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Pediatric Infectious Disease Journal:
Supplement Article

Challenges to Vaccinating Adolescents: Vaccine Implementation Issues

Humiston, Sharon G. MD, MPH*; Rosenthal, Susan L. PhD†

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From the *Department of Emergency Medicine and Pediatrics, University of Rochester Medical Center, Rochester, NY; and the †Department of Pediatrics, Sealy Center for Vaccine Development, University of Texas Medical Branch at Galveston, Division of Adolescent and Behavioral Health, Children's Hospital, Galveston, TX

Address for correspondence: Sharon G. Humiston, MD, MPH, Department of Emergency Medicine, Box 655, 601 Elmwood Avenue, Rochester, NY 14642. Fax 585-473-3516; E-mail sharon_humiston@urmc.rochester.edu.

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Abstract

Background: Adolescent immunization is a growing field, with many new vaccines in development and new or expanded immunization recommendations on the horizon.

Methods: Characteristics of adolescents and their health care are discussed, focusing specifically on the challenges of incorporating a potential recommendation to replace tetanus-diphtheria toxoid with tetanus-diphtheria-acellular pertussis vaccine during early or middle adolescence as part of routine preventive care. Using the framework created by the Centers for Disease Control and Prevention's Task Force on Community Preventive Services, three overlapping levels at which there are opportunities for vaccine intervention are reviewed: (1) health care systems (enhancing access to vaccination services); (2) health care providers (provider-based interventions); and (3) patients and families (“increasing community demand”).

Results: There are several barriers to vaccine implementation that make achieving high immunization coverage rates among adolescents a challenge. Promising interventions for improving vaccination rates at the health care system level include reducing out-of-pocket costs, expanding access to immunizations, and implementing vaccination programs in schools. Provider-based interventions for improving vaccination rates include regular assessments of immunization rate with feedback to all office personnel, provider reminders, and standing orders. Client recall and reminders, education, and requirements for school entry can assist in “increasing community demand” for vaccinations in that they motivate parents and adolescents to follow through with immunizations.

Conclusions: Adolescents are unique from other populations. Previously studied interventions need to be tested in this age group as immunization becomes a more salient issue in adolescent health care.

Adolescent immunization is a growing field, with many new vaccines in various stages of development and new or expanded immunization recommendations for existing vaccines on the horizon. For example, vaccines against herpes simplex virus and human papillomavirus (HPV) may be licensed in the United States in the foreseeable future,1 and newly expanded recommendations for vaccination against meningococcus2 and influenza could increase the number of adolescents protected from these diseases. An immunization combining acellular pertussis vaccine with age-appropriate doses of tetanus and diphtheria toxoids (Tdap) has been licensed for use in the United States, and interest is high because of the rise in the incidence of reported pertussis (Fig. 1). 3–8 If licensure of this Tdap booster is accompanied by new routine immunization recommendations for adolescents, this population may be protected from pertussis for the first time. Additionally, it is conjectured that the number of young infants dying from pertussis may decrease, because adolescents often serve as a reservoir of infection within the community.9

Figure 1
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Undoubtedly, there will be challenges to the delivery of new vaccines to adolescents just as there are challenges to vaccinating this population today. These challenges will vary by the vaccine and the specifics of the recommendations. In this article, characteristics of adolescents and their health care that may create challenges to high immunization coverage rates among this age group will be discussed. Using the framework created by the Centers for Disease Control and Prevention's (CDC's) Task Force on Community Preventive Services, three overlapping levels at which there are opportunities for vaccine intervention will be reviewed: (1) health care systems (enhancing access to vaccination services); (2) health care providers (provider-based interventions); and (3) patients and families (“increasing community demand”). Challenges to potential recommendations to replace tetanus-diphtheria toxoid (Td) with Tdap during early or middle adolescence as part of routine preventive care will be discussed throughout the article.

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CHARACTERISTICS OF ADOLESCENTS AND THEIR HEALTH CARE

Characteristics of Adolescents

Adolescence is the transitional period between childhood and adulthood and is a time when young people develop the skills that allow them to lead responsible adult lives, including taking charge of their own health care. Adolescents have growing abilities to use sophisticated decision-making skills and abstract reasoning. Although they may not always be able to use them in every situation, by age 14, adolescents have been shown to have decision-making skills similar to those of adults.10 In certain situations, adolescents may consult “experts” when seeking advice for making a decision. For example, adolescents may seek peer advice about music and clothing, but they may seek parents’ opinions regarding health care decisions such as vaccination,11 even when the adolescent can legally self-consent.12,13 From the parental perspective, parents often expect to be involved in decisions about vaccination for their adolescent,14 and for multidose vaccines, parents may even want to consent for the administration of each dose.15 With regard to vaccines for sexually transmitted diseases, a study demonstrated that some parents prefer to have their adolescents make this decision independently once they are 18 years old.14

The approach parents and health care providers must use with adolescents varies based on the adolescent's age and developmental stage. Adolescence is typically divided into three phases: early, middle, and late (Table 1). Each of these phases is associated with distinct characteristics that may have implications for an adolescent's role in a vaccination decision. Early adolescence represents the transition out of childhood, and these young persons may well be in the concrete operational stage of thinking. They may have limited abilities to use hypothetical reasoning and to imagine situations or risks that they have not yet encountered. The parent and health care provider may need to describe the need for a vaccine in concrete terms and relate it to something with which the adolescent has had experience. Middle adolescence is what is typically thought of when the word “adolescent” is used (ie, the stereotypical teenager). At this age, adolescents become increasingly preoccupied with their peer group, although not to the exclusion of maintaining close ties with their parents. Vaccines that are recommended for all adolescents may be the most easily accepted, because adolescents will be reassured that they are similar to their peers.11 In addition, to prepare the middle adolescent for greater responsibilities in decision-making, it may be helpful if parents and health care providers model how they weigh the risks and benefits in deciding whether to accept a vaccine. This will help prepare the adolescent for the late adolescence period during which they will transition into adult roles and have the legal right to make their own decisions.

Table 1
Table 1
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Health Care Needs of Adolescents

Although many groups, such as the American Academy of Pediatrics, American Academy of Family Physicians, Society for Adolescent Medicine, American Medical Association's Guidelines for Adolescent Preventive Services, and the U.S. Preventive Services Task Force recommend frequent adolescent preventive visits, the lifetime nadir for number of medical visits per person occurs during the ages of 15–24 for both males and females (Fig. 2). 16 Because adolescents who present in physicians’ offices often do so for sports physicals, acute care, and other visit types not usually associated with vaccination, it may be important to use these opportunities for vaccination. Studies are now being conducted at the Rochester Center for Adolescent Immunization in New York to examine current patterns of health care utilization for adolescents and young adults, including the provider type (eg, pediatrician or family physician), the visit type (eg, well or acute care), the extent of scattering of care, and the location where adolescents receive vaccines.

Figure 2
Figure 2
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Although the timing of vaccinations arguably drives much of the well-child care schedule in infancy, it is not known if vaccination could bring adolescents into the physician's office in the absence of school requirements. Establishing the degree to which multiple-dose vaccines can be administered on a flexible schedule may be an important factor for increasing adolescent vaccination with certain vaccines.17

Another relevant health care issue for adolescent vaccination programs is consent. Ideally, the health care provider should obtain dual consent/assent from both the parent and the adolescent. Obtaining parental consent can be difficult if vaccinations are provided in settings where the adolescent is unaccompanied by parents (eg, school-based vaccination program or late-adolescent visit to which the adolescent arrives alone). Most adolescents will seek parental guidance regarding vaccinations, but the parental signed consent form may not be on hand when the patient is in the office.18 Some adolescents may want to be vaccinated without parental involvement, particularly for vaccines that protect against sexually transmitted infections, although some states no longer permit this level of confidentiality.19 Some states allow adolescents to self-consent for the hepatitis B vaccine as part of their right to receive confidential sexual health services.20 To add to the complexity of the issue, there may be instances in which the parent would like their adolescent to be vaccinated, but the adolescent does not assent.

In the past, age-related vaccination recommendations have been more effective than risk-related vaccinations. Risk-related recommendations often do not work, because people may not choose to be identified with the target group or may not conceptualize themselves as belonging to the targeted group. If, after a considerable time, they do seek preventive services because of risk-related behavior, they may have been exposed already. For example, early U.S. recommendations for the hepatitis B vaccine targeted only persons in those groups most likely to be infected (eg, homosexual males and heterosexuals with more than one partner in a 6-month period) and were, thus, ineffective.21,22 Age-based recommendations are less socially stigmatizing and are easier to implement, especially for physicians’ offices that use patient or provider reminders (as described below).

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POTENTIAL BARRIERS AND PROMISING INTERVENTIONS FOR VACCINATION

In the late 1990s, the CDC created the Task Force on Community Preventive Services, a group of independent topic experts and epidemiologists. The Task Force conducted systematic reviews23 of 17 interventions designed to raise vaccination coverage levels in children, adolescents, and adults.24,25 Their recommendations emphasize three overlapping levels at which there are opportunities for vaccine intervention: (1) health care systems; (2) health care providers; and (3) patients and families (Table 2).

Table 2
Table 2
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Their recommendations were made on “strong” or “sufficient” evidence of effectiveness; interventions that were not well-studied or not effective in studies were not recommended. The Task Force's framework will be used to review potential barriers and promising interventions for vaccination of adolescents.

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Enhancing Access to Vaccination Services
Reducing Out-of-Pocket Costs.

Financing may be the single most important potential barrier for all adolescent immunizations. Strong evidence was found by the Task Force to recommend reducing out-of-pocket vaccination costs,25 that is to say, providing insurance for, reducing copayments associated with, or offering free vaccinations. In a national survey of pediatricians and family physicians, those who did not routinely immunize adolescents often cited insufficient insurance coverage for immunizations as the barrier.26 A review by the National Vaccine Advisory Committee to assess progress in improving immunization coverage in the United States also found that a key barrier in vaccination programs was the lack of financial coverage of vaccination by many insurance programs.27 Among the National Vaccine Advisory Committee's 15 recommendations to achieve a sustainable childhood immunization delivery system, the first was “vaccination financing to ensure full insurance coverage of recommended vaccines and to support the Vaccines for Children (VFC) program.”

What would need to be in place to make booster vaccination with Tdap possible as part of the routine immunization schedule for adolescents? Out-of-pocket costs for families would have to be negligible. VFC funding, which hinges on a vote by the Advisory Committee on Immunization Practices, and private insurer coverage will be essential to vaccine uptake.28 In addition, for primary care offices, upfront costs for the purchase of the vaccine would have to be reasonable and reimbursement swift. Additionally, adequate reimbursement for vaccine administration would be necessary.

The costs and benefits of pertussis booster vaccination need to be identified and analyzed as has been done for other vaccines.23–30 In 2002, Lieu et al31 published a national research agenda that identified the highest-ranking research ideas, including evaluating the cost-effectiveness of adult and adolescent pertussis vaccination programs. A Canadian study has suggested that replacing the Td vaccine with a booster dose of Tdap at 12 years of age may reduce the economic burden of pertussis treatment in the long term at a reasonable cost.32 U.S. cost-benefit analyses of pertussis vaccination of adolescents are reviewed elsewhere in this supplement.33

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Multicomponent Interventions to Expand Access.

Expanding access to immunization in health care settings may be accomplished by increasing the number or convenience of the hours of service, bringing services closer to the client or delivering immunizations in new settings (eg, emergency departments), and reducing the “hassle” associated with obtaining an office visit (eg, vaccine-only nurse visits).25 In the studies evaluating expanding access interventions, other interventions (eg, reducing out-of-pocket costs, sending patient reminders, and establishing standing orders) were being tested simultaneously. For this reason, the effectiveness of the former as stand-alone interventions could not be evaluated sufficiently. Though tested in both adults and children in diverse settings, it is not known which of these interventions could be tailored successfully to adolescents; in any case, increasing health care provider access to adolescents would increase the opportunity for administering a booster dose of Tdap.

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Vaccination Programs in Schools.

Sutton's law was named for Willy Sutton who reportedly, when asked why he robbed banks, replied, “because that is where the money is.”34 Sutton's law can be applied to adolescent vaccination programs in schools. In a national survey conducted by Schaffer et al,26 84% of primary care physicians preferred that adolescent immunizations be administered at their practice, but 71% considered schools to be acceptable alternative adolescent immunization sites, although many had concerns about continuity of care for adolescents receiving immunizations in school.

A better understanding of the successful hepatitis B vaccination programs based in schools may be of use.35,36 The CDC funded a 3-year project in San Francisco to assess the feasibility of a large-scale, school-based hepatitis B vaccination effort targeting ∼5,000 seventh graders and special education students.37 Of the students targeted, 71% presented parental consent for vaccination and received the first dose. Among these students, 93% completed the three-dose series at school. The researchers concluded that, with sufficient attention to political and logistical dimensions, school-based vaccination programs could be successful in large urban schools.

However, there may be difficulties with the school-based approach to vaccination. The San Francisco project noted difficulties with lack of pre-existing health services, diversity of home languages, and an every-50-minute bell schedule.37 Their report emphasized the need for collaborative planning (including planning how to distribute parent materials and schedule vaccination clinics while minimizing school-day interruption), as well as offering an educational component for students and an incentive for those who obtained timely parental consent. Problems reported in other school programs have included that students may not carry information on their insurance or health plans, complicating allocation of costs. Managed care organizations may object to school-based immunization if they lose the “hook” that draws adolescents to the primary care office for comprehensive health services.38 Immunization records may be difficult to obtain, and state immunization registries rarely include adolescents. Despite success in reducing many of the access barriers through this approach, even in school-based programs differences in vaccine uptake based on race, ethnicity, and gender may persist.39 At present, funding for school nurses may be difficult to maintain. In reports of adolescent school-based programs, it is sometimes difficult to separate two effects: increased access and that of school requirements (as discussed below).

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Provider-Based Interventions
Assessment and Feedback for Providers.

Assessment refers to evaluating the performance of providers and their office systems in delivering vaccinations to a target population (eg, all 11- and 12-year-olds). Of course, assessment is of little use without providing data back to all individuals in the system. Assessments can be accomplished through manual chart or database reviews, which require personnel time (although many states will perform this service for free for offices that participate in the VFC program). In the Task Force review,25 5 studies of assessment and feedback-only interventions demonstrated a median immunization rate increase of 16%, and 8 studies in which assessment and feedback were one component of a multicomponent intervention demonstrated an increase of 17%. In addition to the review of the Task Force, a review using Cochrane Collaboration methodology was performed on 44 studies (15 meeting eligibility criteria) involving audit and feedback in at least one arm of the study.40 Twelve of the 15 studies found that audit and feedback, alone or in combination with other interventions, were associated with improvements in immunization rates.

One difficulty in assessment and feedback is deciding which patients to include in the review. If a 12-year-old has not been seen in your office for 2 years, should that early adolescent still “count” in your assessment? Assessment and feedback are an important starting place for offices, because the initial assessment often yields surprisingly low rates, and this awareness may motivate the clinical team to enter the quality improvement cycle.

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Provider Reminders.

Any strategy to inform health care providers that their patients are due (reminder) or overdue (recall) for vaccinations is called a provider reminder.25 A wide array of strategies has been used, such as chart stickers, computer notification, vital sign stamps, and checklists. Provider reminders are effective at increasing immunization rates and are relatively simple and inexpensive to institute. However, there are drawbacks to this approach. The chief purpose of provider reminders is to overcome forgetfulness, but they cannot overcome lack of motivation (eg, withholding a vaccine because it represents extra work) or lack of information (eg, withholding a vaccine because of a false contraindication). After a period of use there is the potential to simply stop noticing the reminder. Unless the reminder is automated, some personnel time is required to review the charts for the day and to place provider reminders on those of eligible patients. Providers may believe that they do such a complete job of remembering to give all early adolescents Td that no reminder would be necessary with the relatively small change to giving Tdap, but the office's current coverage with Td should be formally assessed (see previous section) before this assumption is considered valid.

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Standing Orders.

Standing orders are established protocols that enable nonphysician personnel to prescribe or deliver vaccinations to patients without direct physician involvement during patient visits.25 As an example of their potential, standing orders have been shown to be effective in increasing influenza and pneumococcal vaccination rates for seniors in a wide variety of settings.41 In fact, they have been shown to be more effective than provider reminders to vaccinate. However, there is insufficient evidence of their effectiveness for children or adolescents. Physicians may resist writing standing orders that include vaccines with which they have little or no experience or for adolescent patients with whom they have not had recent contact.

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“Increasing Community Demand”

The Report on Recommendations from the Task Force on Community Preventive Services stated, “When improvement in vaccination coverage is needed, the causes of underimmunization should be assessed and interventions chosen that address local problems…For example…if lack of knowledge among clients regarding need for vaccination contributes to low coverage, a strategy to increase [community] demand can be useful.”25 Most families are aware of the need for immunizations for infants, but this is not the case for adolescents. Motivating patients and parents to follow through with these vaccinations is likely to play a significant role in efforts to achieve high immunization rates.

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Client Recall and Reminder.

Reminding members of a target population (eg, adolescents and parents) that vaccinations are due (reminders) or late (recall) via telephone calls, letters, or postcards has been studied extensively.25 In addition to the review of the Task Force, a review using Cochrane Collaboration methodology was performed on 109 studies (41 meeting eligibility criteria) involving client reminder or recall.42 Patient reminder systems were effective in improving immunization rates in 80% of the studies, irrespective of baseline immunization rates, patient age, setting, or vaccination type. However, none of the studies included adolescent immunizations.

It should be noted that for adolescents these messages may not be perceived as simple “reminders,” but as news of something they did not know the primary care provider expected. A recent study showed that among pediatricians and family physicians, 45% and 62%, respectively, felt lack of adolescent awareness of the need for immunizations was a barrier to immunizing 11–13-year-olds, and this rose to 64% and 65% when the physicians were asked about adolescents 14–18 years of age.43 Currently, few physicians track patients and send reminder or recall messages. In a national survey by Schaffer et al,26 only 21% of primary care providers reported using immunization tracking and recall systems. Difficulties with creating and maintaining such systems include programming complexities and costs. More research is needed to determine the effectiveness and cost-benefit of such systems applied to adolescent immunization.

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Multicomponent Interventions With Education.

The Task Force review included multicomponent interventions in which families or health care providers received education about vaccinations in conjunction with at least one other activity to improve vaccination rates.25 For these multicomponent interventions the evaluations could not separate the contributions of the various components. The importance of adolescent and parent education may be apparent when new and unfamiliar vaccines become available (eg, HPV vaccine). Before families and health care providers embrace new vaccines, they will need to be educated about the incidence and severity of the diseases they prevent, as well as be convinced of the safety and efficacy of the vaccine, even those already commonly used for other age groups (eg, Tdap). Because the high reading level of vaccine educational materials may impede understanding, it is important for these to be written simply44 and published in several languages. It also may be useful to include discussion of vaccine risks and benefits as part of school-based educational programs.

Education about vaccines related to sexually transmitted diseases (eg, herpes simplex virus and HPV) may be controversial. Prelicensure studies of these vaccines have suggested that public and health care provider opinion may be generally positive.14,45–47 Nonetheless, there is concern that some people will view vaccination against sexually transmitted diseases as an encouragement of premarital or promiscuous sex. These views may become barriers to the development of adolescent immunization recommendations.

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Requirements for School Entry.

Vaccination requirements for school entry have been recommended by the Task Force on the basis of sufficient evidence that they are effective in reducing vaccine-preventable disease and improving immunization coverage rates.25 For example, impressive jumps in immunization coverage for seventh-grade students have been demonstrated in states that have initiated requirements for hepatitis B vaccine; a booster dose of Td; and a second dose of measles, mumps, and rubella vaccine.48,49 Currently, there are ∼20 states with Td school entry requirements. It may be decided that, to prevent school outbreaks of pertussis, the Td requirement should be converted to Tdap, assuming the Advisory Committee on Immunization Practices changes its recommendation for Td to Tdap at the 11–12-year visit.50 The difficulty of making legislative changes regarding immunizations can vary from state to state, and some states may choose not to open the legislative process because of concern regarding reactions from antivaccine groups.

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CONCLUSIONS

Adolescent immunization is a growing field with many new vaccines in various stages of development and expansions to current vaccine recommendations being considered. Because the incidence of reported cases of pertussis has risen in the United States, particularly among adolescents, a booster dose of Tdap may be recommended to replace Td in adolescents, just as a meningococcal conjugate vaccine now is recommended for individuals 11–12 years of age, entering high school, or entering college and living in dormitories. Adolescents have unique health care needs, and although some of the barriers to immunizing adolescents are also unique, some are common to other age groups. The Task Force on Community Preventive Services assembled by the CDC developed a report summarizing the recommended interventions for improving vaccination coverage among children, adolescents, and adults. At the health care system level, reducing out-of-pocket costs, expanding access to immunizations, and implementing vaccination programs in schools were effective. Effective provider-based interventions included immunization rate assessment with feedback to the entire office staff, provider reminders, and standing orders. Medical literature also has shown that client recall and reminders, education (coupled with another intervention), and requirements for school entry increased immunization rates. Evaluation of each of these interventions is needed to better understand how to optimize immunization rates among adolescents. Creating adolescent immunization rates comparable to infant immunization rates will require time, consistent effort, and creativity.

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Keywords:

adolescents; immunization; Tdap; vaccination

© 2005 Lippincott Williams & Wilkins, Inc.

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