Parental Vaccine Hesitancy: Clinical Implications for Pediatric Providers

      Abstract

      Despite being recognized as one of the greatest public health achievements, vaccines are increasingly under scrutiny for a multitude of reasons. “Parental vaccine hesitancy,” an emerging term in today's literature, encompasses a wide range of concerns regarding vaccines and is believed to be responsible for decreasing coverage of many childhood vaccines. The threat to herd immunity posed by poor vaccine uptake increases the risk for resurgence of vaccine-preventable diseases. Pediatric primary health care providers have an obligation to respond to the increasing prevalence of vaccine hesitancy by providing education related to vaccines to ensure the safety and health of the population. The purpose of this article is to examine the most common concerns surrounding vaccine hesitancy and outline strategies for pediatric providers to address concerns with parents in the clinical setting.

      Key Words

      Teri Moser Woo, PhD, RN, ARNP, CNL, CPNP, FAANP
      Corresponding Editor
      Pacific Lutheran University
      Tacoma, Washington
      Elizabeth Farrington, PharmD, FCCP, FCCM, FPPAG, BCPS
      University of North Carolina, Eshelman School of Pharmacy
      Chapel Hill, North Carolina
      New Hanover Regional Medical Center
      Wilmington, North Carolina
      Leah Molloy, PharmD
      Children's Hospital of Michigan
      Detroit, Michigan

      Objectives

      • 1.
        Define vaccine hesitancy.
      • 2.
        Identify reasons for parental vaccine hesitancy.
      • 3.
        Discuss the implications of vaccine hesitancy on the child and community.
      • 4.
        Describe ways to approach vaccine concerns with parents.
      Vaccines are one of the greatest achievements of public health and have been proven effective through substantial decreases in morbidity and mortality rates of infectious diseases (
      • Mergler M.J.
      • Omer S.B.
      • Pan W.K.Y.
      • Navar-Boggan A.M.
      • Orenstein W.
      • Marcuse E.K.
      • Salmon D.A.
      • et al.
      Association of vaccine-related attitudes and beliefs between parents and health care providers.
      ). Smallpox is considered to be the first vaccine, dating back to the ancient Chinese, who practiced variolation (). The United States stopped routinely vaccinating against smallpox in 1972, and in 1980, the World Health Assembly declared that smallpox had been eliminated from the human population (
      World Health Organization
      The smallpox eradication programme—SEP (1966-1980).
      ). The creation of additional vaccines over the years has allowed the Advisory Committee on Immunization Practices to currently recommend vaccines that target 17 vaccine-preventable diseases (VPDs;
      Centers for Disease Control & Prevention
      Advisory Committee on Immunization Practices (ACIP).
      ,
      Centers for Disease Control & Prevention
      Vaccines and preventable diseases.
      ,
      Centers for Disease Control and Prevention
      Recommended immunization schedule for persons aged 0 through 18 years—United States, 2015.
      ).
      Healthy People 2020 is a national organization that sets 10-year goals, one of which includes increasing immunization rates to prevent infectious diseases (). Through the accomplishments of routinely vaccinating children, most vaccine-preventable diseases are rarely seen in the United States (
      • Mergler M.J.
      • Omer S.B.
      • Pan W.K.Y.
      • Navar-Boggan A.M.
      • Orenstein W.
      • Marcuse E.K.
      • Salmon D.A.
      • et al.
      Association of vaccine-related attitudes and beliefs between parents and health care providers.
      ). The success of effective immunization programs has resulted in parents who have little experience with VPDs and who question whether vaccines are necessary. The anxiety regarding vaccines among parents has lead to the creation of the term vaccine hesitancy (
      • Larson H.J.
      • Jarrett C.
      • Eckersberger E.
      • Smith D.M.D.
      • Paterson P.
      Understanding vaccine hesitancy around vaccines and vaccination from a global perspective: A systematic review of published literature, 2007–2012.
      ).
      The success of effective immunization programs has resulted in parents who have little experience with VPDs and who question whether vaccines are necessary.
      Vaccine hesitancy can lead to delaying vaccines or even exemption altogether. Currently, all U.S. states allow exemption from vaccines for medical reasons, and 48 states acknowledge exemptions for religious reasons. Nineteen states permit exemptions for personal or philosophical reasons, termed “personal belief exemptions” (
      • Imdad A.
      • Tserenpuntsag B.
      • Blog D.S.
      • Halsey N.A.
      • Easton D.E.
      • Shaw J.
      Religious exemptions for immunization and risk of pertussis in New York state, 2000-2011.
      ,
      • Diekema D.S.
      Personal belief exemptions from school vaccination requirements.
      ). Each state mandates vaccine requirements for public and private schools, as well as day care centers (). If a child does not comply with state vaccination laws and does not have an exemption, the child may not be permitted to attend the school or day care facility. Although overall immunization rates in the United States remain high, this estimate does not account for the growing concerns parents have regarding vaccines.
      The frequency of parents refusing or delaying vaccines for nonmedical reasons is increasing dramatically (
      • Atwell J.E.
      • Salmon D.A.
      Pertussis resurgence and vaccine uptake: Implications for reducing vaccine hesitancy.
      ,
      • Smith M.J.
      • Marshall G.S.
      Navigating parental vaccine hesitancy.
      ). Underimmunized children pose a threat to herd immunity and increase the risk for outbreaks of VPDs, such as measles and pertussis. Herd immunity is established when persons susceptible to a disease are protected because a sufficient proportion of the population is immunized (
      • Diekema D.S.
      Personal belief exemptions from school vaccination requirements.
      ). Establishing herd immunity varies by disease and ranges from 80% for rubella and mumps to closer to 95% for pertussis and measles. Herd immunity is especially important for children who are unable to get vaccines because of medical reasons or those too young for certain vaccines and rely on the vaccination of others to be protected (
      • Diekema D.S.
      Personal belief exemptions from school vaccination requirements.
      ).
      In the year 2014, there were 644 cases of measles in the United States (
      Centers for Disease Control & Prevention
      Measles cases and outbreaks.
      ). These outbreaks of measles are being seen in clusters of unimmunized individuals throughout the country and represent the highest number of cases seen since measles was documented as eliminated within the United States in 2000 (
      Centers for Disease Control & Prevention
      Measles—United States, January 1–May 23, 2014.
      ). Data indicate that approximately 67% of the measles cases from January through May 2014 had occurred in persons who were not immunized (
      Centers for Disease Control & Prevention
      Measles—United States, January 1–May 23, 2014.
      ). Eighty-five percent of those unimmunized persons had previously declined the measles, mumps, and rubella (MMR) vaccine for personal, philosophical, or religious reasons (
      Centers for Disease Control & Prevention
      Measles—United States, January 1–May 23, 2014.
      ). Additionally, there have already been 162 cases of measles from January 1 through April 17, 2015 (
      Centers for Disease Control & Prevention
      Measles cases and outbreaks.
      ). At the time of its report, the
      California Department of Public Health
      California department of public health confirms 59 cases of measles.
      confirmed that 34 of the 59 people diagnosed with measles had an immunization record. Of those 34 people, 28 were not vaccinated against MMR, one person had received one dose of MMR, and only five persons had fulfilled the recommendations of at least two doses of the MMR vaccine (
      California Department of Public Health
      California department of public health confirms 59 cases of measles.
      ).
      Pertussis is another reportable disease that has an increasing trend in incidence. In the year 2012 the most cases of pertussis were reported since 1955. Reporting of cases decreased the following year (
      Centers for Disease Control & Prevention
      National early season flu vaccination coverage, United States, November 2014.
      ). However, from January 1 through August 16, 2014, there were 17,325 cases of pertussis in the United States, which is an increase of 30% from the same period in 2013. Infants represent the age group with the most cases of pertussis, but the number of adolescents contracting pertussis is increasing (
      Centers for Disease Control and Prevention
      Pertussis outbreak trends.
      ).
      Influenza remains among the leading causes of death in the United States every year (HealthyPeople.gov, 2014). Only 42% of children from 6 months to 17 years of age were vaccinated with the influenza vaccine by the end of early flu season, around early November 2014 (
      Centers for Disease Control & Prevention
      National early season flu vaccination coverage, United States, November 2014.
      ). Even fewer U.S. adults 18 years and older (39.7%) received their flu vaccine by early November (
      Centers for Disease Control & Prevention
      National early season flu vaccination coverage, United States, November 2014.
      ). Efforts are needed to improve influenza vaccine coverage among both children and adults to decrease morbidity and mortality from the disease.
      Considering the recent dramatic rise in VPDs, it is important to examine the reasons for vaccine hesitancy. Fully understanding these issues will allow pediatric health care providers to address parental concerns and increase the uptake of childhood vaccines. The purpose of this article is to examine the most common concerns surrounding vaccine hesitancy and outline strategies for pediatric providers to address concerns with parents in the clinical setting.

      Common Themes

      The vaccines that are most frequently denied by parents for children include the hepatitis B, rotavirus, MMR, varicella, pneumococcal, and polio vaccines, with uptake influenza and human papillomavirus (HPV) vaccines remaining suboptimal as well (
      • Rogers C.
      Parents vaccine beliefs: A study of experiences and attitudes among parents of children in private pre-schools.
      ,
      • Staras S.A.S.
      • Vadaparampil S.T.
      • Patel R.P.
      • Shenkman E.A.
      Parent perceptions important for HPV vaccine initiation among low income adolescent girls.
      ). Common themes of parental vaccine hesitancy emerged from the literature: (a) lack of perceived need for vaccines, (b) safety of vaccines, (c) lack of trust in health care providers and government, (d) perceived lack of involvement in the decision-making process, (e) vaccines and autism, (f) immune system overload, (g) lack of adequate time and resources, and (h) religious objections to vaccines (
      • Luthy K.E.
      • Beckstrand R.L.
      • Callister L.C.
      Parental hesitation in immunizing children in Utah.
      ,
      • Rogers C.
      Parents vaccine beliefs: A study of experiences and attitudes among parents of children in private pre-schools.
      ,
      • Smith M.J.
      • Marshall G.S.
      Navigating parental vaccine hesitancy.
      ).
      Parents of both vaccinated and unvaccinated children see their children's health care provider as one of the most important sources of information regarding vaccines, followed by family (25.4%), friends (26.2%), and the news or media (13.9%;
      • Kennedy A.
      • LaVail K.
      • Nowak G.
      • Basket M.
      • Landry S.
      Confidence about vaccines in the United States: Understanding parents perceptions.
      ,
      • Mergler M.J.
      • Omer S.B.
      • Pan W.K.Y.
      • Navar-Boggan A.M.
      • Orenstein W.
      • Marcuse E.K.
      • Salmon D.A.
      • et al.
      Association of vaccine-related attitudes and beliefs between parents and health care providers.
      ,
      • Williams S.E.
      • Rothman R.L.
      • Offit P.A.
      • Schaffner W.
      • Sullivan M.
      • Edwards K.M.
      A randomized trial to increase acceptance of childhood vaccines by vaccine hesitant parents: A pilot study.
      ). Pediatric health care providers are, and can remain, a reliable and trustworthy source of information by having a better understanding of the causes for parental vaccine hesitancy.

      Lack of Perceived Need

      The success of routine immunization programs has resulted in decreased incidences of many VPDs in the United States, prompting some parents to turn their concern from the consequences of diseases to the risks of vaccines themselves (
      • Luthy K.E.
      • Beckstrand R.L.
      • Callister L.C.
      Parental hesitation in immunizing children in Utah.
      ). A recent study found that 8% of parents believed it was better for the child to get the disease naturally rather than receive an immunization for protection (
      • Rogers C.
      Parents vaccine beliefs: A study of experiences and attitudes among parents of children in private pre-schools.
      ). It is proposed that parents perform an informal risk-benefit analysis consistent with the idea of omission bias, meaning that parents perceive there is more risk in action (vaccinating) versus inaction (not vaccinating;
      • Hilton S.
      • Petticrew M.
      • Hunt K.
      ‘Combined vaccines are like a sudden onslaught to the body's immune system’: Parental concerns about vaccine ‘overload’ and ‘immune-vulnerability’.
      ). Parents no longer fear the diseases against which vaccines protect (
      • Mergler M.J.
      • Omer S.B.
      • Pan W.K.Y.
      • Navar-Boggan A.M.
      • Orenstein W.
      • Marcuse E.K.
      • Salmon D.A.
      • et al.
      Association of vaccine-related attitudes and beliefs between parents and health care providers.
      ).
      Additionally, lack of experience with VPDs may lead some parents to believe their child is not susceptible. Parents who delay or refuse vaccines are less likely than parents who vaccinate on time to believe their child might get a disease if they are not vaccinated against it (71% vs. 90%) and less likely to believe vaccines are necessary for children (70% vs. 96.2%;
      • Smith P.J.
      • Humiston S.G.
      • Dorell C.G.
      • Howes C.
      • Hibbs B.
      Parental delay or refusal of vaccine doses, childhood vaccination coverage at 24 months of age, and the health belief model.
      ). Informing parents that VPDs do still exist is imperative to avoid VPD outbreaks (
      • Smith M.J.
      • Marshall G.S.
      Navigating parental vaccine hesitancy.
      ).

      Safety of Vaccines

      The uptake of routine childhood immunizations remains suboptimal, with the safety of vaccines being one of many chief concerns. Unlike medicines, which treat diseases and conditions for sick people, vaccines are given to healthy people. Consequentially, the criteria for establishing vaccine safety must be very high before licensure is granted (
      • Smith M.J.
      • Marshall G.S.
      Navigating parental vaccine hesitancy.
      ). Pediatric providers must be prepared to inform parents that although vaccines are not 100% safe, the most common side effects are usually mild and may include a low-grade fever and pain, erythema, or swelling at the injection site (see the Table;
      • Smith M.J.
      • Marshall G.S.
      Navigating parental vaccine hesitancy.
      ). A systematic review of recent literature regarding the safety of routinely administered childhood vaccines concluded that some vaccines do have a risk of serious adverse events; however, the likelihood of these adverse events taking place is minimal (
      • Maglione M.A.
      • Das L.
      • Raaen L.
      • Smith A.
      • Chari R.
      • Newberry S.
      • Gidengil C.
      • et al.
      Safety of vaccines used for routine immunization of US children: A systematic review.
      ). Parents must weigh the risks of immunization against the sequelae of the VPDs themselves.
      TableSummary of side effects in infants, children, and adolescents for vaccines in the recommended childhood immunization schedule
      VaccineMild (common) side effectsModerate side effectsSevere (rare) side effects
      Diphtheria–tetanus–acellular pertussis (DTaP)Fever (∼1 in 4 children)

      Redness or swelling at injection site (∼1 in 4 children)

      Soreness or tenderness at site of injection (∼1 in 4 children)

      Fussiness (∼1 in 3)

      Tiredness or poor appetite (∼1 in 10)

      Vomiting (∼1 in 50)
      Seizure (∼1 in 14,000)

      Nonstop crying for 3+ hours (∼1 in 1,000)

      High fever > 105°F (∼1 in 16,000)
      Serious allergic reaction (< 1 of 1 million doses)
      Signs of a severe allergic reaction can include hives, swelling of the face and throat, difficulty breathing, a fast heartbeat, dizziness, and weakness. These signs would start a few minutes to a few hours after the vaccination.


      Others
      These side effects are so rare they have not been proven to be from the vaccine.
      : Long-term seizures, coma, or lowered consciousness, permanent brain damage
      Hepatitis BSoreness at injection site (∼1 in 4)Severe allergic reaction (1 in 1.1 million doses)
      Signs of a severe allergic reaction can include hives, swelling of the face and throat, difficulty breathing, a fast heartbeat, dizziness, and weakness. These signs would start a few minutes to a few hours after the vaccination.
      Pneumococcal conjugate 13 (PCV-13)Drowsiness (∼1 in 2)

      Temporary loss of appetite (1 in 2)

      Swelling, redness, soreness at injection site (1 in 2)

      Mild fever (< 102.2°F) (∼1 in 3)

      Fussiness (∼8 in 10)
      Fever higher than 102.2°F (∼1 in 20)Severe allergic reaction (no statistic given)
      Signs of a severe allergic reaction can include hives, swelling of the face and throat, difficulty breathing, a fast heartbeat, dizziness, and weakness. These signs would start a few minutes to a few hours after the vaccination.
      Inactivated polio (IPV)Soreness at injection site (no statistic given)
      Haemophilus influenzae type B (Hib)Redness, warmth, swelling at injection site

      Fever
      RotavirusIrritable

      Mild, temporary diarrhea or vomiting
      Intussusception within a week after first or second dose (range of ∼1 in 20,000 to 1 in 100,000 babies)
      Measles-mumps-rubella

      (MMR)
      Fever (∼1 in 6)

      Mild rash (∼1 in 20)

      Swelling of glands in cheeks or neck (∼1 in 75)
      Febrile seizures (∼1 in 75)

      Temporary pain and stiffness of joints, mostly in teenage or adult women (∼1 in 4)

      Temporary low platelet count, can cause bleeding disorder (1 in 30,000 doses)
      Severe allergic reaction (< 1 of a million doses)
      Signs of a severe allergic reaction can include hives, swelling of the face and throat, difficulty breathing, a fast heartbeat, dizziness, and weakness. These signs would start a few minutes to a few hours after the vaccination.


      Other reported: deafness, long-term seizures, coma, lowered consciousness, permanent brain damage
      VaricellaSoreness and swelling at the injection site (∼1 in 5 children, ∼1 in 3 adolescents)

      Fever (∼1 in 10)

      Mild rash, up to 1 month after vaccination (∼1 in 25)
      Febrile seizure (very rare)Pneumonia (very rare)
      Measles-mumps-rubella-varicella (MMRV)Fever (∼1 in 5)

      Mild rash (∼1 in 50)
      Febrile seizure (∼1 in 1,250 children)

      Temporary low platelet count, bleeding disorder (1 in 40,000)
      Severe allergic reaction (< 1 of a million doses)
      Signs of a severe allergic reaction can include hives, swelling of the face and throat, difficulty breathing, a fast heartbeat, dizziness, and weakness. These signs would start a few minutes to a few hours after the vaccination.


      Other reported: deafness, long-term seizures, coma, lowered consciousness, brain damage
      Hepatitis ASoreness at injection site (∼1 in 6 children)

      Headache (∼1 in 25 children)

      Loss of appetite (∼1 in 12)

      Tiredness (∼1 in 4)
      Severe allergic reaction (no statistic given)
      Signs of a severe allergic reaction can include hives, swelling of the face and throat, difficulty breathing, a fast heartbeat, dizziness, and weakness. These signs would start a few minutes to a few hours after the vaccination.
      Human papillomavirus

      (HPV)
      Pain (∼8 in 10)

      Redness or swelling at injection site (∼1 in 4)

      Mild fever (100°F) (∼1 in 10)

      Headache (∼1 in 3)
      Moderate fever (102°F) (∼1 in 65)

      Fainting (no statistic given)
      Severe allergic reaction (no statistic given)
      Signs of a severe allergic reaction can include hives, swelling of the face and throat, difficulty breathing, a fast heartbeat, dizziness, and weakness. These signs would start a few minutes to a few hours after the vaccination.
      Tetanus–diphtheria–acellular pertussis (TDaP)These side effects did not interfere with activities:

      Pain at injection site (∼3 in 4)

      Redness or swelling at injection site (∼1 in 5)

      Mild fever of 100.5°F (∼1 in 25)

      Headache (∼3-4 in 10)

      Tiredness (∼1 in 3-4)

      Nausea, vomiting, diarrhea (∼1 in 4)

      Chills, body aches, sore joints, swollen glands (uncommon)
      These side effects interfered with activities but did not require medical attention:

      Pain at injection site (∼1 in 5)

      Redness and swelling at injection site (1 in 16)

      Fever > 102°F (∼1 in 100)

      Headache (∼3 in 20)

      Nausea, vomiting, diarrhea (∼1-3 in 100)

      Swelling of the entire arm or where shot was given (∼3 in 100)
      Unable to perform usual activities; required medical attention:

      Swelling, severe pain, bleeding, and redness in the arm where shot was given (rare)

      Severe allergic reaction (< 1 in a million doses)
      Signs of a severe allergic reaction can include hives, swelling of the face and throat, difficulty breathing, a fast heartbeat, dizziness, and weakness. These signs would start a few minutes to a few hours after the vaccination.
      Meningococcal (MCV4)Redness or pain at injection site (∼1 in 2)

      Mild fever (small percentage)
      Severe allergic reaction (no statistic given)
      Signs of a severe allergic reaction can include hives, swelling of the face and throat, difficulty breathing, a fast heartbeat, dizziness, and weakness. These signs would start a few minutes to a few hours after the vaccination.
      Note. Adapted from the
      Centers for Disease Control and Prevention
      Vaccine information statements (VIS).
      .
      Signs of a severe allergic reaction can include hives, swelling of the face and throat, difficulty breathing, a fast heartbeat, dizziness, and weakness. These signs would start a few minutes to a few hours after the vaccination.
      These side effects are so rare they have not been proven to be from the vaccine.
      Reassuring parents that vaccines are safe for their children is critical for population health. Parents may want to know more about the research that has been done on vaccines, so it is essential that health care providers be knowledgeable about each vaccine. Prior to the introduction of a vaccine to the general public, extensive research and licensing by the Food and Drug Administration (FDA) is required (). The health care provider can note that the introduction of a vaccine includes requirements that are extremely comprehensive and can often extend over a period of 10 years or more.
      Even after the vaccine has been licensed and administered to the general public, it is required that both manufacturers and administrators continually monitor its safety (). Manufacturers must submit samples of each vaccine lot to the FDA before sending it to consumers. Each lot must be tested to ensure that both safety and efficacy are preserved. The FDA rarely recalls vaccine lots for reasons including mislabeling, contamination during production, and plant manufacturing problems (). Recall information of biologics, including vaccines, blood products, and medical equipment, is available to the public on the FDA Web site. In the past 5 years, there have been 66 recalls for various biologics, and only 11 have been vaccine recalls for reasons of mislabeling, contamination during production, expiration dates, and plant manufacturing problems (
      Food and Drug Administration
      Vaccines, blood, and biologics: Recalls (biologics).
      ).
      Furthermore, health care providers are required to monitor for adverse events after vaccine administration through the Vaccine Adverse Event Reporting System (VAERS). VAERS is a surveillance system, monitored and maintained by the CDC and the FDA, that serves as a warning system for possible complications associated with a vaccine (
      • Smith M.J.
      • Marshall G.S.
      Navigating parental vaccine hesitancy.
      ). Some rare side effects and delayed reactions to vaccines may not be evident during the clinical trial stages prior to introduction to the public, so the VAERS system allows the FDA to monitor for any problems (). Any time an adverse event occurs after administration of a vaccine, it should be reported to this surveillance system. However, it should not be assumed that there is a causal nexus between the adverse event and the vaccine in any occurrence. VAERS data are available to the public online by downloading raw data or utilizing the CDC WONDER online search tool (
      • Vaccine Adverse Event Reporting System
      VAERS data.
      ). This resource could be a beneficial source of information for health care providers but may not be considered an appropriate resource for all parents because of the complexity of the data and the use of medical terminology.

      Lack of Trust in Health Care Providers and the Government

      The level of trust between a parent and his or her child's health care provider affects the decisions that parents make regarding vaccines. Parents report that they trust the advice of their child's health care provider regarding topics such as nutrition, physical examination, and childhood behavior and development (
      • Glanz J.M.
      • Wagner N.M.
      • Narwaney K.J.
      • Shoup J.A.
      • McClure D.L.
      • McCormick E.V.
      • Daley M.F.
      A mixed methods study of parental vaccine decision making and parent-provider trust.
      ). However, that same level of trust in providers is not reflected in the information given about vaccines. Even when parents reported an adequate amount of time to discuss their concerns regarding vaccines with their child's health care provider, they felt as though the provider was not educated enough and that the information they received was one-sided. Parents believe that health care providers are more likely to discuss the benefits of vaccines and do not provide enough information regarding the risks (
      • Glanz J.M.
      • Wagner N.M.
      • Narwaney K.J.
      • Shoup J.A.
      • McClure D.L.
      • McCormick E.V.
      • Daley M.F.
      A mixed methods study of parental vaccine decision making and parent-provider trust.
      ).
      Parents also question whether the vaccine safety information provided by the government can be trusted (
      • Luthy K.E.
      • Beckstrand R.L.
      • Callister L.C.
      Parental hesitation in immunizing children in Utah.
      ). A general mistrust of the government and pharmaceutical companies that approve and license vaccines may lead parents to have a higher level of trust in illegitimate sources, such as the stories of other parents (
      • Smith M.J.
      • Marshall G.S.
      Navigating parental vaccine hesitancy.
      ). Because the government monitors any adverse events that occur as a result of the administration of vaccines, parents may be skeptical as to whether the government is being honest when reporting any issues (
      • Fernbach A.
      Parental rights and decision making regarding vaccinations: Ethical dilemmas for the primary care provider.
      ).
      The National Childhood Vaccine Injury Act (NCVIA) originated in 1986 and requires health care providers to distribute vaccine information sheets (VIS) to the vaccine recipient or his or her parent or legal guardian (). The CDC creates the VIS, and each one contains information about the risks and benefits of every vaccine. The NCVIA also requires health care providers to report adverse events via the VAERS reporting system. Under this act, those injured by an immunization are eligible for compensation on a “no-fault basis,” meaning that negligence does not have to be proven if an injury occurs (). Providing vaccine information to parents that is balanced by clearly explaining the risks and benefits of vaccines will encourage parents to trust their providers and the information they are being provided.

      Perceived Lack of Involvement in the Decision-Making Process

      Many parents also have concerns regarding the timing of recommended childhood vaccines as recommended by the CDC. Following a strict vaccine administration schedule can sometimes lead to parents feeling as though they are not involved in the decision-making process (
      • Luthy K.E.
      • Beckstrand R.L.
      • Callister L.C.
      Parental hesitation in immunizing children in Utah.
      ). Many parents wonder why so many vaccines are given at such a young age. The majority of childhood vaccines are given prior to 2 years of age because a child's immune system does not achieve maturity until this time. Parents may suggest participating in alternative vaccine schedules so that vaccines can be spread out by delaying or altogether refusing certain vaccines. The desire for alternative vaccine schedules allows parents to feel that their child's plan of care is more individualized rather than standardized and may alleviate any fears related to reactions for receiving too many vaccines at one time (
      • Luthy K.E.
      • Beckstrand R.L.
      • Callister L.C.
      Parental hesitation in immunizing children in Utah.
      ). However, use of alternative vaccine schedules should be avoided because it not only increases the risk for contracting VPDs but forces providers to prioritize vaccines (
      • Smith M.J.
      • Marshall G.S.
      Navigating parental vaccine hesitancy.
      ). Delaying vaccines can be risky because it prolongs the period that a child remains susceptible to infectious diseases (
      • Miller L.
      • Reynolds J.
      Autism and vaccination—The current evidence.
      ).
      Providing information prenatally or at the well-child check preceding the visit necessitating shots may improve the attitudes of parents toward vaccines.
      Parents who refuse vaccines for their children are twice as likely as parents who accept vaccines to report that they began thinking about vaccines before their child was even born (
      • Glanz J.M.
      • Wagner N.M.
      • Narwaney K.J.
      • Shoup J.A.
      • McClure D.L.
      • McCormick E.V.
      • Daley M.F.
      A mixed methods study of parental vaccine decision making and parent-provider trust.
      ). Studies have shown that many parents prefer to receive vaccine information prior to the visit when the child will actually receive the shots (
      • Williams S.E.
      • Rothman R.L.
      • Offit P.A.
      • Schaffner W.
      • Sullivan M.
      • Edwards K.M.
      A randomized trial to increase acceptance of childhood vaccines by vaccine hesitant parents: A pilot study.
      ). Providing information prenatally or at the well-child check preceding the visit necessitating shots may improve the attitudes of parents toward vaccines. Parents who have refused vaccines also report that the decision of whether to refuse a vaccine is one they are continually re-evaluating. Revisiting the topic of vaccines during every well-child visit will allow the provider to assess whether vaccine beliefs have changed and promote parental involvement when making decisions about vaccines (
      • Williams S.E.
      • Rothman R.L.
      • Offit P.A.
      • Schaffner W.
      • Sullivan M.
      • Edwards K.M.
      A randomized trial to increase acceptance of childhood vaccines by vaccine hesitant parents: A pilot study.
      ).

      Vaccines and Autism

      Autism is a developmental disorder that is usually detected in toddlers between the ages of 18 and 30 months (
      American Academy of Pediatrics
      What parents should know about the measles-mumps-rubella (MMR) vaccine and autism.
      ). Concern about vaccines causing autism arose from vaccines containing a mercury-based preservative called thimerosal that was thought to affect brain development (
      • Kuwaik G.A.
      • Roberts W.
      • Zwaigenbaum L.
      • Bryson S.
      • Smith I.M.
      • Szatmari P.
      • Brian J.
      • et al.
      Immunization uptake in younger siblings of children with autism spectrum disorder.
      ,
      • Luthy K.E.
      • Beckstrand R.L.
      • Callister L.C.
      Parental hesitation in immunizing children in Utah.
      ). Thimerosal was previously used to prevent the growth of dangerous bacteria in multidose vial vaccines (
      Food and Drug Administration
      Vaccines, blood, and biologics: Thimerosal in vaccines.
      ). In 1999, the CDC and the AAP recommended the removal of thimerosal from routinely administered childhood vaccines as an initiative to reduce children's overall exposure to mercury, which may have fueled the speculation that this preservative is not safe for children (
      Food and Drug Administration
      Vaccines, blood, and biologics: Thimerosal in vaccines.
      ,
      • Luthy K.E.
      • Beckstrand R.L.
      • Callister L.C.
      Parental hesitation in immunizing children in Utah.
      ). When thimerosal was used in vaccines, it was present in small quantities that were not shown to be harmful to the body.
      Nonetheless, preservatives are no longer needed in vaccines, because almost all are available in single-dose vials (
      • Luthy K.E.
      • Beckstrand R.L.
      • Callister L.C.
      Parental hesitation in immunizing children in Utah.
      ). The only vaccine that still contains thimerosal is the multidose vial of the influenza vaccine (
      Food and Drug Administration
      Vaccines, blood, and biologics: Thimerosal in vaccines.
      ). Because the flu vaccine must be produced in large quantities for the population, production of multidose vials is necessary, and a preservative must be used (
      Food and Drug Administration
      Vaccines, blood, and biologics: Thimerosal in vaccines.
      ). Yet, single doses of the influenza vaccine are available that are preservative free.
      The MMR vaccine is frequently under scrutiny. The belief that vaccines cause autism increased after an article was published in The Lancet in 1998 that claimed there was a direct link between the MMR vaccine and autism disorder (
      • Smith M.J.
      • Marshall G.S.
      Navigating parental vaccine hesitancy.
      ). In 2004, 10 of the 13 original authors of the paper recanted their beliefs. The article was officially retracted in 2010 when the British General Medical Council concluded that the researcher had violated the ethics of research by falsifying information and not following appropriate research protocols, which led to his medical license being revoked (
      • Kuwaik G.A.
      • Roberts W.
      • Zwaigenbaum L.
      • Bryson S.
      • Smith I.M.
      • Szatmari P.
      • Brian J.
      • et al.
      Immunization uptake in younger siblings of children with autism spectrum disorder.
      ,
      • Smith M.J.
      • Marshall G.S.
      Navigating parental vaccine hesitancy.
      ).
      The first MMR vaccine is given between the ages of 1 year and 15 months, which coincides with the time right before the peak onset of signs of autism (
      American Academy of Pediatrics
      What parents should know about the measles-mumps-rubella (MMR) vaccine and autism.
      ). The timing of vaccine administration may lead parents to believe that there is a causal relationship between the two. Additionally, parents who already have a child with autism may be even more cautious when vaccinating younger siblings with the MMR vaccine (
      • Kuwaik G.A.
      • Roberts W.
      • Zwaigenbaum L.
      • Bryson S.
      • Smith I.M.
      • Szatmari P.
      • Brian J.
      • et al.
      Immunization uptake in younger siblings of children with autism spectrum disorder.
      ). The Institute of Medicine committee did not find evidence of a relationship between the MMR vaccine and autism (Maglione et al., 2014). Furthermore, a recent study also concluded that receipt of the MMR vaccine was not associated with an increased risk of autism, regardless of whether older siblings had autism (
      • Jain A.
      • Marshall J.
      • Buikema A.
      • Bancroft T.
      • Kelly J.P.
      • Newschaffer C.J.
      Autism occurrence by MMR vaccine status among US children with older siblings with and without autism.
      ). Having a thorough understanding of the history of vaccines and current research related to autism will assist pediatric providers in offering accurate information to parents.

      Immune System Overload

      Twenty-five percent of parents across the United States believe that children receive too many vaccines and that administration of all required immunizations is not healthy (
      • Luthy K.E.
      • Beckstrand R.L.
      • Callister L.C.
      Parental hesitation in immunizing children in Utah.
      ). A recent study of parental vaccine beliefs indicated that 20% of parents agree that too many vaccines can overwhelm a child's immune system (
      • Rogers C.
      Parents vaccine beliefs: A study of experiences and attitudes among parents of children in private pre-schools.
      ). According to the recommended immunization schedule, between birth and 2 years of age, children could potentially receive up to 25 vaccines during this period, not including the influenza vaccine (
      Centers for Disease Control and Prevention
      Vaccine information statements (VIS).
      ).
      Beginning at birth, an infant is exposed to thousands of antigens at any given time, regardless of vaccine exposure (
      • DeStefano F.
      • Price C.S.
      • Weintraub E.S.
      Increasing exposure to antibody-stimulating proteins and polysaccharides in vaccines is not associated with risk of autism.
      ). When the acellular pertussis vaccine replaced whole-cell pertussis vaccine, it lowered the number of antigens the body is exposed to from about 3,000 to only about 6. Even though the current immunization schedule has grown in the number of vaccines given to children, the maximum number of antigens a child could be exposed to from vaccines by 2 years of age is 315, which is 10 times less than one dose of the previously used whole-cell pertussis vaccine (
      • DeStefano F.
      • Price C.S.
      • Weintraub E.S.
      Increasing exposure to antibody-stimulating proteins and polysaccharides in vaccines is not associated with risk of autism.
      ). Providers should reassure parents that children are capable of responding to any given number of antigens and that receipt of all necessary immunizations is not associated with long-term adverse events.
      Controversy surrounds the safety of combination vaccines, such as MMR, measles-mumps-rubella-varicella (MMRV; ProQuad) and the pentavalent vaccines, tetanus and diphtheria toxoids and acellular pertussis–hepatitis B–inactivated poliomyelitis vaccine (DTaP-Hep B-IPV; Pediarix) or DTaP-Haemophilus influenzae type B (Hib)-IPV (Pentacel;
      • Gidengil C.
      • Lieu T.A.
      • Payne K.
      • Rusinak D.
      • Messonnier M.
      • Prosser L.A.
      Parental and societal values for the risks and benefits of childhood combination vaccines.
      ). Surprisingly, parents do not seem to show the same concern regarding the DTaP vaccine, which contains three combined components of diphtheria, tetanus, and pertussis (
      • Hilton S.
      • Petticrew M.
      • Hunt K.
      ‘Combined vaccines are like a sudden onslaught to the body's immune system’: Parental concerns about vaccine ‘overload’ and ‘immune-vulnerability’.
      ). Other combined childhood vaccines include DTaP-IPV (Kinrix) and Hib-Hep B (Comvax).
      The purpose of combined vaccines is to decrease the number of injections required through the childhood immunization schedule (
      • Gidengil C.
      • Lieu T.A.
      • Payne K.
      • Rusinak D.
      • Messonnier M.
      • Prosser L.A.
      Parental and societal values for the risks and benefits of childhood combination vaccines.
      ). Many parents question whether children's immune systems are mature enough to handle the multiple antigens contained in these combination vaccines at one time (
      • Hilton S.
      • Petticrew M.
      • Hunt K.
      ‘Combined vaccines are like a sudden onslaught to the body's immune system’: Parental concerns about vaccine ‘overload’ and ‘immune-vulnerability’.
      ). The main concern is that too many antigens given all at once could overwhelm the immune system and cause long-term effects seen later in life, leading some parents to choose the route of splitting up the vaccines into individual components (
      • Gidengil C.
      • Lieu T.A.
      • Payne K.
      • Rusinak D.
      • Messonnier M.
      • Prosser L.A.
      Parental and societal values for the risks and benefits of childhood combination vaccines.
      ). Receiving all recommended vaccines during the first year of life is not shown to affect neuropsychological outcomes in children 7 to 10 years later (
      • Smith M.J.
      • Woods C.R.
      On-time vaccine receipt in the first year does not adversely affect neuropsychological outcomes.
      ). These data can reassure parents who are concerned that children receive too many immunizations too soon.
      Some parents also believe that some children have more vulnerable immune systems than others. For example, one study found that parents believed that children who frequently contract common colds, ear infections, and upper respiratory infections or who have chronic health problems such as eczema, asthma, or allergies have more fragile immune systems (
      • Hilton S.
      • Petticrew M.
      • Hunt K.
      ‘Combined vaccines are like a sudden onslaught to the body's immune system’: Parental concerns about vaccine ‘overload’ and ‘immune-vulnerability’.
      ). These parents believe that giving a combined vaccine, such as MMR, could overwhelm the child's body and lead to illness or permanent damage. Conversely, some parents believe their children are so healthy that they are not likely to benefit from vaccines at all. These parents believe that if their healthy child does contract a disease naturally, it would be beneficial and lead to the development of long-lasting immunity (
      • Hilton S.
      • Petticrew M.
      • Hunt K.
      ‘Combined vaccines are like a sudden onslaught to the body's immune system’: Parental concerns about vaccine ‘overload’ and ‘immune-vulnerability’.
      ). Although developing an infection typically induces immunity, children often experience severe sequelae of diseases, including death. In contrast, vaccines offer protective immunity without the risks associated with disease.
      The extent to which parents comply with recommended immunization regimens, which may or may not include combination vaccines, depends on how safe parents perceive the vaccines to be. Pediatric providers must be aware that not every parent who vaccinates will continue to do so. Failure to address the gaps related to parents' knowledge of the immune system or their fears related to vaccines and how they work will lead to a decline in vaccine uptake and possibly an increase in many VPDs.

      Lack of Adequate Time and Appropriate Resources

      Pressure to see patients in a limited time is leaving pediatric providers unable to spend adequate time with patients to address all of their questions. Vaccine-hesitant parents tend to be aggravated with providers rushing through appointments and leaving their questions unanswered (
      • Luthy K.E.
      • Beckstrand R.L.
      • Callister L.C.
      Parental hesitation in immunizing children in Utah.
      ). Pediatric health care providers might ensure that the registered nurses (RNs) within their office have the ability to provide education to patients, because this may better fit the workflow of many providers and is within the scope of practice of RNs. Most parents state that their children's health care provider is their main source of information (86.9%), but as appointment times are getting shorter, parents are forced to look in other places for information about vaccines, like the Internet (39.3%) (
      • Williams S.E.
      • Rothman R.L.
      • Offit P.A.
      • Schaffner W.
      • Sullivan M.
      • Edwards K.M.
      A randomized trial to increase acceptance of childhood vaccines by vaccine hesitant parents: A pilot study.
      ).
      Parents who refuse vaccines are more likely to receive information from the Internet compared with parents who are accepting of vaccines (
      • Ruiz J.B.
      • Bell R.A.
      Understanding vaccination resistance: Vaccine search term bias and the valence of retrieved information.
      ). Internet-based information can be problematic because, depending on what search criteria is used, the information may be inaccurate or biased. People often search for criteria to support already established beliefs; parents who search for risks, rather than benefits, of immunizations are likely to encounter 4.8 times more Web sites perpetuating myths and unfounded beliefs with regard to vaccines (
      • Ruiz J.B.
      • Bell R.A.
      Understanding vaccination resistance: Vaccine search term bias and the valence of retrieved information.
      ).
      To ensure that parents are accessing reliable data on the Internet, parents should be provided with a list of Web sites, and other resources, to ensure they are able to find credible and accurate information (Box) (
      • Ruiz J.B.
      • Bell R.A.
      Understanding vaccination resistance: Vaccine search term bias and the valence of retrieved information.
      ). Although the resources listed in the Box are reliable, they should be viewed as supplementary, rather than primary, to education given by the health care provider.
      Recommended resources for parents on childhood vaccines

        Phone

      • CDC-INFO Contact Center
        • Call (800) CDC-INFO or (800) 232-4636
        • The Center operates 24 hours a day, 7 days a week, in English and Spanish
        • TTY: (888) 232-6348
      Longer visits may be necessary to increase the satisfaction of patients and allow for enough time to address concerns. It has been found that providers who see a large number of patients per day were less likely to be up to date on the recommended guidelines for immunizations (
      • Kennedy A.
      • LaVail K.
      • Nowak G.
      • Basket M.
      • Landry S.
      Confidence about vaccines in the United States: Understanding parents perceptions.
      ). Even when lack of time is not an issue, health care providers may not feel comfortable discussing immunization concerns with parents if they lack the knowledge necessary to engage in these conversations (
      • Kennedy A.
      • LaVail K.
      • Nowak G.
      • Basket M.
      • Landry S.
      Confidence about vaccines in the United States: Understanding parents perceptions.
      ).

      Religious Objections

      Although they are purportedly of religious origin, most objections to vaccines are in regard to safety or personal beliefs rather than having an actual theological basis (
      • Grabenstein J.D.
      What the world's religions teach, applied to vaccines and immune globulins.
      ). However, understanding how religion can influence vaccination beliefs is important to providing education to parents. Certain vaccines have been questioned more than others within the religious community, particularly the HPV vaccine (
      • Shelton R.C.
      • Snavely A.C.
      • Jesus M.D.
      • Othus M.D.
      • Allen J.D.
      HPV vaccine decision making and acceptance: Does religion play a role?.
      ). This vaccine was the first created to prevent a specific type of cancer (
      • Fernbach A.
      Parental rights and decision making regarding vaccinations: Ethical dilemmas for the primary care provider.
      ). According to the CDC, HPV is the most common sexually transmitted infection in the United States, affecting nearly all sexually active men and women at some point during their lifetime (
      Centers for Disease Control & Prevention
      Genital HPV infection—fact sheet.
      ).
      The HPV vaccine is not always well accepted within religious communities whose beliefs strongly identify with views that prohibit premarital sex and adhere to monogamy (
      • Shelton R.C.
      • Snavely A.C.
      • Jesus M.D.
      • Othus M.D.
      • Allen J.D.
      HPV vaccine decision making and acceptance: Does religion play a role?.
      ). Because HPV is a sexually transmitted infection, parents may perceive vaccinating against it as unnecessary and even immoral. Parents belonging to religions that stress beliefs of monogamy and abstinence believe the HPV vaccine might contribute to sexual promiscuity. Yet, it has been shown in some studies that parents who identify themselves as belonging to the Christian faith reported they were highly likely to vaccinate (
      • Walhart T.
      Parents, adolescents, children and the human papillomavirus vaccine: A review.
      ). Ideally, the vaccine should be given prior to the onset of sexual activity before there is ever any risk of being exposed to HPV. Many parents believe that giving the vaccine before the age of 12 years would increase sexual promiscuity and that 15 to 17 years of age would be a more appropriate age of administration (
      • Walhart T.
      Parents, adolescents, children and the human papillomavirus vaccine: A review.
      ). This age preference stated by some parents is challenged by some studies that have found that 7% of school-age children are sexually activate before the age of 13.5 years, making early immunization essential (
      • Walhart T.
      Parents, adolescents, children and the human papillomavirus vaccine: A review.
      ). Education given to parents related to the vaccine must be sensitive to any religious views that may affect vaccine acceptance; utilizing interventions that inform parents of how the virus is transmitted without condoning sexual activity prior to marriage will ensure that the education takes concerns of sexual promiscuity into account (
      • Shelton R.C.
      • Snavely A.C.
      • Jesus M.D.
      • Othus M.D.
      • Allen J.D.
      HPV vaccine decision making and acceptance: Does religion play a role?.
      ).
      In the United States, HPV vaccine rates remain well below the Healthy People 2020 goals of 80% (
      • Staras S.A.S.
      • Vadaparampil S.T.
      • Patel R.P.
      • Shenkman E.A.
      Parent perceptions important for HPV vaccine initiation among low income adolescent girls.
      ). The completion rate for all three vaccines within the HPV series is around only 31% to 33% (
      • Staras S.A.S.
      • Vadaparampil S.T.
      • Patel R.P.
      • Shenkman E.A.
      Parent perceptions important for HPV vaccine initiation among low income adolescent girls.
      ). A parent's decision to vaccinate his or her child with the HPV vaccine relies heavily on the perception of the vaccine regarding its safety and efficacy, as well as a recommendation by the child's health care provider. In one study, provider recommendation for the vaccine resulted in two to seven times higher odds of parents agreeing that the HPV vaccine is safe, HPV vaccine side effects are not concerning, and the HPV vaccine prevents cervical cancer compared with parents who did not receive vaccine recommendations from their providers (
      • Staras S.A.S.
      • Vadaparampil S.T.
      • Patel R.P.
      • Shenkman E.A.
      Parent perceptions important for HPV vaccine initiation among low income adolescent girls.
      ). However, only 44% of parents reported receiving a recommendation for the HPV vaccine from their child's provider. Despite receiving a strong recommendation from their child's provider, parents still may not choose to initiate the HPV vaccine series if they have concerns of the vaccine's influence on sexual activity (
      • Staras S.A.S.
      • Vadaparampil S.T.
      • Patel R.P.
      • Shenkman E.A.
      Parent perceptions important for HPV vaccine initiation among low income adolescent girls.
      ).
      Some parents have voiced hesitancy about accepting the MMR vaccine because of concern that cell lines from an aborted fetus were used in a portion of the vaccine development (
      • Grabenstein J.D.
      What the world's religions teach, applied to vaccines and immune globulins.
      ). This cell line came about in 1960 when a fetus was voluntarily aborted by a mother who was infected with rubella, and cells were harvested to offer immunity to others against the virus (). Since that time, these cell lines have grown independently of the cells collected decades prior and are not the cells of the aborted fetus. If parents raise this concern, pediatric providers can inform them that no abortions were ever performed for the purpose of vaccine development, and no new cells are needed to continue rubella vaccine production today.
      Pediatric health care providers must understand the pivotal aspects of religious views toward vaccines. Working collaboratively with local religious establishments and their leaders to distribute educational materials and address concerns related to vaccines could be helpful. Providing appropriate education to resolve any objections to vaccines may increase vaccine acceptance among religious communities.

      Conclusion

      The threat to herd immunity posed by parents who continue to decline vaccines for their children can have devastating consequences on the health of the population.
      Because of the successes of standardized immunization schedules, VPDs are rarely seen in the United States, which has led to questioning by parents about whether it is necessary to immunize their children. The increasing trend of parental vaccine hesitancy has clear clinical implications for pediatric health care providers, as diseases like as measles and pertussis are making a resurgence. The threat to herd immunity posed by parents who continue to decline vaccines for their children can have devastating consequences on the health of the population. Persons with compromised immune systems or children who are too young to receive vaccines and rely on herd immunity for protection are most at risk.
      Vaccine hesitancy is a complex issue, and parents may be opposed to vaccines for numerous reasons. A major role of pediatric health care providers is health promotion and disease prevention, which includes immunization. Addressing any gaps in parents' knowledge regarding vaccines is a high public health priority. An important first step in increasing vaccine acceptance is being respectful and carefully listening to parents' concerns. Addressing the issues outlined in this article with parents may ease any anxiety the parent is experiencing regarding vaccines. Information given to parents must be balanced, clearly explaining both the risks and benefits of vaccines.
      Pediatric health care providers must consider the issues surrounding vaccine hesitancy that contribute to a parent's decision-making process. By giving parents all of the necessary information regarding vaccines and by addressing their concerns, pediatric health care providers can strengthen the parent-provider relationship by establishing trust and rapport. Even if parents still choose not to immunize their child, it is important for pediatric health care providers to continue delivering preventative care and to revisit the topic of vaccines at every visit. In doing so, providers will earn parents' trust, which may lead a parent who once declined a vaccine to choose immunization.

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      Biography

      Meagan A. Barrows, Pediatric Nurse Practitioner Student, Purdue University School of Nursing, College of Health and Human Sciences, West Lafayette, IN.
      Jennifer A. Coddington, Clinical Associate Professor, Director, Pediatric Nurse Practitioner Program, Director, Doctor of Nursing Practice Program, Director of Practice and Outreach, Co-Clinical Director, North Central Nursing Clinics, Purdue University, West Lafayette, IN.
      Elizabeth A. Richards, Assistant Professor, Purdue University, West Lafayette, IN.
      Pamela M. Aaltonen, Associate Head, School of Nursing, Associate Professor of Nursing, Purdue University, West Lafayette, IN.

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