Vaccination uptake by vaccine-hesitant parents attending a specialist immunization clinic in Australia

Abstract

Vaccine hesitancy (VH) is an issue of global concern. The quality of communication between healthcare providers and parents can influence parental immunization acceptance. We aimed to describe immunization uptake following specialist immunization clinic (SIC) consultation for Australian children of VH parents as a cohort, and according to pre-clinic parental position on immunization. At a single tertiary pediatric SIC (RCH, Melbourne) a retrospective descriptive study classified VH families according to 3 proposed parental positions on immunization at initial clinic attendance. Immunization status at follow up was ascertained via the Australian Children's Immunization Register and National HPV Program Register and compared between groups. Of the VH cohort, 13/38 (34%) families were classified as hesitant, 21 (55%) as late/selective vaccinators and 4 (11%) as vaccine refusers. Mean follow up post-SIC attendance was 14.5 months. For the overall VH cohort, the majority chose selective immunization (42%) following SIC consultation. When analyzed by pre-clinic parental position on immunization, there was a trend for hesitant families to proceed with full immunization, selective families to continue selective immunization and refusing families to remain unimmunised (p < 0.0001). The most commonly omitted vaccines were hepatitis B (66%) and Haemophilus influenzae type B (55%), followed by the meningococcal C conjugate vaccine (53%) and measles, mumps and rubella vaccine (53%). Immunization outcome appears to correlate with pre-clinic parental position on immunization for the majority of families attending a SIC in Australia, with selective immunization the most common outcome. Tailored communication approaches based on parental position on immunization may optimise clinic resources and engagement of families, but require prospective research evaluation.

Introduction

Vaccine Hesitancy (VH) describes parents with varying degrees of concerns about immunization and is receiving increasing attention worldwide.^1-3 It is estimated that between 30–70% of parents in developed countries express some concerns about the safety, effectiveness and necessity of vaccines.^4,5 VH has been linked to outbreaks of vaccine preventable diseases (VPD's), predominantly measles^6,7 and pertussis,^7-10 as increasing numbers of parents choose to adopt selective immunization schedules or forgo vaccines.^11-13 In Australia, 1.61% of children in the age cohort 0 to under 7 y had a parental vaccine objection exemption recorded in March 2015.¹⁴ This figure masks a larger group of parents who fully vaccinate but experience concerns about vaccines.

Parents consistently identify their healthcare providers as the principle source of information regarding immunization.^4,15-17 Positive engagement with healthcare providers has been identified as a key step for VH parents to accept immunization.^1,18 However, with the increasing complexity of immunization schedules and with more well informed parents who have accessed multiple immunization resources of varying validity, including via the internet,^19-21 many primary care providers (PCP's) may not have sufficient time or expertise to discuss and deconstruct complex concerns expressed by parents.^3,16,22

Researchers have described 5 discernable parental positions on immunization from acceptance, through hesitancy to refusal.^23,24 This enables a broader understanding of the spectrum of vaccine acceptance on a continuum rather than viewing parents as adopting either a pro- or anti-vaccine stance. The acceptors include both those who accept all vaccines (unquestioning acceptors) and those who accept vaccines but still have some concerns (cautious acceptors). The focus of this study is the broad group of VH parents, including those who have significant concerns but give all vaccines (called ‘hesitant’ in this paper), those who delay all/most vaccines and/or adopt a selective schedule (late or selective vaccinators) and refusers, who omit all vaccines (Table 1). A framework by Leask et al also described specific goals and communication strategies for each group in an effort to tailor discussions and optimise engagement of parents in all groups.²³ One strategy involves offering parents in the hesitant, selective and refusing categories referral to a specialist immunization clinic (SIC) if their PCP cannot resolve their concerns.

Table 1.

Sub-classification of vaccine hesitancy: definitions

Parental Position	Definition
Unquestioning acceptor	Vaccinate – no specific questions
Cautious acceptor	Vaccinate despite minor concerns
Hesitant (Group 1)	Vaccinate but have significant concerns. Focused on vaccine risk. Trust in healthcare provider key High levels of vaccine knowledge
Late or selective vaccinator (Group 2)	Significant concerns about vaccination result in this group choosing to delay or select only some recommended vaccines Highest level of vaccine knowledge
Refuser (Group 3)	Refuse all vaccines. Strong and specific religious, cultural or philosophical beliefs. Lower levels of vaccine knowledge

Adapted with permission from Leask et al.^23,24

SIC's serve to assist with the diagnosis and management of adverse events following immunization; formulation of immunization plans for children and adults with chronic, complex illnesses and complex immunization catch up schedules, as well as discussions with vaccine hesitant parents.^25-29 These clinics are able to provide specialist vaccine advice and longer consultation times to comprehensively address the concerns of VH parents. PCP's are the principal referral source.^25,30

Two previous retrospective audits on immunization outcome following SIC consultation have reported high rates (>80 %) of immunization uptake in the sub-groups of VH patients attending between 1990–1992²⁸ and 2006–2007.²⁵ However, recent evidence suggesting increasing rates of vaccine exemptions,¹¹ increasing complexity of VH^13,31 and parental preference for selective or alternative schedules^12,32 led to the hypothesis that higher rates of selective immunization would be found in VH parents presenting to a SIC in Australia.

This study aimed primarily to describe vaccine uptake following specialist immunization clinic (SIC) consultation for Australian children of VH parents as a cohort, and according to pre-clinic parental position on immunization. A secondary objective was to describe the referral patterns of VH families to a tertiary hospital SIC. We hypothesized that vaccine uptake following SIC attendance would vary according to pre-clinic parental position. More specifically, we hypothesized that effective discussion with hesitant families would be more likely to result in complete vaccine uptake post SIC attendance compared with vaccine uptake in selective and refusing families, where the effect would be more modest as a result of stronger vaccination concerns.

Results

Demographics

Over the 7-month study period there were 171 new referrals, of which 162/171 (95%) families attended the SIC. The distribution of referrals is presented in Table 2. There were 48/171 (28%) referrals for VH, of which 38/48 (79%) were included in the study: 5 patients did not attend and 5 were excluded. Of the excluded children, 2 were siblings of an included referral and 3 children suffered comorbid medical conditions were excluded (2 with complex seizure disorders and one with antenatal administration of maternal immunomodulating antibody therapy). The median age for VH referrals was 11 months; 53% were male, 68% were first born and 58% were only children (Table 3). PCPs, or general practitioners, referred 74% of VH patients. Pediatricians or emergency physicians referred the remainder.

Table 2.

Indications for referral to the SIC

Referral Indication	Number (%) N = 171
Vaccine Hesitancy	48	(28%)
- attended*	38	(22.2%)
- excluded**	5	(2.9%)
- did not attend	5	(2.9%)
Prior Adverse Event Following Immunisation	84	(49%)
- attended	83	(48.5%)
- did not attend	1	(0.6%)
Pre or Post-Transplant or Post-Chemotherapy	19	(11.1%)
- attended	17	(9.9%)
- did not attend	2	(1.2%)
Immigration to Australia for Catch Up Vaccination	8	(4.5%)
- attended	7	(4.1%)
- did not attend	1	(0.6%)
Allergic to Egg	3	(1.8%)
Vaccination Allergy	3	(1.8%)
Requesting Sedation (Intellectual Disability/Needlephobia)	3	(1.8%)
Hepatitis B Non-Responder	2	(1.2%)
Asplenia	1	(1.6%)
Total Non-Attending	9	(5.3%)
Total Attending	162	(94.7%)

^*All included in the study.

^**Two children were excluded because they were siblings of an included child and 3 were excluded due to comorbid complex medical condition (2 with complex seizure disorders and one baby antenatally exposed to maternal immunomodulating antibody therapy).

Table 3.

Characteristics of vaccine hesitancy groups

	Group 1 Hesitant n = 13	Group 2 Late/Selective n = 21	Group 3 Refusing n = 4	Total n = 38
Male Gender n(%)	8 (62)	11 (52)	1 (25)	20 (53)
Median Age, months [range]	4 [1–56]	20 [3–78]	29 [5–161]	11 [1–161]
Referral Source n(%)
PCP	9 (69)	16 (76)	3 (75)	28 (74)
Pediatrician	3 (23)	4 (19)	1 (25)	8 (21)
Emergency Department	1 (8)	1 (5)	0	2 (5)
Siblings n(%)
0	8 (62)	13 (62)	1 (25)	22 (58)
1–2	4 (31)	7 (33)	0	11 (29)
3+	1 (8)	1 (5)	3 (75)	5 (13)
First Born n(%)	9 (69)	15 (71)	2 (50)	26 (68)
Prior VPD n(%)
in child	1 (8)	5 (24)	2 (50)	8 (21)
in family member	1 (8)	2 (10)	1 (25)	4 (11)
Prior AEFI in family member	6 (46)	4 (19)	2 (50)	12 (32)
Median follow up, months [range]	12 [12–17]	15 [11–18]	14.5 [13–18]	15 [11–18]
ACIR record n(%)	10 (77)	16 (76)	1 (25)	27 (71)
Phone call/PCP n(%)	3 (23)	5 (24)	3 (75)	11 (29)

PCP – Primary Care Practitioner, VPD – vaccine preventable disease, AEFI – adverse event following vaccination, ACIR – Australian Children's Immunisation Register. All results are presented as number and percentage unless otherwise stated.

Classification of VH cohort

Within the VH cohort, 13/38 (34%) of parents were classified as vaccine hesitant, 21/38 (55%) as late/selective vaccinators and 4/38 (11%) as vaccine refusers. One patient presented with a conflict between pre-clinic parental stance and past immunization history: the parents of a teenage girl developed a strong vaccine-refusing stance toward HPV immunization many years after accepting the National Immunization Program vaccines in her childhood. Given the degree of the family's opposition to further immunization we classified them as refusing despite her receipt of previous vaccines. In no other case was an expressed parental immunization plan or opinion incongruent with their classification according to preceding vaccine uptake. Two independent researchers verified all pre-clinic parental position on immunization classifications.

Parents vaccine concerns

Reasons documented for VH were concern about side effects of vaccines (22/38, 58%), concerns about links with developmental disorders, particularly autism (15/38, 39%), overloading the child's immune system (9/38, 24%), a feeling the child was too young (6/38, 16%), concern regarding vaccine ingredients (2/38, 5%), preference for complimentary therapies (2/38, 5%), a belief that vaccines were not effective (1/38, 3%) and a preference to rely on herd immunity (1/38, 3%). Vaccine uptake was obtained for 100% of children via either the Australian Children's Immunization Register (ACIR) records and National HPV Vaccination Program (HPV) Registers (27/38, 71%) or direct phone contact with parents and GP's (11/38, 29%).

Comparison of vaccine uptake between groups

After a mean follow up of 14.5 months following SIC attendance (range 11–18 months), 10/38 (26%) of the entire VH cohort (Groups 1–3) were fully vaccinated, 16/38 were (42%) were selectively vaccinated and 12/38 (31%) received no further immunizations.

Pre-clinic parental position on immunization correlated with immunization outcome at follow up (Fig. 1; p = 0 .002). The most frequent outcome for Group 1 was full immunization (7/13, 54%) with 5/13 (38%) selectively vaccinating and 1/13 (8%) remaining unimmunised. For Group 2, continuing selective immunization was most frequent outcome (11/21, 52%) with 7/21 (33%) remaining unimmunised and 3/21 (14%) being fully immunised at follow up. The small group (n = 4) of vaccine refusers (Group 3) all remained unimmunised at follow-up.

Figure 1.

Vaccination outcome in VH cohort at follow up by presenting hesitancy status.

Uptake of individual vaccines (Table 4)

Table 4.

Omission of individual vaccines at follow up by vaccine hesitant parents, according to pre-clinic hesitancy status

Vaccine Omitted	Group 1 Hesitant n = 13 (%)	Group 2 Late/Selective n = 21 (%)	Group 3 Refusing n = 4 (%)	All Groups n = 38
Diphtheria, Tetanus, Pertussis	3 (23)	13 (62)	3 (75)	19 (50)
H. influenza Type B	4 (31)	14 (67)	3 (75)	21 (55)
Hepatitis B	5 (38)	16 (76)	4 (100)	25 (66)
Polio	3 (23)	13 (62)	3 (75)	19 (50)
Pneumococcal	4 (31)	12 (57)	3/3 (100)*	19/37 (51)*
Rotavirus**	3/10 (30%)	6/8 (75)	0	9/18 (50)
Meningococcal	3 (23)	13 (62)	4 (100)	20 (53)
Varicella	0	10 (48)	2 (50)	12 (32)
Measles, Mumps, Rubella	2 (15)	15 (71)	3 (75)	20 (53)
Human Papillomavirus	0	0	1 (25)	1 (3)
Any Vaccination Omitted	6 (46)	18 (86)	4 (100)	28 (74)

^*Pneumococcal vaccines were not part of one teenage patient's National Immunisation Program Schedule, hence n = 37 for Pneumococcal calculation. Meningococcal immunisation was not on this child's primary schedule either but catch up was advised by her pediatrician and refused by the family.

^**Children too old to permit the safe administration of rotavirus vaccine (3 in Group 1, 13 in Group 2, 4 in Group 3) were excluded from the denominators of these calculations.

A vaccination was deemed ‘omitted’ if it had not been given 2 months following the 2 month, 4 month or 6 month immunisations; 3 months post the 12 month immunisations (ie. child > 15 months) and 6 months post the 18 month immunisations (ie. > 2 years) and 1 y following the 4 y old and subsequent immunisations.

The most frequently omitted vaccines prior to clinic consultation were the 2, 4 and 6-month vaccines (Table 1). More than half of all VH families omitted hepatitis B virus (HBV; 66%), Haemophilus influenzae Type B (Hib; 55%), Meningococcal C conjugate vaccine (MenCCV; 53%) and measles/mumps/rubella (MMR; 53%) at follow up. The most frequently omitted vaccines by Group 2 were HBV (76%), rotavirus (75%) and MMR (71%). Only 2/15 (13%) selective parents who omitted MMR administered MenCCV.

Prior vaccine preventable disease

A family history of prior VPD was reported by 11/38 (29%) of families. VPD's in the referred child included 3 varicella cases and 5 pertussis cases. VPD's in other family members included antenatal measles (1 case), HBV (1 case) and pertussis (2 cases) (Table 5). The outcomes for the VPD vaccine and for all vaccines, according to the pre-clinic parental position on immunization, are shown in Table 5.

Table 5.

Vaccination outcome with history of vaccine preventable disease

Family Member Affected (relationship to referred child)	VPD	Outcome for VPD Vaccine	Outcome for All Vaccines
Hesitant (Group 1) n = 13
Mother	Measles (antenatal)	Given	Selectively Immunised
Referred Child	Pertussis	Given	Fully Immunised
Late/Selective (Group 2) n = 21
Mother	Pertussis (antenatal)	Omitted	Selectively Immunised
Grandmother	Hepatitis B	Given	Selectively Immunised
Referred Child	Pertussis	Given	Fully Immunised
Referred Child	Pertussis	Omitted	Unimmunised
Referred Child	Varicella	Given	Selectively Immunised
Referred Child	Varicella	Omitted	Unimmunised
Referred Child	Pertussis	Omitted	Unimmunised
Refusing (Group 3) n = 4
Referred Child	Varicella	Seropositive (granted exemption)	Unimmunised
Referred Child and Father	Pertussis	Omitted	Unimmunised

VPD – vaccine preventable disease. Eight children presented to clinic with a history of VPD. In one family the father was also infected with the same VPD at the same time (pertussis). Three other families reported a family history of VPD. ‘Outcome for VPD Vaccine’ indicated whether the child was immunised for the illness that the child or family had suffered. ‘Outcome for All Vaccines’ indicates the primary study outcome of vaccination uptake following clinic attendance.

Site of subsequent vaccinations

The Royal Children's Hospital Immunization Drop In Center and immunization clinic provided 40/77 (52%) of post-clinic vaccinations and PCP's provided 36/77 (47%) of vaccinations.

Discussion

This is the first study to report vaccine outcomes according to a pre-clinic parental position on immunization classification system and referral patterns of VH parents attending a tertiary hospital SIC in Australia.

Source of referrals

The majority of referrals for VH families in our study came from PCP's and this is consistent with previous audits of SIC's in the United Kingdom.^25,28 Barriers to conducting immunization discussions reported by PCP's include lack of time, less detailed knowledge of current vaccine safety evidence or how to communicate risk with parents.³ In a recent US survey, significantly more primary care pediatricians than family physicians reported spending more than 10 minutes conducting vaccination discussions with families. Furthermore, over half (54%) of pediatricians reported an increased workload as a result of requests for selective vaccination schedules by parents.³³ These trends highlight the need for more specialist referral services to which PCP's can refer families with higher degrees of hesitancy, vaccination knowledge or more complex concerns or requests, such as selective vaccinations schedules. SIC's also able to provide longer appointments and vaccination facilities for these families.

Vaccination concerns

The most prevalent concerns expressed by VH parents were vaccine side effects (58%) and a possible association of vaccines with autism (40%). Vaccine safety, including serious adverse events, are repeatedly shown to be a top concern for parents^13,34,35 and the possible association between MMR and autism still lingers,³⁶ despite clear evidence to the contrary.³⁷ The observation that 52% of post clinic vaccines were given at the Immunization Drop In Center at the hospital (affiliated with the SIC and staffed by specialist pediatric nurses) may indicate that parents feel more reassured about possible adverse events in the context of a specialized immunization service.

Vaccination uptake

We found only 26% of the total VH cohort proceeded with full vaccine uptake according to the National Immunization Program Schedule, with 31% receiving no further vaccines. This finding is difficult to interpret without a comparison group of VH families who saw their PCP without SIC consultation. Low numbers of non-attending patients precluded this analysis in our study. In an audit of 358 referrals to a SIC in Essex, United Kingdom between 1990 and 1992, 13/32 (41%) of referred families attended to discuss pertussis vaccines due to “other reasons [such as] homeopathy or unexplained fear of vaccines.”²⁸ The uptake of pertussis vaccine for those whom attended the clinic to discuss pertussis vaccine concerns was higher than for non-attenders (85% vs 16%, p < 0.001).²⁸ Similarly, an audit of all consultations to a SIC in Manchester, UK between 2006–2007 reported 91.3% (20/23) of VH parents consented to immunization but actual vaccine uptake is not reported.²⁵ The low proportion of complete vaccine uptake in our study compared to these previous SIC reports may be due to definitional differences between studies, small sample sizes, differing communication styles and broader secular trends in the prevalence of parents seeking alternative immunization schedules.^11-13,32 It may equally be related to documented increases in complexity and the multi-factorial nature of vaccination concerns, which have continued to evolve.^11,13,31

Communication approaches

We found that immunization outcome at follow up varied according to parental position on immunization at initial SIC consultation. In our study, complete vaccination uptake was highest in the ‘hesitant’ group (Group 1), who represent the group with the lowest degree of hesitancy among concerned parents and those most amenable to change, compared to the selective (Group 2) and refusing (Group 3) groups.³⁸ These data suggest that communication approaches should be tailored based on the pre-clinic parental position.²³ Various communication approaches have been described in the literature but the most effective approach remains unclear. Recently, Opel et al evaluated participatory vs presumptive communication styles to address vaccine hesitancy in primary care. In a participatory consultation, the physician invites the parents to express their thoughts on vaccination using a collaborative discussion style when resistance to vaccination is encountered. With a presumptive approach, the physician declares the necessity for vaccines up front and pursues vaccination in the face of parental resistance with relatively less collaborative discussion.^23,39 This study found that presumptive communication was associated with improved intention to vaccinate but reduced parental satisfaction. ^39,40 Vaccine outcome was not measured. This study raises the question of whether PCP's elicit valid consent from parents if a predominantly presumptive communication style is used, especially as only 38% of providers elicited the parents' questions or concerns about vaccinations. Clearly, a presumptive approach needs to be studied longitudinally to ensure long-term vaccine acceptance if many parents are not voicing their concerns. Furthermore, a presumptive approach would not be appropriate in a SIC as the parents have already declared their vaccine concerns by referral to and attendance at the clinic.

A recent RCT evaluating targeted physician training for vaccine communication in primary care found that a 45 minute physician training intervention did not reduce maternal vaccine hesitancy or improve physician self efficacy over a 6-month period.⁴¹ Most of the physician training was didactic and there was no practical component or feedback, which may reduce the likelihood of changing physician behavior.⁴² This study highlights the need to target parental satisfaction, which may be more likely to be achieved through the use of a guiding communication style. This style is offered in Motivational Interviewing and is potentially appropriate for all parents on the VH spectrum.⁴³ The guiding style represents a balance between the presumptive and ‘participatory’ approaches identified by Opel et al.²³ The intent is to first ask permission to discuss a parent's concerns and then utilize active listening techniques to demonstrate to the parent an empathic understanding of the aspirations behind their point of view (in this context: maintaining the health of their child).⁴³ Rather than offering direct, paternalistic recommendations, the clinician then guides the conversation using open questions, developing discrepancies between these aspirations and the current adverse health behavior or belief (non-vaccination in this context) inducing the parent's own motivations for change.⁴³ Using this style, the physician can discuss both the vaccine and disease risks and benefits, supported by easily digestible written and online resources.^24,38,44,45 It is possible for a recommendation to vaccinate be included with such an approach.

Future research should validate the use of a guiding style in both SIC's and in primary care. The objective for all families should be to gently guide them along the continuum toward full vaccine acceptance. For selective (Group 2) and refusing (Group 3) parents, confrontational discussions incorporating “a scientific Ping-Pong” of ideas, are counter-productive and increase the risk of a backfire effect via a cognitive process known as disconfirmation.⁴⁶ The poor uptake by refusing parents in our study, albeit a small sample size, suggest that time with refusing patents should be limited and focused maintaining trust such in the hope that parents will return for review appointment.

Selective immunization schedules

The most common outcome following SIC attendance in our study was selective immunization, which has been reported before.^12,32 This is concerning as selective or delayed immunization schedules do not have an equivalent safety profile to complete immunization.^47,48 Additionally, parents who intentionally omit or delay immunizations are significantly less likely to have received all scheduled immunizations by 19 months of age leading them to be less protected.⁴⁹ The long-term impact of selective schedules on herd immunity is also unknown.⁵⁰ Thus, with more parents choosing selective vaccination, defining the safety of alternative vaccine schedules and explaining this to parents, should be a priority for health care providers. However, a recent survey of pediatricians and family physicians in the US suggested that one third of respondents acquiesced to parental requests for delayed and/or separated vaccinations in the interest of maintaining a therapeutic relationship with the family.³³ This was despite the majority of respondents acknowledging that this placed both the child and community at greater risk of harm from VPD's.³³ The combination of physicians' reported futility in dealing with these requests and the high frequency of this outcome reported in our study emphasize the need for development and training in optimal communication approaches for these discussions.

Within selective immunization schedules at our SIC, HBV (76%) and Hib (67%) vaccines were often omitted in favor of the 4-component DTPa-IPV vaccine compared to the 6-component HBV-DTPa-Hib-IPV vaccine. MMR was also frequently omitted (71%), due to the concerns regarding a perceived association between MMR and autism.³⁷ In the literature, there exists considerable variation between studies with regards to the rates of omitted antigens. International studies describe HBV,⁵¹ varicella^18,52 and MMR³² as the most frequently omitted vaccines. In our study, the unexpectedly high rates of MenCCV omission at follow up may be attributed to the scheduled co-administration with MMR vaccine. It may be that parents electing to omit MMR may have selected against this scheduled time point altogether, with MenCCV coverage suffering as a result.  A similar observation was made following the introduction of HPV vaccine in South Australia, with significantly lower HBV uptake.⁵³ The potential for poor acceptance for one vaccine to affect uptake of a co-administered vaccine in our SIC is concerning and requires ongoing research.

Vaccine preventable diseases

A history of a VPD in the child or family member, which occurred in 23% of VH families in our study, may be a strong motivator to attend our SIC. Existing literature suggests that parents of under-immunised children often perceive VPD's as low risk and low severity,^35,52 but personal experience or even anecdote of a severe VPD clearly challenges this perception and may promote vaccine acceptance.^54,55 Therefore, while vaccine uptake in our study may be considered unexpectedly low in families with prior experience of a VPD, it may have been the motivation for clinic attendance due to greater decision conflict in families who would otherwise not have the vaccine in question.⁵⁶

Potential limitations to this study include the retrospective design and small sample size. As this was a retrospective study, standardised documentation forms were not used but clinic notes and referral letters were reviewed and were available for all children. Parental concerns about vaccination were clearly documented by clinic doctors and the fact that the spectrum of concerns reported in this study correlated well with prior studies^13,34,35 advocates against documentation bias. A qualitative study exploring these parents' attitudes, beliefs and concerns regarding immunization in more detail has been undertaken and will be reported separately. Furthermore, reporting bias exists for VPD's in either the child or a family member, for which questioning and documentation was not standardised.

Assignment of pre-clinic parental position regarding immunization was clearly applicable in all but one case. One patient was classified as refusing because of strong parental opposition to HPV immunization and a HBV booster that had manifest since the earlier administration of childhood vaccines. One could argue this case could have been classified as selective but we elected assign vaccine stance at clinic presentation. The distinction between hesitant but still fully vaccinating parents and those who are more hesitant and have already started to delay or omit vaccines is representative of parents along a continuum of VH.^1,2 Although not yet formally evaluated, our preliminary investigations show that these categories resonate strongly with healthcare providers and parents alike.⁵⁷ However, perhaps allocation of parental position could be more objectively measured with the prospective use of a validated survey such as Opel et al's Parental Attitudes about Childhood Vaccines (PACV) survey at initial clinic attendance.⁵⁸

Lastly, we studied families who were motivated to seek specialist immunization advice and thus may have higher degrees of hesitancy than the diverse population of VH parents who seek vaccine advice in primary care. Future research will aim to compare VH parents who attend a hospital-based SIC with a control group of VH parents who attend their PCP in the community to discuss their vaccine concerns and the difference in vaccine uptake.

In response to these findings, our SIC pediatricians are limiting the offer of review appointments to hesitant or selective parents. Every attempt is made to schedule appointments at time points when parents have specific questions that coincide with the National Immunization Program (eg MMR vaccine around 12 months). Effective communication strategies continue to be discussed at post-SIC meetings with all the pediatricians and we are developing targeted, easy-to-read immunization resources addressing both the general and specific immunization concerns encountered.

Conclusion

Vaccine hesitancy exists on a continuum and patients with lesser degrees of hesitancy are more likely accept full vaccine uptake post by SIC consultation than selective or refusing families. Furthermore, selective vaccination following SIC consultation for VH families is common and parents need to be aware that equivalent safety of selective schedules cannot be guaranteed. Tailored communication approaches for vaccine discussions with vaccine hesitant and selective families should use a collaborative, guiding style and aim to stimulate a change in beliefs toward vaccine acceptance while addressing specific concerns with appropriate resources.

Methods

Study design

A retrospective descriptive study of new referrals for VH to a specialist immunization clinic between June 2012 and January 2013 was performed. The primary outcome was immunization status at follow up, classified as completely vaccinated, selectively vaccinated or unvaccinated.

Study setting

Parents were seen at the The Royal Children's Hospital in Melbourne, Australia. This tertiary immunization clinic was established in 1997 and sees over 400 new referrals each year, divided into 4 main categories:

1. children requiring evaluation following the report of an adverse events following immunization to the state based vaccine safety service (https://www.saefvic.org.au/)

2. immigrated children for catch up immunization,

3. children with special risk medication conditions (transplantation, post-chemotherapy) and

4. vaccine hesitancy.

The SIC is a publicly funded clinic staffed by 5 consultant pediatricians. Three of the pediatricians have PhDs and focus almost exclusively on immunization research, including vaccine safety, clinical trials, vaccine epidemiology and social science research on vaccine hesitancy. The other 2 pediatricians have over 10 y of specialist clinical immunization experience. All cases are discussed at a weekly post-clinic meeting to help ensure consistency of medical advice.

If special risk vaccines are indicated, such as the quadrivalent conjugate meningococcal vaccine, families may purchase the vaccines from the hospital pharmacy and have them administered by immunization nursing staff in the hospital immunization drop in center. Most states in Australia have SICs²⁷ and where not available, patients are directed to seek advice from a nominated pediatrician or infectious diseases specialist who will review families who have concerns regarding immunizations, especially following an adverse event.

The pediatrician spends 30 minutes with a family for an initial consultation and 15 minutes for review appointments. During a consultation, the pediatrician attempts to understand the parents' main vaccine concerns and to address these specifically with balanced information on the risks of the diseases for their child at their age and the risks of the vaccines. General vaccine concerns, such as too many vaccines overwhelming the immune system, and vaccine specific concerns, such as diarrhea after rotavirus vaccines or the potential association of MMR and autism, are also addressed. Conversations are supported by resources including Australian disease surveillance data from the national Notifiable Disease Surveillance Database, facts sheets, decision aids, videos and websites.⁵⁹ Follow up consultation is offered if necessary.

Data collection

New referrals during the study period were identified from clinic lists generated by the electronic hospital administration system. Manual review of all referral letters, consultation notes and dictated letters identified VH families. Children with complex medical problems giving rise to reasonable medical concern regarding immunization (eg. epilepsy, immunosuppression) were excluded. If more than one child from the same family was referred, only the first listed child was included to avoid skewing the data by that family's outcome. Clinical data collection included: demographics, referral source, clinician seen, prior history of VPD in the referred patient or family, immunization concern(s) and catch up immunizations advised/required.

Prior to outcome assessment, 2 researchers independently classified VH families into 3 groups according to the definitions published by Leask et al^23,24 The ‘hesitant' group (Group 1) was defined as ‘parents who vaccinate their child but have significant concerns', thus children were only included in this group if no vaccines were deemed omitted (see definition below) according to the Australian National Immunization Program schedule for their age prior to clinic attendance. The late or selective group (Group 2) were defined as ‘choosing to delay all vaccines or select only some recommended vaccines', thus children who were only partially vaccinated at clinic attendance were included in this group, as well as those unvaccinated children where the parent clearly described an intention to administer delayed immunizations. The vaccine refusing group (Group 3) was defined as ‘refusing all vaccines for their child', and thus included only children who had received no scheduled vaccines at clinic attendance as well as those who presented expressing a clear philosophical, religious or other intention to exclude all immunizations.

The ACIR/HPV Register provided data on vaccine uptake pre- and post- clinic attendance for all recorded vaccines. The RCH Immunization Clinic have approval to access for the ACIR data for all patients as part of routine clinical care to validate immunization status and crosscheck with the child health record. ACIR was also used to confirm immunization status following the clinic appointment to document the outcomes of the clinical interaction and location of vaccine administration. Where ACIR records were unavailable, parents were contacted and immunization history was obtained from them (if unimmunised), or their General Practitioner (if immunizations given) with parental consent.

Outcome was classified as follows: families who gave all advised routine or catch up immunizations after SIC attendance were classified as ‘Fully Immunised’ families who gave some but not all immunizations were classified as ‘Selectively Immunised' and families who gave no further immunizations were classified ‘Unimmunised'. An immunization was deemed ‘omitted' if it had not been given 2 months following the 2 month, 4 month or 6 month immunizations; 3 months following the 12 month immunizations (ie. child > 15 months); 6 months following the 18 month immunizations (ie. > 2 years) and 1 y following the 4 y old and subsequent immunizations. These intentionally generous definitions of ‘omission' permitted a greater delay beyond the scheduled immunization time point than the more generally accepted 4-weeks. This allowed more accurate classification of parents based on intent to vaccinate into the hesitant or selective groups by allowing a greater margin for receipt of the vaccines. The birth HBV immunization is not routinely recorded on the ACIR register and was therefore omitted from the expected schedule for the purposes of the study.

Statistics

All statistics were performed using Prism v6.0f (Graphpad Software Inc., 2014). Outcomes were expressed as proportions with 95% confidence intervals. The Chi squared test was used to compare the distribution of outcomes between groups. The null hypothesis was rejected when p < 0.05.

Disclosure of Potential Conflicts of Interest

No potential conflicts of interest were disclosed.

Ethics

All information collected was de-identified. The study protocol was approved by the Hospital Research and Ethics Committee at The Royal Children's Hospital in Melbourne.

Supplemental Material

Supplemental data for this article can be accessed on the publisher's website.

Funding

The study was funded by the Victorian Department of Health – Immunization Section.