Introduction
The human papillomavirus (HPV) causes almost all cervical cancer cases as well as the majority of anal, penile, vaginal, vulvar and oropharyngeal cancers [1]. The Centers for Disease Control and Prevention (CDC) estimate that 92% of these HPV-attributable cancers could be prevented by the HPV vaccine [2] and therefore can mitigate HPV-associated cancer disparities before they can even occur. However, despite the compelling evidence for cancer prevention [3], a 10-year record of safety, efficacy [4], support from cancer prevention and adolescent health leaders from across the nation [5], and recommendations from the Advisory Committee on Immunization Practices (ACIP) [6], uptake of the HPV vaccine remains well below the Healthy People 2020 target of 80% [7]. In 2019, among U.S. adolescents aged 13-17, HPV vaccination coverage with ≥1 dose was 71.5% (69.8% for boys and 73.2% for girls) and the percentage of adolescents up-to-date (UTD) with the HPV vaccine series was 54.2% (51.8% for boys and 56.8% for girls) [8]. HPV vaccine uptake remains much lower compared to the other two vaccines included in the adolescent vaccine platform, meningococcal conjugate vaccine (MenACWY) and the tetanus, diphtheria, pertussis vaccine (Tdap). In 2019, vaccination coverage for ≥ 1 MenACWY was 88.9% and 90.2% for Tdap [8].
The Advisory Committee on Immunization Practices (ACIP) recommends routine vaccination against HPV at age 11 or 12 years with catch-up recommendations for all persons through age 26 years. For adults 27 through 45 years of age, shared clinical-decision making is recommended [9]. Increasing the HPV vaccination completion rates from current levels to 80% could prevent an additional 53,000 future cervical cancer cases in the U.S among girls who are 12 years or younger over the course of their lifetime as well as many additional cases of other cancers, pre-cancers, and genital warts in both sexes [10-11].
Most HPV-attributable cancers disproportionately affect racial and ethnic minorities compared to non-Hispanic Whites [12-13]. Hispanic women have the highest rates of HPV-associated cervical cancer compared to women of other races, more black women get HPV-associated vaginal cancer than women of other races, and Hispanic men have the highest rates of HPV-associated penile cancer compared to non-Hispanic men [2]. Gender disparities also exist in HPV-associated oropharyngeal cancers with these cancers occurring 4.5 times more often in men than in women [14]. Additionally, studies have reported that racial and ethnic minorities are more likely than Whites to initiate the HPV vaccine series but are less likely than Whites to complete it [15-16].
Recent data, however, suggest that some of these trends may be shifting. Data from the National Immunization Survey-Teens (NIS-Teen) 2019 indicated that racial and ethnic minorities have higher initiation and HPV UTD rates than Whites, and the overall increase in HPV vaccination coverage is primarily due to increase among boys [8]. Given the racial/ethnic and gender disparities in HPV-attributable cancers and the current trends in HPV vaccine uptake, it is necessary to identify factors associated with HPV vaccine uptake in diverse patient populations and adolescent boys. To the best of our knowledge, no other study utilizes electronic health records to examine adolescent patient and their primary care clinician data in analyzing factors potentially affecting HPV series initiation and being HPV UTD. Previous research largely focused on only adolescent girls and either HPV vaccine acceptance, intent to vaccinate and/or self-reported uptake [17]. Parent, primary care team and clinic level factors that may influence HPV vaccine uptake have been explored through key informant interviews and is reported elsewhere [18].
Using electronic health record (EHR) and administrative data from a primary care network, the goal of the study is to 1) investigate whether current trends in HPV vaccination uptake persist in a diverse primary care setting and 2) identify clinician characteristics associated with HPV vaccination. These data provide a unique opportunity to simultaneously examine patient sociodemographic and healthcare utilization and clinician characteristics associated with HPV vaccination uptake in a single health care setting. Identifying key factors associated with HPV vaccination uptake could help practitioners and researchers co-develop and implement multi-level interventions for patient populations with low HPV vaccine uptake and primary care clinicians.
Material and Methods
Study setting and study population
Electronic health records (EHR) from an academic and community-based primary care network were queried to capture all outpatient visits for girls and boys ages 11-17 years old that occurred within the following departments: family practice, general practice, and pediatrics between January 2017 and June 2018. These encounters occurred at 13 outpatient clinics of University of California, Davis Health (UCDH) primary care network. Although academically affiliated with UC Davis, the network functions as a Medical Group with each clinic designated as a Patient Centered Medical Home. These clinics are located in Sacramento, CA and 9 surrounding communities. During the study period these clinics saw 13,150 unique patients ages 11-17.
Eligible encounters were identified using the International Classification of Diseases, 9th Revision (ICD-9) codes. Contraindications and precautions for administering the HPV vaccine include people who have a moderate or severe acute illness and women who are pregnant [19]. The Chief of Pediatric Diseases for UCDH reviewed the list of IDC-9 codes and excluded any patients with encounters for these ICD-9 code from the analysis: current pregnancy (V22 and V23); acute appendicitis (5400 and 5409); acute leukemia (20802); acute osteomyelitis (73006, 73008); acute pancreatitis (5770); acute parametritis and pelvic cellulitis (6143); acute pharyngitis (462); acute pyelonephritis without lesion of renal medullary necrosis (59010); acute respiratory failure (51881); acute tonsillitis (463); diabetes with ketoacidosis, type I, uncontrolled (25013); fever (78060); influenza (4878 and 4871); malaria (0846); malignant hyperthermia (99586); meningitis (3207 and 3229); pneumococcal pneumonia (481); pneumonia (4830, 4838, and 486); Q fever (Q830); relapsing fever (0879); scarlet fever (0341); and varicella without mention of complication (0529). These exclusions are consistent with how PCN clinicians offer HPV vaccination. Encounters with all other ICD-9 codes were included in the analysis.
Clinician level data were obtained from the UCD EHS system, queries of the UCDH clinician biography webpages (webpages are updated annually based on new information and were reviewed in September 2019) and through conducting an internet search for clinicians who did not have a biography webpage (i.e., those no longer with the network). Demographic data include clinicians’ gender, specialty, clinician type (faculty clinicians practicing at clinics on the main health system campus, clinicians in training, or clinicians practicing at community-based sites) and years in practice. Some patients did not have a designated primary care clinician and we were unable to locate years in practice for all clinicians (67 clinicians). We excluded 16.6% of patients based on encounters with ineligible ICD-9 codes; 1.2% of patients due to clinician specialization other than pediatrics or family/general practice specialties; and 1% due to not having a primary care clinician. This resulted in a final sample size of 10,682 patients (81.2%).
The study’s outcome variables are: 1) HPV vaccine initiation (≥ HPV1) and 2) HPV UTD. HPV UTD is defined as having ≥ 3 doses or having 2 doses when the first HPV vaccine dose was initiated before the age of 15 and there was at least 149 days (five months minus four days) between the first and second dose [20].
Conceptual Framework
The Andersen Behavioral Model of Health Care Utilization was used to first understand the domains involved with obtaining the HPV vaccine and to secondly select, identify and sequence relevant variables associated with those domains. The Model applies a systems perspective to integrate a range of domains associated with the decision to seek care: 1) population characteristics; 2) environment; 3) health behavior; and 4) health outcome [21]. Population characteristics consist of predisposing factors (socio-demographic variables and health beliefs), enabling factors (personal and community resources), and need factors (individual perceived need and professional evaluated need). Environmental factors consist of external physical, economic, and political components including health-care system. Health behavior consists of personal health practices and use of health services (type, site, purpose, and time interval). Health outcomes consist of perceived health status, evaluated health status and consumer satisfaction. The model acknowledges the multiple levels of influences that affect whether or not an individual will get vaccinated for HPV. First providers must make the recommendation, parents must accept and follow through with that recommendation, and the practice environment needs to be conducive to implementing that recommendation. At each level-provider, parent, and practice setting—intermediate outcomes are needed, and characteristics of each level can influence the process.
Variables
Patient predisposing, personal enabling and personal health practices variables included the following: gender (boy or girl); race/ethnicity (race and ethnicity categories were combined to create the following: non-Hispanic White, African American (AA)/Black, American Indian/Alaskan Native-AIAN, Asian American/Native Hawaiian/Pacific Islander-AANHPI, Hispanic, and Other); language preference (English or other); insurance type (private, public, or self-pay); age at first medical visit; number of medical visits during the study period (1, 2, 3, 4, or ≥ 5 ) and whether or not the patient received the meningococcal (MenACWY), tetanus-diphtheria-pertussis (Tdap), HPV and the influenza vaccines.
Clinician predisposing variables included: age, gender (male or female); specialty (pediatrics or family/general); type (faculty, community based, or in-training) and years in practice.
Statistical Analyses
The distribution of patient demographics and patient health care utilization were compared across 3 HPV vaccination coverage groups: 1) 0 dose; 2) ≥ 1 dose; and 3) HPV UTD. We compared patients who did not receive any doses of the HPV vaccine to those who initiated the HPV vaccine series and compared patients who are HPV UTD to those who are not HPV UTD using Chi square tests. Patient characteristics were also compared by gender using Chi square tests given the established differences in uptake for boys and girls. Clinician demographics were summarized by gender using frequencies and percentages or means and standard deviations as appropriate.
Multivariable logistic regression models were estimated to examine the extent to which patient and clinician characteristics were associated with the uptake of the HPV vaccine among adolescents. Mixed effects models were used because of the hierarchical structure of the data; random clinician and clinic effects were used to account for the clustering of patients within clinicians, who were clustered within clinics. Separate analyses were conducted to identify correlates of: 1) initiation of the HPV vaccination series (≥1 dose versus 0 dose); and 2) initiation but not being up to date with the HPV vaccination series (not UTD versus UTD among those with ≥1 dose).
The fully adjusted regression models included the following variables: patient characteristics (gender, race/ethnicity, English language preference, age and insurance type); patient health care utilization (number of medical visits and vaccinations received); and clinician characteristics (specialty, gender, type and years in practice). Results are expressed in terms of odds ratios (ORs) and 95% confidence intervals (CIs). Statistical significance was assessed at the 0.05 level (2-sided). All analyses were performed using STATA version 14 [22]. The study protocol was approved by the University of California, Davis Institutional Review Board (IRB).
Results
Table 1 displays the characteristics of the study population by HPV vaccination uptake. In terms of race/ethnicity, the patients were: 53.4% White; 7.8% AA/Black; 0.9% AI/AN; 14.9% AANHPI; 14.6% Hispanic/Latino; and 8.4% unknown. Most patients were English-speaking (97.9%); had private insurance (80.5%); and received the Tdap (87.6%), MenACWY (82.0%), and influenza (70.3%) vaccines.
Table 1.
Demographics and Health Care Utilization Among Patients Ages 11-17 by HPV Vaccine Uptake, UCD Health Primary Care Network, January 1, 2017 – June 30, 2018a
| 0 (n = 3952) |
≥ 1 (n= 6730) |
UTD (n= 4023) |
All (n = 10682) |
P-Valueb | |
|---|---|---|---|---|---|
| Patient Demographics | |||||
| Gender | |||||
| Boy | 2093 (52.9%) | 3310 (49.2%) | 1863 (46.3%) | 5402 (50.6%) | <0.001 |
| Girl | 1860 (47.1%) | 3420 (50.8%) | 2160 (53.7%) | 5280 (49.4%) | |
| Race/Ethnicity | |||||
| White | 2238 (56.6%) | 3469 (51.5%) | 2094 (52.1%) | 5707 (53.4%) | <0.001 |
| AA/Black | 260 (6.6%) | 573 (8.5%) | 312 (7.8%) | 833 (7.8%) | |
| AI/AN | 37 (0.9%) | 57 (0.8%) | 26 (0.6%) | 94 (0.9%) | |
| AANHPI | 487 (12.3%) | 1104 (16.4%) | 663 (16.5%) | 1591 (14.9%) | |
| Hispanic/Latino | 553 (14.0%) | 1008 (15.0%) | 635 (15.8%) | 1561 (14.6%) | |
| Unknown | 377 (9.5%) | 519 (7.7%) | 293 (7.3%) | 896 (8.4%) | |
| Language | |||||
| English | 3864 (97.8%) | 6589 (97.9%) | 3939 (97.9%) | 10453 (97.9%) | 0.7 |
| Other | 88 (2.2%) | 141 (2.1%) | 84 (2.1%) | 229 (2.1%) | |
| Insurance Type | |||||
| Private | 3103 (78.5%) | 5494 (81.6%) | 3286 (81.7%) | 8597 (80.5%) | <0.001 |
| Public | 155 (3.9%) | 273 (4.1%) | 147 (3.7%) | 428 (4.0%) | |
| Self-Pay | 694 (17.6%) | 963 (14.3%) | 590 (14.7%) | 1657 (15.5%) | |
| Age, mean (SD) | 14.1 | 14.6 | 15.0 | 14.4 | <0.001 |
| Patient Health Care Utilization | |||||
| Medical Visits | |||||
| 1 | 1501 (38.0%) | 1847 (27.4%) | 963 (23.9%) | 3348 (31.3%) | <0.001 |
| 2 | 959 (24.3%) | 1568 (23.3%) | 938 (23.3%) | 2527 (23.7%) | |
| 3 | 549 (13.9%) | 1111 (16.5%) | 675 (16.8%0 | 1660 (15.5%) | |
| 4 | 323 (8.3%) | 769 (11.4%) | 484 (12.0%) | 1098 (10.3%) | |
| ≥ 5 | 614 (15.5%) | 1435 (21.3%) | 963 (23.9%) | 2049 (19.2%) | |
| Vaccines | |||||
| Influenza | 2010 (50.9%) | 5497 (81.7%) | 3458 (86.0%) | 7507 (70.3%) | <0.001 |
| MenACWY | 2368 (59.9%) | 6392 (95.0%) | 3901 (97.0%) | 8760 (82.0%) | <0.001 |
| Tdap | 2882 (72.9%) | 6477 (96.2%) | 3938 (97.9%) | 9359 (87.6%) | <0.001 |
Percentages may not total 100% because of rounding. Percentages are percentages of the row total.
0 shots versus at least 1 dose comparison using Chi-square tests
Abbreviations: AA = African American; AI/AN = American Indian/Alaskan Native; AANHPI = Asian American, Native Hawaiian, and Pacific Islanders; Tdap = Tetanus, diphtheria, & pertussis; MenACWY = Meningococcal group A, C, W-135, & Y
Altogether 63.0% of patients had initiated the HPV vaccine series (≥ HPV1), and 37.7% were up to date with the series. AANHPIs had the greatest proportion of those who initiated the HPV vaccine series (≥ HPV1, 69.4%) and those who were HPV UTD (41.7%) followed by Hispanics (≥ HPV1, 64.6% and HPV UTD, 40.7%), AA/Blacks (HPV ≥ HPV1, 68.8% and UTD, 37.5%), Whites (≥ HPV1, 60.8% and HPV UTD, 36.7%), AI/AN (≥ HPV1, 60.6% and HPV UTD, 27.7%) and those in the unknown race/ethnicity category had the lowest proportion of HPV vaccine initiation (≥ HPV1, 57.9%) and HPV UTD (32.7%).
Table 2 shows the characteristics of the study population, by gender. HPV vaccination initiation (61.3% versus 64.8%) and being up to date with the series (34.5% versus 40.5%) was higher for girls than boys.
Table 2.
Demographics and Health Care Utilization Among Patients Ages 11-17 by Gender, UCD Health Primary Care Network, January 1, 2017 – June 30, 2018a
| Boys (n = 5402) |
Girls (n = 5280) |
All (n = 10682) |
P-Value | |
|---|---|---|---|---|
| Patient Demographics | ||||
| Race/Ethnicity | ||||
| White | 2905 (53.8%) | 2802 (53.1%) | 5707 (53.4%) | 0.65 |
| Black | 412 (7.6%) | 421 (8.0%) | 833 (7.8%) | |
| AI/AN | 46 (0.9%) | 48 (0.9%) | 94 (0.9%) | |
| AANHPI | 791 (14.6%) | 800 (15.2%) | 1591 (14.9%) | |
| Hispanic | 774 (14.3%) | 787 (14.9%) | 1561 (14.6%) | |
| Unknown | 474 (8.8%) | 422 (8.0%) | 896 (8.4%) | |
| Language | ||||
| English | 5281 (97.8%) | 5172 (98.0%) | 10453 (97.9%) | 0.49 |
| Other | 121 (2.2%) | 108 (2.0%) | 229 (2.1%) | |
| Insurance Type | ||||
| Private | 4388 (81.2%) | 4209 (79.7%) | 8597 (80.5%) | 0.07 |
| Public | 197 (3.6%) | 231 (4.4%) | 428 (4.0%) | |
| Self-Pay | 817 (15.1%) | 840 (15.9%) | 1657 (15.5%) | |
| Age, mean (SD) | 14.4 | 14.4 | 14.4 | 0.92 |
| Patient Health Care Utilization | ||||
| Medical Visits | ||||
| 1 | 1739 (32.2%) | 1609 (30.5%) | 3348 (31.3%) | <0.001 |
| 2 | 1357 (25.1%) | 1170 (22.2%) | 2527 (23.7%) | |
| 3 | 855 (15.8%) | 805 (15.2%) | 1660 (15.5%0 | |
| 4 | 537 (9.9%) | 561 (10.6%) | 1098 (10.3%) | |
| ≥ 5 | 914 (16.9%) | 1135 (21.5%) | 2049 (19.2%) | |
| Vaccines a | ||||
| Influenza | 3837 (71.0%) | 3670 (69.5%) | 7507 (70.3%) | 0.09 |
| MenACWY | 4440 (82.2%) | 4320 (81.8) | 8760 (82.0%) | 0.16 |
| Tdap | 4757 (88.1%) | 4602 (87.2%) | 9359 (87.6) | 0.62 |
| HPV | ||||
| ≥ 1 | 3310 (61.3%) | 3420 (64.8%) | 6730 (63.0%) | <0.001 |
| UTD | 1863 (34.5%) | 2160 (40.9%) | 4023 (37.7) | <0.001 |
Percentages may not total 100% because of rounding. Percentages are percentages of the row total.
Girls versus boys comparison using Chi-square tests
Abbreviations: AANHPI = Asian American, Native Hawaiian, and Pacific Islanders; AI/AN = American Indian/Alaskan Native; Tdap = Tetanus, diphtheria, & pertussis; MenACWY = Meningococcal group A, C, W-135, & Y; UTD = Up to Date
Table 3 summarizes clinician characteristics by gender. Between January 2017 and June 2018, 198 clinicians of the primary care network had at least one medical encounter with eligible patients. The majority of the clinicians specialized in Family/General Medicine (69.2%) and were women (59.6%). There were more community-based clinicians (43.4%) than faculty clinicians (21.1%) and those that were in-training (35.4%). The average number of years the clinicians have been in practice was 11.0 years (SD = 14.3).
Table 3.
Primary Care Clinician Characteristics of Patients Ages 11-17 by Gender, UCD Health Primary Care Network, January 1, 2017 – June 30, 2018
| Male (n = 80) |
Female (n = 118) |
All (n= 198) |
|
|---|---|---|---|
| Specialty | |||
| Pediatrics | 25 (31.3%) | 36 (30.5%) | 61 (30.8%) |
| Family/General | 55 (68.8%) | 82 (69.5%) | 137 (69.2%) |
| Provider Type | |||
| Faculty | 21 (26.3%) | 21 (17.8%) | 42 (21.2%) |
| Community based | 37 (46.3%) | 49 (41.5%) | 86 (43.4%) |
| In training | 22 (27.5%) | 48 (40.7%) | 70 (35.4%) |
| Clinician Years in practice, mean (SD) | 15.6 (11.9) | 13.5 (10.2) | 11.0 (14.3) |
Percentages may not total 100% because of rounding. Percentages are percentages of the row total.
HPV Vaccine Initiation (≥ 1)
In multivariable analyses, among adolescent patients aged 11-17 years, characteristics independently associated with higher odds of initiating the HPV vaccine series included: AANHPI patients compared to White patients ( OR = 1.2, 95% CI: 1.0 - 1.4); being older (OR = 1.2, 95% CI: 1.2 – 1.2); patients with 2 or more medical visits compared to patients with only 1 visit (2 visits OR = 1.2, 95% CI: 1.1-1.4; 3 visits OR = 1.4, 95% CI: 1.2 - 1.6; 4 visits OR = 1.6, 95% CI: 1.3-1.9; 5 or more visits OR = 1.4, 95% CI: 1.2 - 1.6); patients who received the Tdap (OR = 2.5, 95% CI: 2.0 - 3.1), MenACWY (OR = 8.1, 95% CI: 6.8 – 9.8) or influenza vaccines (OR = 2.7, 95% CI: 2.4 – 3.0). Boys had lower odds than girls (OR = 0.8, 95% CI: 0.7 - 0.9); AI/AN had lower odds than Whites (OR = 0.6, 95% CI: 0.4 - 1.0); and those who self-pay for medical care had lower odds than those with private insurance (OR = 0.8, 95% CI: 0.7 – 0.9) to have initiated the HPV vaccine series. (Table 4)
Table 4.
Patient Ages 11-17 and Clinician Characteristics Associated with Uptake of the HPV Vaccine, by HPV Vaccination Uptake, UCD Health Primary Care Network, January 1, 2017 – June 30, 2018
| ≥ 1 dose (n=10,423)a | UTD (n= 6,560)b | |||
|---|---|---|---|---|
| Odds Ratio (95% CI) |
P-Value | Odds Ratio (95% CI) |
P-Value | |
| Patient Demographics | ||||
| Gender | ||||
| Boy | 0.8 (0.7 – 0.9) | <0.001 | 0.7 (0.7 – 0.8) | <0.001 |
| Girl | Ref. | |||
| Race/Ethnicity | ||||
| White | Ref. | Ref. | ||
| Black | 1.2 (0.9-1.5) | 0.1 | 0.8 (0.6 – 1.0) | 0.030 |
| AI/AN | 0.6 (0.4-1.0) | 0.042 | 0.5 (0.3 – 0.9) | 0.019 |
| AANHPI | 1.2 (1.0 – 1.4) | 0.020 | 1.1 (0.9 – 1.2) | 0.4 |
| Hispanic | 1.0 (0.9 – 1.2) | 0.7 | 1.1 (1.0-1.3) | 0.1 |
| Unknown | 1.0 (0.8 – 1.2) | 0.9 | 0.9 (0.7 – 1.1) | 0.2 |
| Language | ||||
| English | Ref. | Ref. | ||
| Other | 0.8 (0.6 – 1.2) | 0.3 | 0.9 (0.6 – 1.3) | 0.5 |
| Insurance Type | ||||
| Private | Ref. | Ref. | ||
| Public | 0.9 (0.7 – 1.2) | 0.6 | 0.9 (0.6 – 1.2) | 0.5 |
| Self-Pay | 0.8 (0.7 – 0.9) | 0.002 | 1.1 (0.9 – 1.3) | 0.3 |
| Age | 1.2 (1.2 – 1.2) | <0.001 | 1.4 (1.3 – 1.4) | <0.001 |
| Patient Health Care Utilization | ||||
| Medical Visits | ||||
| 1 | Ref. | Ref. | ||
| 2 | 1.2 (1.1 – 1.4) | 0.003 | 1.6 (1.3 – 1.8) | <0.001 |
| 3 | 1.4 (1.2 – 1.6) | <0.001 | 1.5 (1.3 – 1.8) | <0.001 |
| 4 | 1.6 (1.3 – 1.9) | <0.001 | 1.7 (1.4 – 2.1) | <0.001 |
| ≥ 5 | 1.4 (1.2 – 1.6) | <0.001 | 1.9 (1.6 – 2.2) | <0.001 |
| Vaccines | ||||
| Tdap | 2.5 (2.0 – 3.1) | <0.001 | 2.8 (2.1 – 3.9) | <0.001 |
| MenACWY | 8.1 (6.8 – 9.8) | <0.001 | 1.6 (1.2 – 2.1) | 0.002 |
| Influenza | 2.7 (2.4 – 3.0) | <0.001 | 1.9 (1.6 – 2.2) | <0.001 |
| Primary Care Clinician | ||||
| Specialty | ||||
| Pediatrics | Ref. | Ref. | ||
| Family | 1.0 (0.7 – 1.4) | 0.9 | 0.8 (0.6 – 1.0) | 0.019 |
| Appointment Type | ||||
| Faculty | Ref. | Ref. | ||
| Community based | 0.6 (0.3 – 1.2) | 0.1 | 1.0 (0.6 – 1.5) | 0.8 |
| In-training | 1.1 (0.6 – 2.0) | 0.8 | 1.0 (0.6 – 1.7) | 0.9 |
| Gender | ||||
| Female | Ref. | Ref. | ||
| Male | 1.0 (0.8 – 1.3) | 1.0 | 0.9 (0.8 – 1.1) | 0.5 |
| Years in practice | 1.0 (1.0 – 1.0) | 0.8 | 1.0 (1.0 – 1.0) | 0.8 |
- Clinic = 0.14; S.E. = 0.10
- Provider = 0.29; S.E. = 0.07
- Clinic = 0.03; S.E. = 0.02
- Provider = 0.06; S.E. = 0.03
Odds ratios are adjusted for all tabulated variables using logistic regression mixed effects models.
Abbreviations: AANHPI = Asian American, Native Hawaiian, and Pacific Islanders; AI/AN = American Indian/Alaskan Native; Tdap = Tetanus, diphtheria, & pertussis; MenACWY = Meningococcal group A, C, W-135, & Y
HPV Up to Date
Among adolescent patients aged 11-17 years, characteristics independently associated with higher odds of being up to date with the HPV vaccine series included: Being older (OR = 1.4, 95% CI: 1.3 – 1.4); patients with 2 or more medical visits compared to patients with only 1 visit (2 visits OR = 1.6, 95% CI: 1.3-1.8; 3 visits OR = 1.5, 95% CI: 1.3 - 1.8; 4 visits OR = 1.7, 95% CI: 1.4 - 2.1; 5 or more visits OR = 1.9, 95% CI: 1.6 - 2.2); patients who received the Tdap (OR = 2.8, 95% CI: 2.1 - 3.9), MenACWY (OR = 1.6, 95% CI: 1.2 – 2.1) and influenza vaccines (OR = 1.9, 95% CI: 1.6 – 2.2) compared to those who did not receive these vaccines. Boys had lower odds than girls (OR = 0.7, 95% CI: 0.7 - 0.8) and AA/Blacks (OR = 0.8, 95% CI: 0.6 – 1.0) and AI/ANs (OR = 0.5, 95% CI: 0.3 - 0.9) had lower odds than Whites to be up to date with HPV vaccine. Patients whose primary care clinician specialized in family practice had lower odds of being up to date with the HPV vaccine series compared to patients whose primary care clinician specialized in pediatrics (OR = 0.8, 95% CI: 0.6 – 1.0). (Table 4)
Discussion
In this racially and ethnically diverse population of 11-17-year-old girls and boys we found lower HPV vaccine uptake (≥1 = 63.0%; HPV UTD = 37.7%) compared to national estimates as well as differences in uptake by patient gender, race/ethnicity, age, health care utilization and clinician specialty. These findings provide information that support the need to develop locally tailored multilevel evidence-based strategies to increase HPV vaccine uptake by identifying sub-groups to target for interventions and improving patient-provider communication approaches.
The most recent NIS-Teen survey reported that racial/ethnic male and female adolescents have higher rates of initiating and being up to date with the HPV vaccine series compared to White adolescents [8]. Interestingly, compared to White adolescents, our study found lower odds of initiating and being up to date with the HPV vaccine series among AI/AN adolescents; lower odds of being up to date with the HPV vaccine series among AA/Black adolescents; and higher odds of initiating the HPV vaccine series among Asian adolescents. Our results are consistent with smaller, more localized studies that have reported that Black/AA adolescents were significantly less likely to complete the vaccination series than White adolescents [23-25]. Historical mistrust in the health care system [26-27] coupled with lower HPV awareness and knowledge among AA/Black [28] and AI/AN [29] may contribute to greater HPV vaccine hesitancy in these two communities resulting in lower HPV uptake. McRee et al., reported that perceptions of hesitancy may discourage providers from routinely recommending the HPV vaccine [30] and our prior qualitative study, is aligned with this hypothesis which revealed that primary care team members would often postpone administering the HPV vaccine when confronted by vaccine hesitant parents. This is alarming since both AI/AN [31] and AA/Black women [32] have higher cervical cancer incidence and mortality compared to white women and AA/Black adolescents have a higher HPV prevalence than other racial/ethnic groups [33]. More research is needed to examine factors associated with racial/ethnic differences in HPV vaccine hesitancy and its effects on patient-provider communication, as the provider’s HPV recommendation is one of the strongest predictors of HPV vaccine uptake [34].
One possible explanation for the higher odds of initiating the HPV vaccine series among Asian adolescent could be the result of a decades-long effort to mitigate the significant disparities in cervical cancer incidence and mortality among Asian American women [35]. Asian language media campaigns, lay health worker interventions and targeted efforts have not only drastically improved cervical cancer rates among Asian American women but have also created greater awareness in this community regarding the devasting effects of cervical cancer [36]. The Sacramento region where the PCN’s are located have benefited from numerous grassroots, community, and academic efforts to increase awareness of cervical cancer and access to Pap testing in the Asian American community [37-38]. More research is needed to explore the underlying mechanisms contributing to the higher odds of initiating the HPV vaccine among Asian adolescents, and whether these factors can be utilized to improve HPV vaccine uptake in other racial/ethnic communities. These findings underscore the importance of developing culturally tailored education and communication interventions to ensure disparate populations like AI/AN and AA/Blacks are initiating and completing the HPV vaccine series.
Our study also found gender differences in HPV vaccine uptake. Boys had a 20% lower odds of initiating the HPV vaccine series and a 30% lower odds of being HPV UTD. This finding is consistent with parent surveys reporting that their sons had not received the HPV vaccine [39-40]. Gender differences in HPV vaccine uptake may be attributable to the initial different ACIP recommendations for boys and girls [41], and the stronger recommendation for routine recommendation for females [42]. These findings support results from our prior qualitative study in which parents expressed a lack of knowledge about HPV-related cancers that can affect boys, with one interviewee not aware that the vaccine was even available for boys. This is concerning since nearly four out of ten cases of cancer caused by HPV occur among men [43] and recent studies have found gender differences in the prevalence of genital HPV with males having higher rates compared to females [44-45]. Parent education and provider communication strategies need to emphasize the importance of vaccinating both boys and girls because the burden of HPV-associated cancers are increasing in men [46].
The strongest predictor of receiving the HPV vaccine was receiving a MenACWY vaccine. Among those who received the MenACWY vaccine, the odds of initiating the HPV vaccine series were approximately 8.1 times higher compared to those who did not receive the MenACWY vaccine. This is similar to a study conducted by Kepka et al., that reported receipt of other vaccines as the strongest predictor of the likelihood of HPV vaccine initiation and completion [47]. Our finding provides empirical evidence that support the widely accepted strategy of “bundling” all vaccines in the adolescent platform [48] and underscores missed clinic opportunities for HPV vaccination. The uptake rates for the other vaccines in the adolescent platform are much higher than the rates for the HPV vaccine (influenza vaccine, 70.3%; MenACWY vaccine, 82.0%; and Tdap, 87.6%). HPV vaccines can be safely co-administered with other routine recommended vaccines, and the ACIP recommends administering all age-appropriate vaccines during a single visit [49]. Clinicians of this PCN have reported utilizing bundling techniques to introduce the HPV vaccine to families and commented on the administrative ease of ordering the vaccine for their patients [18]. This includes PCN policies that outlines the use of standing orders and EHS provider reminder prompts. More research is needed to examine how provider communication strategies can effectively incorporate the messaging of bundling the HPV vaccine with others and to explore how clinic level factors such as recall and reminder systems, standing orders and the role of the primary care team relate to missed opportunities for vaccination.
While clinician characteristics such as gender, years in practice and clinician type were not associated with HPV vaccine uptake, clinician specialty was. Adolescent patients who had a primary care clinician who specialized in family practice had a 20% lower odds of being up to date with the HPV vaccine series compared to adolescent patients with pediatricians. Other studies have also reported that patients of pediatricians are more likely to be vaccinated than those of other specialties [50-51]. Interventions to increase HPV vaccine uptake should include targeting clinicians beyond pediatricians.
Although HPV vaccination is recommended for boys and girls at 11 or 12 years of age, like other studies we found that older adolescents had higher odds of initiating and be up to date with the HPV vaccine series [52]. This is in line with the literature that suggest that clinicians are more likely to recommend the HPV vaccine strongly to older adolescents [53], despite PCN policies that allow patients to start the HPV vaccine series as early as 9 years of age. This preference to vaccinate older adolescents compared to younger adolescents is concerning because younger adolescents have a stronger immune response to the HPV vaccine than older adolescents [54], they require fewer doses (two compared to three) and the HPV vaccination is meant to be administered prior to possible exposure, the onset of sexual activity. Interventions to increase HPV vaccine uptake should emphasize the importance of on time and early vaccinations.
Limitations
Several study limitations should be considered when interpreting the findings. First, there is potential for misclassified data in the EHR. HPV vaccinations may be administered outside of the PCN such as in school or pharmacies and not entered into the PCN EHR. Misclassification can occur if this information is not reported by the patient/parent. However, since the vaccine is covered by health plans accepted by the PCN and the California Immunization Registry (CAIR) data is reflected in the EHR, the impact of misclassification is likely low. Additionally, our population while racially and ethnically diverse, most were privately insured, and all were drawn from a single health system. Our findings may not be generalizable to Medicaid, uninsured or underinsured populations; and to other populations with varying sociodemographic characteristics. Finally, although our analysis utilized EHS and administrative data and controlled for patient, clinician and visit characteristics, we did not have access to data on other potential patient, clinician and visit characteristics that may influence initiation and completion of the HPV vaccine series. Future research should include additional measurements at the patient-, clinician- and practice-level determinants.
Strengths
Despite limitations, our study is one of the largest to utilize electronic health records to examine factors related to initiating and being up to date with the HPV vaccine series for both adolescent girls and boys. As such, the study is not subject to self-report/recall biases of other HPV vaccination research [16, 55]. Additionally, our study allowed for simultaneous assessment of primary care clinician factors as well as health utilization data such as receipt of Tdap and MenACWY for the same cohort of patients, which have been limitations of prior research.
Conclusion
Over an 18-month period, less than half of adolescents of a primary care network were up to date with the HPV vaccine series. We found racial/ethnic as well as gender disparities in HPV vaccine initiation and being up to date with the vaccine series. Further, HPV vaccine uptake varied by clinician specialty, patient age, other adolescent vaccines received and number of patient medical visits. The findings emphasize the need for developing culturally tailored multilevel evidence-based interventions to enhance clinician-patient HPV communication and reduce missed clinic opportunities for vaccination. More research is needed to understand the influence of patient/parent-, primary care team-, and clinic level factors on uptake of the HPV vaccine in different patient sub-groups.
Acknowledgement
We thank-you to Drs. Joan R. Bloom and Mahasin S. Mujahid for their review of drafts of this article. We would also like to thank Duke LeTran for preparing the data.
Funding
This work was supported by the National Cancer Institute [P30 CA093373 and U54153499].
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