US Health Care Clinicians’ Knowledge, Attitudes, and Practices Regarding Human Papillomavirus Vaccination: A Qualitative Systematic Review

Abstract

Clinicians’ recommendation for the human papillomavirus (HPV) vaccine appears to be an important driver of parental decisions about vaccination. Our aim was to synthesize the best available evidence exploring the perceptions and experiences regarding HPV vaccination, from the perspective of the US clinician. We conducted a comprehensive literature search of Academic Search Complete, CINAHL Plus, Communication & Mass Media Complete, Consumer Health Complete (EBSCOhost), ERIC, Health and Psychosocial Instruments, MEDLINE with full text, and PsycINFO databases. We identified 60 eligible articles: 48 quantitative and 12 qualitative. We extracted the following information: study purpose, use of theory, location, inclusion criteria, and health care provider classification. Results were organized into 5 categories: 1) clinicians’ knowledge and beliefs about HPV and the HPV vaccine, 2) clinicians’ attitudes and beliefs about recommending HPV vaccines, 3) clinicians’ intention to recommend HPV vaccines, 4) clinicians’ professional practices regarding HPV vaccination, and 5) patient HPV vaccination rates. Although clinicians were generally supportive of HPV vaccination, there was a discrepancy between clinicians’ intentions, recommendation practices, and patient vaccination rates. Studies reported that clinicians tended not to provide strong, consistent recommendations, and were more likely to recommend HPV vaccines to girls versus boys and to older versus younger adolescents. Analyses revealed a number of facilitating factors and barriers to HPV vaccination at the clinician, parent/patient, and systems levels, including clinician knowledge, clinician beliefs, and office procedures that promote vaccination. This review provides an evidence base for multilevel interventions to improve clinician HPV vaccine recommendations and vaccination rates.

HUMAN PAPILLOMAVIRUS (HPV) is the most common sexually transmitted infection, with a prevalence rate of 43% among US adults.¹ HPV might have serious health consequences for men as well as women, including anogenital cancers (cervical, vaginal, vulvar, penile, and anal), oropharyngeal cancers, and anogenital warts.² To prevent the potential health consequences, 3 HPV vaccines (2-valent, 4-valent, and 9-valent) have been licensed in the United States. Data from clinical trials have shown that these vaccines are almost 100% effective in preventing infection and precancers caused by the targeted HPV types, if given before HPV acquisition,^3–8 and that the 4-valent and 9-valent vaccines are highly effective in preventing anogenital warts.^5–7 HPV vaccine introduction in real-world settings has led to dramatic declines in vaccine-type HPV prevalence and anogenital warts.^9–11 Despite the potential for HPV vaccines to decrease morbidity and mortality associated with these outcomes, vaccine uptake remains below the Healthy People 2020 objective of 80% coverage. In the United States during 2014 to 2015, only 43% of 13- to 17-year-old girls and 32% of 13- to 17-year-old boys had completed the HPV vaccine series.¹²

Health care clinicians play a key role in HPV vaccine uptake, and clinicians’ recommendation for the vaccine appears to be an important driver of parental decisions to vaccinate their child.¹³ However, research has shown that there are considerable missed clinical opportunities to recommend and administer the HPV vaccine. Furthermore, higher quality and strength of HPV vaccine recommendations predict a higher odds of initiation and vaccine series completion.¹⁴ However, the strength and consistency of clinician recommendations for HPV vaccine is lower than for other adolescent vaccines: in 1 study, two-thirds of 11- and 12-year-old girls did not receive an HPV vaccine at a visit during which they received at least 1 other vaccine.¹⁵ Missed opportunities to vaccinate have been cited as the primary reason the United States has not achieved high HPV vaccination rates.¹⁶

Because of relatively low rates of HPV vaccination, the importance of clinicians’ vaccine recommendation, and missed opportunities to vaccinate, understanding health care clinicians’ knowledge, attitudes, and professional practices regarding the HPV vaccine is important for developing evidence-based interventions to improve the consistency and strength of HPV vaccine recommendations. Therefore, our aim was to synthesize the best available evidence on the perceptions and experiences regarding HPV vaccination, from the perspective of the US clinician.

Methods

For the purpose of this review, health care clinician was defined as an individual qualified to deliver health care services (eg, physicians, clinical nurses, school nurses) to patients within the recommended age group for vaccination (9–26 years of age). A comprehensive literature search of Academic Search Complete, CINAHL Plus with Full Text, Communication & Mass Media Complete, Consumer Health Complete (EBSCOhost), ERIC, Health and Psychosocial Instruments, MEDLINE with Full Text, and PsycINFO databases was conducted, using variations and Boolean connectors with the following terms: human papillomavirus, vaccine, immunization, vaccine, health care provider, perception, and practice. In addition to the electronic searches, each article was scanned in Scopus for potentially missed citations that cited the article produced in the initial search.

The following criteria were used for inclusion of articles in this review: 1) original empirical reports (including quantitative and qualitative studies) published in a peer-reviewed, English language journal, 2) studies conducted in the United States, 3) data collection took place after the US Food and Drug Administration approval of the vaccine (2006), and 4) methodology included examination of the knowledge, perceptions, and/or professional practices of health care professionals regarding the HPV vaccine. Articles were excluded if they were commentaries, editorials, or personal perspectives. All articles published through August 2016 were retrieved (the date in which searching began). Information concerning the time frame the data were collected, purpose of the study, use of theory, location of study, inclusion criteria, classification of health care provider, study design, and sample size were extracted from eligible studies. Additionally, information about clinicians’ knowledge about, perceptions of, and practices regarding the HPV vaccine were extracted. Data were abstracted and entered into a database by Dr Rosen and Ms Shepard. Dr Rosen independently abstracted the data from the first 35 articles (all articles published from 2008 to 2014), and Ms Shepard independently abstracted the data from the remaining 22 articles (published from 2015 to 2016). Dr Rosen and Ms Shepard also identified themes and subthemes through content analysis on the basis of the data in the articles. Dr Kahn conducted an independent review of the themes and subthemes providing validation of data classification, as well as reviewing the abstracted data to ensure the data were aligned with the themes and subthemes. Any discrepancies in classification were resolved through discussion between Dr Rosen, Ms Shepard, and Dr Kahn.

Results

Sixty articles were identified for this review, including 48 quantitative and 12 qualitative studies. The range of publication dates included 2008 through 2016: most studies (n = 15) were published in 2016, and most of these (n = 13) were conducted in 2010. Five studies did not provide information about the geographic area where the research was conducted. In 25 studies, data were derived from a national data set. The remainder of the studies reported data collected from states in the Northeast (n = 6), Midwest (n = 10), South (n = 12), and West (n = 2) as defined by the US Census Bureau. Participants in the studies included pediatricians (n = 29), family practitioners (n = 26), obstetricians and gynecologists (n = 12), physicians not otherwise classified (n = 13), nurse practitioners (n = 13), general practitioners (n = 8), internal medicine physicians (n = 7), registered nurses (n=6), physician assistants (n = 5), preventive medicine physicians (n = 2), and school nurses (n = 2). Of the 48 quantitative studies, the sample size ranged from 50 to 2119 clinician participants. The sample size in the 12 qualitative studies ranged from 8 to 61 participants. Twelve of the 48 quantitative studies explicitly stated using a theory or model to collect and/or analyze data, including theory of planned behavior (n 5), competing demands model (n = 4), diffusion of innovations (n = 3), health belief model (n = 2), shared decision-making framework (n = 1), and transtheoretical model (n=1). Four of the studies reported using more than 1 theory or model. Analytic methods included grounded theory/constant comparison methods in 6 of the qualitative studies. Study characteristics are shown in Table 1.

Table 1.

Study Characteristics

				Measure
Reference	Study Design	N	Study Population	HPV and Vaccine Knowledge	Recommending Attitudes	Intentions to Recommend	Professional Practice	Patient Vaccine Rates
Feemster et al17	Quantitative, cross-sectional	101	Pediatrics			•
Ishibashi et al18	Quantitative, cross-sectional	373	Pediatrics	•
Ishibashi et al19	Quantitative, cross-sectional	373	Pediatrics	•	•	•
Jensen et al20	Quantitative, cross-sectional	204	Pediatrics, NP, FM, and gynecology			•
Kahn et al21	Quantitative, cross-sectional	1122	Pediatrics, OBGYN, FM, IM, and other	•	•	•	•
Askelson et al22	Quantitative, cross-sectional	207	Physicians (FM, IM, and pediatrics)	•	•	•		•
Barnack et al23	Quantitative, cross-sectional	100	Pediatrics, OBGYN, FM, IM, and other		•	•
Cook et al24	Quantitative, cross-sectional	550,048	Girls aged 9–20 years*					•
Daley et al25	Quantitative, cross-sectional	680	Pediatrics and FM	•	•		•	•
Ko et al26	Quantitative, cross-sectional	424	Pediatrics, OBGYN, and IM	•	•		•	•
McCave27	Quantitative, cross-sectional	227	Pediatrics, physicians, OBGYN, PA, and NP	•	•		•	•
Weiss et al28	Quantitative, cross-sectional	1094	Pediatrics and FM	•			•
Hughes et al29	Qualitative, individual interviews	20	Physicians	•	•		•
Roberto et al30	Quantitative, cross-sectional	406	Pediatrics				•
Tan et al31	Quantitative, cross-sectional	733	OBGYN, FM, and IM		•			•
Vadaparampil et al32	Quantitative, cross-sectional	1013	Pediatrics, OBGYN, and FM				•
Young et al33	Quantitative, cross-sectional	385	OBGYN and FM	•	•	•	•
Zimet et al34	Quantitative, cross-sectional	271	OBGYN, FM, and IM		•
Javanbakht et al35	Qualitative, in-person interviews	21	Physicians, PA, medical assistants, and case managers		•
Perkins and Clark36	Qualitative, in-depth interviews	34	Physicians and NP	•	•		•
Aragones et al37	Quantitative, cross-sectional	93	Pediatrics, FM, and IM	•	•	•
Head et al38	Qualitative, semistructured interviews	8	Physicians, NP, and licensed practical nurses		•
Holder et al39	Quantitative, cross-sectional	254	Doctors of medicine, pediatrics, adolescent medicine subboarded, RN, certified NP	•			•
Malo et al40	Quantitative, cross-sectional	433	Pediatrics, OBGYN, FM, IM, and preventive medicine				•	•
Perkins et al41	Quantitative, cross-sectional	366	OBGYN	•	•	•	•
Perkins and Clark42	Qualitative, semistructured interviews	34	Pediatrics, FM, and NP	•	•
Post et al43	Quantitative, cross-sectional	112	Recent graduates from FM residencies	•	•		•
Hill and Okugo44	Quantitative, cross-sectional	50	Emergency medicine physicians and residents		•	•
Malo et al45	Quantitative, cross-sectional	728	FM and pediatrics				•	•
McRee et al46	Quantitative, cross-sectional	575	Physicians and NP		•		•
Roland et al47	Quantitative, cross-sectional	98	Physicians, NP, certified nurse midwives, and physicians	•			•
Vadaparampil et al48	Quantitative, 2 cross-sectional	1013 (2009),	FM, pediatrics, and OBGYN				•
Alexander et al49	surveys	928 (2011)
	Qualitative, semistructured interviews	20	Pediatrics (IM and adolescent)	•	•		•
Berkowitz et al50	Quantitative, cross-sectional	1753	FM, IM, NP, pediatrics, and OBGYN	•			•
Gilkey et al51	Quantitative, cross-sectional	1022	Pediatrics and FM	•	•		•
Gilkey et al52	Quantitative, cross-sectional	1022	Pediatrics and FM		•		•
Katz and Paskett53	Qualitative, cross-sectional	Not stated	Physicians, nurses, and medical assistants	•	•
Rahman et al54	Quantitative, cross-sectional	23,564	Unspecified medical providers				•	•
Rosen et al55	Quantitative, cross-sectional	413	School nurses	•			•
Suryadevara et al56	Quantitative, cross-sectional	680	Nurse, midlevel provider, and physician	•		•	•
Allison et al57	Quantitative, cross-sectional	582	Pediatrics and FM			•	•	•
Askelson et al58	Quantitative, cross-sectional	127	Clinic managers		•
Berkowitz et al59	Quantitative, cross-sectional	2119	OBGYN and primary care providers (IM, FM, and midlevel providers)	•			•
Dempsey et al60	Quantitative, cross-sectional	356	Parents of adolescent children‡				•
Gilkey et al14	Quantitative, cross-sectional	1495	Parents of 11- to 17-year-old adolescents§				•	•
Grout et al61	Quantitative, retrospective study	2932	13- to 18-year-old patients‖					•
Henrikson et al62	Qualitative, semistructured face- to-face interviews and telephone interviews	44	Physicians, NP, and PA	•			•
Hudson et al63	Qualitative, semistructured interview	61	Immunization Nurses, FM, and Pediatrics	•	•		•
Hyun et al13	Quantitative, cross-sectional	Not stated	Parents of adolescents¶				•	•
Javaid et al64	Quantitative, cross-sectional	1132	Pediatrics, Nurse, FM, OBGYN, and PA	•	•		•
Kasting et al65	Qualitative, semistructured interviews	22	Physicians and NP with Pediatric Specialty	•
Kulczycki et al66	Quantitative, cross-sectional	301	FM and Pediatrics		•	•	•
Malo et al67	Quantitative, cross-sectional	367	Pediatrics and FM				•
Perkins et al68	Qualitative, semistructured interviews	33	Physicians, NP, and RN		•		•
Rosen et al69	Quantitative, cross-sectional	137	School nurses	•		•	•
Ylitalo et al72	Quantitative, cross-sectional	9274	Girls aged 13–17 years†				•	•

FM indicates family medicine; HPV, human papillomavirus; IM, internal medicine; NP, nurse practitioner; OBGYN, obstetrics-gynecology; PA, physician’s assistant; and RN, registered nurse.

^†Study included female adolescent patients with provider-verified vaccination records.

^*Study included girls aged 9 to 20 years of age enrolled in Medicaid for $6 months to identify claims for HPV vaccination along with individual, provider, and practice characteristics linked to vaccination.

^‡Study included parents of adolescent children at 16 primary care practices to assess current provider communication practices and influence on HPV vaccine uptake.

^§Study included parents of adolescents between the ages of 11 and 17 years of age assessing the quality of recommendations parents received for the HPV vaccine from health care providers.

^‖Study included electronic medical records of 13- to 18-year-old patients to assess patient and provider characteristics associated with initiating the HPV vaccine.

^¶Study included parents of adolescents to assess vaccination rates, missed opportunities for vaccination, and role of health care provider recommendations in vaccine uptake.

We organized study results into the following primary categories: 1) clinicians’ knowledge and beliefs about HPV and the HPV vaccine, 2) clinicians’ attitudes and beliefs about recommending HPV vaccines, 3) clinicians’ intention to recommend HPV vaccines, 4) clinicians’ professional practices regarding HPV vaccination, and 5) patient HPV vaccination rates. For the last 3 categories (intention to recommend HPV vaccines, professional practices regarding HPV vaccination, patient HPV vaccination rates) we also included factors associated with each of these outcomes if the data were available. Within each category, themes were identified and subthemes classified through content analysis. For results that are summarized in the following sections and also presented in tables, citations are included in each table.

Clinicians’ Knowledge and Beliefs About HPV and the HPV Vaccine

Studies assessing clinicians’ knowledge of HPV and HPV vaccine showed that knowledge varied widely. Correct responses to items assessing HPV knowledge ranged from 22% to 95%^21,25,28,69 and correct responses to items assessing HPV vaccine knowledge ranged from 17% to 91%.^25,50,55,69 Clinicians’ knowledge level about HPV in men was generally lower than their knowledge level for women, and was particularly low with respect to understanding of vaccine recommendations for men, such as the upper age limit of the recommendation and which male HPV-related cancers the vaccines prevents.^39,49 In 1 study, knowledge level about the vaccine’s effectiveness in preventing cervical cancer was higher than for knowledge about the prevention of anal, oropharyngeal, vulvar, and vaginal cancers.⁵⁰ Clinicians also reported deficits in knowledge about the risk of HPV infection in gay and bisexual men.⁵¹ Clinicians generally believed that HPV infection caused serious health complications (eg, cervical cancer) and warranted a vaccine.^37,55,70

Clinicians’ Attitudes and Beliefs About Recommending HPV Vaccines

Clinicians’ attitudes and beliefs about recommending HPV vaccines are summarized in Table 2. We identified 2 main themes: facilitating factors and barriers to recommending HPV vaccines. Within each of these themes, study findings were classified into the following subthemes: personal, parent/patient-related, and systems-level facilitating factors or barriers. Personal facilitating factors for recommending HPV vaccines included personal beliefs about vaccine benefits (eg, prevention of cancer,^{22,28,33,42,47,49,50,59,63} prevention of HPV transmission,²⁸ decreased health care costs,⁴⁹ and benefits specific to men^28,49 and vaccine safety^33,49,69). Parent and patient-related facilitating factors included cultural beliefs⁴² and vaccine education for patients and families.^38,42 Systems-level facilitating factors included office procedures that reduce missed opportunities to vaccinate,³⁸ financial support for vaccination (eg, the Vaccines for Children program),²⁷ and policies that promote vaccination.^27,34 Barriers to recommending HPV vaccines related to personal knowledge and beliefs included insufficient knowledge about HPV and HPV vaccines²⁷ and a number of concerns about HPV vaccines. Parent and patient-related barriers included a lack of parental interest,^26,38 lack of parental understanding about the vaccines,^21,31,38,64 and a number of parental concerns that clinicians either anticipated or had experienced. These included concerns about vaccine safety,^{21,25,26,31,35,43,53,64,70} vaccine efficacy,^21,25,43 negative media reports,²¹ behavioral consequences of vaccination,^21,25,26,35 discussions about sexual topics,^{21,25,35,46,53} child being too young or not yet sexually active,^{25,35,43,46,53,64} and vaccine cost.^22,31 Systems-level barriers included lack of clinic procedures to support vaccination,²⁶ insufficient vaccine supply,^21,33 insufficient reimbursement^{19,22,25–27,33,37,41,44,64} or insurance coverage,^21,23,25,49 and difficulty getting patients to return for subsequent vaccine doses.^{25,35,38,43,64}

Table 2.

Clinicians’ Attitudes and Beliefs About Recommending HPV Vaccines

Theme	Results
Facilitating factors to recommending HPV vaccines
Personal beliefs
	Vaccine benefits
	Prevention of cancer22,28,33,42,47,49,50,59,63
	Prevention of genital warts28
	Prevention of transmission to and disease in future partners28
	Decreased health care costs49
	Better method of cervical cancer prevention than Papanicolaou test18
	Vaccine benefits specific to young men
	Prevents genital/anal warts49
	Protect future partners from HPV infection and cervical cancer28,49
	Herd immunity49
	Vaccine safety33,49,69
Parent-/patient-related
	Cultural beliefs
	Latino families, immigrants more accepting42
	Education of patients/families
	Sheets exploring parental concerns, focus on cancer prevention42
	Communication about clinic vaccine appointment protocol38
Systems-level
	Office-level
	Reducing missed opportunities through recall/reminder systems38
	Financial support for vaccination (eg, VFC)27
	Policies
	State-level policies27,34
	Mandated vaccination35,36,49,52
Barriers to recommending HPV vaccines
Personal knowledge and beliefs
	Knowledge
	Insufficient knowledge of HPV and HPV vaccines27
	Beliefs and attitudes about HPV vaccines
	Concerns about vaccine safety,25,27,56 efficacy,25,27,56 duration of immunity26,37
	Low perceived risk of HPV-related diseases in one’s patients and belief HPV-related disease can be prevented in other ways (eg, Papanicolaou screening)36
	Perception that HPV vaccine is “less important” than other vaccines29,36
	Hesitancy to recommend multiple vaccines at once36
	Discomfort communicating about sexual topics36,51
	Concerns about behavioral consequences of vaccination (sexual behaviors,65 decreased Papanicolaou screening)19,27,33,53,69
	Low perceived control over recommending22
	Mistrust because of the emphasis on marketing of the vaccine in the media and by industry36
	Beliefs and attitudes specific to young men: discomfort vaccinating young boys,49 lack of direct benefit/causes too few cancers in men,28 genital/anal warts can be managed in other ways,28 too late to vaccinate if already sexually active,28 no need to vaccinate men if women already being vaccinated28,64
Parent/patient-related
	Lack of interest/parents not requesting26,38
	Parental lack of education/understanding21,31,38,64
	Belief that adolescents do not need vaccines35
	Anticipated/experienced parental concerns
	Vaccine safety/adverse effects,21,25,26,31,35,43,53,64,70 concern about “new” vaccine25,35,42,53
	Lack of vaccine efficacy21,25,43
	Concern that parent will think clinician is implying their child is sexually active49
	Parental refusal because of negative media reports21
	Parental request to delay vaccination41,46 (especially for patients 11–12 years old42)
	Parental concerns about behavioral consequences of vaccination21,25,26,35
	Parental mistrust of vaccines in general21,31
	Parental reluctance for clinician to discuss sex, STI, or STI vaccine with their child21,25,35,46,53
	Parental beliefs their child is not at risk42 (too young,25 not sexually active35,43,46,53,64)
	Parental concerns about cost,22,31 HPV vaccine not covered by VFC35
	Lack of a mandate leads parents to think HPV vaccine less important than other vaccines51
Systems-level
	Clinic-related
	Lack of staff to administer vaccines,26 lack of space to store vaccine,26 lack of system to track vaccines,26 lack of vaccination records in Emergency Department44
	Insufficient vaccine supply21,33
	Financial
	Cost to provide vaccination/low reimbursement,19,22,25–27,33,37,41,44,64 lack of insurance coverage21,23,25,49
	Insufficient time to recommend vaccine25,33,37,44,46,63
	Competing priorities37
	Multidose vaccine
	Difficulty getting patients to return for subsequent doses25,35,38,43,64

HPV indicates human papillomavirus; STI, sexually transmitted infection; and VFC, Vaccines for Children program.

Clinicians’ Intention to Recommend HPV Vaccines

Data summarizing clinicians’ intention to recommend HPV vaccines, as well as factors associated with intention, are shown in Table 3. In studies that examined intention among clinicians, rates varied widely, from 16% to 96%.^{17,19–23,33,37,41,44,57,69,71} The mean for intention rates was 66.9 (SD = 23) and the median was 73; the 16% intention rate was an outlier. In 2 studies that examined intention according to patient age, intention was higher for 13- to 18-year-olds (92%–96%) than 11- to 12-year- olds (73%–78%).^41,71 In a study on clinicians’ intention to recommend the HPV vaccine according to patient gender, 67% of clinicians intended to recommend HPV vaccines only to female patients, whereas 14% intended to recommend the vaccine to girls and boys equally.²⁰ In another study on implementation of the HPV vaccine for boys, 62% of clinicians reported intending to recommend the vaccine to boys.³⁷ Intention to recommend to boys varied according to age in 1 study, with the highest intention rates (61%) reported for boys 13 to 17 years of age.²¹ Clinician-related factors included higher knowledge levels about HPV,²¹ professional factors (eg, specialty^20,23,57 and national or professional society recommendations²⁰), and beliefs and attitudes about HPV vaccines (eg, beliefs about vaccine safety and efficacy,²² about early vs late adoption of new vaccines,^17,33 and about behavioral effects of vaccination⁵⁶). Parent/patient-related factors associated with intention included perception that the patient was at high risk for HPV infection.⁴⁴ Systems-level factors negatively associated with intention included insufficient staff time³³ and lack of reimbursement for vaccination.^33,44

Table 3.

Clinicians’ Intentions to Recommend HPV Vaccination

Theme	Results
Intention rates
	Overall range
	16% to 96%17,19–23,33,37,41,44,57,69,71
	Intention by patient age
	11–12 years: 73%41 to 78%71
	13–18 years: 92%71 to 96%41
	Intention by patient gender
	67% intended to recommend only to female patients20
	14% intended to recommend to both boys and girls equally20
	Overall intention to recommend to boys: 62%37
	Boys 9–10 years: 22%21
	Boys 11–12 years 42%21
	Boys 13–17 years: 61 %21
	Boys 18–26 years: 60%21
Factors associated with intention to recommend
Clinician-related
	Knowledge
	Higher knowledge about HPV21
	Professional factors
	Specialty (pediatricians more likely to report intention to recommend vs other specialties)20,23,57
	National recommendations (Food and Drug Administration20) and professional society recommendations20
	Clear recommendation guidelines66
	Beliefs and attitudes
	Beliefs that vaccines are safe and effective22
	Being an early adopter versus late adopter17,33
	Anticipating parental concerns17
	Belief that vaccination would increase riskier behaviors (negative association)56
	Belief that vaccines should be mandated21
	Subjective norms (ie, willingness to adhere to the Advisory Committee on Immunization Practices recommendations, and perceived people they thought were important expected them to vaccinate patients) and perceived behavioral control (ie, if the clinician believed it was within their control to vaccinate the patient)22
Parent/patient-related
	Perceived patient to be at high risk44
Systems-level
	Insufficient staff time (negative association)33
	Lack of reimbursement (negative association),33,44 cost (negative association)22
	Lack of time to discuss HPV vaccine during visit (negative association)44

HPV indicates human papillomavirus.

Clinicians’ Professional Practices Regarding HPV Vaccination

Clinician’s professional practices regarding HPV vaccination are summarized in Table 4. Themes identified were as follows: 1) communication with parents/patients about HPV vaccination, 2) clinician-reported vaccine recommendations and factors associated with vaccine recommendations, and 3) patient vaccination rates and factors associated with vaccination rates. Studies on communication with parents and patients about HPV vaccination addressed various aspects of communication including strategies for introducing the vaccine, population targeted for communication, and consistency of recommendation. Recommendation rates ranged from 34% to 93% across studies that reported data not stratified according to age or gender.^{14,21,25,26,28,32,33,39,43,45–47,50,52,54,60,70,72,73} In studies on recommendation rates according to gender, rates for girls ranged from 59% to 79%,^43,54 and for boys ranged from 7% to 84%.^39,43,54,67 In studies on recommendation rates according to age group, rates increased with age for girls as well as boys: the highest reported rates were for 13- to 17- and 18- to 26-year-old girls^{21,28,47,59,72,73} and boys.^28,45,47,67 Several studies examined strength of HPV vaccine recommendation, and to recommend the HPV vaccine less strongly for younger versus older adolescents and for boys versus girls.^{19,46,50,51,57,64} Some studies showed that clinicians tend to recommend the HPV vaccine as an “optional” vaccine, especially for 11- to 12-year-olds.^29,46,62 Factors associated with higher recommendation rates included clinician’s ethnicity (eg, Latino clinicians were more likely to recommend vs those with non-Latino ethnicity^32,40,48), clinician professional characteristics (eg, pediatricians more likely to recommend vs other specialties^27,32,46,57), higher level of clinician knowledge about HPV vaccines,^45,69 clinician attitudes and beliefs about vaccination, patient-related factors (eg, girls more likely to receive recommendation vs boys,²⁸ older adolescents more likely to receive recommendation vs younger adolescents²⁷), and systems-related factors (eg, higher number of office procedures to maximize vaccination positive associated²¹ and lack of reimbursement for vaccination negatively associated^45,52 with vaccination).

Table 4.

Clinicians’ Professional Practices Regarding HPV Vaccination

Theme	Results
Communication with parents and patients about HPV vaccination
Content of communication
	Emphasis on cancer prevention over STI/genital wart prevention19,25,30,35,49,51,67
	Personal protection was emphasized more than protection of partners25,67
	Importance of vaccination before sexual initiation29,50,53,67
	Provide materials developed by the Centers for Disease Control and Prevention, vaccine manufacturer, the Immunization Partnership, American Cancer Society46,49,51,64,69
Strategies for introducing vaccine
	Saying child is due for HPV vaccination29,51
	Suggesting child get HPV vaccine51,64
	Tend to recommend other vaccines (eg, Tdap) first, HPV vaccine last29,51,52,64
Population targeted for communication
	Recommend to girls more frequently than boys51
	More likely to recommend in older versus younger patients19,25,50,57,62,64
Consistency of recommendation
	Less likely to recommend vaccines at sick versus well visits (if recommended at sick visits, less likely to recommend HPV compared with other vaccines)22,51,52,58
	Communication if parent deferred initiation at a previous visit: some clinicians not likely to recommend at future visit29,46,57
Sources of information about HPV vaccine
	Professional organizations, scientific literature, professional conferences/meetings, academic lectures/grand rounds (less commonly cited: colleagues, media, industry)21
Clinician-reported vaccine recommendations
Recommendation rates
	Overall recommendation rates
	Range: 34% to 93%14,21,25,26,28,32,33,39,43,45–47,50,52,54,60,70,72,73
	Recommendation according to patient age
	9–10 years: 13%25
	11–12 years: 56%−73%25,52
	13–15 years: 90%25
	16–18 years: 94%25
	19–26 years: 94%25
	Recommendation according to patient gender
	Girls
	All age groups: 59%−79%43,54
	9–10 years: 18%−68%21,28,47,73
	11–12 years: 49%−76%21,28,46,47,59,73
	13–17 years: 60%−98%21,28,47,59,72,73
	18–26 years: 57%−98%21,28,47,59
	Boys
	All age groups: 7%−84%39,43,54,67
	9–10 years: 9%−24%28,47,67
	11–12 years: 11%−64%28,45,47,67
	13–17 years: 13%−93%28,45,47,67
	18–26 years: 13%−93%28,45,47,67
Type/strength of recommendation
	Recommendations lack in consistency (recommending routinely vs risk-based approach) and urgency (recommending same-day vaccination)51
	Strength of recommendation compared with other vaccines and for specific age groups and genders
	Recommend HPV vaccine as an “optional” vaccine,67 especially for 11- to 12-year-old adolescents29,46,62
	Recommend HPV vaccine less strongly than for other vaccines, recommend less strongly for younger versus older age groups and boys versus girls19,46,50,51,57,64
	More likely to “highly endorse” other vaccines versus HPV vaccines for 11- to 12-year old adolescents,51,67 studies of parents support these findings (ie, HPV vaccine reported by parents as less strongly recommended than other adolescent vaccines)14,51
	Strength of recommendation according to specialty
	Pediatricians more likely to strongly recommend than family physicians27,40,46,50,57,74
Trends in recommendation
	Increasing recommendations over time since vaccines were licensed for early adolescents (11–12 years old)48
Factors associated with vaccine recommendations
Clinician personal characteristics
	Ethnicity/race: Latino clinicians more likely to recommend versus non-Latino, nonwhite versus white32,40,48
	Vaccines for Children provider40,72
Clinician professional characteristics
	Pediatrician more likely to recommend versus other specialties27,32,46,57
Clinician knowledge
	Higher knowledge of HPV45,69
	Ambivalence about the clarity of HPV vaccination guidelines (negative association)66
Clinician attitudes and beliefs
	Facilitating factors
	Higher intention to recommend46
	Being an early adopter19,45
	Belief that vaccines are effective and safe19,70
	Perceived risk among their patient population62
	Belief that immunity is long-lasting19,70
	Perception that professional organizations are valuable sources of information21
	Belief in mandated vaccination21
	Lower (in one study, higher) number of barriers to recommendation experienced21
	Barriers
	Concern about vaccine efficacy19
	Concern about waning immunity70
	Personal belief that the vaccine not necessary because patient is not at risk because not yet sexually active or too young62
	Discomfort discussing STIs with parents, perception that having to talk about an STI will make conversations about the HPV vaccine uncomfortable25
	Concerns about riskier sexual behaviors after vaccination70
	Insufficient time to discuss HPV or vaccine25,29
	Perceived/experienced parent-related barriers: belief that parents believe the vaccine is not important,35 expectation that parent will refuse,29 parental concerns about vaccine safety and efficacy,29 parental belief that girls should be the ones to take preventive measures,64 parents deferring vaccination when offered,25,29,57 parents believe vaccine will promote sexual activity35
Patient-related factors
	Demographic-related
	Boys receiving fewer recommendations versus girls28
	Older adolescents more likely to receive recommendation versus younger27
	Race (inconsistent associations): non-Hispanic white versus non-Hispanic black, higher Latino population, non-Hispanic black versus other35,40,57,72
	Insurance status
	Higher proportion of Medicaid/nonprivate insurance patients25,45,72
	Lower rates of uninsured72
Systems-related factors
	Higher number of office procedures that maximize vaccination21
	Lack of reimbursement for vaccination (negative association)45,52
	Lack of time to discuss vaccine during the office visit (negative association)25,29
	Vaccines for Children program provider45,72
Patient vaccination rates
	Overall vaccination rates
	Range: 24%−62%24,40,54,72,74
	Vaccination rates according to age:
	11–12: 28%24
	13–15: 28%24−76%61
	16–18: 24%24−78%61
	Vaccination rates according to patient gender:
	Girls: 35%−84%13,54,61,72,74
	Boys: 44%13−65%61
Factors associated with patient vaccination rates
Clinician personal characteristics
	Demographic-related factors
	Physician gender (men less likely to report that most of patients were vaccinated)41
Clinician knowledge
	Higher knowledge about vaccine31
	Centers for Disease Control and Prevention/professional society guidelines31
Clinician professional characteristics
	Specialty (vaccination rates higher among pediatricians vs other)27,61 ,74
	Practice characteristics
	Private practice more likely to have higher vaccination rates versus ambulatory care/urgent care/community health clinic74
	Residency training on vaccine use31
	Experience with vaccine31
	Vaccines for Children provider27,40,72
Patient-related
	Demographic-related factors
	Girls versus boys (girls more likely to initiate HPV vaccine series)61
	Insurance: Medicaid/State Children’s Health Insurance Program (compared with patients with private insurance)25,72
Systems-related
	Lack of reimbursement for vaccine (negative association)31
	Practice policies
	Recall/reminder systems and other systems to ensure vaccine completion38,68
	Use of vaccination database/registry40
	Higher patient volume40

HPV indicates human papillomavirus; STI, sexually transmitted infection; and Tdap, tetanus, diphtheria, pertussis.

Patient HPV Vaccination Rates

Several studies reported patient vaccination rates. Specifically, 6 studies reported on vaccination rates on the basis of review of medical records,^{24,40,54,61,72,74} and 5 studies detailed clinicians’ self-reported vaccination rates.^{25,27,31,40,68} Rates on the basis of medical records tended to be lower than clinician-reported recommendation rates, ranging from 24% to 62%,^{24,40,54,72,74} and rates did not increase with patient age according to 1 study.²⁴ Factors associated with patient vaccination included clinician personal characteristics (eg, patients of female clinicians were more likely to be vaccinated than those of male clinicians⁴¹), higher level of clinician vaccine knowledge,³¹ clinician professional characteristics (eg, patients of pediatricians more likely to be vaccinated than those of other specialists),^27,61,74 patient-related factors (eg, girls vs boys were more likely to be vaccinated⁶¹), and systems-related factors (eg, lack of reimbursement for vaccination was negatively associated with vaccination rates³¹ and office systems that facilitate vaccination^38,40,68).

Discussion

In this study, we found parallels in the findings of studies examining clinicians’ intention to recommend the HPV vaccine, clinicians’ HPV vaccine recommendation practices, and rates of HPV vaccination. Intention to recommend vaccines, recommendation practices, and rates of vaccination varied widely across studies, and tended to be higher for older versus younger adolescents and for girls versus boys. These data are consistent with the suboptimal rates of HPV vaccination across the United States, and for the disparities in vaccination rates according to age and gender observed in national studies.^12,75 Studies consistently reported that actual vaccination rates tended to be lower than clinician-reported recommendation rates. Furthermore, Cook et al²⁴ reported that although clinician-reported vaccine recommendations increased with increasing patient age, there were nearly identical vaccination rates across the age groups. Factors that were identified in these studies as contributing to the difference between recommendation and actual vaccination rates included insufficient time to discuss vaccination and address parental concerns during office visits, patient or parent refusal when a clinician recommended vaccination, clinician deferral of vaccination at a parent’s request, and lack of a strong and consistent clinician recommendation for HPV vaccination. Numerous studies have reported that clinicians recommend the HPV vaccine less strongly than other vaccines, recommend the HPV vaccine as “optional,”^{14,19,46,50,51,57,64,67} and believe that the lack of HPV vaccine school entry mandate is a barrier to providing strong recommendations.^32,36,52

The findings of the studies reviewed suggest that interventions to reduce missed clinical opportunities for vaccination and improve HPV vaccination recommendations for younger adolescents and for boys should focus on: 1) disseminating evidence-based strategies for providing strong HPV vaccine recommendations and effective communication at the initial vaccine recommendation visit, 2) emphasizing the rationale for vaccinating young men as well as young women, and 3) highlighting the importance of vaccinating at the target age of 11 to 12 years and not delaying vaccination. These studies also suggest that clinicians would benefit from guidance to effectively explain to parents the rationale for vaccinating younger adolescents and men.⁵⁷ Furthermore, rigorous evaluations of strategies used in the interventions, such as motivational interviewing to engage reluctant parents in the vaccine discussion,²⁹ will be critical in determining the most effective methods to increase vaccination rates.

We also found notable similarities between the predictors of intention to recommend, vaccine recommendations, and vaccination rates. Predictors associated with all 3 outcomes included clinician-related, parent/patient-related, and systems-level factors, and there was substantial overlap between the specific predictors of each of these outcomes. Clinician-related factors associated with these outcomes included higher level of knowledge about HPV, female gender, specialty (pediatrician vs other specialties), and attitudes about HPV vaccines (eg, beliefs that vaccines are safe and effective were positively associated with the outcomes). Parent/patient-related factors associated with these outcomes included older patient age, female patient gender, and perception that the patient was at risk for HPV-related disease. Systems-level factors included office procedures (eg, recall/reminder systems), vaccine registries, insurance coverage, and vaccine reimbursement.

Interventions are likely to be more successful if they are multilevel and address the predictors of vaccine intentions, recommendations, and vaccination identified in this review. The results of these studies suggest that clinician-focused interventions should focus on improving knowledge about HPV vaccines and vaccine recommendations and ensuring that interventions are inclusive of clinicians who are not pediatricians, such as family physicians and nurse practitioners. Interventions should focus on promoting factors that facilitate vaccine recommendation, using strategies such as providing information about vaccine safety, efficacy, and duration of immunity; disseminating professional society recommendations; and identifying and supporting early adopters to help diffuse HPV vaccine guidelines.⁴⁵ Parent/patient-related intervention components should include provision of educational materials that improve understanding of HPV vaccines and vaccine recommendations, and that address key beliefs that drive decisions about vaccination as well as parental concerns. Communication strategies should be designed to be responsive to the interpersonal subtleties of the clinical encounter between clinicians, parents, and patients. Such strategies should also be culturally sensitive (ie, educational materials should be available in multiple languages and should be accessible to patients and families who have low health literacy). Interventions should also test the effectiveness and acceptability of different communication styles and materials.⁵¹

In addition to focusing on clinician- and parent-level factors, interventions must address systems-level factors to be maximally effective. Systems-level intervention components should include promotion of procedures and policies that maximize vaccination rates, such as recall and reminder procedures, use of vaccination databases or registries to track when the next dose is due and to document vaccine completion, standing orders, and solutions to financial barriers for clinicians (initial cost of vaccine, adequate reimbursement) and families (lack of insurance, deductible and copayment costs). In addition, noncompletion of the HPV vaccine series is often unintentional (eg, because of miscommunication occurring between the provider and parent; parents might assume the clinician will provide reminders for subsequent doses, whereas the clinician might expect the parent to schedule the subsequent doses without the need for a reminder).⁶⁸ Recall and reminder systems are a cost-effective solution to miscommunication. Studies are needed that assess the barriers and facilitators to using recall and reminder systems or vaccine registries. Additional systems-level strategies include high-quality after-visit summaries, effective scheduling methods, walk-in hours, and extended hours.⁶⁸ Finally, studies should address how to include other health care professionals, such as school nurses, in providing information and education to parents about the HPV vaccine and subsequent doses.^55,69 School nurses can play a valuable role in addressing parents’ concerns regarding the HPV vaccine and providing medically accurate information to parents and adolescent patients.

There are limitations to our review. Most studies were cross-sectional, precluding an understanding of changes in attitudes and practices over time, and most recruited convenience samples, limiting generalizability. Most studies of clinician practices were self-reported and data were not validated; these data might be subject to reporting bias. Furthermore, this review did not include interventions, because this was outside of the scope of the review. However, there would be substantial benefit to conducting a review of the emerging literature on interventions designed to improve HPV vaccination. In addition, this was a systematic qualitative review that focused on identifying themes within the literature, and that used selective sampling with no formal quality assessment of the studies included in the review. Therefore, we did not quantitatively assess differences between clinician type, trends of data over time, or geographic trends. However, quantitative reviews and meta-analysis are needed to examine these differences and trends to provide additional evidence to inform the design of interventions that will lead to higher HPV vaccination rates.

Despite these limitations, this review provides valuable data about clinicians’ knowledge, attitudes, intentions to recommend, and practices regarding HPV vaccination. This review suggests that although clinicians are generally supportive of HPV vaccination, many clinicians miss opportunities to recommend vaccination and do not recommend HPV vaccines strongly or consistently. In addition, recommendations vary substantially according to clinician specialty, patient age, and patient gender. Finally, the studies included in this review identified a number of facilitating factors and barriers to HPV vaccination including clinician knowledge, clinician beliefs and attitudes, patients’ gender and age, recall/reminder systems, and reimbursement for the vaccine. These studies provide a comprehensive empirical evidence base for the design of interventions to improve clinician recommendations for HPV vaccination, which in turn will increase vaccination rates and decrease morbidity and mortality due to HPV-related cancers in women as well as men.