Human papillomavirus (HPV) is the most common sexually transmitted viral infection in the United States.1 There are approximately 79 million infected individuals in the United States, with 14 million new infections each year in individuals ages 15 to 59 (of which approximately 50% are ages 15 to 24).1 Transmission of this virus increases as the number of sexual partners and incidents of unprotected intercourse increase.2 Generally, HPV infections clear without treatment in 1 to 2 years; however, persistent HPV can lead to precancerous lesions or cancer.2 Untreated patients can spread the infection to other nonimmunized individuals.
When evaluating the most common HPV-related cancers by gender, women and men were diagnosed with an average of 17,000 and 9,000 HPV-related cancers each year in the United States, respectively.3 The incidence of HPV-related cervical cancer in women in the United States is higher among Black, Hispanic, and American Indian populations; the incidence of HPV-related vulvar cancers is more prevalent in White Americans, and the incidence of HPV-related vaginal cancers is more common in Black Americans.3 The incidence of HPV-related oropharyngeal cancers has risen across both genders and most ethnic groups (except for Black Americans) and is found much more frequently among males.3
Along with the physical and emotional costs of HPV and the increased risk of cancer, there are financial costs as well. The cost of treating, screening, and preventing HPV-related cancers is approximately $8 billion dollars annually in the United States.4 Of that $8 billion, $6.6 billion is spent on cervical cancer screening and follow-ups, and $1 billion is spent on HPV-related cancers (predominantly cervical and oropharyngeal).4
The HPV vaccine can reduce HPV transmission and decrease subsequent HPV-related cancers. Reducing the total number of sexual partners and occurrences of unprotected intercourse also reduces spread of HPV.2 Over the course of the next 70 years, if the HPV vaccination program stays in effect, it is estimated that the human papillomavirus 9-valent vaccine, recombinant (9vHPV) could prevent 690,000 HPV-related cancers and 222,000 associated deaths, assuming no cross protection from the vaccine.5 Cross protection for HPV means that immunization with a specific vaccine type provides clinically significant protection against infection due to another HPV type.
These estimates do not include the reduction in anogenital warts or the potential savings from a decrease in testing and treatment. The HPV vaccine three-dose series is administered with the second dose given 1 to 2 months after the first dose and the third dose given 6 months after the initial injection.6 According to Healthy People 2020, only 6.9% of males ages 13 to 15 in the United States received at least three doses of HPV vaccine in 2012, with the target being 80%.7
In October 2011, the Advisory Committee on Immunization Practices (ACIP) updated their HPV immunization recommendations to state that the quadrivalent HPV (types 6,11,16, and 18) vaccine would be recommended for both males and females ages 9 through 26. Previously, the HPV vaccine was recommended for females and permissively allowed for males.6 Since the 2011 revision, HPV vaccination rates have gradually increased among females (from 53.8% in 2012 to 57.3% in 2013) and males (from 20.8% in 2012 to 34.6% in 2013).8
Vaccination for HPV is more efficacious when administered prior to any HPV exposure.1 Although the HPV vaccination rate is improving, the rate of increase is slow, and a distinct gender gap remains in HPV vaccination rates. In March 2015, the ACIP updated their recommendations to include the 9vHPV, which provides protection against five additional strains of HPV in comparison with the quadrivalent vaccine; the additional five strains covered in the 9vHPV account for 15% of all cervical cancers.9
In October 2016, after this quality improvement project was completed, the ACIP updated the schedule for HPV vaccination. The newest recommendation for the 9vHPV is for a two-dose schedule given 6 months apart for males and females who begin the vaccination series at ages 9 through 14. HPV vaccination initiation after age 15 will remain on a three-dose schedule.10 More information is needed to assess potential strategies for improving HPV vaccination rates in males ages 11 to 18 to help decrease the physical, emotional, and financial cost of HPV and preventable HPV-related cancers. This information can be useful not only to eliminate gender disparity but also to guide primary care providers (PCPs) in their approach when recommending the HPV vaccine to parents/guardians and their male children.
The Health Belief Model (HBM), combined with self-efficacy, was used to construct the intervention for someone considering whether or not to immunize. Lewin's Change Theory was also incorporated in the quality improvement project framework because the providers were dealing with a change by utilizing a reminder system. The core assumptions of the HBM applied to this quality improvement project were first to capitalize on the parents'/guardians' desires to avoid potential adverse outcomes or illnesses for their male children. Secondly, parents/guardians are self-actualized through education and begin to understand that the recommended preventive measure will prevent adverse reactions or illnesses and that the benefits of performing the preventive measure are greater than the barriers to participating in it.11,12
Each of the core components of the HBM were considered in relation to HPV vaccination uptake among males ages 11 to 18. Modifying variables of the HBM in relation to HPV vaccination might include age, gender, socioeconomic status, knowledge, and personality. Individual perceptions regarding HPV vaccination might include perceived susceptibility and perceived seriousness. Perceived susceptibility of their male children over time was highlighted for each parent/guardian and served to increase perception of HPV risk, genital warts, or even HPV-related cancer. Highlighting each male child's susceptibility served to avoid the mistaken notion of some parents/guardians that their male children should not receive the vaccine due to a lack of current sexual activity.
Perceived seriousness was increased for many parents/guardians when a trusted provider took time to educate them on HPV and then offer the vaccine. The level of concern regarding HPV, genital warts, or HPV-related cancer became foremost in the parents'/guardians' minds when leaving the office. The likelihood of action, in this case receiving the HPV vaccine, was dependent upon the overall perceived benefits outweighing the perceived barriers. Perceived benefits to receiving the HPV vaccine include reduced risk for developing HPV-related cancers and reduced risk for genital and oropharyngeal warts caused by HPV. Self-efficacy can be enhanced simply by educating the parents/guardians and instilling confidence that they are making the correct decision for their children.13
Lewin's Change Theory was incorporated into the project to encourage PCPs and staff to adopt the new HPV protocol for identifying and educating families. This theory consists of three steps: unfreezing, movement, and refreezing.14 It can be an important tool for organizations using evidence-based practice demonstration projects in clinical settings.15
Several studies in the literature address improving vaccination rates, specifically HPV vaccine administration rates. One study looked at using an HBM intervention in college-aged males to positively impact HPV vaccination rates.16 The study compared traditional knowledge-based intervention to HBM intervention with the HBM, showing a higher rate of efficacy in HPV vaccination initiation and completion.16
A survey given to parents/guardians of vaccination-aged males detailed the top five reasons for not vaccinating their male children for HPV:
- They did not realize the vaccine was recommended.
- They did not feel the vaccine was necessary.
- They recognized they had a lack of knowledge.
- They thought that because their male children were not sexually active, it was not needed.
- They did not believe in the vaccination's safety.8
Data from the 2007-2013 National Immunization Survey-Teen reported that one-third of parents/guardians of females and half of parents/guardians of males stated that their PCP had not recommended that their child receive the HPV vaccine.8 A statewide sample (N = 575) of Minnesota PCPs (20% pediatricians, 47% family medicine physicians, and 33% NPs) were surveyed regarding HPV vaccination behaviors, and 76% of PCPs reported routinely recommending the HPV vaccine for females ages 11 to 12; however, only 46% did so for males.17
It is important that barriers (both real and perceived) are addressed in order to increase the vaccination rate. In North Carolina, the HPV vaccination rates in both uninsured and publicly insured children remained low despite having full coverage through age 18 via the state vaccine program.18 Differences in vaccination rates for males were geographically determined, and HPV vaccination rates among males were similar to that of their neighbors, especially in rural areas.18
One study evaluated decision-making support influence. The large study used a randomized control trial methodology (N = 22,486 females ages 11 to 19) due for an HPV vaccine dose (first, second, or third in the series) and evaluated whether the most effective mode of decision support came from family-focused support, clinician-focused support, both family- and clinician-focused support, or no intervention/support.19 The results showed that clinician-focused decision support improved initial HPV vaccination, and family-focused decision support improved HPV series completion; however, the model combining family- and clinician-focused support showed the most effective rates of HPV series completion. Communication with both those receiving the vaccine and their parents/guardians has been shown to achieve a higher HPV vaccination rate.19
A qualitative study (N = 609) surveyed family practice physicians and pediatricians to determine possible perceived and real barriers to HPV vaccination.20 The ranked order from greatest barrier to vaccination to least was cost of vaccine, perceived parental attitude toward vaccine, decreased office visits in the adolescent age group, and lower recommendation rates in rural practice.20 According to Allison and colleagues, PCPs who reported recommending HPV vaccination for 11- to 12-year-old males were more likely to be from urban locations, believed that the HPV vaccine was efficacious, had a concern regarding the severity of HPV-related illnesses, and routinely discussed sexual health with 11- to 12-year-olds.20
Another qualitative study (sponsored by Merck & Co., Inc.) sent out an Internet survey to parents/guardians of males ages 11 to 17 assessing HPV vaccine knowledge, attitudes, and behaviors.21 Parents/guardians indicated that the largest barrier to HPV vaccination for their male children was their PCP not recommending the vaccine.21 This study is limited, as it only included parents/guardians with Internet access and was not a nationally representative sample.21
Common reasons for HPV vaccine acceptance among rural males included recommendation from PCPs; education regarding vaccine importance, safety, and efficacy; and vaccine availability. The President's Cancer Panel Annual Report 2012-2013, released in February 2014, identified three urgent goals: reducing or eliminating missed clinical opportunities for HPV vaccination or recommendation; increasing HPV vaccine acceptance among parents/guardians, caregivers, and adolescents; and increasing access to HPV vaccination services.22
Prior to beginning the quality improvement project, a review of HPV vaccination rates in the clinic's target population (males ages 11 to 18) was conducted. The vaccination rate at this rural clinic was comparable to regional rural clinics with a rate of over 64% not having received a single dose of HPV vaccine. The study facility did not have a human subject review board; therefore, the institutional review board's permission was obtained from the University of Alabama, and those protocols followed.
The primary focus of the intervention is for HPV information to be provided to the parents/guardians and their male children as well as for providers to recommend the HPV vaccine and answer questions regarding the vaccine. The proposed plan of action was then presented to all staff who would be involved in the project intervention. The first step was identification of the target population, which took place at the front desk upon check-in. Once a patient was identified as the appropriate age and gender for intervention, his chart was flagged for easy identification by the nursing staff and PCP. When the nurse brought the patient from the waiting room to the exam room, the patient and the parent/guardian received HPV vaccination information in the form of easy-to-read brochures with pictures to review prior to the provider entering the room.
The nurses then accessed and printed the vaccine record from the electronic medical record and the North Carolina Immunization Registry and placed them on the chart. The PCPs (comprised of two family practice physicians and four family NPs) noted the flagged chart and the immunization record, provided HPV vaccination education and recommendation of vaccine, and answered questions regarding vaccination regardless of the nature of the visit.
At this point, the patient, along with the parent/guardian, made a decision whether or not to vaccinate for HPV or to plan future vaccination. In accordance with Lewin's Change Theory, the unfreezing step consisted of the PCP's willingness to change by recognizing the purpose of the flagged chart to initiate education with the patient; the front office staff's willingness to participate by placing flags or reminder tools on charts of all males ages 11 to 18 who have an appointment; and the office manager's willingness to allow these changes to take place.
The movement component consists of the actual recognition of the reminder flags or tools to initiate education, the actual placement of the reminder tool, and the allowance and encouragement of such practice. The refreezing component consists of making this standard practice so it is readily identifiable and encourages the desired behavior: initiation of an HPV vaccination conversation between provider, patient, and parent/guardian.
The HPV vaccination rate was then measured again during the 3-month intervention period and compared with the HPV vaccination rate the 3 months prior to the intervention. An independent t-test was used to analyze the data, and statistical analysis was performed using Statistical Package for the Social Sciences, version 22.0. A brief, anonymous survey was given to consenting parents/guardians at the end of the visit to share why they did or did not vaccinate their male children for HPV.
There were 226 participants who received no additional HPV vaccination education and 191 participants who received additional HPV vaccination education. In the 3 months prior to the intervention (N = 226), 35.84% had received at least one HPV injection, and 15.02% had received the complete HPV series. In the 3 months during the intervention (N = 191), 38.22% had received at least one HPV injection, and 17.28% had received the complete HPV series. This would include those males who started the vaccine series prior to intervention (some even several years prior), but for various reasons, had not continued the vaccine series until seeing their PCP again.
An independent-samples t-test was calculated to determine if there were differences in vaccination rates between those who received HPV vaccination education and those who did not (P = 0.530). Vaccination rates for those receiving additional HPV vaccination education and those who did not were normally distributed, as assessed by visual inspection of normal Q-Q plots. There was homogeneity of variances, as assessed by Levene's test for equality of variances (P = 0.448).
The HPV vaccination rate was greater in those receiving additional HPV vaccination education (X = 0.83, standard deviation [SD] = 1.176) than those who did not (X = 0.76, SD = 1.137); however, it was not a statistically significant difference (P = 0.530). A chi-square test was used to examine the differences between those who completed the series before (15%) and after intervention (17%). While this was an increase, it was not a significant chi-square (degrees of freedom = 1 = 0.593, Cramer's V = 0.030). However, the increase in HPV vaccinations is encouraging and did trend toward significance. It is also promising that there was an increase in the number of patients who completed the series.
According the parental survey (N = 37), there were various reasons for choosing whether or not to vaccinate their male children (see Parental survey: Reasons for allowing or disallowing the HPV vaccine). The most common reason for HPV vaccination acceptance was “to protect my child from cancer/HPV,” and the most common reason for refusing HPV vaccination was “I do not want his arm to be sore for sports/activities.”
Although there was slight improvement in vaccination rates with the intervention, the improvement was not statistically significant. This can partly be explained due to the study's timing. The first group (with no additional HPV vaccination information provided) was evaluated from July through October, which is a common time to come in for well-physical exams and sports physicals, and is generally a more accepted time to receive vaccinations.
The intervention time was late October through late January, which is a time when fewer well exams are performed and visits consist of predominately sick visits; in addition, many sports-related activities take place during this time. Being active in sports/activities was a common reason for denying the vaccine due to fear of arm soreness or weakness as well as being too sick to receive the vaccine. Therefore, it is thought that the intervention vaccination rates may be artificially low due to timing and short duration of the intervention period, requiring evaluation for a longer duration.
Surveyed parental attitudes are similar to those of previous studies mentioned in that the provider recommendation is one of the top reasons for vaccination, with concerns regarding safety and necessity being reasons for not vaccinating. However, the HPV vaccine is a difficult one for parents/guardians to follow through with, and in rural areas, many parents/guardians will “wait and see” what their community members are doing prior to acting.18 It is probable that the intervention, although not statistically significant, does show clinical significance.
The importance of HPV vaccination has opened the door for discussions regarding sexual activity in teens and other available vaccines for this age group (tetanus, diphtheria, and pertussis; hepatitis A; meningococcal), so this study still has value.
Researchers are still exploring which avenues are most effective in increasing HPV vaccine rates among young males ages 11 to 18, especially in areas of rural practice. Further studies are needed to determine specific ethnic disparities regarding HPV vaccination. Multi-focused strategies have been identified as being the most effective because they include the patient, parent/guardian, and PCP working together for improved care. In order for HPV vaccination rates to improve, the PCP should recommend vaccination.
Vaccination for HPV prior to exposure has been shown to improve immunity to HPV. Vaccination education for HPV should be provided to all young males ages 11 to 18 and their parents/guardians, regardless of the reason for the visit, to capitalize on clinical opportunities for HPV vaccination. PCPs need to also recognize the value and guidance provided by midrange theories, such as HBM, self-efficacy, and Change Theory when planning evidence-based quality improving interventions.
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