Human Papillomavirus Vaccination Practices: A Survey of US Physicians 18 Months After Licensure Matthew F. Daley, Lori A. Crane, Lauri E.

Markowitz, Sandra R. Black, Brenda L. Beaty, Jennifer Barrow, Christine Babbel, Sami L. Gottlieb, Nicole Liddon, Shannon Stokley, L. Miriam Dickinson and Allison Kempe Pediatrics 2010;126;425; originally published online August 2, 2010; DOI: 10.1542/peds.2009-3500

The online version of this article, along with updated information and services, is located on the World Wide Web at:
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PEDIATRICS is the official journal of the American Academy of Pediatrics. A monthly publication, it has been published continuously since 1948. PEDIATRICS is owned, published, and trademarked by the American Academy of Pediatrics, 141 Northwest Point Boulevard, Elk Grove Village, Illinois, 60007. Copyright 2010 by the American Academy of Pediatrics. All rights reserved. Print ISSN: 0031-4005. Online ISSN: 1098-4275.

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Human Papillomavirus Vaccination Practices: A Survey of US Physicians 18 Months After Licensure

AUTHORS: Matthew F. Daley, MD,a,b,c,d Lori A. Crane, PhD, MPH,c,e Lauri E. Markowitz, MD,f Sandra R. Black, DVM, MSPH,b,c Brenda L. Beaty, MSPH,b,c Jennifer Barrow, MSPH,b,c Christine Babbel, MSPH,b,c Sami L. Gottlieb, MD, MSPH,f Nicole Liddon, PhD,f Shannon Stokley, MPH,g L. Miriam Dickinson, PhD,h and Allison Kempe, MD, MPHa,b,c
Departments of aPediatrics and hFamily Medicine and bColorado Health Outcomes Program, University of Colorado, Aurora, Colorado; cChildrens Outcomes Research Program, Childrens Hospital, Aurora, Colorado; dInstitute for Health Research, Kaiser Permanente Colorado, Denver, Colorado; eDepartment of Community and Behavioral Health, Colorado School of Public Health, Aurora, Colorado; and fDivision of Sexually Transmitted Diseases Prevention, National Center for HIV/AIDS, Viral Hepatitis, Sexually Transmitted Diseases, and Tuberculosis Prevention; and gImmunization Services Division, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia KEY WORDS human papillomavirus vaccine, physicians, attitudes, practices, survey ABBREVIATION HPVhuman papillomavirus 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 ndings 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. [Link]/cgi/doi/10.1542/peds.2009-3500 doi:10.1542/peds.2009-3500 Accepted for publication 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: [Link]@[Link] PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275). Copyright 2010 by the American Academy of Pediatrics FINANCIAL DISCLOSURE: The authors have indicated they have no nancial relationships relevant to this article to disclose.

WHATS 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 nancial obstacles to vaccination.

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 ofces (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 nancial, 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% condence interval: 1.071.51]) and reporting more vaccine refusals among parents of younger versus older adolescents (risk ratio: 2.09 [95% condence 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 nancial obstacles to vaccination. Pediatrics 2010;126:425433

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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 11to 12-year-old female patients, with catch-up vaccination being recommended for unimmunized 13- to 26year-old female patients.5 The policy decision to target 11- to 12year-old female adolescents for HPV vaccination was based on HPV-specic and broader health care delivery considerations. Although the median age of rst 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
426 DALEY et al

coverage while enhancing broader health care provision to adolescents.13 Several studies examined physician attitudes and intended practices regarding HPV vaccination1418; however, those surveys were conducted either before vaccine licensure1417 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.

work 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 ndings1416,24,25 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 ofces. HPV vaccine refusal was dened in the survey instrument as outright refusal without plans for future vaccination; deferral was dened 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,

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, vaccinerelated 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 net-

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the Internet group received a nal 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 HPVrelated knowledge, attitudes, and practices were compared between pediatricians and family physicians. Bivariate and multivariate analyses were performed to examine the association between prespecied 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-yearold 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 nal multivariate model. Although it was not statistically signicant at P .05, physician specialty was retained in the multivariate model because of the potential inuence 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).

TABLE 1 Characteristics of Survey Respondents

Characteristic Year of medical school graduation, mediana Male, % Location of practice, %b Urban, inner city Urban, noninner city/suburban Rural Type of practice, % Private practice Community- or hospital-based Managed-care organization Estimated proportion of patients with public health insurance, %b 10% 10%24% 25%49% 50% Participates in federal VFC program, %b Proportion of patients 1118 y of age, %b 10% 10%24% 25% Estimated no. of gynecologic examinations performed for women 18 y of age in average month, %b 1 14 5 Pediatricians (N 349) 1985 51 44 44 13 86 12 2 Family Physicians (N 331) 1987 56 25 47 28 80 17 2

33 26 23 17 81 8 46 46

48 26 17 10 58 51 44 5

82 10 7

36 41 23

Column percentages do not always total 100% because of rounding. VFC indicates Vaccines for Children. aP .05 for comparison between pediatricians and family physicians. bP .01 for comparison between pediatricians and family physicians.

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 nonrePEDIATRICS Volume 126, Number 3, September 2010

spondents 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. 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.
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TABLE 2 Respondent Knowledge Regarding HPV Infections and HPV Vaccination (N

True/False Statementsa Pediatricians HPV is a relatively uncommon sexually transmitted infection (false) Almost all cervical cancers are caused by HPV infection (true)b The incidence of HPV in women is highest among women in their 30s (false) Most people with genital HPV infections are symptomatic (false) Genital warts are caused by the same HPV types that cause cervical cancer (false)b Sexually active women should be tested for HPV before starting HPV vaccination (false)c A pregnancy test should be performed before giving HPV vaccine (false)b HPV vaccine is not licensed for women 26 years of age (true) Women who have been diagnosed with HPV should not be given HPV vaccine (false)
a

680)

Correct Response, % Family Physicians 91 95 55 86 58 85 69 79 80

92 85 51 85 43 91 86 78 77

ance coverage, reimbursement for HPV vaccination, and vaccine purchasing costs. Parent opposition to HPV vaccination for moral or religious reasons was perceived as denitely 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 denitely or somewhat a barrier, physicians rarely reported that they themselves were concerned about HPV vaccine safety. 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 ofces (P

Correct responses are indicated in parentheses. P .01 for comparison between family physicians and pediatricians. cP .05 for comparison between family physicians and pediatricians.
b

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. 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 onehalf reported that parents were concerned about this issue. Perceived Barriers to HPV Vaccine Use Physician perceptions regarding barriers to administering HPV vaccine in
428 DALEY et al

their ofces are presented in Table 4. The most-frequently reported barriers for both pediatricians and family physicians were nancial, related to insur-

TABLE 3 Attitudes and Experiences Regarding HPV Vaccination Among Providers Currently
Administering HPV Vaccine in Their Ofces (N 619)
Response, % Pediatricians Strongly Agree Parents of 1112 year-old patients have been more likely to refuse HPV vaccine than parents of 1618 year-old patients. It is necessary to discuss issues of sexuality before recommending HPV vaccine to patients.a Other new vaccine recommendations for adolescents (ie, meningococcus, pertussis) have made it easier for my practice to introduce HPV vaccine. I am concerned that syncope is more likely to occur after HPV vaccination, compared with other vaccinations.a Parents of my adolescent patients are concerned that vaccination against a sexually transmitted infection may encourage earlier or riskier sexual behavior. Parents of 1112 year-old patients have been upset that I am offering a vaccine against a sexually transmitted infection to someone 1112 years old. I dont have much condence in the safety of new vaccines until they have been on the market for several years. I think that vaccination against a sexually transmitted infection may encourage earlier or riskier sexual behavior in my adolescent patients. I am concerned that Guillain-Barr syndrome may occur after HPV vaccination. 23 Somewhat Agree 55 Family Physicians Strongly Agree 17 Somewhat Agree 48

15 14

27 53

23 15

30 55

24

10

39

43

22

23

17

26

Items are presented in rank order, according to the proportion of pediatricians who reported that they strongly agree with the statement. aP .01 for comparison of strongly agree responses between pediatricians and family physicians.

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TABLE 4 Perceived Barriers to HPV Vaccination Among Surveyed Pediatricians and Family
Physicians (N 680)
Response, % Pediatricians Denitely A Barrier Failure of some insurance companies to cover HPV vaccinationa Lack of adequate reimbursement for HPV vaccinationa Up-front costs for my practice to purchase HPV vaccinea Parent concerns about the safety of HPV vaccine Parent opposition to HPV vaccination for moral or religious reasons Parent concerns that vaccination against a sexually transmitted infection may encourage earlier or riskier sexual behavior Parent concerns about the efcacy of HPV vaccine Difculty ensuring that patients will complete a 3-dose vaccine seriesb The time it takes me to discuss HPV vaccination with parentsb My concern about adding another vaccine to the vaccine scheduleb My concerns about the safety of HPV vaccineb My concerns about the efcacy of HPV vaccine 26 18 15 5 4 4 Somewhat A Barrier 21 20 19 27 19 19 Family Physicians Denitely A Barrier 36 27 24 4 5 4 Somewhat A Barrier 28 25 21 21 28 26

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. When discussing HPV vaccination for the rst 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 patients 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 rst 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
429

1 1 1 1 1 1

16 11 10 5 2 1

2 4 3 3 3 2

14 14 13 8 5 5

Items are presented in rank order, according to the proportion of pediatricians who perceived the issue as denitely a barrier. aP .01 for comparison of responses of denitely a barrier between pediatricians and family physicians. bP .05 for comparison of responses of denitely a barrier between pediatricians and family physicians.

.001). Ninety-ve percent of female family physicians reported giving HPV vaccine in their ofces, compared with 83% of male family physicians (P .001). In addition, 79% of family physicians from the South reported administering HPV vaccine in their ofces, 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 vac-

cine 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 ofces, whether they strongly recommended the vaccine varied depending on the age of the patient (Fig 1). In both specialties, greater proportions of physicians

FIGURE 1
Proportions of physicians who strongly recommend HPV vaccine to female patients in various age groups.

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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 12year-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 parents 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 11to 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.

TABLE 5 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)
n Proportion Not Strongly Recommending, % Risk Ratio (95% Condence Interval) Unadjusted Adjusteda

Provider strongly or somewhat agrees with statementb It is necessary to discuss sexuality before recommending HPV vaccine Other new adolescent vaccines have made it easier to introduce HPV vaccine Parents of 1112 year-old patients have been upset that provider is offering a vaccine against a sexually transmitted infection to someone this age Parents of 1112 year-old patients have been more likely to refuse HPV vaccine than parents of 1618-yearold patients Provider perceives this issue as denitely or somewhat a barrier to HPV vaccinationc Time it takes to discuss HPV vaccination with parents Provider concern about adding another vaccine to vaccine schedule Parent concern about HPV vaccine safety Parent concern about HPV vaccine efcacy Estimated proportion of patients with public health insurance 0%9% 10%24% 25%49% 50% Region South Northeast Midwest West Specialty Pediatrics Family medicine
a b

283 415

53.0 43.9

1.29 (1.091.53) 1.27 (1.071.51) 0.83 (0.700.99)

152

51.3

1.14 (0.951.37)

440

54.8

2.23 (1.682.96) 2.09 (1.662.81)

77 40 171 94

62.3 72.5 54.4 59.6

1.41 (1.161.72) 1.30 (1.041.58) 1.61 (1.311.99) 1.25 (1.051.49) 1.35 (1.111.63)

221 157 118 87 174 141 158 135 337 271

56.6 52.2 33.9 32.2 47.7 55.3 42.4 40.7 43.6 50.2

Reference Reference 0.92 (0.761.12) 0.85 (0.701.05) 0.60 (0.450.79) 0.63 (0.460.81) 0.57 (0.410.79) 0.59 (0.400.80) Reference Reference 1.16 (0.941.44) 1.17 (0.941.41) 0.89 (0.701.13) 0.86 (0.671.05) 0.85 (0.661.10) 0.83 (0.641.06) Reference Reference 1.15 (0.981.36) 1.17 (0.991.36)

All variables with adjusted risk ratios were included in nal multivariate model. Reference group is provider somewhat or strongly disagreeing with the statement. c Reference group is provider perceiving this issue as a minor barrier or not at all a barrier to HPV vaccination.

DISCUSSION
Eighteen months after licensure of the rst 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 ofces. However, fewer physicians strongly recommended the vaccine for 11- to 12-year430 DALEY et al

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 nancial barriers to HPV vaccination. Although widespread availability of HPV vaccine in primary care ofces should facilitate immunization delivery to targeted patient populations, these data sug-

gest 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

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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 nding 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, nancial 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 nancial concerns; some physicians who reported that vaccine purchase cost and reimbursement issues were denitely a barrier to vaccine use were nonetheless providing HPV vaccine in their ofces. Although this is relatively reassuring, nancial 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 nancial concerns.35 Given that quadrivalent HPV vaccine is one
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of the more-expensive vaccines currently licensed, at approximately $120 per dose,36 continued and expanded use may depend in part on practice-level nancial considerations.37 If the US vaccine system is at risk of a future nancial 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, ndings consistent with results of prelicensure studies with physicians1417 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 difcult to achieve than the wellsynchronized 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 ndings 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 nancial 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
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upward shift in the age at receipt of a rst 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 REFERENCES
1. Cates W, Jr. Estimates of the incidence and prevalence of sexually transmitted diseases in the United States. Sex Transm Dis. 1999;26(4 suppl):S2S7 2. Weinstock H, Berman S, Cates W, Jr. Sexually transmitted diseases among American youth: incidence and prevalence estimates, 2000. Perspect Sex Reprod Health. 2004; 36(1):6 10 3. Muoz N, Bosch FX, de Sanjos S, et al. Epidemiologic classication of human papillomavirus types associated with cervical cancer. N Engl J Med. 2003;348(6):518 527 4. Koutsky LA, Galloway DA, Holmes KK. Epidemiology of genital human papillomavirus infection. Epidemiol Rev. 1988;10:122163 5. Centers for Disease Control and Prevention. Quadrivalent human papillomavirus vaccine: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep. 2007;56(RR-2): 124 6. Food and Drug Administration. FDA approves new vaccine for prevention of cervical cancer. Available at: [Link]/ NewsEvents/Newsroom/PressAnnouncements/ [Link]. Accessed November 17, 2009 7. Food and Drug Administration. FDA approves new indication for Gardasil to prevent genital warts in men and boys. Available at: [Link]/NewsEvents/Newsroom/ PressAnnouncements/[Link]. Accessed November 17, 2009 8. Abma JC, Martinez GM, Mosher WD, Dawson BS. Teenagers in the United States: sexual activity, contraceptive use, and childbearing, 2002. Vital Health Stat 23. 2004;(24): 1 48 9. Eaton DK, Kann L, Kinchen S, et al. Youth risk behavior surveillance: United States, 2007. MMWR Surveill Summ. 2008;57(4):1131 10. Centers for Disease Control and Prevention. Prevention and control of meningococcal disease: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep. 2005; 54(RR-7): 121 11. Centers for Disease Control and Prevention.

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.

12.

13.

14.

15.

16.

17.

18.

19.

20.

Preventing tetanus, diphtheria, and pertussis among adolescents: use of tetanus toxoid, reduced diphtheria toxoid and acellular pertussis vaccines: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep. 2006; 55(RR-3):134 McCauley MM, Fishbein DB, Santoli JM. Introduction: strengthening the delivery of new vaccines for adolescents. Pediatrics. 2008;121(suppl 1):S1S4 Broder KR, Cohn AC, Schwartz B, et al. Adolescent immunizations and other clinical preventive services: a needle and a hook? Pediatrics. 2008;121(suppl 1):S25S34 Kahn JA, Zimet GD, Bernstein DI, et al. Pediatricians intention to administer human papillomavirus vaccine: the role of practice characteristics, knowledge, and attitudes. J Adolesc Health. 2005;37(6):502510 Daley MF, Liddon N, Crane LA, et al. A national survey of pediatrician knowledge and attitudes regarding human papillomavirus vaccination. Pediatrics. 2006;118(6): 2280 2289 Riedesel JM, Rosenthal SL, Zimet GD, et al. Attitudes about human papillomavirus vaccine among family physicians. J Pediatr Adolesc Gynecol. 2005;18(6):391398 Raley JC, Followwill KA, Zimet GD, Ault KA. Gynecologists attitudes regarding human papilloma virus vaccination: a survey of Fellows of the American College of Obstetricians and Gynecologists. Infect Dis Obstet Gynecol. 2004;12(3 4):127133 Feemster KA, Winters SE, Fiks AG, Kinsman S, Kahn JA. Pediatricians intention to recommend human papillomavirus (HPV) vaccines to 11- to 12-year-old girls postlicensing. J Adolesc Health. 2008;43(4):408 411 Kahn JA, Cooper HP, Vadaparampil ST, et al. Human papillomavirus vaccine recommendations and agreement with mandated human papillomavirus vaccination for 11-to12-year-old girls: a statewide survey of Texas physicians. Cancer Epidemiol Biomarkers Prev. 2009;18(8):23252332 Huey NL, Clark AD, Kluhsman BC, Lengerich EJ. HPV vaccine attitudes and practices

21.

22.

23.

24.

25.

26.

27.

28.

29.

30.

31.

among primary care providers in Appalachian Pennsylvania. Prev Chronic Dis. 2009; 6(2):A49 Keating KM, Brewer NT, Gottlieb SL, Liddon N, Ludema C, Smith JS. Potential barriers to HPV vaccine provision among medical practices in an area with high rates of cervical cancer. J Adolesc Health. 2008;43(4 suppl): S61S67 Babbie ER. The Practice of Social Research. 4th ed. Belmont, CA. Wadsworth Publishing; 1986 Crane LA, Daley MF, Barrow J, et al. Sentinel physician networks as a technique for rapid immunization policy surveys. Eval Health Prof. 2008;31(1):43 64 Esposito S, Bosis S, Pelucchi C, et al. Pediatrician knowledge and attitudes regarding human papillomavirus disease and its prevention. Vaccine. 2007;25(35):6437 6446 Kahn JA, Rosenthal SL, Tissot AM, Bernstein DI, Wetzel C, Zimet GD. Factors inuencing pediatricians intention to recommend human papillomavirus vaccines. Ambul Pediatr. 2007;7(5):367373 Schuman H, Presser S. Questions and Answers in Attitude Surveys: Experiments on Question Form, Wording, and Context. Thousand Oaks, CA: Sage; 1996:161178 McMahon SR, Iwamoto M, Massoudi MS, et al. Comparison of e-mail, fax, and postal surveys of pediatricians. Pediatrics. 2003; 111(4): Available at: [Link]/ cgi/content/full/111/4/e299 Hosmer DW, Lemeshow S. Applied Logistic Regression. New York, NY: Wiley; 1989: 82134 Schaffer SJ, Szilagyi PG, Shone LP, et al. Physician perspectives regarding pneumococcal conjugate vaccine. Pediatrics. 2002; 110(6): Available at: [Link]/ cgi/content/full/110/6/e68 Davis MM, Ndiaye SM, Freed GL, Clark SJ. One-year uptake of pneumococcal conjugate vaccine: a national survey of family physicians and pediatricians. J Am Board Fam Pract. 2003;16(5):363371 Zhang J, Yu KF. Whats the relative risk? A method of correcting the odds ratio in co-

432

DALEY et al

Downloaded from [Link] by guest on November 6, 2012

ARTICLE

hort studies of common outcomes. JAMA. 1998;280(19):1690 1691 32. Kleinman LC, Norton EC. Whats the risk? A simple approach for estimating adjusted risk measures from nonlinear models including logistic regression. Health Serv Res. 2009;44(1):288 302 33. Freed GL, Bordley WC, Clark SJ, Konrad TR. Universal hepatitis B immunization of infants: reactions of pediatricians and family physicians over time. Pediatrics. 1994; 93(5):747751 34. Kempe A, Patel MM, Daley MF, et al. Adoption of rotavirus vaccination by pediatricians and family medicine physicians in the United States. Pediatrics. 2009;124(5): Available at: [Link]/cgi/content/ full/124/5/e809 35. Freed GL, Cowan AE, Clark SJ. Primary care physician perspectives on reimbursement for childhood immunizations. Pediatrics. 2008;122(6):1319 1324 36. Centers for Disease Control and Prevention. CDC vaccine price list. Available at: www. 37.

38.

39.

40.

41.

42.

[Link]/vaccines/programs/vfc/[Link]. Accessed August 7, 2009 Freed GL, Cowan AE, Gregory S, Clark SJ. Variation in provider vaccine purchase prices and payer reimbursement. Pediatrics. 2008;122(6):13251331 Berman S. Is our vaccine system at risk for a future nancial meltdown? [letter]. Pediatrics. 2008;122(6):13721373 Dempsey AF, Zimet GD, Davis RL, Koutsky L. Factors that are associated with parental acceptance of human papillomavirus vaccines: a randomized intervention study of written information about HPV. Pediatrics. 2006;117(5):1486 1493 Kahn JA, Ding L, Huang B, Zimet GD, Rosenthal SL, Frazier AL. Mothers intention for their daughters and themselves to receive the human papillomavirus vaccine: a national study of nurses. Pediatrics. 2009; 123(6):1439 1445 Ziv A, Boulet JR, Slap GB. Utilization of physician ofces by adolescents in the United States. Pediatrics. 1999;104(1):35 42 Rand CM, Shone LP, Albertin C, Auinger P,

43.

44.

45.

46.

Klein JD, Szilagyi PG. National health care visit patterns of adolescents: implications for delivery of new adolescent vaccines. Arch Pediatr Adolesc Med. 2007;161(3): 252259 Rand CM, Szilagyi PG, Albertin C, Auinger P. Additional health care visits needed among adolescents for human papillomavirus vaccine delivery within medical homes: a national study. Pediatrics. 2007;120(3): 461 466 Szilagyi PG, Bordley C, Vann JC, et al. Effect of patient reminder/recall interventions on immunization rates: a review. JAMA. 2000; 284(14):1820 1827 Dempsey AF, Singer D, Clark SJ, Davis MM. Parents views on 3 shot-related visits: implications for use of adolescent vaccines like human papillomavirus vaccine. Acad Pediatr. 2009;9(5):348 352 Centers for Disease Control and Prevention. National, state, and local area vaccination coverage among adolescents aged 1317 years: United States, 2008. MMWR Morb Mortal Wkly Rep. 2009; 58(36):9971001

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 individualat 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 ngertips and computer keyboards and found they could match the genetic material on the keyboard to a particular individual and months later, could still nd the same bacteria on their ngertips 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

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Human Papillomavirus Vaccination Practices: A Survey of US Physicians 18 Months After Licensure Matthew F. Daley, Lori A. Crane, Lauri E. Markowitz, Sandra R. Black, Brenda L. Beaty, Jennifer Barrow, Christine Babbel, Sami L. Gottlieb, Nicole Liddon, Shannon Stokley, L. Miriam Dickinson and Allison Kempe Pediatrics 2010;126;425; originally published online August 2, 2010; DOI: 10.1542/peds.2009-3500
Updated Information & Services References including high resolution figures, can be found at: [Link] ml This article cites 36 articles, 14 of which can be accessed free at: [Link] ml#ref-list-1 This article has been cited by 8 HighWire-hosted articles: [Link] ml#related-urls This article, along with others on similar topics, appears in the following collection(s): Infectious Disease & Immunity [Link] disease Information about reproducing this article in parts (figures, tables) or in its entirety can be found online at: [Link] ml Information about ordering reprints can be found online: [Link]

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PEDIATRICS is the official journal of the American Academy of Pediatrics. A monthly publication, it has been published continuously since 1948. PEDIATRICS is owned, published, and trademarked by the American Academy of Pediatrics, 141 Northwest Point Boulevard, Elk Grove Village, Illinois, 60007. Copyright 2010 by the American Academy of Pediatrics. All rights reserved. Print ISSN: 0031-4005. Online ISSN: 1098-4275.

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