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Lj oo TOFAMILYPRACTICEAddressing immunizationbarriers, benefits, and risksSANFORD R, KIMMEL, MD; ILENE TIMKO BURNS, MD, MPH; ROBERT M , WOLFE, MD;AND RICHARD KENT ZIMMERMAN, MD, MPHVaccines have been highly effective in eliminating or significantly decreasing the occurrence ofmany once-common diseases. Barriers to immunization are a significant factor in the risingincidence rates of some vaccine-preventable diseases. Cost, reduced accessibility to immuniza-tions, increasingly complex childhood and adolescent/adult immunization schedules, andincreasing focus on the potential adverse effects of vaccines all contribute to difficulty in meet-ing the 2010 immunization goals. Physicians must not only be knowledgeable about vaccinesbut they must incorporate systems in their offices to record, remind, and recall patients for vac-cinations.They must also clearly communicate vaccine benefits and risks while understandingthose factors that affect an individual's acceptance and perception of those benefits and risks.Vaccines have almost eliminated or significantlyreduced the incidence of many diseases, but tensof thousands of children and adults in the UnitedStates continue to develop vaccine-preventable dis-eases. Reported cases of pertussis have increased froma low of 1010 cases in 1976' to 25,827 in 2004,' withthe majority of these cases occurring in adolescentsand adults. Potential reasons for this include geneticchanges in Bordetella pertussis (which make vaccinesless effective), decreased potency of pertussis vaccines,greater awareness of pertussis, and improved diagnos-tic tests.* However, many of these cases are believed tobe caused by waning immunity or inadequate immu-nization. In 2005, only 76.1% of US children aged 19to 35 months had received all of the recommendeddoses of DTaP, Hib, hepatitis B, MMR, polio, and vari-cella vaccines, although rates of those who receivedmost individual vaccines were higher.'' A HealthyPeople 2010 goal is to immunize 90% of young chil-dren and adolescents with age-appropriate vaccines.'Barriers to immunization are grouped as systemsbarriers (eg, those involving the organization of thehealth care system and economics), health careprovider barriers (eg, inadequate clinician knowledgeabout vaccines and contraindications to their use), andparent or patient barriers (eg, fear of immunization-related adverse events).' These barriers affect immu-nization rates and increase the burden of preventabledisease in our society.Systems Barriers to ImmunizationFactors affecting the supply and distribution of vaccinesare among the most noticeable systems barriers. Thesupply of influenza, conjugate pneumococcal, and,most recently, tetravalent conjugate meningococcal(MCV4) vaccines have been inadequate due to a lack ofmanufacturing capacity.' A misdistribution of vaccineshas also occurred. Uninsured and Medicaid-insuredchildren may qualify to receive vaccines through theVaccines for Children program (VFC), but VFC doesnot provide funding to reimburse providers for thecosts of administering those vaccines. Uninsured adultsrepresent another major systems problem.Provider Barriers to ImmunizationProviders may lack knowledge about the indicationsfor and contraindications to immunization.Expanded uses for current vaccines such as hepatitisA vaccine for children aged 12 months or older andnew vaccines against rotavirus and zoster make itdifficult for health care providers to stay currentwith immunization schedules. A study of CaliforniaThe J o u r n a l of Fami ly P r a c t i c e FEBRUARY 2 0 0 7 V O L . 5 6 , N O . 2 S61A D D R E S S I N G I M M U N I Z A T I O N B A R R I E R S , B E N E F I T S , A N D R I S K Spractices found that knowledge deficits regardingimmunization schedules, vaccine contraindications,and vaccine side effects were present among physi-cians and nonphysician office staff."One early study indicated that almost one half ofnurses (as reported by physicians) were resistant togiving children 3 or more injections and that parentsand physicians were also uncomfortable about this.'However, a later study at an inner-city pediatric clin-ic indicated that parents overwhelmingly compliedwith physicians' recommendations for immuniza-tions.'" Thus, the attitude the physician transmits tohis or her staff about the importance of immuniza-tions is crucial. Combination vaccines that decreasethe number of shots administered at a single visitalso enhance compliance.Logistical barriers faced by health care providersinclude the cost of immunizations, vaccine storageor capacity, and lack of access to patients' prior immu-nization records. Vaccines with stringent storagerequirements, such as varicella vaccine or live attenuat-ed influenza vaccine, may present a challenge.Fragmentation of patient care makes it more likely thatproviders will not have complete immunization recordsfor patients currently in their care. This can lead toincomplete immunization and overimmunization.Missed visits and missed opportunities for immu-nization when necessary vaccines are not administeredat a visit are also notable barriers to timely completionof immunization requirements. When health careproviders have routinely assessed a patient's immu-nization status and notified patients and parents aboutvaccinations that were due (reminders) or overdue(recalls), immunization rates have improved.Reminder/recall systems can be time-consuming andcost-intensive, and they are used infrequently." Greateruse of electronic medical record systems should makereminder/recall systems more efficient.Immunization registries are computerized databasesthat consolidate vaccination data from multiple healthcare providers within a defined geographic area andcan generate reminder and recall notices. Currently,48% of children younger than 6 years old participatein an immunization registry.'^ One national healthobjective calls for a participation rate of 95% of chil-dren younger than 6 years old by the year 2010.'Patient and ParentBarriers to ImmunizationPatients or their parents or guardians may lackknowledge about immunizations, be fearful of vac-cine safety, or lack transportation. They may beunaware of the threat of vaccine-preventable dis-eases or that safe and effective vaccines are availableagainst these diseases. Complicated immunizationschedules, fragmented care records, inconvenientclinic hours, long wait times for immunizations,transportation problems, and cost are other exam-ples of logistical barriers to immunization. Onestudy found that mothers in rural West Virginia weremore likely to have fully immunized children if theyfelt that the clinic they attended was "supportive,"which included variables such as staff who wouldclarify immunization schedules, convenient officehours, and limited wait time for immunizations.'The VFC program has funded immunizations foruninsured and Medicaid-insured children since itsinception in 1994, but not all underinsured childrencan visit their usual source of health care and receivethese vaccines at no cost. Even low-income parentsof children who qualify for immunizations through aVFC program at their usual source of care may notbe aware of this program, and these parents contin-ue to cite cost as a barrier to immunization.'^Families who might qualify for free vaccinationsmay face other barriers such as transportation prob-lems. To limit additional patient trips to health careproviders, all eligible physicians should become VFCproviders so that immunizations can be given at thechild's medical "home." However, children who havehealth insurance that does not cover immunizationsmust continue to receive their vaccinations at publicor federally funded health clinics.SolutionsDespite the many barriers described above, researchhas shown that some interventions canand doimprove immunization rates (TABLE 1). In diverseadult populations, one of the strongest predictors ofinfluenza immunization is a physician's recommenda-tion to receive the vaccine.'""' In low-income pediatricpopulations, enrollment in the Special SupplementalNutrition Program for Women, Infants and Children(WIC)which offers programs to educate parentsabout the importance of immunizationsimprovesimmunization rates among both urban and nonurbanpediatric populations.'^-'"Educational resources for parents who declinevaccination because of antivaccine misinformationcan be found both in print and on the Internet.Providers should tell parents about Web sites thatpresent more balanced and useful information on theS62 T h e J o u r n a l of Fami ly P r a c t i c e FEBRUARY 2 0 0 7 V O L . 5 6 , N O . 2A D D R E S S I N G I M M U N I Z A T I O N B A R R I E R S , B E N E F I T S , A N D R I S K STflBIF 1 ,BarriersKnowledge deficits Patients and families ProvidersFragmented careVaccine shortagesMissed visits, missed opportunitiesAAFP = American Academy of Family PhysSupplemental Nutrition Program for WomeBarriers and solutions to vaccinationSolutions Education through WIC, community outreach, provider recommendation. Web sites Recognized sources of information/guidelines (AAFP, AAP, and CDC Web sites, AAP Red Book,Shots software from vi/ Immunization registries Improved vaccine infrastructure Fair reimbursement for vaccines Reminder/recall systems Fair reimbursement for vaccination Standing orders Shared responsibility for identifying needed vaccines with nursing personnelduring vital signs or through smart electronic records Combination vaccines to decrease number of shots required at a visiticians; AAP = American Academy of Pediatrics; CDC = Centers for Disease Control and Prevention; WIC = Specialn, Infants and Children.risks and benefits of vaccination as well as links toother sources. Among these Web sites are the following: American Association of Pediatrics (AAP) US Centers for Disease Control and Pre-vention (CDC): Society of Teachers of Family Medicine'sGroup on Immunization Education (GIE) Vaccine Information Center at the Children'sHospital of Philadelphia: Immunization Action Coalition (IAC):www.vaccineinformation.orgParents opposed to immunizations are often dis-trustful of "official" sources but may be more willingto accept information from their personal physicianwho takes time to listen to their concerns andrespond in a thoughtful manner.Immunization registries are being developed in allstates and in the District of Columbia.'' In 2002, 43%of all US children had at least 2 immunizations record-ed in a registry. However, about 40% of children in theregistries had incomplete or missing data on adminis-tered doses of vaccine.'' Lack of time or staff to enterdata as well as possible transcription errors may makesome physicians hesitant to use these systems; howev-er, they save time when immunization records arerequested for school or camp forms and improveimmunization rates." Another study also showed thatcomplete computerization of paper immunizationrecords saved both time and money."The Task Force on Community PreventiveServices recommended or strongly recommendedimplementation of the following measures toincrease immunization rates' ": Reminder/recall systems for patients, families,and providers Requirement of vaccination as a prerequisitefor enrollment in school and childcare Decreases in out-of-pocket costs for patients/families Assessment ofand collection of feedbackregardingimmunization rates for individualproviders Issuance of standing orders for adult immunization Provision of immunization services in homesand WIC settings Implementation of multicomponent interven-tions that expand access to services and provideeducation to target populations.Interventions tailored to the culture of aprovider's practice and its patients should increaseimmunization rates. A study of tailored standingorders, reminders, and express vaccination servicesin inner-city clinics found that these measures led toan increase in influenza immunizationCommunicating the Benefitsand Risks of VaccinesThe benefits of immunization are often obvious tohealth care providers; however, patients, parents, andthe general public may have questions or concerns.T h e J o u r n a l o f F a m i l y P r a c t i c e F E B R U A R Y 2 0 0 7 V O L . 5 6 , N O . 2 S 6 3A D D R E S S I N G I M M U N I Z A T I O N B A R R I E R S , B E N E F I T S , A N D R I S K SAs knowledge of the devastation caused by manyvaccine-preventable diseases fades from public mem-ory, attention shifts to the occasionally seriousadverse events that may follow immunization. Thedissemination of (mis)information and anecdotalreports of alleged vaccine reactions by the media, theInternet, and antivaccine groups causes parents,patients, and even some health care providers toquestion the justification for immunizations.^^ Somephysicians may be reluctant to administer immuniza-tions because of liability concerns. An Ohio studydemonstrated that liability concerns influenced thedecisions of 9% of family physicians and 23% ofpediatricians in their choice of polio vaccines."Consequently, vaccines have become victims of theirown success. If a loss of confidence in the vaccinedevelops, then an outbreak of disease may ensue,resulting in resumption of vaccine use."Public Perceptions of Vaccine SafetyParents of incompletely immunized British childrenwere likely to report that immunization was riskier fortheir child than was nonimmunization due to concernsabout vaccine-related side effects, the belief that theirchild was not at risk for the disease, or the belief thatthe disease was not serious." In the United States, con-cerns about vaccine safety are more common amongparents of underimmunized children, but many par-ents of fully immunized children have also expressedsuch concerns." Most family physicians and almost allpediatricians reported at least 1 vaccine refusal fromparents during the year 2000. " A Canadian studyfound that most mothers would accept a 1:100,000 to1:1,000,000 risk for a severe vaccine side effect; how-ever, 14% would not tolerate any serious risk."Common MisconceptionsAbout VaccinesMost parents support immunizations for their chil-dren, but misconceptions do exist. Some parentsbelieve that the administration of too many immu-nizations will weaken their child's immune system^'or cause chronic diseases such as asthma, autism,diabetes mellitus (DM), or multiple sclerosis (MS).^'Some believe that vaccine-preventable diseases hadalready begun to disappear prior to the use of vac-cines or that there are "hot lots" of vaccines thathave a greater frequency and/or severity of adverseevents.^' Others believe that vaccines are not "natu-ral" and thus prefer disease-induced immunity.Individuals often use cognitive shortcuts or heuris-tics to simplify complex decisions and judgments."'Parents who are nonvaccinators may believe theycan control their child's susceptibility to disease,have doubts about the reliability of vaccine informa-tion, prefer errors of omission over errors of com-mission, or rely on herd immunity to protect theirchild.^' TABLE 2 summarizes heuristic factors thataffect vaccine-related risk perception.Multiple Vaccines and the Immune SystemAlmost 25% of parents believe that "children getmore immunizations than are good for them."^*However, most parents and many providers may notrealize that the actual number of antigens in thesevaccines has decreased. For example, the olderwhole-cell pertussis vaccine had approximately 3000antigens compared with 1 to 7 for newer acellularpertussis vaccines.-"^ Rather than weakening theimmune system, vaccines may prevent infections thatpredispose individuals to serious diseases. For exam-ple, varicella is often complicated by necrotizinggroup A beta-hemolytic streptococcal fasciitis inchildren or by pneumonia in adults.^^Explaining Vaccine Benefits and RisksPhysicians serve as the primary source of immuniza-tion information for most parents and patients. Inone national survey, 84% of respondents indicatedthat they received immunization information from adoctor.^* Physicians must accurately portray the ben-efits of immunization while acknowledging that vac-cines are not always effective andin rare casesmay be accompanied by serious adverse events.Providers should inform patients that vaccines arebiologic agents intended to stimulate immunity andcommonly cause local reactions such as redness,swelling, and soreness at the injection site.Physicians or other providers must provide thecurrent Vaccine Information Statement (VIS) eachtime they administer a vaccine covered under theNational Vaccine Injury Compensation Program( orpurchased through a CDC grant." They must record ineach patient's medical record the date of administra-tion, the vaccine manufacturer, the lot number, and thename and business address of the provider, along withthe edition of the VIS that was given to the patient andthe date on which the vaccine was administered.^^Copies of each VIS can be obtained from the CDC or the ImmunizationAction Coalition at Because physi-S64 T h e J o u r n a l of Fami ly P r a c t i c e FEBRUARY 2 0 0 7 V O L . 5 6 , N O . 2A D D R E S S I N G I M M U N I Z A T I O N B A R R I E R S , B E N E F I T S , A N D R I S K STflRI F ) .Factors or heuristic processes that affect vaccine acceptanceFactors or Processes That May Decrease Vaccine AcceptanceFactorCompression1 Omission (not taking action) biasversus commission (action) biasAmbiguity aversionVoiuntary, controllable risiA D D R E S S I N G I M M U N I Z A T I O N B A R R I E R S , B E N E F I T S , A N D R I S K S6 times more likely to develop pertussis than werevaccinated children.^^Common Vaccine RisksPain, swelling, and redness at the injection site arecommon local reactions following immunization.Sterile abscesses occasionally occur after injection ofinactivated vaccines. ^ Fever and irritability are com-mon systemic reactions that may be attenuated by giv-ing acetaminophen. More reports of fever, redness,swelling, and pain at the injection site have been madeafter the fourth dose than the first dose of each of thelicensed DTaP vaccines. Swelling of the entire thigh orupper arm that lasts for a mean of 4 days has occurredin 2% to 3% of children after their fourth or fifthdose of the same DTaP.'* However, local reactions tovaccines or their components usually are not consid-ered contraindications for vaccine administration.Uncommon Vaccine RisksAllergic reactions occur infrequently after immu-nizations. For example, the rate of anaphylaxis afterhepatitis B vaccine is 1 in 600,000.^^ Yeast proteinsmay cause this reaction." Gelatin, a vaccine stabiliz-er, is used in the production of the MMR and vari-cella vaccines. However, persons with a history offood allergy to gelatin rarely develop anaphylaxisafter vaccine administration.^^ The MMR vaccinebut not the influenza vaccinemay be given to per-sons with egg allergy. Neomycin is used in the pro-duction of the MMR, varicella, inactivatedpoliovirus vaccines, and some combination vaccines(eg, HAV/HBV and DTaP/IPV/HBV) and may causea delayed-type local hypersensitivity reaction 48 to96 hours after administration.^^Febrile seizures, persistent crying that lasts 3hours or more, and hypotonic-hyporesponsiveepisodes have been reported very rarely after DTaP. "TABLES 3 AND 4 compare the risks for wildmeasles, mumps, rubella, and varicella disease with therisks for adverse events reported after administrationof the MMR and varicella vaccines.""'" The temporalrelation of adverse events to vaccine administrationdoes not prove causation. TABLES 3 AND 4 also citethe efficacy of the vaccines in preventing disease.Controversial and Unproven RisksChronic diseases such as autism often are attributed tovaccines because immunizations are given at a time inchildren's lives when the signs and symptoms of thosediseases first become apparent. Parents are under-standably frustrated by the lack of an identifiablecause of their child's autism and, in their search foranswers, may allege that vaccines caused their child'sillness because of the temporal relationship betweenimmunization and disease manifestation.Well-controlled studies have not documented acausal relation between administration of theMMR vaccine and development of autism. A studyby Wakefield et al of 12 children with gastrointesti-nal diseases and developmental regression hypoth-esized that such a causal relation might exist."However, Taylor et al conducted a study thatincluded 498 autistic children in the North Thameshealth district of the United Kingdom and found nocausal association between MMR vaccine andautism." Patja et al did not identify any cases ofautism associated with almost 3 million doses ofMMR vaccine given to 1.8 million individuals inFinland over 14 years.'''' Madsen et al compared therecords of more than 400,000 Danish children whoreceived MMR vaccine with those of more than90,000 unvaccinated children.''' The investigatorsdid not find any increase in the relative risk forautistic disorder in vaccinated children over thatfor unvaccinated children.^''Allegations also have been made that hepatitis Bvaccine causes chronic fatigue syndrome, MS, orother autoimmune disorders." The Nurses' HealthStudy in the United States evaluated more than200,000 women and did not find an associationbetween hepatitis B vaccine and MS." A Europeanstudy found that administration of the tetanus,hepatitis B, or influenza vaccines did not increasethe risk for short-term relapse in MS patients."Vaccines have not been shown to increase therisk for type 1 DM.^'-" A Swedish study found thatvaccination against tuberculosis, smallpox, tetanus,pertussis, rubella, or mumps did not increase therisk for type 1 DM.*" A Vaccine Safety Datalinkproject of the CDC did not find an increased risk fortype 1 DM with any of the routinely recommendedchildhood vaccines, including those for DTaP, hepa-titis B, Hib, MMR, and varicella." A Danish studydid not find any significant association of type 1DM with Hib, DTaP, MMR, or oral polio vaccines.'^"Concern also has been expressed that thimerosal,an ethyl mercury-containing vaccine preservative,might lead to greater mercury exposure in infantsreceiving multiple thimerosal-containing vaccines.However, multiple epidemiologic studies have notfound a causal association between autistic-T h e J o u r n a l o f F a n i i l y P r a c t i c e F E B R U A R Y 2 0 0 7 V O L . 5 6 , N O . 2A D D R E S S I N G I M M U N I Z A T I O N B A R R I E R S , B E N E F I T S , A N D R I S K SI. Risks and SequelaeRisk of acquiring diseasei Highest numberof US cases111 Recent number' of US cases! Transmission routeiRate of transmission toj susceptible household, contactsRisk of sequelaej Case-fatality rate: Encephalitis1 Subacute sclerosing; panencephaiitis1 PneumoniaThrombocytopeniaj Orchitis' Anaphylaxis1 Vaccine efficacyMeasles, mumps, and rubella disease and vaccine fact sheetMeasles Disease894,134 in 1941'66 in 200?Droplet spray90%'1-3 deaths/I 000measles cases'''1-2 cases/1000measles cases'8.5 cases/1 millionmeasles cases"1%-6%=Copyright 2005, Society of Teachers of Faniily Medicine'Maldonado Y. In: Behrman ct alMMWR Morh Mortal Wkly RepAmerican Academy of Pediatrics;eds. Nelson Textbook of2006:5S;883-903; 'PickeMumps Disease152,209 in 1968'314 in 2005'Direct contact.airborne droplets.and fomites'1.6-3.8 per10,000 cases'2% fatality ifpatient developsencephalitis'2.5 cases per 1000mumps cases'14%-35%adolescentand adult men'Used with permission.Pediatrics. Philadelphia,Rubella Disease12 million in 1964-1965':57,686 in 1969 (20,000cases of congenital rubellain 1964-1965)'11in2005''"(1 case of congenitalrubella in 2005FDirect contact.nasopharyngeal dropletcontact, or transplacental50%-60% of susceptiblefamily members andalmost 100% inclosed populations'1 death per 30,000 casesdue to 20% fatality fromencephalitis'1/5000-1/6000 rubellacases'*20 total cases of progressiverubella panencephalitissince 1974'1/3000 rubella cases'Measles, Mumps, Rubella VaccineNo cases of congenital rubellareported after immunization ofpregnant women, but the theoreticalmaximum risk is 2% vs at least 30%risk after wild rubella infection infirst trimester*1 death not attributed to vaccine."Fatal measles pneumonitis in one21-year-old man with advanced HIVA D D R E S S I N G I M M U N I Z A T I O N B A R R I E R S , B E N E F I T S , A N D R I S K STABLE 4 i = r r - ' =1 Risks and SequelaeRisk of acquiring diseaseAverage number of US cases/yearRate of transmission tosusceptible contactsTransmission routeRisk of sequelae Localized rashGeneralized varicella-like rash; Invasive group A streptococcal diseaseAnaphylaxisHerpes zoster (children A D D R E S S I N G I M M U N I Z A T I O N B A R R I E R S , B E N E F I T S , A N D R I S K SR e f e r e n c e s1. 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