Abstract
OBJECTIVES: The objectives of this study were to assess, in a nationally representative network of pediatricians and family physicians, (1) human papillomavirus (HPV) vaccination practices, (2) perceived barriers to vaccination, and (3) factors associated with whether physicians strongly recommended HPV vaccine to 11- to 12-year-old female patients.
METHODS: In January through March 2008, a survey was administered to 429 pediatricians and 419 family physicians.
RESULTS: Response rates were 81% for pediatricians and 79% for family physicians. Ninety-eight percent of pediatricians and 88% of family physicians were administering HPV vaccine in their offices (P < .001). Among those physicians, fewer strongly recommended HPV vaccination for 11- to 12-year-old female patients than for older female patients (pediatricians: 57% for 11- to 12-year-old patients and 90% for 13- to 15-year-old patients; P < .001; family physicians: 50% and 86%, respectively; P < .001). The most-frequently reported barriers to HPV vaccination were financial, including vaccine costs and insurance coverage. Factors associated with not strongly recommending HPV vaccine to 11- to 12-year-old female patients included considering it necessary to discuss sexuality before recommending HPV vaccine (risk ratio: 1.27 [95% confidence interval: 1.07–1.51]) and reporting more vaccine refusals among parents of younger versus older adolescents (risk ratio: 2.09 [95% confidence interval: 1.66–2.81]).
CONCLUSIONS: Eighteen months after licensure, the vast majority of pediatricians and family physicians reported offering HPV vaccine. Fewer physicians strongly recommended the vaccine for younger adolescents than for older adolescents, and physicians reported financial obstacles to vaccination.
WHAT'S KNOWN ON THIS SUBJECT:
A HPV vaccine was licensed in 2006. In surveys before vaccine licensure, physicians generally viewed HPV vaccines positively, but some expressed reservations about vaccinating young adolescents. Little is known about current HPV vaccination practices of US physicians.
WHAT THIS STUDY ADDS:
This study found that, 18 months after licensure, the vast majority of pediatricians and family physicians reported offering HPV vaccine. Fewer physicians strongly recommended the vaccine for younger adolescents than for older adolescents, and physicians reported financial obstacles to vaccination.
Approximately 20 million people in the United States currently are infected with genital human papillomavirus (HPV).1,2 HPV types 16 and 18 cause ∼70% of cervical cancer cases throughout the world,3 and types 6 and 11 are responsible for ∼90% of anogenital warts.4 Substantial proportions of HPV-associated morbidities and deaths may be prevented through vaccination, however. A quadrivalent (types 6, 11, 16, and 18) HPV vaccine was licensed in the United States in June 2006 and was approved initially for female patients 9 to 26 years of age.5 In October 2009, a bivalent (types 16 and 18) HPV vaccine was licensed,6 and quadrivalent HPV vaccine was approved for male patients.7 HPV vaccination is recommended currently for 11- to 12-year-old female patients, with “catch-up” vaccination being recommended for unimmunized 13- to 26-year-old female patients.5
The policy decision to target 11- to 12-year-old female adolescents for HPV vaccination was based on HPV-specific and broader health care delivery considerations. Although the median age of first sexual intercourse in the United States is 17 years, 13% of girls initiate sexual activity before 15 years of age8 and 4% before 13 years of age.9 HPV vaccination does not protect against HPV types to which women have already been exposed, and vaccination at 11 to 12 years, rather than older ages, increases the likelihood that immunization would occur before any sexual activity. There also have been efforts to synchronize HPV vaccine delivery with delivery of other adolescent vaccines10,11 and with recommended well-adolescent visits, a concept referred to as the “adolescent immunization platform.”12 The intent has been to coordinate delivery of adolescent vaccines with delivery of preventive care, thereby creating mechanisms for achieving high adolescent immunization coverage while enhancing broader health care provision to adolescents.13
Several studies examined physician attitudes and intended practices regarding HPV vaccination14,–,18; however, those surveys were conducted either before vaccine licensure14,–,17 or after licensure but before vaccine was widely available.18 Although additional data regarding HPV vaccination practices were gathered from Texas physicians19 and from geographic areas with high cervical cancer incidence,20,21 more current nationwide data have been unavailable. The objectives of this study were to assess, in a nationally representative network of pediatricians and family physicians, HPV-related attitudes and vaccination practices, perceived barriers to vaccination, and factors associated with whether physicians strongly recommended HPV vaccine to 11- to 12-year-old female patients.
METHODS
Study Setting
In January to March 2008, a survey was administered to a national network of primary care physicians. The human subjects review board at the University of Colorado Denver approved the study, and written informed consent was not required.
Study Population
The study was conducted by the Vaccine Policy Collaborative Initiative, a program designed with the Centers for Disease Control and Prevention to perform assessments of physician attitudes about important, timely, vaccine-related issues. For this program, a national network of physicians was developed, with pediatricians and family physicians being recruited from the American Academy of Pediatrics and the American Academy of Family Physicians, respectively. Quota sampling22 was performed to ensure that network physicians were similar to the American Academy of Pediatrics and American Academy of Family Physicians memberships overall with respect to several practice characteristics (region of country, urban versus rural location, and practice type). As described elsewhere,23 the representativeness of the network has been examined in a systematic manner. Demographic characteristics, practice attributes, and reported attitudes regarding a range of vaccination issues were generally similar when network physicians were compared with physicians sampled randomly from the American Medical Association physician database.23
Survey Design and Administration
The survey instrument was developed on the basis of existing literature findings14,–,16,24,25 and was pilot-tested with a community advisory panel of pediatricians and family physicians. Items regarding physician attitudes and perceived barriers to vaccination were asked by using 4-point Likert-type scales.26 Questions regarding HPV vaccination practices and experiences with vaccine refusal were asked only of physicians who reported administering HPV vaccine in their offices. HPV vaccine refusal was defined in the survey instrument as outright refusal without plans for future vaccination; deferral was defined as postponing vaccination with the intention of considering it in the future.
Physicians were surveyed through the Internet or, if they preferred, by mail. The Internet survey was administered by using an Internet-based program (Vovici, Dulles, VA). The Internet group received an initial e-mail and up to 8 e-mail reminders to complete the survey, whereas the mail group received up to 3 surveys by mail. Because of the possibility of incorrect or nonfunctional e-mail addresses, the Internet group received a final survey by mail if they had not responded by Internet.
Analytic Methods
Respondents were compared with nonrespondents with respect to all available characteristics. Internet and mail surveys were pooled for all analyses, because physician attitudes have been found to be comparable when assessed with the 2 methods.27 HPV-related knowledge, attitudes, and practices were compared between pediatricians and family physicians. Bivariate and multivariate analyses were performed to examine the association between prespecified independent factors (demographic and practice characteristics, HPV-related attitudes, and perceived barriers to vaccination) and whether physicians strongly recommended HPV vaccine to 11- to 12-year-old female patients. Factors with P < .25 in bivariate analyses were tested by using multivariate logistic regression,28 and factors with P < .05 were retained in the final multivariate model. Although it was not statistically significant at P < .05, physician specialty was retained in the multivariate model because of the potential influence of specialty on vaccination practices.29,30 Because odds ratios may overestimate effect sizes when outcomes of interest are common,31 odds ratios were converted to risk ratios by using generalized linear modeling.32 Statistical analyses were performed by using SAS 9.2 (SAS Institute, Cary, NC).
RESULTS
Survey Response Rates and Characteristics of Respondents
Survey response rates were 81% (349 of 429 physicians) for pediatricians and 79% (331 of 419 physicians) for family physicians. For pediatricians, respondents were similar to nonrespondents with respect to gender, year of graduation, region of the country, urban versus rural practice location, and type of practice. For family physicians, respondents were similar to nonrespondents with respect to practice location and type. Survey response rates were higher for family physicians in the Northeast (84%) and West (88%), relative to the South (72%) and Midwest (77%; P = .02 for comparison of response rates according to region). Data on gender and year of graduation were not available for family physician nonrespondents.
The characteristics of survey respondents are presented in Table 1. Pediatricians were more likely than family physicians to participate in the Vaccines for Children program and reported larger proportions of adolescent patients in their practices. Family physicians were more likely to report performing gynecologic examinations for female adolescent patients.
Characteristics of Survey Respondents
Attitudes Regarding Adolescent Health Care
Five percent of pediatricians strongly agreed and 38% somewhat agreed with the statement, “It is hard to establish continuity of care with female adolescent patients”; corresponding proportions for family physicians were 9% and 42%, respectively. Fifteen percent of pediatricians strongly agreed and 53% somewhat agreed with the statement, “Female adolescents are coming in for preventive health visits to receive HPV vaccine”; corresponding proportions for family physicians were 11% and 40%, respectively. The vast majority of respondents (84% of pediatricians and 89% of family physicians) reported feeling comfortable discussing sexuality with female adolescent patients.
Knowledge and Attitudes Regarding HPV Infection and HPV Vaccination
As shown in Table 2, most physicians were knowledgeable about several aspects of HPV infections, although only 43% of pediatricians and 58% of family physicians knew that genital warts are caused by different HPV types than the types that cause cervical cancer. Most respondents also were knowledgeable about HPV vaccination, although only 69% of family physicians knew that a pregnancy test was not required before HPV vaccination.
Respondent Knowledge Regarding HPV Infections and HPV Vaccination (N = 680)
Physicians reported a range of attitudes about administering HPV vaccine to female adolescents in their practices (Table 3). Forty-two percent of pediatricians and 54% of family physicians considered it necessary to discuss sexuality before recommending HPV vaccine. Few physicians thought that vaccination against a sexually transmitted infection would encourage earlier or riskier sexual behavior among patients, although almost one-half reported that parents were concerned about this issue.
Attitudes and Experiences Regarding HPV Vaccination Among Providers Currently Administering HPV Vaccine in Their Offices (N = 619)
Perceived Barriers to HPV Vaccine Use
Physician perceptions regarding barriers to administering HPV vaccine in their offices are presented in Table 4. The most-frequently reported barriers for both pediatricians and family physicians were financial, related to insurance coverage, reimbursement for HPV vaccination, and vaccine purchasing costs. Parent opposition to HPV vaccination for moral or religious reasons was perceived as definitely or somewhat a barrier by 23% of pediatricians and 33% of family physicians. Although 32% of pediatricians and 25% of family physicians perceived parent concerns about HPV vaccine safety as definitely or somewhat a barrier, physicians rarely reported that they themselves were concerned about HPV vaccine safety.
Perceived Barriers to HPV Vaccination Among Surveyed Pediatricians and Family Physicians (N = 680)
Reported HPV Vaccination Practices
Overall, 98% of pediatricians and 88% of family physicians reported that HPV vaccine was being administered to female patients in their offices (P < .001). Ninety-five percent of female family physicians reported giving HPV vaccine in their offices, compared with 83% of male family physicians (P = .001). In addition, 79% of family physicians from the South reported administering HPV vaccine in their offices, compared with 89% from the Northeast, 95% from the Midwest, and 92% from the West (P = .005 for comparison of administration rates according to region). Comparisons of HPV vaccine administration rates according to physician gender and region were not performed for pediatricians, because of the small number of pediatricians (n = 6) who did not offer HPV vaccine.
Among physicians who administered HPV vaccine in their offices, whether they strongly recommended the vaccine varied depending on the age of the patient (Fig 1). In both specialties, greater proportions of physicians strongly recommended the vaccine for older age groups. For 11- to 12-year-old female patients, 56% of pediatricians strongly recommended the vaccine and an additional 38% recommended the vaccine but not strongly; corresponding proportions for family physicians were 50% and 43%, respectively.
Proportions of physicians who strongly recommend HPV vaccine to female patients in various age groups.
When discussing HPV vaccination for the first time, 25% of pediatricians and 38% of family physicians reported that they personally discussed the vaccine with adolescent patients and their parents for ≥5 minutes. In comparison, 6% of physicians in both specialties reported ≥5 minutes of discussion about tetanus toxoid-reduced diphtheria toxoid-acellular pertussis vaccination. When discussing HPV vaccination with adolescents and their parents, 96% of pediatricians and 94% of family physicians strongly emphasized cervical cancer prevention. In contrast, 35% of pediatricians and 34% of family physicians strongly emphasized prevention of genital warts in the patient herself and 9% and 11%, respectively, strongly emphasized prevention of genital warts in the patient's sexual partners.
Respondents were queried about their use of strategies to promote series completion among patients who started the 3-dose HPV vaccine series. Because responses generally did not differ according to specialty, results from pediatricians and family physicians were combined. Eighty-one percent of physicians reported having patients schedule future appointments at the time they received their first dose, 59% reported recording when the next dose was due on a paper-based card that the patient kept, 35% reported using reminder/recall letters or telephone calls, and 33% reported using a computerized immunization information system (ie, registry) to track when the next dose was due.
Eighteen percent of pediatricians and 29% of family physicians reported that at least one-fourth of parents of 11- to 12-year-old patients refused HPV vaccine (P < .01). In addition, 45% of pediatricians and 49% of family physicians reported that at least one-fourth of parents of this age group deferred HPV vaccine (P = .36). Vaccine refusal and deferral were reported less frequently for parents of 13- to 15-year-old patients than for parents of 11- to 12-year-old patients. Commonly reported parental reasons for refusal and deferral included the following: the vaccine was “too new,” the adolescent was “too young,” and the parent's health insurance did not cover HPV vaccination.
Factors Associated With Not Strongly Recommending HPV Vaccination at 11 to 12 Years of Age
The result of bivariate and multivariate analyses of factors associated with vaccination recommendations for 11- to 12-year-old female patients are presented in Table 5. Factors associated with greater likelihood of not recommending HPV vaccine strongly to this age group included considering it necessary to discuss sexuality before recommending HPV vaccine, the time it takes to discuss HPV vaccination, and reports of more parental vaccine refusals among younger patients than among older adolescent patients. Physicians who reported larger proportions of publicly insured patients were more likely to recommend the vaccine strongly to 11- to 12-year-old female patients.
Factors Associated With Not Strongly Recommending HPV Vaccine to 11- to 12-Year-Old Female Patients Among Pediatricians and Family Physicians Administering HPV Vaccine in Their Practices (N = 608)
DISCUSSION
Eighteen months after licensure of the first HPV vaccine in the United States, nearly all surveyed pediatricians and the vast majority of family physicians reported administering HPV vaccine to female patients in their offices. However, fewer physicians strongly recommended the vaccine for 11- to 12-year-old patients than for older patients, and physicians reported more vaccine refusals from parents of younger patients, compared with older female adolescents. In addition, physicians in both specialties reported financial barriers to HPV vaccination. Although widespread availability of HPV vaccine in primary care offices should facilitate immunization delivery to targeted patient populations, these data suggest that HPV vaccination often may not be started until after 12 years of age. Most surveyed physicians were not using active strategies to ensure that patients who started HPV vaccination received all 3 doses, which may further delay the age at which patients are fully immunized.
Historically, pediatricians have more rapidly incorporated new vaccines into their practices, compared with family physicians.29,30,33,34 Between 8 and 17 months after licensure of a pneumococcal conjugate vaccine, 92% to 99% of pediatricians, compared with 55% to 68% of family physicians, were using the vaccine.29,30 Approximately 18 months after licensure of a new human-bovine rotavirus vaccine, 85% of pediatricians, compared with 45% of family physicians, reported using the vaccine.34 In the current study, although more pediatricians (98%) than family physicians (88%) reported HPV vaccine use, the difference was relatively small. This finding may be related to the fact that, in contrast to pneumococcal and rotavirus disease, family physicians are likely to have much more clinical experience treating HPV-related disease in their practices. Family physicians also may have adult female patients (ie, 19–26 years of age) in their practices inquiring about HPV vaccination.
For primary care practitioners, financial concerns continue to be perceived as prominent barriers to the delivery of new vaccines.35 The high rates of vaccine use reported in this study were noted despite these financial concerns; some physicians who reported that vaccine purchase cost and reimbursement issues were definitely a barrier to vaccine use were nonetheless providing HPV vaccine in their offices. Although this is relatively reassuring, financial concerns might well have contributed to the decision of 12% of surveyed family physicians not to provide HPV vaccine at all. In fact, in a 2007 survey of US pediatricians and family physicians, 49% of respondents reported that their practice had delayed purchase of a new vaccine in the previous 3 years only because of financial concerns.35 Given that quadrivalent HPV vaccine is one of the more-expensive vaccines currently licensed, at approximately $120 per dose,36 continued and expanded use may depend in part on practice-level financial considerations.37 If the US vaccine system is at risk of a future financial “meltdown,” as some have suggested,38 then HPV and other newer vaccines will be at particular risk.
These survey data indicate that there may be substantial challenges to timely initiation and completion of the 3-dose HPV vaccine series. Physicians were more likely to endorse HPV vaccination strongly for female adolescents of older ages and reported more vaccine refusals among parents of younger than older adolescents, findings consistent with results of prelicensure studies with physicians14,–,17 and parents.39,40 Because adolescents are seen infrequently in primary care settings,41,–,43 proactive strategies such as patient reminder/recall44 may be needed to ensure that female patients who initiate HPV vaccination complete the 3-dose series in a timely manner. However, almost two-thirds of physicians in the current study were not conducting any reminder/recall activities for female patients needing a second or third HPV vaccine dose. Therefore, developing a coordinated adolescent vaccination platform may be more difficult to achieve than the well-synchronized infant platform on which it was modeled. For example, if HPV vaccine is refused or deferred until after 12 years of age, then subsequent visits for HPV vaccination may need to be uncoupled from well-adolescent care visits, particularly for the second and third vaccine doses.45 To place these findings in the context of current US immunization rates, 37% of adolescent female patients 13 to 17 years of age had received ≥1 HPV vaccine dose and 18% had received all 3 doses in 2008.46
This investigation is subject to several limitations. The survey was conducted with a previously recruited national network of physicians; although the representativeness of this network was examined previously,23 the attitudes of network physicians might differ from those of physicians outside the network. In addition, the attitudes of survey respondents might differ from those of nonrespondents, although the high survey response rate likely minimized this type of bias. The study assessed physician-reported behavior, rather than observing actual vaccination practices. It is not known how physicians convey a “strong vaccination recommendation” to patients and parents, and this may differ among physicians and between pediatricians and family physicians. Only pediatricians and family physicians were surveyed, although other physicians, such as obstetricians/gynecologists and internists, may provide HPV vaccine to adolescents. However, female adolescents <18 years of age are much more likely to have health care visits with either pediatricians or family physicians than with other primary care physicians.42
CONCLUSIONS
According to data from this national survey, nearly all pediatricians and the vast majority of family physicians started using quadrivalent HPV vaccine within 18 months after vaccine licensure. In some cases, HPV vaccination occurred despite the perception that substantial financial barriers to vaccine use were present. With physicians being more likely to recommend the vaccine strongly at older ages and parents reportedly being more likely to refuse or to defer vaccination at younger ages, an upward shift in the age at receipt of a first dose of HPV vaccine may occur, despite national recommendations for vaccination at 11 to 12 years of age. It also is likely that proactive, innovative strategies will be needed to achieve high levels of 3-dose HPV vaccination coverage in the United States.
ACKNOWLEDGMENTS
This investigation was funded by the Centers for Disease Control and Prevention (grant 5-U48-DP000054-03). This funding was obtained and administered through the Rocky Mountain Prevention Research Center, University of Colorado (Denver, CO).
We thank the participating physicians for their time and effort in responding to this survey.
Footnotes
- Accepted May 13, 2010.
- Address correspondence to Matthew F. Daley, MD, Institute for Health Research, Kaiser Permanente Colorado, 10065 E. Harvard Ave, #300, Denver, CO 80231. E-mail: matthew.f.daley{at}kp.org
Portions of this work were presented at the meeting of the Advisory Committee on Immunization Practices, October 22, 2008, Atlanta, GA; the National Immunization Conference, April 1, 2009, Dallas, TX; and the annual meeting of the Pediatric Academic Societies, May 5, 2009, Baltimore, MD.
The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention.
FINANCIAL DISCLOSURE: The authors have indicated they have no financial relationships relevant to this article to disclose.
- HPV =
- human papillomavirus
REFERENCES
The Newest Forensic Tool: Bacterial Fingerprints: Bacterial ecosystems that live on our skin and are left behind when we touch objects appear to be unique to each individual—at least according to an article in Discover Magazine (Talkington M, July 2010). According to Noah Fierer, a microbial ecologist at the University of Colorado at Boulder, “Once you look at these microbes at the species level, we are all pretty much distinct.” Dr Fierer and his colleagues showed this by sequencing short stretches of bacterial DNA swabbed from fingertips and computer keyboards and found they could match the genetic material on the keyboard to a particular individual and months later, could still find the same bacteria on their fingertips suggesting that these unique ecosystems are permanent residents on our unique skin. Dr Fierer plans to study how the environment can shape or reshape these predictable bacterial patterns, which may someday help forensic investigators not only identify a suspect, to solve a crime, but also the environment or locale in which that suspect might have been living. This is one forensic technique where good hand-washing will not destroy what appears to be a permanent bacterial ecosystem unique to each of us.
Noted by JFL, MD
- Copyright © 2010 by the American Academy of Pediatrics
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