The incidence of vaccine-preventable diseases is at an all time low, and preschool immunization coverage levels are at an all time high. This is in marked contrast to the situation 9 years ago when there was a measles resurgence due, in part, to low preschool vaccination rates. In 1991, surveys conducted in several US cities revealed immunization rates as low as 10-42% among children aged 24 months.1 One of the goals established by Healthy People 2000 is 90% immunization coverage for 2year-olds by this year,2 but the recent findings of a 77% coverage rate in this age group3 suggest that we are not there yet.
Achieving high coverage rates requires an understanding of the barriers to childhood immunization. A great deal of research regarding these barriers has been conducted since the measles resurgence. The purpose of this review is to summarize findings of that research (Table 1). We will first examine several factors that, although mentioned frequently as barriers to timely receipt of immunizations, have not held up in the literature. Second, we will review a number of factors consistently supported by strong evidence to be associated with underimmunization.
FACTORS WHOSE ASSOCIATION WITH UNDERIMMUNIZATION IS NOT SUPPORTED BY STRONG EVIDENCE
The first factor, parental attitudes, includes health beliefs about tlie safety and efficacy of vaccines, the severity of vaccine-preventable diseases, and the priority parents place upon immunizing their children. It was commonly believed, and research supported the idea, that poor parent attitudes prevented children from being vaccinated. One frequently-cited Utah study, for example, demonstrated an association between pertussis immunization and accurate parent knowledge about vaccines and illness.4 Health care providers were among those who believed that parent attitudes and knowledge were largely responsible for low immunization rates among their patients. In one community-wide survey of pediatricians and family practitioners in Ohio, more than 95% of those surveyed reported parental forgetfulness and not knowing when immunizations are due as barriers to immunization.5 While such studies certainly suggest that parental knowledge plays a role in immunization, they do not specifically address parental health beliefs or attitudes.
Several investigators have conducted studies designed to focus upon this relationship between immunization coverage rates and parental beliefs and attitudes. These investigators have found no differences in maternal health beliefs (including perceived severity, susceptibility, benefit, and cost; health motivation; and locus of control) between infants who are up to date and those who are not.6,7 Using a community-based approach in inner-city Baltimore, with children living in poverty, another group of investigators found a disappointingly low immunization coverage rate of 54% at 24 months of age, despite the fact that 86% of parents believed shots were effective and 71% believed that children were vulnerable if not up to date.8 Similar results have been demonstrated in more affluent populations as well.9 Substantial evidence, it seems, fails to support an association between parental attitudes toward vaccination and immunization status - parents want their children protected by vaccination.
One final issue relevant to parental attitudes about immunization is worth mentioning. That issue involves a group of parents with religious or philosophical objections to childhood immunizations. Certain religions forbid vaccination, and almost all states recognize this by allowing religious exemption from school-entry vaccination laws. In addition, some states allow exemption from vaccination for philosophical reasons - ie, the parents do not have a religious contraindication to vaccination, but they are philosophically opposed to vaccination. The decision by a parent to exempt his/her child from vaccination should not be taken lightly, even though the proportion of parents taking philosophical exemption appears to be less than two percent (given the 98% coverage rate at school entry).10 Clinicians should help parents understand the critical importance of high vaccination coverage levels in protecting not only those children who are vaccinated, but also those who cannot be vaccinated for medical or religious reasons.11
Barriers to childhood Immunization
A second factor that has been implicated as a cause of underimmunization in children is provider attitudes. Simply put, it was once believed that a major reason for underimmunization was that providers did not place a high priority upon childhood vaccinations. A number of studies, however, have failed to support this hypothesis. For example, in a survey of primary care providers in New York state, the majority of providers in the study ranked immunizations as one of their top two priorities.12 There was no association, however, between how highly these providers ranked immunizations and the immunization coverage rates in their practices. In fact, there was evidence that some providers practicing in sites with the lowest immunization levels and the most high-risk patients were actually more aggressive in their vaccination policies than providers in sites with lower-risk patients. In another study involving primary care physicians from several specialties and practice settings, 86% of the physicians surveyed reported that they would encourage DTP vaccination, even to parents who voiced strong concerns about potential side effects.13 Finally, the American Academy of Pediatrics has stated clearly in a recent position paper its commitment to "continue efforts to ensure that every child receives age-appropriate vaccination."14 Research findings, as well as this current policy statement, reflect that poor immunization coverage rates occur despite the good intentions of primary care physicians - providers want to vaccinate their patients.
Ability to Access a Primary Care Provider
A third factor that has long been considered a barrier to age-appropriate immunization is the ability to access a primary care provider. Certainly, if children do not have adequate contact with primary care providers, they cannot receive recommended immunizations in a timely fashion. In the past five years, however, a number of national surveys have demonstrated that access to primary care providers exceeds immunization coverage, a finding that casts doubt upon its importance as a dominant barrier to immunization. For example, the 1988 National Health Interview Survey on Child Health, found that 90% of children reported a source of routine care.15 That same year, the National Maternal and Infant Health Survey revealed that although 82% of white infants and 75% of black infants surveyed had made an adequate number of well-child visits, only 46% and 34%, respectively, were appropriately immunized.16 More recently, the 1993 National Health Interview Survey, demonstrated that access to primary care is high, even among underimmunized children, 90% of whom reported having a usual source of care.17
Anothet study which surveyed low- income families in Baltimore produced findings similar to these national survey results.18 Approximately 99% of the participants in this Baltimore study reported a source of primary care. Among those children who had a regular source of health care, there was an important discrepancy between the proportion of children who made a well-child visit between 12-16 montns of age (75%) and that of children who received an MMR vaccine at the appropriate age (53%). In their conclusion, the authors state that low vaccination coverage leveb exist "despite the presence of a large network of primary health care facilities to which these children have access and despite the availability of health insurance (via Medicaid), sufficient preventive health visits during the first two years of life, and free vaccines (to about one-third of the providers in the survey area)." As these and other studies suggest, there is an important distinction between access to a primary care provider and use of services19 such as immunization.
FACTORS WHOSE ASSOCIATION WITH UNDERIMMUNIZATION IS SUPPORTED BY STRONG EVIDENCE
Poverty. Living in poverty has been consistently identified as a major contributor to underimmunization. The 1994 National Immunization Survey, for example, showed that children living below the poverty level had 4%-9% lower coverage rates than children living at or above the poverty level for individual vaccine series (eg, >4 DTP or >3 Polio or >1 MMR).3 Moreover, the combined series (4DTP/3 Polio/1 MMR/3 HIB) coverage rate for children living below the poverty level was a full 1 1 % lowet than that for children living above the poverty level. Additional studies have shown that socioeconomic status,20 as well as some of its correlates (eg, insurance type, household size, and maternal age, education and marital status)7·21,22,23 are associated with immunization status. The importance of one particular correlate of poverty, transportation difficulties, was quantified in a recent population-based study in Virginia.24 By comparing parent interview responses with provider records, investigators found that children whose parents reported problems obtaining transportation to the clinic were 2.6 times more likely to be underimmunized at 12 months than children whose parents did not report such problems.
Cost to Families. Another important economic factor is rhe cost that families must pay for vaccinations. In the public sector, the cost for a full series of vaccines in 1987 was approximately $34- The 1997 public sector cost (which incorporates all current ACIP recommendations) was approximately $185. Private sector costs for the same time periods were $1 16 and $350, respectively (CDC, unpublished data). This increase in vaccine costs over the past decade is certainly a daunting one for parents who must pay for vaccines out of pocket. While increases in the prevalence of managed care may eventually reduce the number of families without insurance coverage for vaccines, it was estimated in 1991 that only 30% of Americans employed in medium and large-sized firms received some vaccine coverage from their health benefit plans.25 Finally, several studies have shown that immunization rates are the lower among uninsured children26,2' whose families are least likely to have the resources required to pay for immunizations. It should be noted, however, that although vaccine costs certainly represent an important barrier to immunization for some segments of the population, studies conducted in settings such as military clinics and HMO's reveal suboptimal immunization coverage rates, despite the fact that vaccine costs have been eliminated.28,29 Thus, cost to families is important, but it is not the sole factor affecting vaccine coverage levels.
Cost to Providers. Another economic issue to consider is the cost that vaccines impose upon immunization providers who must often purchase vaccines up front, while being reimbursed only after billing the parent. This cost barrier has predominately been mediated through referrals to health department clinics. There is some evidence that the Vaccines for Children Program, which provides free vaccines to providers for eligible children, is helping to overcome this barrier,30 with reduced referrals to health department clinics,31 and improved immunization coverage levels.32
JLate Start of Vaccination
In 1994, a study of low-income children in Baltimore demonstrated a link between late start of the vaccination series and underimmunization in two-year-olds.18 After surveying parents and reviewing medical records for a random sample of lowincome two-year-olds, these investigators found that infants who received their first DTP on time were twice as likely to be up to date at 24 months as those who received their first DTP late. That same year, a survey conducted among employees of a large US company showed almost identical results.25 Of note is tliat, in contrast to the Baltimore study whose participants were largely Medicaid-insured, the majority of employees participating in this second study had health benefits that explicitly included immunization coverage. Similar findings have also been reported in military primary care clinics, which are part of a health care delivery system that is relatively free of cost and organizational barriers to immunization.28
Parents. The vaccine literature provides many examples of an important information gap that affects parents, providers, and medical records. Parents are often unaware of their children's immunization status and rely on their provider to tell them when and whether their children need vaccination. This is not surprising, given the growing complexity of the vaccine schedule. One study, for example, conducted in an emergency department found that only 2/3 of parents who reported their children's immunization status as up-to-date were actually correct.33 Similarly, in a survey conducted in public clinics in Idaho, although almost 90% of parents reported that their children were fully immunized, a medical record review revealed complete immunization coverage among only 19%-32% of the children.34 Finally, in the 1994 National Health Interview Survey, which includes a provider record check, nearly 75% of parents of underimmunized children reported that their child's immunization status was up to date.35 These studies suggest that messages targeted toward the parents of underimmunized children are unlikely to be effective because many of those in the target authence believe that their children are up-to-date.
Providers. Similarly, providers tend to believe that the coverage of their patients is higher than it actually is. Bushnell describes a study of Massachusetts providers who reported coverage rates ranging from 85%- 100% among two-year-olds in their practices.36 A sample of medical records drawn from these practices, however, revealed much lower coverage rates ranging from 19%-93%, with an average of 61%. A study of primary care providers in New York state revealed significant overestimation of practice coverage rates as well, with coverage among 20-month-olds reported to be 40%-57% higher than it actually was.12 To compound this problem, surveys indicate that few providers actually assess immunization levels in their own practices,36,37'38 despite the availability of free software from the Centers for Disease Control and Prevention39 and technical assistance from state immunization programs. Thus, in terms of the information gap, providers are similar to parents: both believe coverage among those for whom they are responsible to be better than it is.
Medical Records. Given the discrepancy between perceived immunization rates and actual immunization rates that makes up this information gap, it would be logical to assume that medical records might provide some sort of safety net. Unfortunately, problems with record scattering only widen the information gap, and, consequently, present yet another barrier to immunization. Record scattering is a problem that comes about when children receive vaccines from multiple sources and providers whose recordkeeping systems do not communicate with one another. It is also a problem that affects poor children disproportionately because poor children are three times more likely than non-poor children to have a source of sick care that is not the same as their source of preventive care.15 Most providers are aware of the challenges of record scattering whenever they see new patients in their practices, and a study conducted in an inner-city primary care clinic in Seattle illustrates this point.40 In this study, providers ascertained a reliable immunization history (ie, information based upon immunization records brought by the parent or telephone contact with another physician) for only 27% of children at the time of their first visit.
Hand-held immunization cards do little to address the problem of record scattering, as the results of two large-scale studies indicate. Both studies consisted of household interviews in which parents were questioned about their children's immunization status, and both revealed that only about half of the participating parents were able to produce hand-held immunization cards, despite being interviewed in their own homes.24,41 In contrast to hand-held immunization cards, state or local immunization registries may provide valuable assistance inbridging the medical record information gap. InOlmstead County, MN, for example, investigators created a simulated county immunization registry by combining data collected from all medical care facilities within the county.42 Coverage rates based on this simulated registry were then compared with rates based on records at each individual facility. Adding data from the simulated county immunization registry to the medical records of the individual facilities increased coverage rates within these facilities by 7% to 28%.
The consequences of record scattering include overimmunizing as well as underimmunizing. For example, one relevant study took place in four Los Angeles public health centers that operate well-child clinics which are separate and distinct from their immunization-only clinics, provide immunizations in both types of clinics, and maintain separate records systems.43 Investigators reconstructed immunization histories of randomly selected children by combining records from both clinic types within each center. Study findings revealed that children who attended both types of clinics received twice as many inappropriately-timed vaccinations as children who attended only well-child care clinics. Another study, conducted in a Texas public clinic system with an explicit policy of not recording immunizations given by outside providers in the child's clinic record, showed that children in such a clinic system were six times more likely to receive unnecessary immunizations than children seen by private providers or in clinics without such a policy.44
Another major barrier to the timely delivery of childhood immunizations involves suboptimal practices and policies of health care providers. These provider factors include: (1) missed opportunities for immunizations, (2) lack of tracking, reminder, or recall systems to contact patients who are due or who are behind in immunizations, and (3) difficulty in implementing immunization practice standards.
Missed Opportunities for Immunisations. A missed opportunity is a healthcare encounter in which a child is eligible to receive a vaccination but is not vaccinated. Missed opportunities occur in three types of settings: (1) primary care offices or public health clinics that offer immunizations, (2) health care settings that do not traditionally offer immunizations, such as emergency departments and subspecialty clinics, and (3) public health settings that do not traditionally offer vaccinations, such as Women, Infants and Children (WIC) program sites.
Missed opportunities have been found to occur in virtually all primary care settings, including private offices45'51 and public health department clinics.52,53 The frequency of missed opportunities varies, as does the impact of missed opportunities on immunization status. In one study in upstate New York that investigated missed opportunities in several office settings,46 the frequency of missed opportunities varied across practices from 0.3 to 1.8 per patient per year during the first year of life, and the proportion of office visits that were missed opportunities ranged from 2% to 18% of all visits.
Missed opportunities have also been noted in health care settings that do not traditionally provide preventive care; examples include emergency departments,49,54,35 hospital inpatient units,56 and subspecialty clinics.56 There has been considerable debate about the appropriateness of emergency departments for immunization services,33,49,54 and it is unlikely that either emergency departments or subspecialty clinics will become major sites for the provision of childhood immunizations.
Impact of Missed Opportunities on Immunization Rates. Studies have evaluated the potential contribution of missed opportunities toward underimmuruzation of children. The impact of missed opportunities depends on a number of related factors: First, the frequency of missed opportunities influences the length of time patients remain underimmunized. Second, visit rates to the office determine the number of immunization opportunities. Patients who have many office visits also have many chances for immunizations, and a single missed opportunity may not be as detrimental as it is for patients who make few visits to the office. Third, baseline immunization rates differ among populations, and missed opportunities have the greatest impact on populations with low baseline rates.
In general, studies have found that if missed opportunities were eliminated, coverage leveb would be substantially higher. For example, the impact of missed opportunities on immunization coverage levels was evaluated in four inner-city settings: Philadelphia, Baltimore, Los Angeles, and Rochester, New York.58 Hypothetical coverage levels were determined at ages 12 and 24 months based on theoretically eliminating all missed opportunities. Coverage levels (defined as the proportion of the population up-to-date) at 12 months would have increased by 4% to 27% at all four sites, and coverage levels at 24 months (4:3:1) would have increased by 8% to 16%.
Reasons for Missed Opportunities. Table 2 lists several potential reasons for missed opportunities in primary care settings. As discussed previously, providers are often unaware that their patients are in need of vaccinations. Sometimes medical charts containing immunization data are not available during acute illness visits.48 Patients frequently lack immunization cards, and data on cards are sometimes incomplete. Accurate tracking systems or registries do not yet exist in the vast majority of settings. In short, immunization data are often not readily available to providers during medical visits, and providers would have to make extra efforts in order to obtain immunization dates. It is difficult to make these additional efforts during busy patient care sessions.
A second reason for missed opportunities involves failure to provide simultaneous vaccinations.12,37,51,58 While recent studies suggest that this misguided practice appears to be declining,51,58 it still occurs far too frequently. In one study, reported reasons cited for failure to vaccinate simultaneously included pain (57% of physicians would not vaccinate simultaneously), parental objection (41%), costs (44%), concern about adverse side effects (65%), concern about reduced immune response (66%), and specific contraindication to administer all 4 vaccines (7%).37
Concern about parental objection to multiple injections appears to be more in the minds of providers than parents. In fact, in a recent study in which parents and physicians were asked about their preferences for multiple vaccinations during a single visit versus requiring a follow-up visit, most parents preferred simultaneous vaccinations.59 Additionally, the cost is often greater to parents if vaccines are provided over several visits. Finally, studies have found that the immune response is adequate during simultaneous vaccinations.60,61 In short, simultaneous vaccinations must become the rule.
A third reason for missed opportunities involves individual provider policies or practice policies resulting in failure to vaccinate, even if adequate immunization history (ie, dates) is available. For example, a national survey of pediatricians and family physicians noted that only 29% of providers routinely vaccinated children during acute illness visits. Reasons for not vaccinating during acute illness visits included provider focus on the acute problem (54%), lack of time (24%), lack of immunization records (13%), and the belief that vaccinations during acute visits might decrease compliance with scheduled preventive visits (10%).37 Another common practice policy leading to missed opportunities is failure to screen charts routinely for immunization dates during all encounters,12,52 leaving providers unaware that certain children are due for immunizations.
Reasons for missed opportunities, impact on immunization levels and "fixability" (ease of elimination)
A fourth and very important reason for missed opportunities involves inappropriate contraindications for vaccinations. Studies utilizing medical chart reviews have found that the presence of a minor acute illness, such as a common cold or otitis media, is often associated with a missed opportunity for immunizations. This issue is complex because in primary care settings many factors affect the decision to vaccinate and there are many "relative contraindications". True vaccine contraindications are listed in the Report of the Committee on Infectious Diseases or "Redbook,"60 in ACIP guidelines,61 and in the Standards for Immunization Practices;62 these rare contraindications usually do not present a management dilemma. Relative contraindications, on the other hand, are common and difficult to manage. These include fever, acute illness, and chronic illness. In one study,37 less than half of physicians stated that during a scheduled preventive visit they would immunize a toddler with DTP or with MMR if the child had gastroenteritis, otitis media, bronchiolitis, or a fever of less than 39°, though 80% would immunize a child with a common cold. Finally, provider beliefs about vaccine side effects and efficacy in the setting of a mild, intercurrent illness have been shown to influence whether or not vaccines are recommended during an encounter.63
Another concern about vaccinating during minor illnesses involves the potential for "masking" a serious illness because of the fever and malaise that may follow a routine vaccination. Immunizations are obviously not recommended for children with potentially serious acute illnesses. However, the vast majority of children with minor acute conditions are not very ill, and with proper education parents can be taught the difference between common, minor vaccine side effects and potentially serious signs that should be reported to physicians. Some parents are reluctant to accept immunizations when their children have an acute illness, but given accurate information about the benefits and risks of vaccinations, most parents would probably desire immunizations even in the presence of a minor acute illness.
Potential methods to reduce missed opportunities for immunizations
Degree of difficulty associated with eliminating particular types of missed opportunities in primary care practices.
A fifth reason for missed opportunities involves administrative and system barriers. One barrier is cost, as described above. Other administrative barriers such as requirements for physical examinations and limited hours of operations for immunization services will be discussed below.
Table 3 summarizes possible strategies for eliminating missed opportunities, and Table 4 classifies missed opportunities into those that are easy, moderate, or difficult to eliminate.
Lack of tracking, reminder, or recall systems. Surveys have noted that only a small proportion (generally less than 10%) of primary care practitioners systematically track and identify those patients who are behind in immunizations.12,37 An even smaller proportion of providers utilize reminder systems for patients who are due for vaccinations. Until immunization registries are implemented, primary care practices will offer the best opportunities to identify underimmunized preschool children and to contact them for follow-up. Many primary care providers already utilize reminders prior to upcoming preventive care visits. These reminders probably are effective in minimizing the rates of appointments-not-kept and may help promote immunization delivery. Inoerporating tracking and recall systems for children who are behind on immunizations would likely improve immunization rates even further.
Difficult} in implementing immunisation practice standards. In response to the measles outbreaks that occurred between 1989-1991, the National Vaccine Advisory Committee called for the development of standards to guide immunization practices in the United States. In 1992, an ad hoc working group, which consisted of CDC staff, as well as representatives from state and local health departments, physician and nursing organizations, and public and private providers, published 18 standards "as to what constitutes the most essential and desirable immunization policies and practices in an immunization service."64 While these standards were a critical first step, they are unlikely to solve the problem of underimmunization completely because they suggest relatively major changes in provider practice styles but do not provide specific advice about how to implement these changes. Baseline surveys of primary care providers conducted prior to the distribution of CDOs published standards demonstrated that many providers followed practices that did not conform to the 1992 standards.37,65 A national survey conducted in 1995, two years after the publication of the standards, also revealed suboptimal conformity to the immunization standards among pediatricians and family practitioners.66 Additional follow-up studies are needed, but it is likely that a significant number of providers will continue to report difficulty in implementing CDC standards.
Office and clinic factors
A number of studies in the literature document parental report of office/clinic factors that present barriers to obtaining immunizations. Among the reported barriers are requirements for appointments and physical exams, long waiting times, and inconvenient clinic hours that conflict with work or other priorities.22 23,61-68 In a survey of 54 immunization program managers in 1990, 50% of rhose surveyed reported the existence of organizational barriers (eg, insufficient staff or clinic hours, appointment-only systems, and physical exam or well-child care requirements) within their programs.69 Despite the frequency with which parents have reported and described the existence of these office and clinic barriers, it has been difficult to determine the magnitude of the eñect that such barriers have upon immunization status. A recent population-based study conducted in Virginia was able to quantify the effect of at least one such barrier: clinic waiting time. Children whose parents reported long waiting times were more likely to be underimmunized than children whose parents did not report long waiting times. In fact, for each additional hour that their parents reported waiting, children were 1.6 times more likely to be underimmunized. Although further research is required to quantify the effects of other office and clinic barriers, it is clear that the effect of one such barrier (waiting time) in this population was quite substantial.
A deeper understanding of the barriers to childhood immunization has been gained in the decade since the measles resurgence. Many of these barriers can be overcome through programmatic efforts and determination by providers. Cost-related barriers are being lowered by vaccine financing changes, for example. Physicians can reduce the information gap barrier by conducting assessments of their practice coverage levels and implementing recall/reminder systems. The use of state and local immunization registries currently being developed may facilitate both of these efforts. Finally, provider practices can be modified to help reduce missed opportunities, and office/clinic policies can be reorganized to make appointment requirements, waiting times, and clinic hours more convenient for parents. These and other interventions, suggested by our understanding of the barriers to childhood immunization, will help us to reach or exceed the 90% immunization coverage goals of Healthy People 2000.
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5. Salsberry P], Nickel JT, Mitch R. Why aren't preschoolers immunized.' A comparison of parents' and providers' perceptions of die barriers to immunization. Journal of Community Health Nursing. 1993,10:213-224.
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12. Szilagyi PG. Roghmann KJ. Campbell JR, Humiston SG, Winter NL, Räubern RF, Rodewald LE. Immunization practices of primary care practitioners and their relation to immunization levels. Arch Peàaa Adoiesc Med. 1994;148:158-166.
13. Zimmerman RK, Schlesselman JJ, Mieczkowski TA, Medsger AR, Raymund M. Physician concerns about vaccine adverse effects and potential litigation. Arch Pediatr Adoiesc MeA 1998;152:12-19.
14. American Academy of Pediatrics. October 1996, Where We Stand. Elk Gtove Village, IL: American Academy of Pediatrics; 1996.
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39. CDC. Clinical Assessment Software Application (CASA). http.-//www.cdc.gov/nip/casa.
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Barriers to childhood Immunization
Reasons for missed opportunities, impact on immunization levels and "fixability" (ease of elimination)
Potential methods to reduce missed opportunities for immunizations
Degree of difficulty associated with eliminating particular types of missed opportunities in primary care practices.