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1 SUPPLEMENT ARTICLE Knowledge, Attitudes, and Practices Regarding Varicella Vaccination among Health Care Providers Participating in the Varicella Active Surveillance Project, Antelope Valley, California, 2005 Tina Carbajal, 1 Rachel Civen, 1 Meredith Reynolds, 2 Sandra S. Chaves, 2 and Laurene Mascola 1 1 Acute Communicable Disease Control Program, Los Angeles County Department of Public Health, Los Angeles, California; 2 National Center for Immunization and Respiratory Diseases, Division of Viral Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia Knowledge, attitudes, and practices regarding varicella vaccination and disease were assessed among health care providers participating in the Varicella Active Surveillance Project in Antelope Valley, California, in Compared with those of a similar survey conducted in 1999, results suggest a reduction in concerns about vaccine safety and efficacy. Routine assessment of adolescents for varicella susceptibility was reported by 87% of respondents, but only 42% reported routine assessment of adults. Several respondents were unaware that disease in a vaccinated person is infectious, and some did not know the vaccination recommendations pertaining to susceptible health care workers, suggesting a need for provider education on these issues. Health care providers knowledge, attitudes, and practices (KAP) regarding vaccination influence vaccine acceptance in a community and could determine how successfully vaccine recommendations are implemented [1, 2]. Acceptance of varicella vaccine among health care providers after its licensure in 1995 was not initially uniform, as evidenced by a national coverage estimate of 25.8% in 1997 for children months of age, but vaccination gradually gained acceptance, with coverage reaching 87.9% in 2005 [3, 4]. Health care providers practicing in Antelope Valley, California are surveyed periodically with regard to varicella vaccination and disease, as part of their participation in the Varicella Active Surveillance Project (VASP). Because of their participation in VASP, these providers are expected to Potential conflicts of interest: L.M. is a member of the Merck speakers bureau. All other authors report no potential conflicts. Financial support: supplement sponsorship is detailed in the Acknowledgments. Reprints or correspondence: Dr. Rachel Civen, Acute Communicable Disease Control Program, Los Angeles County Dept. of Public Health, 313 N. Figueroa St., Rm. 212, Los Angeles, CA (rciven@ph.lacounty.gov). The Journal of Infectious Diseases 2008; 197:S by the Infectious Diseases Society of America. All rights reserved /2008/19705S2-0008$15.00 DOI: / be better informed about varicella and more likely to recommend vaccination than are other health care providers. Thus, among VASP-participating providers, identification of incorrect knowledge regarding varicella disease or vaccination recommendations or concerns about vaccine safety and efficacy can be viewed as a sentinel for larger issues of misunderstanding and concern among the general population of providers. This report presents data from a 2005 KAP survey administered to VASP-participating providers practicing in Antelope Valley and, when possible, compares these results to data from a similar KAP survey in METHODS A description of VASP has been reported elsewhere [5]. All 117 health care providers, including pediatric and family physicians, physician assistants, and nurse practitioners, who worked at the 48 family and pediatric medical practices participating in VASP in 2005 (estimated to represent nearly 100% of family and pediatric medical practices in Antelope Valley) were mailed a KAP survey in September 2005; follow-up of nonrespondents was done by phone and mail. Providers were queried about their specialty (e.g., pediatric or family S66 JID 2008:197 (Suppl 2) Carbajal et al.

2 Table 1. Varicella vaccination practices: Antelope Valley, California, 1999 and Respondents answering true Survey statement No. Percentage (95% CI) No. Percentage (95% CI) Varicella vaccination is provided in my practice ( ) I recommend vaccine as part of childhood immunization schedule ( ) I recommend vaccine be given at months of age ( ) I recommend vaccine for susceptible children at any office visit ( ) ( ) I routinely assess varicella susceptibility among children!13 years of age ( ) I routinely assess varicella susceptibility among adolescents 13 years of age ( ) I recommend vaccine for susceptible adolescents 13 years of age at any office visit ( ) I routinely assess varicella susceptibility among adult patients a ( ) NOTE. A minus sign ( ) indicates that the question was not asked that year. CI, confidence interval. a Pediatricians were excluded. medicine), practice type (e.g., group or health maintenance organization), sources of information about varicella vaccination, varicella susceptibility screening, and KAP regarding varicella vaccination and disease and their perception of parents attitudes regarding varicella vaccination and disease. Most knowledge statements had a true/false format. Attitudes were queried by use of a 5-point Likert scale (strongly agree to strongly disagree), which was collapsed into 3 categories (agree, neutral, or disagree) for the analysis. Responses were excluded from the analysis if the statement was not applicable to the respondent (e.g., pediatricians were excluded from the analysis of statements regarding adult vaccination). When possible, results were compared with data from a KAP survey mailed in March 1999 to the 136 health care providers then participating in VASP, of which 53% returned surveys. Some survey statements were added, deleted, or modified between 1999 and 2005, to reflect the changing epidemiology of varicella [5], as well as the additions and modifications made to the original varicella vaccination recommendations passed by the Advisory Committee on Immunization Practices (ACIP) in 1996 [6]. Results for statements that were not phrased identically in the 2 surveys are presented only if the statements were similar enough in content for the purposes of general comparison, with phrasing differences noted in all such cases. The 2 survey samples are not independent, because several providers have participated in VASP since its inception. However, because the 1999 data set is no longer identified with particular providers, data from providers participating in both survey years could not be linked for paired analyses. Data were entered into Microsoft Access and analyzed by use of SAS statistical software (version 9.1; SAS Institute); 95% confidence intervals (CIs) were calculated for proportions, by use of the adjusted Wald method. For the 2005 data, we compared responses from providers in pediatric and family medical practices by using the x 2 test and Fisher s exact test. Because no significant differences were found, results are not presented by specialty. RESULTS Overall, 73 (62.4%) of the 117 health care providers queried returned a completed survey. Response rate varied by specialty, with 79% of pediatricians completing the survey, compared with 53% of family medical practitioners and 50% of internists. Most of the 73 respondents worked in either family (49.3%) or pediatric (46.6%) medical practices, with the remaining worked in internal medicine (4.1%). The distribution of respondents by title that is, 69.9% physicians, 21.9% nurse practitioners, and 8.2% physician assistants was nearly identical to that of the respondents in the 1999 survey. The Centers for Disease Control and Prevention was identified by the largest proportion of respondents (82.2%) as the source used for information regarding varicella vaccination, followed by medical journals (65.8%), the American Academy of Pediatrics or the American Academy of Family Physicians (AAP/AAFP) (61.6%), the health department (43.8%), the vaccine manufacturer (37.0%), and the news media (20.5%). This distribution was mostly consistent with the 1999 results, although the proportion of respondents in 1999 who reported the AAP/AAFP as an information source (73.6%) was higher than that for medical journals (62.5%). Data concerning administration of varicella vaccine and screening practices for varicella susceptibility are shown in table 1. All but 2 respondents (96.5% [95% CI, ]), both of Attitudes Regarding Varicella Vaccine JID 2008:197 (Suppl 2) S67

3 whom worked at the same practice, reported recommending vaccination by months of age. The 2 respondents who disagreed with this statement recommended that vaccination be given at months of age or at 24 months of age. In both 2005 and 1999, 91% of respondents (52 and 53, respectively) reported that they would recommend vaccination of susceptible children at any office visit. The proportion of respondents in 2005 who reported routine assessment of varicella susceptibility among children (88.5% [95% CI, ]) and adolescents (87.0% [95% CI, ]) was nearly equivalent and significantly higher than the proportion who reported routine assessment of varicella susceptibility among adult patients (42.3% [95% CI, ]). Responses to knowledge and attitude statements are presented in table 2. All but 1 respondent in 2005 correctly answered statements about vaccine storage and handling. Only 1 respondent in 2005 (1.6% [95% CI, ]), compared with 9 in 1999 (14.5% [95% CI, ]), incorrectly identified as true the statement Immunization of a person who had natural varicella is harmful. However, 27 respondents (40% [95% CI, ]) did not agree with the true statement Varicella disease in vaccinated children (i.e., breakthrough cases) is infectious, and 12 respondents (19.3% [95% CI, ]) incorrectly disagreed with the statement Health care providers without a reliable history of varicella disease should receive 2 doses of varicella vaccine, 4 8 weeks apart. Greater acceptance of the varicella vaccine and less concern about its safety and efficacy were reported (table 2): in 2005, 2 respondents (2.8% [95% CI, ]) did not perceive a need for the varicella vaccine, 3 respondents (4.3% [95% CI, ]) did not view varicella as a serious enough disease to warrant vaccination, and 5 respondents (7.1% [95% CI, ]) had concerns about the safety of the vaccine, compared with 7 respondents (10.4% [95% CI, ]), 5 respondents (7.5% [95% CI, ]), and 10 respondents (14.9% [95% CI, ]), respectively, in In 2005, almost half the respondents (32 [46.4%; 95% CI, ]) were concerned about the duration of vaccine-induced immunity, which was similar to the proportion of respondents in 1999 who expressed this concern (29 [44.6%; 95% CI, ]). Concern that the vaccination program might result in more adults getting varicella was reported by 11 respondents in both years (2005: 15.7% [95% CI, ]; 1999: 16.4% [95% CI, ]). In 2005, more respondents (17 [25%; 95% CI, ]) reported perceiving concerns about vaccine safety among parents than reported having concerns themselves (5 [7.1%; 95% CI, ]), and just over half of respondents (38 [55.1%; 95% CI, ]) felt that parents would accept a second dose of varicella vaccine for children if it was recommended by their health care provider. DISCUSSION This survey demonstrates that the varicella vaccine continues to be widely accepted among health care providers participating in VASP. Nearly all survey respondents provided varicella vaccine in their practices, routinely recommended the vaccine for susceptible children, administered the vaccine to children months of age as recommended by the ACIP [7], understood vaccine storage and handling requirements [7], and agreed that varicella is a serious enough disease to warrant vaccination. These responses are consistent with the high vaccination coverage in Los Angeles County, of which Antelope Valley is a part and which was estimated to reach 92.3% (95% CI, ) in 2005 [8]. High levels of routine assessment and vaccination of children among respondents is, in part, a reflection of California state law, which has required varicella vaccination at school entry for preschool and kindergarten children since 2001 [9]. California currently does not have varicella vaccination entry requirements for middle school, high school, or college students. In June 2006, the ACIP recommended that entry requirements for middle school, high school, and college students be added to the varicella vaccination entry requirements for child care centers and elementary schools, which are already covered by the 1999 recommendations [6]. Despite high varicella vaccination coverage and acceptance of the vaccine as part of the childhood vaccination schedule, concerns about the vaccine remain. Less than half of respondents who treat adults reported routinely assessing varicella susceptibility among their adult patients, whereas 87% routinely assess susceptibility among adolescents. With the circulation of varicella-zoster virus declining, as evidenced by a significant decline in varicella incidence [5], the screening and vaccination of susceptible adults and adolescents by health care providers will become increasingly important, since increasing age is an important risk factor for severe disease and hospitalization from varicella-related conditions and complications [10]. Results also suggest possible high levels of misunderstanding regarding the infectiousness of varicella disease in previously vaccinated patients. Health care providers who participate in VASP are expected to be better educated with regard to varicella, since they receive periodic informative reports. Similarly, it is a concern that almost 20% of the respondents surveyed did not know that health care providers without a reliable history of varicella should receive the 2-dose vaccination series [7]. Although significant decreases in varicella-associated morbidity and mortality have been well documented [5, 11], varicella outbreaks continue to occur even in settings with high vaccination coverage [12, 13]. To address this issue, the ACIP voted in June 2006 to recommend a second dose of varicella vaccine for children!13 years of age. The providers who participated in this survey did not expect a high degree of parental S68 JID 2008:197 (Suppl 2) Carbajal et al.

4 Table 2. Knowledge and attitudes regarding varicella vaccination: Antelope Valley, California, 1999 and Respondents answering true Survey statement No. Percentage (95% CI) No. Percentage (95% CI) Change, % True/false Vaccine must be stored at 15 C or colder at all times ( ) ( ) 8.9 Vaccine must be administered within 30 min of reconstitution with diluent ( ) ( ) 1.7 Immunization of a person who had natural varicella is harmful ( ) ( ) 12.9 Health care providers without a reliable history of varicella disease should receive 2 doses of varicella vaccine, 4 8 weeks apart ( ) NA 5-point Likert scale Respondents answering strongly agree or agree The vaccine is too expensive for me ( ) ( ) 12.5 The vaccine is too expensive for patients/parents ( ) ( ) 9.6 I do not perceive a need for the vaccine ( ) ( ) 7.6 Patients/parents do not perceive a need for the vaccine ( ) ( ) 0.7 Varicella is not a serious enough disease to warrant immunization ( ) ( ) 3.2 I am concerned about safety of the vaccine ( ) ( ) 7.8 Patients/parents are concerned about safety of the vaccine ( ) ( ) 11.8 I am concerned about efficacy of the vaccine ( ) ( ) 9.8 Patients/parents are concerned about efficacy of the vaccine ( ) ( ) 14.0 I am concerned about duration of immunity following vaccination ( ) ( ) 1.8 Varicella disease in vaccinated children (i.e., breakthrough cases) is infectious ( ) NA Parents of breakthrough cases are typically upset that the vaccine did not prevent their child from getting varicella ( ) NA I am concerned that vaccine virus could be transmitted to contact ( ) ( ) 8.1 I am concerned that vaccine usage might result in more adults getting varicella ( ) ( ) 0.7 I am concerned that vaccination may increase risk of zoster ( ) ( ) 7.2 If recommended by physicians, most parents would accept a second dose of varicella vaccine for healthy children ( ) NA NOTE. A minus sign ( ) indicates that the question was not asked that year. CI, confidence interval; NA, not applicable.

5 acceptance of the 2-dose regime, suggesting that successful implementation of the new recommendation may be challenging. However, this survey was conducted 1 year before the recommendation of a second dose and, therefore, should be considered exploratory. Actual acceptance and barriers to implementation of this recommendation should be assessed now that the recommendation has been made. We did not find varicella knowledge and vaccination practices to vary between pediatric and family medical practitioners, unlike a previous KAP survey of physicians in Minnesota that was conducted in 1997 [14]. This may simply reflect low statistical power for such an analysis, owing to the small sample size of our study, but also may be a result of participation in VASP. A much lower proportion of physicians (42%) in the Minnesota survey reported routinely offering the vaccine to children, and a higher proportion (86%) reported concerns about waning immunity. Some of this difference may be related to changes over time, since the Minnesota survey was conducted 2 years before the Antelope Valley survey in However, it also may reflect differences between VASP-participating providers and providers in general, with VASP-participating providers being more likely than others to screen for susceptibility and to vaccinate patients. As such, the proportion of VASP-participating providers with concerns might reflect an underestimate of the proportion of other providers with concerns. There are several limitations to these survey data. The small sample size did not provide much statistical power for the comparison analysis between survey years, as evidenced by the overlapping confidence intervals between years for the survey statements. In addition, the results of this KAP survey of VASPparticipating health care providers cannot be generalized to all health care providers, because it is reasonable to assume that participants in VASP are more knowledgeable about varicella and about vaccination recommendations. Thus, their level of incorrect knowledge probably underestimates the true level of incorrect knowledge among providers in general. In addition, survey statements regarding perceived parental concerns may not accurately reflect actual parental concerns. As varicella incidence declines, the lack of universal vaccination coverage may lead to pockets of susceptible older children and adults, owing to the absence of vaccine-induced immunity or the lack of disease exposure during childhood. It will be important to educate health care providers about the recent ACIP recommendations for routine 2-dose vaccination of children [6] and to emphasize the importance of assessing varicella immunity in adolescents and adults. Acknowledgments We thank all the health care providers who completed the surveys and the staff of the Varicella Active Surveillance Project in Antelope Valley, California, particularly Dora Railsback and Vishva Lakshman, for their assistance in collecting the data for this study. Supplement sponsorship. This article was published as part of a supplement entitled Varicella Vaccine in the United States: A Decade of Prevention and the Way Forward, sponsored by the Research Foundation for Microbial Diseases of Osaka University, GlaxoSmithKline Biologicals, the Sabin Vaccine Institute, the Centers for Disease Control and Prevention, and the March of Dimes. References 1. Mieczkowski TA, Wilson SA. Adult pneumococcal vaccination: a review of physician and patient barriers. Vaccine 2002; 20: Bovier PA, Chamot E, Bouvier Gallacchi M, et al. Importance of patients and general practitioners recommendations in understanding missed opportunities for immunization in Swiss adults. Vaccine 2001; 19: Luman ET, Ching PL, Jumaan AO, Seward JF. Uptake of varicella vaccination among young children in the United States: a success story in eliminating racial and ethnic disparities. Pediatrics 2006; 117: National Immunization Program, Centers for Disease Control and Prevention (CDC). Estimated vaccination coverage with individual vaccines and selected vaccination series among children months of age by state and immunization action plan area US, National Immunization Survey, Q1/2005-Q4/2005. Atlanta: CDC, Available at: tab02_antigen_iap&qtrpq1/2005-q4/2005. Accessed 1 October Seward JF, Watson BM, Peterson CL, et al. Varicella disease after introduction of varicella vaccine in the United States, JAMA 2002; 287: Marin M, Guris D, Chaves SS, Schmid S, Seward JF. Prevention of varicella: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep 2007; 56(RR-4):1 40. Available at: 7. Centers for Disease Control and Prevention. Prevention of varicella: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep 1996; 45(RR-11): National Immunization Program, Centers for Disease Control and Prevention (CDC). National Immunization Survey (NIS). Atlanta: CDC, Available at: age.htm#nis. Accessed 21 September Immunization Branch, California Department of Health Services. California immunization handbook: for schools and child care programs. 7th ed. Berkeley, CA: California Department of Health Services, Available at: Text.pdf. Accessed 26 September Galil K, Brown C, Lin F, Seward J. Hospitalizations for varicella in the United States, 1988 to Pediatr Infect Dis J 2002; 21: Nguyen HQ, Jumaan AO, Seward JF. Decline in mortality due to varicella after implementation of varicella vaccination in the United States. N Engl J Med 2005; 352: Lee BR, Feaver SL, Miller CA, Hedberg CW, Ehresmann KR. An elementary school outbreak of varicella attributed to vaccine failure: policy implications. J Infect Dis 2004; 190: Varicella outbreak among vaccinated children Nebraska, MMWR Morb Mortal Wkly Rep 2006; 55: Ehresmann KR, Mills WA, Loewenson PR, et al. Attitudes and practices regarding varicella vaccination among physicians in Minnesota: implications for public health and provider education. Am J Public Health 2000; 90: S70 JID 2008:197 (Suppl 2) Carbajal et al.

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