Identifying healthcare professionals with lower HPV vaccine recommendation quality: A systematic review

Abstract

Purpose:

Strengthening healthcare professionals’ (HCPs) communication is an evidence-based approach to increasing human papillomavirus (HPV) vaccine uptake among adolescents. To better target future interventions, we sought to synthesize evidence on HCP subgroups who most need to improve their HPV vaccine recommendation quality.

Methods:

We searched 5 databases for quantitative studies published from 2012 to 2022 on HPV vaccine recommendation quality, including recommendation consistency and strength, for US adolescents. Two coders independently abstracted data from each eligible study, following PRISMA guidelines. We summarized variation in recommendation quality by clinical and HCP characteristics.

Results:

The 28 eligible studies indicated that relatively low proportions of HCPs used higher-quality recommendation practices (median: 61% across 30 measures) and that recommendation quality varied across HCP subgroups. The most consistent findings were that more pediatric HCPs used higher-quality recommendations than family medicine HCPs (8 of 11 studies, 2 to 60 percentage point difference) and that HPV-related knowledge was associated with higher recommendation quality (4 of 7 studies). Most studies observed no differences in recommendation quality by clinical role (e.g., provider vs. nurse) or HCP demographics (e.g., gender, age, race/ethnicity).

Conclusion:

Studies suggest a substantial need to improve HCPs’ recommendation quality, with opportunities for targeting future interventions.

INTRODUCTION

Persistent infection with human papillomavirus (HPV) is responsible for approximately 37,000 cancer cases diagnosed in the United States (US) every year.¹ HPV vaccination can prevent about 90% of these cancers,² and 2 doses of the vaccine are recommended for children ages 9 to 12 years as part of the routine immunization schedule.³ However, only half (50%) of 13-year-olds had completed the series by 2022,⁴ indicating that guideline-consistent HPV vaccination remains a challenge. Continued efforts are needed if we are to achieve the national goal of 80% coverage.⁵

Receipt of a healthcare professionals’ (HCP) recommendation is the single largest influence on HPV vaccine uptake.⁶ HCPs’ recommendation is associated with about 9 times higher odds of HPV vaccine initiation among adolescents ages 11 to 17 years.⁷ Yet the most recently available data indicate that almost one-quarter of parents (23%) do not receive a recommendation for their age-eligible adolescents.⁸ Furthermore, recommendations that parents do receive are not always strong, consistent, and timely,⁹ which is problematic because these recommendation qualities are associated with HPV vaccine uptake.¹⁰ Leading public health authorities, including the Centers for Disease Control and Prevention, National Cancer Institute, and President’s Cancer Panel, have emphasized the need for HCPs to improve their HPV vaccine recommendations.¹¹

Fortunately, research in the last decade has yielded evidence-based interventions for improving HPV vaccine communication and uptake. Most notably, several randomized clinical trials have found that training HCPs to improve their communication, including by more consistently recommending HPV vaccination for all age-eligible adolescents, is effective.^12,13 Strong national investment in HCP communication training has likely contributed to improvements in HPV vaccine communication, but the impact has been uneven with the proportion of parents reporting receipt of a recommendation ranging from 91% in Massachusetts to just 60% in Mississippi.⁸ Given the high direct and indirect costs of HCP communication training,^14,15 targeting future trainings to HCPs with lower recommendation quality may help to maximize the impact of these interventions. Thus, we conducted a systematic review of quantitative evidence on which clinical and HCP characteristics are associated with HCPs’ vaccine recommendation quality.

METHODS

We followed the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines¹⁶ in reporting a systematic review of studies on HCP recommendations of HPV vaccination. This systematic review was prospectively registered on PROSPERO (CRD42022329054).¹⁷

Data sources and searches

We searched CINAHL Plus, Embase, PsycINFO, PubMed, and Scopus databases on June 2, 2022, for relevant studies published since January 1, 2012. We started the search period at 2012 because the Advisory Committee on Immunization Practices extended their recommendations for routine HPV vaccination to male adolescents in October 2011.¹⁸ A medical librarian (RC) developed search strings for each database that included terms related to human papillomavirus, vaccine, and communication (Supplemental Table 1). After the initial search, we removed duplicated studies using EndNote (Clarivate, Philadelphia, PA) and Covidence (Veritas Health Innovation, Melbourne, Australia). We also manually searched the reference list of each included study to identify other relevant studies.

Study selection

Pairs of reviewers (KLK, MBG, NLO, WYK) independently screened studies in 2 steps using Covidence. We first reviewed each title and abstract for eligibility. For potentially eligible studies, we then conducted full-text reviews. We resolved disagreements at each stage by discussing studies with the remaining reviewers.

Eligible papers were peer-reviewed quantitative studies published in English that stratified findings on HPV vaccine recommendation quality for adolescent patients in US clinical contexts by clinical or HCP characteristics. We defined HPV vaccine recommendation as verbal communication in which the HCP advised, or intended to advise, the adolescent to be vaccinated. Included measures operationalized this concept with words such as “recommend,” “advise,” or “offer,” while excluded measures used less directive words such as “talk about” or “discuss.” We focused on recommendation quality given its association with vaccine initiation.¹⁰ To characterize higher-quality recommendation, this concept included measures of recommendation strength (emphasizing the importance of vaccination), consistency (recommending for all age-eligible adolescents), timeliness (starting recommendation at ages 9 to 12 years versus later), and urgency (recommending getting vaccinated on the same day).¹⁹

We defined healthcare professionals as including physicians, nurse practitioners, physician assistants, nurses, and medical assistants who deliver primary care to adolescents, while excluding community health workers, dentists, and pharmacists. Adolescents were children ages 9 to 17 years, and we excluded studies with a patient population entirely outside of this age range. Clinical contexts included medical encounters in public or private medical practices and school-located health centers, and excluded alternative vaccination settings, such as emergency departments and pharmacies, as well as events, such as mass vaccine campaigns in community settings. Given variations in healthcare systems as well as HPV vaccination guidelines and access across countries, we included only US studies. We included quantitative, peer-reviewed journal articles and excluded qualitative studies, commentaries, conference abstracts and proceedings, meta-analyses, and narrative, rapid, scoping, or systematic reviews.

Data abstraction

Pairs of reviewers (WYK with KLK or NLO) independently conducted data abstraction using a standardized form and resolved disagreements through discussion. Abstracted data centered on findings about variation in HPV vaccine recommendation quality by clinical or HCP characteristics. Clinical characteristics included specialty (e.g., pediatrics or family medicine), clinical setting (e.g., private or public practice, urban or suburban or rural clinic location), and other characteristics (e.g., patient volume, vaccine delivery system strategies). HCP characteristics included clinical role (e.g., physician, nurse), vaccine cognitions (e.g., HPV knowledge, vaccine concerns), and other demographic and professional characteristics (e.g., gender, age, years in practice).

Reviewers also abstracted data on study characteristics, including study design, data source, and sample size and description. We contacted authors for unreported study information, such as study period and sampling approach. Reviewers also assessed study quality using 8 indicators from Sirriyeh et al.’s Quality Assessment Tool for Studies with Diverse Designs (QATSDD), such as on sample representativeness and size, description of participant recruitment and data collection processes, and appropriateness of data analysis.²⁰ Reviewers scored these quality indicators on a 4-point scale from “not at all” (coded as 0) to “complete” (3), and we summed the scores into an overall score that could range from 0 (lowest study quality) to 24 (highest study quality).

Data synthesis

We qualitatively summarized variation in recommendation quality by each clinical and HCP characteristic. We report absolute percentage point (pp) differences in the proportion of HCPs using higher-quality recommendations by each characteristic (e.g., HCPs in public vs. private practices, female vs. male HCPs). We denote our unit of analysis (i.e., studies) with k.

RESULTS

Our search yielded 4,389 unique records, with 28 studies meeting eligibility criteria (Figure 1). All eligible studies used cross-sectional data, with most analyzing data collected from HCP versus parent reports (k=27 vs. 1, Supplemental Table 2). Over half of the included studies used regional versus national samples (k=16 vs. 12). Study quality scores ranged from 12 to 24 on the QATSDD index (median=22.5). Some studies assessed discrete aspects of recommendation quality in terms of recommendation consistency (k=14), strength (k=5), timeliness (k=1), or intention to recommend (k=1). Other studies assessed multiple aspects of recommendation quality combined (k=7).

Figure 1.

PRISMA flow diagram of studies reviewed

Recommendation quality in overall samples

Of the 28 included studies, 20 studies provided data on the overall proportion of HCPs who used higher-quality recommendations. Across 30 measures, a median of 61% of HCPs used higher-quality recommendation practices (range: 21% to 97%, Supplemental Table 2).^21,22 In only 5 of these measures did over 80% of HCPs use the higher-quality practice.

Variation in recommendation quality by clinical characteristics

Specialty (17 studies^21–37).

Most studies that compared medical specialties on recommendation quality found that more HCPs in pediatric specialties used higher-quality recommendations, compared to those in non-pediatric specialties. For example, 11 studies compared pediatrics to family medicine.^{21–23,27–31,34–36} Eight of these studies found higher proportions of pediatrics HCPs used higher-quality recommendations compared to family medicine HCPs (difference in proportion: 2 to 60 pp),^{22,23,27–31,34} and the remaining 3 studies found no statistically significant differences.^21,35,36 Similarly, studies that compared pediatrics to other non-pediatric specialties, such as internal medicine and obstetrics/gynecology,^{24,26,29,31,33,35,37} found more HCPs in pediatrics used higher-quality recommendations (4 of 7 studies, 32 to 93 pp)^24,26,29,31 or found no statistically significant differences (3 of 7 studies).^33,35,37 Other studies assessed recommendation quality among HCPs in specialties outside of primary care and found higher-quality recommendations in pediatric subspecialties such as hematology/oncology versus rheumatology,³² but no differences among gynecology subspecialties.²⁵

Clinical setting (9 studies^{21,23,25,28,32,37–40}).

Studies did not find consistent differences in recommendation quality by clinical setting. For example, 7 studies compared clinics in urban, suburban, and rural areas on recommendation quality.^{21,23,25,32,37,38,40} Three of these studies found no statistically significant differences between urban, suburban, or rural clinics,^23,32,40 2 studies found more HCPs in urban versus non-urban (i.e., rural and suburban) clinics used higher-quality recommendations (5 to 8 pp),^21,37 1 study found more HCPs in suburban versus non-suburban (i.e., rural and urban) clinics used higher-quality recommendations (5 to 31 pp),²⁵ and 1 study found more HCPs in non-suburban (i.e., rural and urban) versus suburban clinics used higher-quality recommendations (13 pp).³⁸ An additional 2 studies found no statistically significant differences in recommendation quality by US Census regions.^21,32

A total of 7 studies compared practice types, such as private practices, health system-affiliated practices, and federally qualified health centers, on recommendation quality.^{21,23,25,28,32,37,39} Three of these studies found more HCPs in publicly funded versus private or other practices used higher-quality recommendations (6 to 14 pp),^21,28,37 1 study found more HCPs in private versus publicly funded practices used higher-quality recommendations (12 pp),³⁹ and 3 studies found no statistically significant differences.^23,25,32

Other clinical characteristics (7 studies^{21,25,32,33,36,37,40}).

Findings about differences in recommendation quality across other clinical characteristics were mixed or limited in number. For example, 2 studies found a positive correlation between Vaccine for Children affiliation and recommendation quality.^33,37 Another 6 studies compared patient volume on recommendation quality.^{21,32,33,36,37,40} Four of these studies found no statistically significant differences,^21,33,36,37 and 2 studies found more HCPs with higher versus lower patient volume used higher-quality recommendations (5 to 18 pp).^32,40 An additional 3 studies found no statistically significant differences in recommendation quality associated with the use of most vaccine delivery system strategies such as electronic medical record prompts.^25,33,37

Variation in recommendation quality by HCP characteristics

Clinical role (9 studies^{21,28,29,34,35,41–44}).

Studies that compared clinical role on recommendation quality found few consistent differences among physicians, advanced practitioners (nurse practitioners and physician assistants), and nursing staff. For example, 5 studies compared the recommendation quality of providers (physicians and advanced practitioners) versus other clinical staff (nursing staff and other HCPs).^{21,35,41,42,44} Four of these studies found no statistically significant differences.^21,35,41,44 An additional 5 studies compared recommendation quality among different provider types (physicians versus advanced practitioners).^{21,28,29,34,43} Three of these studies found no statistically significant differences,^28,29,34 1 study found more physicians versus advanced practitioners used higher-quality recommendations (7 pp),²¹ and 1 study found more advanced practitioners versus physicians used higher-quality recommendations (12 pp).⁴³

Vaccine cognitions (11 studies^{23,25,26,32,34,36,37,45–48}).

Most studies that compared vaccine cognitions on recommendation quality found that quality correlated with HPV-related knowledge but less consistently with other cognitions. Seven studies compared recommendation quality by HCPs’ knowledge of HPV (e.g., infection, associated cancers) or HPV vaccination (e.g., effectiveness, vaccination guidelines).^{23,25,26,32,37,46,47} Four of these studies found more HCPs with higher versus lower levels of knowledge used higher-quality recommendations (27 to 38 pp),^25,26,46,47 and the other 3 studies found no statistically significant differences.^23,32,37

A total of 10 studies compared HCPs’ other cognitions on recommendation quality.^{23,25,26,32,34,36,37,45,46,48} Of these, 2 studies found positive associations of HCPs’ confidence in addressing parental concerns³⁴ and descriptive norms about other obstetricians/gynecologists’ HPV vaccine recommendation practices²⁵ with recommendation quality. Another 3 studies found that perceived parental hesitancy was positively (2 of 3 studies, 31 to 36 pp)^36,46 or negatively (1 of 3 studies) associated with recommendation quality.³⁷ Few studies found statistically significant differences in recommendation quality by HCPs’ discomfort with discussing sex (2 of 5 studies),^{23,32,36,37,46} vaccine efficacy concerns (1 of 5 studies),^{23,26,32,37,46} vaccine safety concerns (1 of 3 studies),^36,37,46 perceived increase in sexual behavior (1 of 3 studies),^36,37,48 or other perceived barriers in communicating with parents about HPV vaccine (0 of 1 study).²⁶

Other HCP demographic and professional characteristics (11 studies^{21,23,25,28,29,32,33,36–38,41}).

Very few studies found statistically significant differences in recommendation quality by HCPs’ gender (1 of 11 studies),^{21,23,25,28,29,32,33,36–38,41} age (1 of 8 studies),^{25,29,32,33,36–38,41} or race/ethnicity (1 of 6 studies).^{21,25,29,33,37,38} No studies found statistically significant differences in recommendation quality by years in practice (0 of 7 studies).^{21,25,28,29,36–38}

DISCUSSION

Our systematic review of 28 studies sought to characterize variation in HCPs’ HPV vaccine recommendation quality for US adolescents. Across these studies, the overall proportion of HCPs who reported delivering higher-quality recommendations was low. Consistent with earlier reviews,^49,50 recommendation quality was even lower among HCPs in non-pediatric specialties, such as family medicine, compared to pediatrics. Studies in our review observed this recommendation deficit despite family physicians serving as a key source of primary care for adolescents,⁵¹ and professional health organizations, including the American Academy of Family Physicians, encouraging HPV vaccine recommendations.⁵² Lower adolescent patient volume^34,51 and the broader range of health conditions seen in family medicine practices⁵³ may be contributing to lower recommendation quality. Future studies should identify and address recommendation barriers, such as not having adequate adolescent medicine subspecialty knowledge, that HCPs in family medicine may face more often than those in pediatrics. At the same time, our findings suggest that family medicine HCPs could benefit from evidence-based communication training interventions to improve their recommendations. Because not all family medicine HCPs serve adolescents, targeting efforts to those with higher adolescent patient volumes may be needed to ensure that interventions achieve sufficient reach.

Interestingly, studies did not consistently find lower recommendation quality in rural versus non-rural areas, despite persistent rural disparities in HPV vaccination coverage.^4,54 This finding also contrasts parents’ report of receiving fewer recommendations for adolescents residing in rural areas.⁹ Reasons for this divergence in HCP and parent reports of recommendations are unclear, but could reflect rural families’ lower access to healthcare services. Indeed, national data indicate that adolescents living in non-metropolitan versus metropolitan areas have fewer preventive care visits.⁵⁵ Tsai and colleagues also recently found having a low number of primary care providers was a barrier to vaccination for low-income families in rural settings.⁵⁶ Thus, rural adolescents could receive fewer recommendations due to having fewer interactions with HCPs, even if rural-serving HCPs recommend HPV vaccination with comparable quality to those serving non-rural areas. In this case, interventions seeking to reduce the rural disparity in HPV vaccination may benefit from concomitantly targeting more distal environmental factors, such as transportation and community outreach, to improve vaccine uptake. An alternative explanation for the divergence in HCP versus parent reports could be due to differences in how recommendation quality is measured in each population; parents are typically asked whether they have ever received a recommendation for their children with dichotomous, yes/no response options,⁹ while HCPs are often asked more complex questions about recommendation consistency, strength, or timeliness across their patient populations. As such, more consistent measures of recommendation quality may be needed to triangulate findings on recommendation delivery and receipt. Given the narrower differences in rural-urban coverage for other adolescent vaccinations,⁴ greater hesitancy toward HPV vaccination among rural parents could also be contributing to the difference between HPV vaccine recommendation quality and coverage in rural areas. Future studies should consider examining parental barriers to HPV vaccination in rural areas to further inform multi-level approaches in increasing vaccine uptake.

Most studies found that recommendation quality did not vary by HCPs’ gender, age, race/ethnicity, or years in practice. These findings suggest that targeting interventions to HCPs based solely on their demographic and professional characteristics is unlikely to contribute to significant increases in HPV vaccination rates via recommendation delivery. Most notably, our findings on years in practice suggest that communication training should be implemented among HCPs at every career stage, including medical school for physicians in training and continuing education for HCPs who are already in practice.

Our findings highlight additional practice- and research-based implications for increasing HPV vaccine recommendation quality. First, similar recommendation quality found across clinical roles points to the potential of employing a team-based approach in HPV vaccine recommendations. For example, the Community Preventive Services Task Force highlights standing orders as a promising strategy in increasing vaccination rates,⁵⁷ suggesting that nursing staff should be empowered to deliver vaccine recommendations to support and extend provider recommendations. Second, variation in recommendation quality by HCPs’ vaccine cognitions further highlights the opportunity of increasing high-quality recommendations, such as via clinical education, to improve HPV-related knowledge and, in turn, recommendations from both providers and other clinical staff. Finally, our review found wide variation in how recommendation quality is measured, with half of included studies assessing only recommendation consistency. This finding suggests an opportunity for future studies to measure recommendation quality more comprehensively, including consistency, strength, timeliness, and urgency,¹⁹ and to more specifically identify which aspects of quality that communication trainings should address.

Our findings should be interpreted in light of several limitations, including in the quality and scope of the eligible studies. First, all 28 studies included in this review analyzed cross-sectional data, thereby limiting our ability to understand the extent to which factors, such as HPV-related knowledge, foster versus merely coexist with recommendation quality. Second, all available data relied on HCPs’ self-report which is vulnerable to biases, including social desirability. Future research should consider including objective measures of recommendation quality, such as from recordings,^58–63 to minimize such biases. Studies could also employ more rigorous designs such as randomized trials to demonstrate the impact of strategies aimed at improving HPV vaccine communication and uptake. Third, the clinical and HCP characteristics presented in this review are not comprehensive, but rather reflect what is available in the literature. Assessing the association of other place-based factors, such as school entry requirements and other vaccine-related policy, with HCP recommendations could yield further insights for future intervention targets and help to explain why recommendation receipt and HPV vaccination coverage vary so widely by state. Lastly, most eligible studies used non-probability samples that may have generated biased prevalence estimates but externally valid statistical associations,⁶⁴ hence the generalizability of the percentage point differences reported for each HCP subgroup across studies in this review is unclear. Our review findings nonetheless offer usable insights on the associations of clinical and HCP characteristics with HPV vaccine recommendation quality to guide future intervention studies.

CONCLUSION

Our review found overall low HPV vaccine recommendation quality across studies and consistently lower recommendation quality among HCPs in non-pediatric specialties, such as family medicine. Communication interventions should identify family medicine HCPs who see higher adolescent patient volumes and explore the mechanisms of their recommendation practices to increase their delivery of high-quality recommendations. Given no variation in recommendation quality by clinical role, interventionists should also consider making use of team-based approaches to HPV vaccine recommendations that engage providers and other clinical staff. In summary, continued efforts to promote strong, consistent, timely, and urgent recommendations are needed to increase HPV vaccine uptake among adolescents. Targeting those efforts to where they are most needed may help to make the best use of limited time and resources available for interventions around HCP recommendations for HPV vaccine uptake.

Table 1.

Summary of studies on HPV vaccine recommendation quality (k = 28 studies)

Author, year	HPV vaccine recommendation quality measure	Key findings by clinical and HCP characteristics
		Higher recommendation quality among:	No difference in recommendation quality by:
Alcalá, 201841	Consistent recommendation for female patients ages 11–12 (74% of the time) and male patients ages 11–12 (67% of the time)	• Female vs. male HCPs for male patients (83% vs. 39%, p=.02) • Younger vs. older HCPs for male patients (82% vs. 34%, p=.02)	• Physicians vs. other clinical staff for female or male patients • HCP gender or age for female patients
Allison, 201623	Strong recommendation for female and male patients ages 11–12	• Pediatricians vs. family physicians for male patients • HCPs with more vs. less HPV vaccine efficacy concerns for female patients	• Pediatricians vs. family physicians for female patients • HCPs with more vs. less HPV vaccine efficacy concerns for male patients • Locale (urbanicity), practice type (e.g., private clinics vs. hospitals), HPV vaccine knowledge and other cognitions (e.g., discussing sex), and HCP gender for female or male patients
Ayres, 202242	Consistent recommendation or urgent recommendation (“almost always”) for patients ages 11–12	Consistent recommendations: • Clinicians vs. nurses and other HCPs (odds ratio=3.31, 95% CI 1.11–9.88) • Urgent recommendations: • Clinicians vs. nurses and other HCPs (odds ratio=3.55, 95% CI 1.29–9.72)
Berkowitz, 201524	Consistent recommendation for female patients ages 11–12	• Pediatricians vs. internists (74% vs. 30%, p<.001)
Bonville, 201743	Consistent recommendation (“always”) for patients ages 13–18	• Advanced practitioners vs. physicians (95% vs. 83%, p<.05)
Brennan, 202225	Strong and consistent recommendation for patients ages 9–26	• HCPs with more vs. less positive HPV vaccination beliefs (61% vs. 31%, p=.01) • HCPs with more vs. less HPV knowledge (mean=5.4 vs. 4.9, p=.002) • HCPs with high vs. low descriptive norms about other OB/GYNs’ recommendation practice (aOR=24.33, 95% CI 2.56–231.14) • HCPs in suburban vs. urban and rural clinics (64% vs. 59% and 33%, p<.05)	• OB-GYN vs. other gynecology specialty, FQHC status, EHR prompt, descriptive norms about other primary care providers, and HCP demographics (gender, age, race/ethnicity, or years in practice)
Btoush, 202226	Consistent recommendation (“always”) for patients ages 11–13	• HCPs in pediatrics vs. non-pediatrics specialty (aOR=1.98, 95% CI 1.09–3.57) • HCPs with more vs. less HPV vaccine knowledge (aOR=6.86, 95% CI 2.3020.43) • HCPs with fewer vs. more HPV vaccine concerns	• Perceived HPV vaccine effectiveness, facilitators, or barriers
Cataldi, 202127	Consistent recommendation for female and male patients ages 11–12	• Pediatricians vs. family physicians for female patients in 2018 (99% vs. 96%) and for male patients in 2013–2014 (90% vs. 86%) and 2018 (99% vs. 94%, all p<.05)	• Pediatrics vs. family medicine specialty for female patients in 2013–2014
Chopp, 201645	Intention to recommend for female and male patients ages 11–12	• HCPs with more positive HPV vaccine attitudes for female patients (t-test value=4.69, p<.0001) • HCPs with more positive self-efficacy for female patients (t-test value=9.63) and male patients (t-test value=8.32, all p<.0001)	• HPV vaccine attitudes for male patients
Dempsey, 201628	Strong recommendation for patients ages 11–12	• HCPs in pediatrics vs. family medicine specialty (58% vs. 32%, p=.03) • HCPs in publicly funded vs. private practices (54% vs. 46%, p<.01)	• Physicians vs. nurse practitioners vs. physician assistants, and HCP demographics (gender or years in practice)
Deupree, 201746	Consistent recommendation for female and male patients ages 11–26	• HCPs with vs. without HPV cancer knowledge for male patients (37% vs. 3%, p<.05) • HCPs with vs. without HPV vaccine knowledge for male patients (39% vs. 1%, p<.05) • HCPs with vs. without perceived parental barrier for male patients (36% vs. 5%, p<.05)	• HPV cancer or vaccine knowledge and perceived parental barrier for female patients • Other HPV vaccine cognitions (e.g., vaccine efficacy and safety concerns) for female or male patients
Finny Rutten, 201729	Strong recommendation or consistent recommendation for female and male patients ages 11–12	• Strong recommendations: • HCPs in pediatrics vs. family medicine vs. OB-GYN or internal medicine clinics for female patients (95% vs. 67% vs. 50%) and male patients (88% vs. 52% vs. 25%, all p<.001) • HCPs with pediatrics vs. family medicine board certification for female patients (95% vs. 67%) and male patients (87% vs. 53%, all p<.01) • Consistent recommendations: • HCPs in pediatrics vs. family medicine vs. OB-GYN or internal medicine clinics for female patients (98% vs. 76% vs. 20%) and male patients (93% vs. 57% vs. 0%, all p<.001) • HCPs with pediatrics vs. family medicine board certification for female patients (97% vs. 75%) and male patients (95% vs. 55%, all p<.01)	• Physicians vs. advanced practitioners, and HCP demographics (gender, age, race/ethnicity, or years in practice) for female or male patients
Gilkey, 201530	Strong recommendation (“extremely” or “very” important) for patients ages 1112	• Pediatricians vs. family physicians (77% vs. 69%, p<.05)
Hansen, 202031	Consistent recommendation (“always”) for female and male patients ages 11–12	• Pediatrics vs. family medicine vs. OB-GYN residents for female patients (76% vs. 16% vs. 0%, p<.05) • Pediatrics vs. family medicine residents for male patients (67% vs. 10%, p<.05)	• Residency year for female or male patients
Hofstetter, 201732	Consistent recommendation (“always” or “sometimes”) for adolescent patients with chronic medical conditions (patient age range not specified)	• HCPs in hematology/oncology vs. rheumatology, pulmonology, and endocrinology (66% vs. 46%, 31% and 26%, p<.001) • HCPs without vs. with discomfort discussing sex • HCPs without vs. with adequate HPV vaccine information • HCPs with higher vs. lower patient volume (aOR=1.01, 95% CI 1.00, 1.02)	• Locale (urbanicity or U.S. region), practice type (e.g., private clinics vs. community health centers), HPV knowledge, HPV vaccine efficacy beliefs, and HCP demographics (gender, age, or years in practice)
Hopfer, 201938	Strong and urgent recommendation by “engagers” and “protocol followers” (patient age range not specified)	• HCPs in suburban vs. non-suburban clinics (64% vs. 77%, p<.05)	• HCP demographics (gender, age, race/ethnicity, or years in practice)
Hswen, 201747	Strong, consistent, timely, and urgent recommendation for female and male patients ages 11–12	• HCPs who were vs. were not aware of their professional organizations’ HPV vaccination guidelines for female patients (52% vs. 25%) and male patients (54% vs. 26%, both p<.001)
Kempe, 201922	Consistent recommendation for female and male patients ages 11–12	• Pediatricians vs. family physicians for female patients (99% vs. 96%) and male patients (99% vs. 94%, both p<.05)
Kong, 202221	Timely recommendation for patients ages 9–10	• Physicians vs. advanced practitioners (23% vs. 16%, p<.05) • HCPs who were black vs. Asian and white (32% vs. 29% and 20%, p<.05) • HCPs in publicly funded practices vs. hospitals, solo and group practices (32% vs. 26%, 20% and 18%, p<.05) • HCPs in urban vs. rural and suburban clinics (26% vs. 21% and 18%, p<.05)	• Physicians vs. nurses, pediatrics vs. family medicine specialty, locale (U.S. region), practice/system size (with vs. without affiliation with health systems), patient volume, and HCP demographics (gender or years in practice)
Lake, 201933	Strong recommendation or consistent recommendation for patients ages 11–12	• Strong recommendations: • HCPs who were vs. were not VFC providers (aOR=2.62, 95% CI 1.23, 5.59) • Consistent recommendations: • HCPs who were vs. were not VFC providers (aOR=2.84, 95% CI 1.26, 6.39) • HCPs who received vs. did not receive reminders from healthcare team members (aOR=2.26, 95% CI 1.23, 4.16)	• Specialty (e.g., pediatrics vs. family medicine), patient volume, other vaccine-related quality improvement strategies (e.g., EHR reminders), and HCP demographics (gender, age, or race/ethnicity)
Lu, 201939	Receipt of a provider recommendation	• Parents visiting private vs. publicly funded clinics (67% vs. 55%, p<.05)	• Private clinics vs. hospitals
McRee, 201434	Consistent recommendation (“most of the time”) for female and male patients ages 11–12	• Pediatricians vs. family physicians and nurse practitioners for male patients (67% vs. 42% and 41%, p<.001) • HCPs with more vs. less positive self-efficacy for female and male patients	• Clinical role/specialty for female patients
Mills, 201635	Strong recommendation (“very strong” or “somewhat strong”) for patients (patient age range not specified)		• Pediatrics vs. family/internal medicine vs. OB-GYN, and physicians vs. nonphysicians
Roberts, 202044	Consistent recommendation (“75%” or “>90%” of the time) for patients (patient age range not specified)		• Clinicians vs. nurses
Rohrbach, 201740	Consistent recommendation (“always”) for eligible patients (patient age range not specified)	• HCPs who see >21 patients/week vs. 1120, 6–10, and 1–5 patients/week (74% vs. 70%, 60% and 56%, p=.01)	• Locale (urbanicity)
Soon, 201536	Strong recommendation for female and male patients ages 11–12	• HCPs who did not vs. did perceive parental or patient concern about HPV vaccine efficacy as a barrier for female patients (64% vs. 100%, p=.025) • HCPs who did not vs. did perceive the need to discuss sexuality before recommending for male patients (78% vs. 42%, p=.005)	• Pediatrician vs. family physicians, patient volume, other HPV vaccine cognitions (e.g., association with sex, vaccine safety concerns), and HCP demographics (gender, age, or years in practice) for female or male patients
Suryadevara, 201548	Consistent recommendation for adolescent patients (patient age range not specified)	• HCPs without vs. with HPV vaccine misperception of increased risky sexual behavior (figures not reported, p=.002)
Vadaparampil, 201637	Strong and consistent recommendation for male patients ages 11–12	• HCPs who were vs. were not VFC providers (aOR=3.80, 95% CI 1.70–8.54) • HCPs in urban vs. non-urban clinics (aOR=2.08, 95% CI 1.08–4.02) HCPs with fewer vs. more HPV vaccine safety concerns HCPs in non-private vs. private practices	• Pediatrics vs. non-pediatrics specialty, practice/system size (e.g., single vs. multispecialty practices), patient volume, vaccine-related quality improvement strategies (e.g., EHR prompts), HPV knowledge, other HPV vaccine cognitions (e.g., vaccine efficacy concerns, associations with sex, perceived parental barriers), and HCP demographics (gender, age, race/ethnicity, or years in practice)

aOR = adjusted odds ratio, CI = confidence interval, EHR = electronic health record, FQHC = federally qualified health center, HCPs = healthcare professionals, HPV = human papillomavirus, OB-GYNs = obstetricians/gynecologists, VFC = Vaccines for Children.

IMPLICATIONS AND CONTRIBUTION.

To inform future communication interventions, this systematic review of 28 studies examined clinical and healthcare professional (HCP) characteristics associated with human papillomavirus vaccine recommendation quality. Studies consistently found lower recommendation quality among family medicine versus pediatric HCPs. Quality was consistent across HCPs’ demographic factors, including gender and race/ethnicity.

Abbreviations:

HCP

Healthcare professional

HPV

Human papillomavirus

pp

percentage point

US

United States