 3836) who reported ever diagnosing anogenital warts at their principal practice site.
Respondent Characteristics
The majority of clinicians reported practicing in a private practice office (76%), were of white race (83%), and were male (59%) (Table 1). Most reported being in practice >10 years (mean 16 years); had a majority of patients that were female, white, and half that were privately insured (Table 1). Of these 3836 clinicians who reported ever diagnosing anogenital warts, 74% diagnosed anogenital warts in the past 12 months. The median reported number of patients with anogenital warts diagnosed in the past 12 months was 5. The remaining 22% of clinicians who did not diagnose anogenital warts in the last 12 months reported a median of 3 years since their last diagnosis (Table 1). Most clinicians also reported prior experience diagnosing other STDs, with a median of 5 and 10 diagnoses of chlamydia and genital herpes in the last 12 months, respectively. Ninety percent of clinicians reported offering Pap test screening in their practices, and 56% reported that they use HPV tests for any reason at their principal practice site.
HPV and Anogenital Wart-Related Knowledge
Most clinicians were aware that genital HPV infection is fairly common (90%), that HPV infection may be asymptomatic (95%), that HPV infection causes anogenital warts (89%), and that treatment of anogenital warts does not always permanently eliminate the causative infection (93%). However, less than half of clinicians knew that HPV types usually associated with warts differ from HPV types usually associated with cancer (48%), that anogenital warts do not increase the risk of cancer at the same anatomical site where the warts are located (38%), or that most genital HPV infections clear without medical intervention (36%) (Table 2). Obstetrician/gynecologists and nurse midwives were significantly more likely to respond correctly to more HPV knowledge questions than clinicians in the other specialties. Of the 3 topics in which knowledge was least up-to-date, gaps in knowledge were associated with specialty, gender, and age (Tables 2 and 3). In addition, practice type (group vs. solo), and wart diagnosis experience were associated with knowledge gaps regarding HPV genotypes and spontaneous clearance of HPV infection (Table 3). Multivariate analysis revealed that these knowledge gaps were greatest among clinicians who were older (AOR for statements ranged from 1.30-1.43, 95% CIs did not overlap 1.0) and practiced specialties other than obstetrics/gynecology (for spontaneous HPV clearance and HPV genotype differences, AORs for all specialties exceeded 1.73; for cancer risk at site of warts, AORs exceeded 1.44 for internal medicine, physician assistants, and dermatologists). In addition, male clinicians were significantly more likely to be unaware that most HPV infections clear spontaneously (AOR 1.48, 95% CI 1.10-1.98) and that wart and cancer-related HPV genotypes usually differ (AOR 1.62, 95% CI 1.23-2.14), and clinicians in solo practice were more likely to be unaware that most infections clear spontaneously (AOR 1.74, 95% CI 1.28-2.37).
Information Needs and Sources of Clinicians to Guide Management of Patients With Anogenital Warts
When asked which information sources were most valuable in guiding clinical decisions in the management of patients with anogenital warts, 68% of all clinicians who have ever diagnosed anogenital warts rated guidelines or materials of their own specialty organization as somewhat or quite valuable, and 60% rated materials of the CDC as somewhat or quite valuable. A total of 52% respondents, of whom 67% were not obstetrician/gynecologists, rated materials of the American College of Obstetricians and Gynecologists as somewhat or quite valuable. Although other sources were less highly rated, over one-third of clinicians rated materials of the American Medical Association, information from companies that market drugs, devices or equipment to diagnose or treat warts, and the clinical practice guidelines of the health system at their principal practice site as valuable (Table 4).
Most of the clinicians in this survey reported that there is a need for information to guide management and counseling of patients with anogenital warts. Over 90% of clinicians rated the following topics as important to include in clinical training materials or clinical decision support tools: modes of transmission of genital HPV infection associated with warts; diagnosis and treatment of external anogenital warts; methods to prevent transmission of warts to sex partners; influence of treatment on persistent HPV infection and infectiousness; value of informing sex partners and what to say; whether external anogenital warts are related to cervical cancer; information on vaccines that prevent acquisition of genital HPV or genital warts, if they become available; biologic causes of external anogenital warts; whether external anogenital warts are related to fertility, pregnancy outcomes, or newborn health; and possible intervals between HPV infection and first detection of warts.
Counseling Practices of Clinicians Who Have Diagnosed Anogenital Warts
Nearly all clinicians reported telling patients that anogenital warts are sexually transmitted and are caused by a virus; that their current sex partners may have or may acquire warts, and that they may have been infected months or years before (Table 5). About three-quarters reported telling patients that not much is known about the duration of the infection with or without treatment. The majority of clinicians in all specialties also indicated that they usually or always discuss STD prevention, discuss ways to prevent HPV transmission to sex partners, tell patients to notify sex partners, and ask about a patient's sexual behavior to assess risk for STD (Table 5).
The majority of clinicians reported usually or always telling patients that they can prevent transmission of the infection to sex partners by using condoms (90%), practicing monogamy or limiting the number of lifetime sex partners (79%), talking to current or future sex partner(s) about preventing the infection (70%), or by avoiding contact with warts, especially during sexual foreplay (61%). However, only 43% of all clinicians reported usually or always discussing prevention of wart transmission by abstaining from sex although abstinence is a highly effective method10 (Table 4). On univariate analysis, specialty and region were significantly associated with clinicians explaining abstinence as a prevention method; adolescent medicine physicians were significantly more likely to report usually or always recommending abstinence than clinicians in other specialties (Table 5), while clinicians practicing in the Northeast (38%) and West (38%) were least likely to make this recommendation (Midwest 49%, South 47%, data not in tables). These 2 clinician characteristics remained associated with this counseling practice in multivariate analyses (adolescent medicine physicians AOR 2.95, 95% CI 2.16-4.03, reference category obstetrics/gynecology; Northeast and West AOR 0.67, 95% CI 0.48-0.93, AOR 0.65 95%CI 0.47-0.90 respectively, reference category Midwest). Telling patients that they can prevent transmission of HPV infection by avoiding contact with warts was not associated with any clinician characteristics examined.
Clinicians reported that many issues are problematic when counseling patients with anogenital warts, including providing definitive answers about when or from whom HPV infection was acquired (86%); dealing with patients' emotional, psychosocial, and relationship issues (76%); reimbursement for time needed for patient counseling or education (73%); motivating patients to adopt measures to prevent wart transmission (67%); or finding time to counsel or educate patients (56%).
Relation of HPV Knowledge and Clinician Characteristics With Cervical Cancer Screening Recommendations for Female Patients With Anogenital Warts
Most (82%) clinicians reported usually or always recommending a Pap test promptly to female patients diagnosed with anogenital warts, and 52% reported usually or always recommending future Pap testing more frequently than the patient's usual interval. To determine whether knowledge about HPV and anogenital warts influenced Pap testing recommendations for female patients with warts, we compared clinicians who responded correctly to certain knowledge questions with clinicians who responded incorrectly. We found that clinicians who were aware that wart-related HPV types usually differ from cancer-related HPV types were significantly less likely to usually or always recommend a prompt Pap test (78% vs.87%, P = 0.0001) and more frequent future Pap testing (47% vs. 57%, P = 0.0005) for their female patients with anogenital warts than clinicians who were not aware of this HPV genotype distinction. Similarly, clinicians who knew that warts do not increase cancer risk at the same anatomical site where the warts are located were also significantly less likely than those who did not know this to usually or always recommend a prompt Pap test (79% vs. 84%, P = 0.0193) or more frequent Pap testing (45% vs. 56%, P = 0.0003) to female patients with warts.
Univariate analysis revealed that clinicians with less wart diagnosis experience were more likely to recommend that female patients with warts have a Pap test promptly; the recommendation to provide more frequent Pap testing was significantly more common among clinicians who were male, older (age >45 years), solo practitioners (compared with group practitioners), clinicians with limited wart diagnostic experience (<5 patients with anogenital warts in the last year), as well as internists, nurse practitioners, and physician assistants (as compared with obstetrician/gynecologists, the reference category). On multivariate analysis, clinicians with these characteristics were more likely to usually or always recommend more frequent future Pap testing to female patients with warts: limited wart diagnostic experience (AOR 1.61, 95% CI 1.22-2.14), solo practice (AOR 1.86, 95% CI 1.35-2.55), older age (AOR 1.90, 95% CI 1.43-2.50), and selected specialties (internal medicine physicians: AOR 2.01, 95% CI 1.26-3.19; nurse practitioners: AOR 1.50, 95% CI 1.04-2.14; physician assistants: AOR 1.68, 95% CI 1.18-2.40).
Relation of HPV Knowledge and HPV Testing Practices for Female Patients With Anogenital Warts
Of clinicians who reported using HPV tests at their principal practice site, 34% reported ever ordering HPV DNA tests to check the infection status for female patients with anogenital warts, a use that is not approved by the FDA. The use of HPV tests for female patients with warts was not significantly associated with any of the HPV-related knowledge issues we assessed.
Discussion
This study is the first nationally representative survey to examine current knowledge of anogenital warts, counseling practices, and clinical follow-up advice of US clinicians who care for patients diagnosed with anogenital warts. Strengths of this study include the large sample size and high response rate and the use of a stratified sampling design and weighted analysis, which make the results more nationally representative of each specialty and of the composite across all 9 specialties. We also included midlevel providers who provide a large amount of anogenital wart care but are often overlooked in clinician surveys. The clinicians included in this analysis represent those with a range of diagnostic experience, making it more representative of the wide range of providers who provide wart care. Survey question format and content were developed using extensive formative research with focus groups on key HPV and wart issues, expert review, and piloting several drafts with practicing clinicians in all specialties. Use of close-ended formats posed questions consistently and concisely and listed possible responses based on this formative research, but may have missed some important issues.
Like all surveys, this one has some limitations. First, knowledge and practices of responders may have differed substantially from those of nonresponders. However, the survey's high response rate and weighting for nonresponse minimizes possible bias. Other studies show that nonresponse bias tends to be less problematic among physicians than other groups.17 Second, because we did not compare survey responses to medical records or other clinical data that may more accurately reflect actual practice, we may have slightly overestimated delivery of appropriate counseling messages if clinicians reported best practices that did not reflect their actual practices, a phenomenon seen in other studies.18-20 To minimize this bias, the survey cover letter did not detail plans to compare reported practices with best practices or guidelines.
Despite these limitations, some important findings emerge. Most clinicians were aware of the latest scientific evidence that HPV is common, usually asymptomatic, sexually transmitted, and causes anogenital warts. However, many clinicians in all specialties were unaware that most genital HPV infections clear without medical intervention, that HPV types usually associated with warts differ from HPV types usually associated with cancer, and that anogenital warts do not usually increase the risk of cancer at the same anatomical site where warts are located. This knowledge gap was least evident among obstetrician/gynecologists, nurse midwives, and female clinicians. A recent survey in Mexico found that 62% of obstetrician/gynecologists and general practitioners were not aware that high-risk HPV types do not usually cause anogenital warts.21 Confusion about wart- and cancer-related HPV types may explain why about a third of clinicians reported ever ordering HPV tests for female patients with anogenital warts, although the test is not approved for managing warts.7 Although genital warts may be a marker for exposure to HPV of various types, many studies have shown that the predominant HPV types associated with anogenital warts (HPV-6 and -11) usually pose no risk of malignant progression.22 The rare reports of malignant transformation of warts caused by high-risk HPV genotypes have been reported in immunocompromised patients.23,24
The misperception that benign warts may become malignant or that women exposed to low-risk HPV types may be at increased risk for exposure to high-risk types may explain why about half of all clinicians recommended prompt or more frequent Pap testing for female patients with warts. A study of college health care providers also found that providers reported practicing more aggressive management approaches on several aspects of HPV infection, including genital warts, than what is recommended by guidelines.25 Current evidence and guidelines do not support the clinical value of immediate or more frequent Pap testing in female patients with warts.10,26,27 Unnecessary Pap testing may lead to unnecessary clinician and patient burden, health care costs, and patient discomfort and anxiety. These gaps in knowledge and practices suggest that knowledge-based interventions such as training and clinical decision support tools may help reduce unnecessary Pap testing of female patients with warts. Interventions should prioritize male, older, and solo practitioners with less diagnosis experience, as well as internists, nurse practitioners, and physician assistants who most commonly reported more aggressive Pap testing in patients with warts.
A diagnosis of anogenital warts can be quite distressing to patients, and education and counseling are integral to proper management of this condition.12,28 Thus, it was reassuring that most surveyed clinicians reported counseling practices about the cause and prevention of anogenital warts that are consistent with current evidence, including that HPV is sexually transmitted, that the timing of initial HPV acquisition is uncertain, and that sex partners may be infected and should be informed of possible exposure. Moreover, about three-quarters of respondents reported telling patients that not much is known about the duration of infection with or without treatment. This may reflect the fact that information about the typically short duration of infection detectable with HPV tests from cervicovaginal specimens is relatively new,29-31 data on the duration of HPV infection in wart tissue is limited, and HPV testing may miss latent infection in some tissue.32 We found that most clinicians reported usually or always asking about a patient's sexual behavior to assess risk for STDs, in contrast to another study which found that 75% of patients with warts reported their provider did not ask about sexual practices.12 Although abstinence eliminates risk of wart transmission, clinicians were less likely to address abstinence than less effective prevention methods of condom use or reducing sex partner number. This probably reflects the view that abstinence is effective but not likely to be adopted by sexually active patients.
In a 1996 survey of patients diagnosed with anogenital warts, patients reported dissatisfaction with their providers' counseling about HPV; nearly 60% rated their providers' openness to discussion, provision of adequate information, and emotional support as either poor or fair.12 Many patients also reported that providers failed to offer advice on emotional issues surrounding HPV infection (84%).12 This is consistent with our finding that most clinicians in our study reported that dealing with patients' emotional, psychosocial, and relationship issues is problematic when counseling patients with anogenital warts. Many potential barriers to STD counseling have been described in the literature, such as time constraints, limited staff, limited reimbursement, and discomfort of clinicians or patients with discussing sexual issues.33-36 Similarly, the majority of clinicians in our survey identified inadequate reimbursement or finding time to counsel or educate patients as key challenges for most of their patients with anogenital warts. Interventions to improve counseling for these patients should address these issues.
To improve clinician knowledge and promote appropriate counseling of patients with anogenital warts, up-to-date educational materials are needed, including information regarding Pap screening guidelines for female patients with warts, materials to help patients communicate with sex partners, and information to help patients deal with the anxiety and stigma associated with warts. Clinicians rated as valuable some of the most accurate available information sources to guide management of patients with anogenital warts, and indicated that these materials need to address multiple, complex, and sensitive topics, including partner notification.
Evaluations of clinician training and patient educational materials about HPV and anogenital warts available until recently found that many materials were too complex, included marginal or out-of-date HPV information content, required college-level literacy, and were not suitable for culturally diverse patients with low literacy levels.37,38 Fortunately, new clinician training curricula, decision-support tools, and patient education materials that have been developed reflect the latest information about anogenital wart diagnosis, management, and counseling, including information that details the differences between wart and cancer-related HPV genotypes.9,39-41 Some of these materials address key knowledge gaps we identified and highlight appropriate Pap testing practices for female patients with warts, are appropriate for diverse patient populations, and are available in Spanish.39-41.
Although patients with anogenital warts may gain access to information about their condition from many nonclinical sources, including friends or family, the mass media, and commercial sources,11 clinicians are in a unique position to reinforce correct messages, fill knowledge gaps and dispel myths. Risk-reduction counseling and education are both integral to management of patients with anogenital warts and are needed to encourage patients to adopt healthy sexual behaviors and to give them the information needed to allay unwarranted fears. In order for clinicians to provide these much-needed services, they must be equipped with the most current information, so that the messages they communicate to their patients are clear, relevant, and complete.
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