Barriers to early uptake of tetanus, diphtheria and acellular pertussis vaccine (Tdap) among adults—United States, 2005–2007

Vaccine 29 (2011) 3850–3856

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Barriers to early uptake of tetanus, diphtheria and acellular pertussis vaccine (Tdap) among adults—United States, 2005–2007 Brady L. Miller a,∗ , Katrina Kretsinger b , Gary L. Euler a , Peng-Jun Lu a , Faruque Ahmed a a b

Immunization Services Division, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention, Atlanta, GA, USA Global Immunization Division, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention, Atlanta, GA, USA

a r t i c l e

i n f o

Article history: Received 27 January 2011 Received in revised form 3 March 2011 Accepted 17 March 2011 Available online 1 April 2011 Keywords: Immunization Vaccine Adult Pertussis Tdap

a b s t r a c t Background: The tetanus, diphtheria and acellular pertussis vaccine (Tdap) was recommended by the Advisory Committee on Immunization Practices (ACIP) for U.S. adults in 2005. Our objective was to identify barriers to early uptake of Tdap among adult populations. Methods: The 2007 National Immunization Survey (NIS)-Adult was a telephone survey sponsored by the Centers for Disease Control and Prevention (CDC). Immunization information was collected for persons aged ≥18 years on all ACIP-recommended vaccines. A weighted analysis accounted for the complex survey design and non-response. Results: Overall, 3.6% of adults aged 18–64 years reported receipt of a Tdap vaccination. Of unvaccinated respondents, 18.8% had heard of Tdap, of which 9.4% reported that a healthcare provider had recommended it. A low perceived risk of contracting pertussis was the single most common reason for either not vaccinating with Tdap or being unwilling to do so (44.7%). Most unvaccinated respondents (81.8%) indicated a willingness to receive Tdap if it was recommended by a provider. Conclusions: During the first two years of availability, Tdap uptake was likely inhibited by a low collective awareness of Tdap and a low perceived risk of contracting pertussis among U.S. adults, as well as a paucity of provider-to-patient vaccination recommendations. Significant potential exists for improved coverage, as many adults were receptive to vaccination. Published by Elsevier Ltd.

1. Introduction Although a vaccine affording protection against pertussis has been available to children for over 60 years in the United States, pertussis is not exclusively a childhood disease [1–4]. Adults (≥18 years of age) and adolescents aged 10–17 years may become susceptible to pertussis due to waning immunity from childhood vaccinations; collectively, they comprised 50.1% of 13,278 reported U.S. cases in 2008 [2–5]. While persons ≥10 years of age account for a greater number of cases, the age-specific annual incidence of pertussis, as well as mortality from pertussis, is most burdensome on infants. Infants represented 92% of reported U.S. pertussis deaths during 2000–2004 [4]. Potential protection against pertussis is not maximized until the primary, three-dose vaccination series is complete at approximately 6 months of age [6]. Adults and adolescents in close contact with an infant during this time are a potential transmission source of pertussis [7].

∗ Corresponding author at: Centers for Disease Control and Prevention, 1600 Clifton Road, MS E-52, Atlanta, GA 30333, USA. Tel.: +1 404 639 8806; fax: +1 404 639 8615. E-mail address: [email protected] (B.L. Miller). 0264-410X/$ – see front matter. Published by Elsevier Ltd. doi:10.1016/j.vaccine.2011.03.058

To protect adolescents and adults against pertussis, as well as to prevent transmission of pertussis to susceptible populations, the Advisory Committee on Immunization Practices (ACIP) of the Centers for Disease Control and Prevention (CDC) recommended the newly licensed tetanus, diphtheria, and acellular pertussis vaccine (Tdap) in 2005 as a one-time replacement for the decennial tetanus diphtheria (Td) booster dose, for persons aged 10–64 years [8]. For some populations (e.g., adults with infant contact, healthcare personnel [HCP]) and circumstances (e.g., outbreaks), the suggested interval between the most recent tetanus vaccination and Tdap was ≥2 years.1 High Tdap vaccination coverage among U.S. adolescents and adults has the potential to ameliorate the national pertussis burden among persons of all ages [9–12], especially infants [13,14]. Significant benefits exist for healthcare settings as well. Vaccinating HCP against pertussis can be a cost-effective strategy to prevent outbreaks [15–18].

1 ACIP voted to remove this suggested interval on October 27, 2010. Tdap can now be administered regardless of the interval since the last tetanus vaccination. The recommendation was also expanded to include persons ≥65 years of age that have or anticipate having contact with infants less than 12 months of age [23].

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Fig. 1. Timeline of adult Tdap licensure, availability and ACIP recommendation status, in relation to data collection period—United States, 2005–2008. Tdap was licensed by the U.S. Food and Drug Administration on June 10, 2005, and recommended for adults aged 19–64 yrs by the ACIP on October 26, 2005. From this date, and until the ACIP recommendation was approved by the CDC Director and subsequently published in MMWR in December 2006, it remained provisional. Beginning December 2006, the ACIP recommendation was considered official. During May through August of 2007, NIS-Adult survey interviews were conducted. Tdap: tetanus, diphtheria, acellular pertussis vaccine; ACIP: Advisory Committee on Immunization Practices; MMWR: Morbidity and Mortality Weekly Report; CDC: Centers for Disease Control and Prevention; NIS: National Immunization Survey.

To date, these potential benefits have been unrealized. Through 2009, approximately four years after Tdap was first available, estimated vaccination coverage among U.S. adults aged 19–64 years reached just 6.6% [19]. By comparison, 55.6% of adolescents aged 13–17 years were vaccinated at approximately the same time [20]. Despite evidence that some healthcare providers serving adolescent populations are using Tdap in favor of Td [21], little is known about factors influencing Tdap vaccination among U.S. adult populations. We used data from the 2007 National Immunization Survey (NIS)-Adult to identify potential barriers to Tdap uptake among adults aged 18–64 years, during the first two years of vaccine availability. 2. Methods 2.1. National Immunization Survey (NIS)-Adult description The NIS-Adult was a one-time, ad-hoc telephone-based survey that was fielded in 2007 and funded by the Centers for Disease Control and Prevention (CDC). Immunization information, including awareness of and attitudes toward vaccines, was collected for

persons aged ≥18 years on all vaccines recommended by ACIP, including those protecting against tetanus, diphtheria, and pertussis (Td and Tdap). Interviews took place during May–August 2007, approximately two years after Tdap was licensed in June 2005 (Figs. 1 and 2), and used methods similar to that of a previous survey version [22]. Two lists were used to generate the NIS-Adult sample of telephone numbers: the National Health Interview Survey (NHIS) list of telephone numbers that included basic demographic information; and a Survey Sampling International (SSI) list of age-targeted telephone numbers. Provided age and race/ethnicity information was not missing, all telephone numbers from the NHIS sample were included in the NIS-Adult sampling frame. Additional telephone numbers were selected from the SSI list with equal probability to achieve the required sample size for a specified age by racial/ethnic strata. One person was randomly selected per household, and telephone interviews were administrated in English or Spanish. The Council of American Survey Research Organization (CASRO) standardized, overall response rate was 31%. This rate is the product of the telephone number resolution rate (64.4%), the screening completion rate (63.9%), and the interview completion rate (74.2%).

Fig. 2. Conditional branching of NIS-Adult questions on factors associated with Tdap uptake. All survey respondents aged 18–64 years who did not report receiving a Tdap vaccination were asked the above (paraphrased) questions. Verbatim questions are as follows: Q1. Before today, had you ever heard of the new tetanus–diphtheria–pertussis vaccine? Q2. Has a doctor or other health professional ever recommended that you get Tdap or pertussis shot? Q3. Would you get Tdap (which has the whooping cough vaccine) instead of Td (without the whooping cough vaccine) if your doctor or health professional recommended it? Q4. What is the main reason you [would not receive Tdap shot/did not get a Tdap shot when it was recommended]? For the purposes of branching, responses other than those shown above (e.g., missing, DON’T KNOW) were treated as NO. Tdap: tetanus, diphtheria, acellular pertussis vaccine; NIS: National Immunization Survey.

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Table 1 Self-reported tetanus, diphtheria, acellular pertussis (Tdap) vaccination coverage among adults aged 18–64 years—United States, 2007. Characteristic

Sample, no.a

Total 3,217 Age 18–49 1,502 50–64 1,715 Sex Male 1,204 Female 2,013 Race/ethnicity Non-Hispanic white 1,221 Non-Hispanic black 838 Hispanic 853 Region Northeast 468 Midwest 692 South 1,295 West 752 Poverty At or above 200% 1,931 Below 200% 875 Education College level or above 1,961 High school level or below 1,240 Saw healthcare provider, past 12 mo. Yes 2,437 No 779 Medical insurance Yes 2,552 No 500 Influenza vaccination, past influenza season Yes 1,050 No 2,143 Persons with regular, close infant (<12 mo.) contact Yes 588 No 2,627 Healthcare personnel Yes 420 No 2,796

%b

Vaccination coveragec % (95% CI)

Pd

100.0

3.6 (2.7–4.7)

72.2 27.8

3.6 (2.6–5.1) 3.4 (2.4–4.9)

0.84

49.3 50.7

3.6 (2.4–5.4) 3.6 (2.5–5.2)

0.99

71.1 13.5 15.4

2.9 (2.0–4.1) 6.7 (3.3–13.1)e 2.4 (1.4–4.1)

0.11

18.5 22.4 36.1 23.0

3.2 (1.7–5.9) 2.6 (1.3–5.0) 3.7 (2.3–5.7) 4.7 (2.9–7.4)

0.59

70.4 29.6

3.3 (2.4–4.7) 4.4 (2.5–7.5)e

0.43

56.2 43.8

4.5 (3.3–6.1) 2.4 (1.4–4.1)

0.04

72.2 27.8

4.1 (3.1–5.5) 2.2 (1.0–4.6)

0.06

83.9 16.1

3.5 (2.6–4.8) 3.7 (1.8–7.6)e

0.93

30.1 69.9

6.1 (4.3–8.9) 2.5 (1.6–3.9)

< 0.01

21.0 79.0

4.5 (2.6–7.5) 3.4 (2.4–4.6)

0.41

12.0 88.0

6.1 (3.6–10.4) 3.2 (2.4–4.4)

0.10

CI: confidence interval. a Unweighted sample sizes (no.). The subgroups might not total 3217 because of missing data. b Weighted proportion. c Estimates and confidence intervals are weighted proportions. d P determined at the ˛ = 0.05 level by Wald F test (two-tailed). e Estimate may be unreliable. Relative standard error is >0.30 of the estimate.

2.2. Descriptive characteristics Survey responses were stratified by levels of demographic, socioeconomic and access to care characteristics. Age group (18–49, 50–64), sex (male or female), race/ethnicity (non-Hispanic white, non-Hispanic black, Hispanic), U.S. census region (Northeast, Midwest, South, West), poverty (below 200% of the federal poverty level or at/above), education (high school education or less or college level or above), seeing a healthcare provider during the previous 12 months (yes or no), influenza vaccination during the previous influenza season (yes or no), regular and close contact with an infant aged <12 months (yes or no), and current employment in a healthcare setting (yes or no) were all considered. Medical insurance status (yes or no) was determined by coverage with one of the following: Medicare, Medicaid, Indian Health Service, any private insurance, military insurance, or any other medical insurance plan. 2.3. Data analysis Two separate analyses were performed: one estimated Tdap vaccination coverage, while the other described potential barriers to vaccination. Because Tdap was recommended for adults aged 18–64 years at the time of the survey (Tdap is now also recommended for adults ≥65 who have or anticipate having close contact

with an infant) [23], only respondents aged 18–64 years were considered for both analyses. Prior to any questions related to tetanus, diphtheria or pertussis vaccination, respondents were given the following background information: “There have been two types of tetanus shots available for adults since June 2005. One is the Td or tetanus–diphtheria vaccine and the other is called Tdap or AdacelTM . They are similar except the Tdap shot also includes a pertussis or whooping cough vaccine.” Tdap vaccination coverage was estimated by using responses to the questions, “Approximately how many years ago did you receive your most recent tetanus shot?”, and “Did your healthcare provider tell you your most recent tetanus vaccination included a pertussis or whooping cough component?” Respondents were excluded from this analysis if they met one of the following criteria: (1) did not know the approximate date (yrs) of their most recent tetanus vaccination, (2) had received a tetanus vaccination during 2005–2007 but the doctor didn’t say whether the vaccine was Td or Tdap, or (3) had received a tetanus vaccination during 2005–2007 but could not recall the vaccine type. The remaining sample represented those for whom Tdap uptake could be assessed. The proportion who reported receiving Tdap represents the estimated vaccination coverage. The objective of the second analysis was to describe potential barriers to vaccination. Questions of interest came after those used to estimate Tdap vaccination coverage (Table 2). A separate

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Table 2 Awareness of tetanus, diphtheria, acellular pertussis vaccine (Tdap), prevalence of provider-to-patient recommendation, and relationship of provider recommendation with intent to receive Tdap, among unvaccinated adults aged 18–64 years—United States, 2007. Characteristic

Have you ever heard of the tetanus, diphtheria, acellular pertussis vaccine?a (n = 3558) %b YES

Total 18.8 Age 18–49 19.1 50–64 18.0 Sex Male 12.6c Female 24.9 Race/ethnicity Non-Hispanic white 20.8c Non-Hispanic black 13.5 Hispanic 14.2 Region Northeast 21.2 Midwest 20.9 South 17.8 West 16.3 Poverty At or above 200% 19.3 Below 200% 17.8 Education College level or above 23.4c High school level or below 12.8 Saw healthcare provider, past 12 mo. Yes 19.2 No 17.8 Medical insurance Insurance 20.0c No insurance 14.0 Influenza vaccination, past influenza season Yes 24.1c No 15.1 Persons with regular, close infant (<12 mo.) contact Yes 22.7 No 17.8 Healthcare personnel Yes 38.8c No 16.2 a b c

Has a provider recommended that you get Tdap [past 2 years]?a (n = 651) %b YES

Would you get Tdap instead of Td if your provider recommended it?a (n = 3172) %b YES

9.4

81.8

11.2c 4.4

82.6 79.5

14.3 7.1

83.1 80.5

8.7 10.2 16.6

82.6c 75.8 86.2

15.3 6.9 6.3 12.7

79.6 82.9 84.2 78.5

10.5 9.9

83.8 79.4

9.6 9.3

80.9 83.1

10.1 7.8

82.5 79.9

10.1 5.4

83.0 81.7

7.8 13.7

87.1c 83.8

7.0 10.3

87.0c 80.4

15.4 7.5

80.5 81.9

Responses other than YES/NO (e.g., missing) are excluded. Weighted proportion. P < 0.05 (determined by Wald F test, two-tailed). Responses other than YES/NO (e.g., missing, DON’T KNOW) are excluded.

sample of participants aged 18–64 years was considered; only those who did not report receiving Tdap during 2005–2007 (i.e., unvaccinated) were included. When calculating the proportion of participants who answered each question affirmatively, responses other than YES/NO (e.g., missing, DON’T KNOW) for that question were excluded. Verbatim responses to open-ended questions were classified into nominal categories by at least two CDC staff members. Some open-ended responses revealed respondents that had been previously vaccinated with Tdap (n = 33). For these persons, responses to questions used to estimate Tdap vaccination coverage were changed to reflect this. SUDAAN (Software for the statistical analysis of complex sampling data, Research Triangle Institute, Research Triangle Park, NC) was used to generate point estimates and 95% confidence intervals for both analyses, and accounted for the complexity of the NISAdult sampling frame. The analyses utilized weighted data to reflect age and race/ethnicity of the U.S. civilian, non-institutionalized population. Weights were adjusted for non-response, more than one telephone line, and non-coverage of persons in non-landline telephone households. Wald F tests were used to assess associations across levels of demographic, socioeconomic and access to care characteristics, with the significance level set at ˛ = 0.05 (twotailed).

3. Results 3.1. Tdap vaccination coverage Of 7055 NIS-Adult participants, 3866 were aged 18–64 years. After excluding those without a YES/NO response on time (yrs) since most recent tetanus vaccination (n = 360 [9.3%]) and Tdap status during 2005–2007 (doctor didn’t say, n = 124 [3.2%]; don’t know, n = 165 [4.3%]), 3217 respondents remained. Overall, 3.6% (95% confidence interval [CI] = 2.7–4.7%) reported receipt of a Tdap vaccination at the time of the survey (Table 1). There were modest differences in vaccination coverage by a number of descriptive characteristics. Those who possessed at least a college level education (4.5% vs. 2.4%, P = 0.04), and those who received a recent influenza vaccination (6.1% vs. 2.5%, P < 0.01) were more likely to report receiving Tdap. 3.2. Potential barriers to Tdap uptake Of 3866 participants aged 18–64 years, 110 reported receiving Tdap during 2005–2007 and were excluded from further analysis. Those without YES/NO responses were also excluded prior to analysis for each of the following questions: Ever heard of Tdap? (n = 198

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Table 3 Main reasona for not receiving Tdap, among unvaccinated adults aged 18–64 years who were unwilling to receive Tdap even if recommended by a healthcare provider, or did not receive Tdap despite receiving a provider recommendation—United States, 2007. Main reason

Low perceived risk of contracting pertussis Low perceived risk of transmitting pertussis to susceptible contacts Fear of needles Distrust of vaccines Too many vaccine components Perceived side effects Tdap was not recommendede Cost Would need more information to make a decision to vaccinate Otherf a b c d e f

Total

Persons with close infant (<12 mo.) contactb

Healthcare personnelc

(%d ), n = 474

Yes (%d ), n = 82

No (%d ), n = 392

Yes (%d ), n = 86

No (%d ), n = 388

44.7 0.0

33.6 0.0

46.7 0.0

30.7 0.0

47.7 0.0

7.2 6.0 2.4 5.4 3.5 4.0 11.0

3.0 8.0 0.0 10.5 7.1 0.0 21.3

8.0 5.6 2.8 4.4 2.8 4.7 9.2

3.5 5.7 1.0 4.7 8.5 10.7 12.2

8.0 6.0 2.7 5.5 2.4 2.6 11.0

15.6

16.5

15.8

23.0

14.1

Respondents were asked to cite one main reason only. Distribution of responses among persons with and without infant contact was not statistically different (P = 0.22). Distribution of responses among persons classified as healthcare personnel and those who were not was not statistically different (P = 0.54). Weighted proportion. May suggest respondent did not understand the question. Includes following responses: did not want one, have a medical contraindication, don’t know, and those unable to be categorized.

of 3,756 [5.3%]), Healthcare provider ever recommend Tdap? (n = 25 of 676 [3.7%]), Willing to receive Tdap if recommended? (n = 528 of 3,700 [14.3%]). Indecipherable responses to the question, “What is the main reason you [did/would] not receive Tdap [when/if] recommended” (n = 145 of 619 [23.4%]) were also excluded. Among unvaccinated respondents (n = 3558), just 18.8% had ever heard of Tdap (Table 2). Females (24.9% vs. 12.6%), nonHispanic whites (20.8% vs. 13.5% [non-Hispanic, blacks], 14.2% [Hispanics]), persons with at least a college level education (23.4% vs. 12.8%), persons with medical insurance (20.0% vs. 14.0%), persons who received a recent influenza vaccination (24.1% vs. 15.1%), and healthcare personnel (38.8% vs. 16.2%) were all more likely to have heard of Tdap. Of those having heard of Tdap (n = 651), 9.4% reported that it had been recommended by a healthcare provider. The majority of unvaccinated respondents asked were willing to be vaccinated with Tdap if it was recommended by a healthcare provider (81.8% of 3172). Non-Hispanic blacks (75.8%) were significantly less likely to report this than non-Hispanic whites (82.6%) and Hispanics (86.2%). Persons who reported receipt of a recent influenza vaccination (87.1% vs. 83.8%) and persons in regular and close contact with an infant (87.0% vs. 80.4%) were also more likely to express a willingness to be vaccinated. The most commonly cited single main reason for being unwilling to receive Tdap was a low perceived risk of contracting pertussis (44.7% of 474) (Table 3). The second most common main reason was that the respondent did not have enough information to make a decision (11.0%). Fear of needles (7.2%), distrust of vaccines (6.0%) and perceived side effects (5.4%) were less commonly cited. No respondent cited a low perceived risk of transmitting pertussis to susceptible contacts. Main reasons stated for participants with regular and close infant contact and those employed in a healthcare setting were similar to main reasons stated by the total sample. 4. Discussion Although Tdap uptake is monitored annually [19], to our knowledge, the NIS-Adult is the only source of data that is both nationally representative and informative of U.S. adults’ awareness of and attitudes toward pertussis vaccination. The first pertussis vaccine available to adults, Tdap, was licensed in June of 2005 and recommended by ACIP in October of 2005. ACIP recommendations are considered provisional and available online until approval by the CDC director and subsequent publication in Morbidity and Mortal-

ity Weekly Report (MMWR) [24]. Survey interviews were conducted approximately 6 months after the adult Tdap recommendation was published—two years after Tdap was licensed. Previously published NIS-Adult results show that just 57.2% of adults aged 18–64 years had received a decennial tetanus vaccination in 2007; at this time, Tdap accounted for just 20.7% of total tetanus vaccinations since 2005 [25]. Not surprisingly, we estimated that Tdap vaccination coverage was low (3.6%) at the time of the survey. However, uptake of other newly licensed vaccines included in NIS-Adult was not necessarily restricted by proximity of survey interviews to publication date of their respective ACIP recommendations. Approximately 10% of women aged 18–26 years reported that they had initiated a human papillomavirus vaccine (HPV) despite the recommendation being published in March of 2007 [26], while vaccination coverage among indicated populations was approximately 2% prior to publication of the herpes zoster vaccine recommendation [27]. Tdap vaccination coverage has since climbed to just 6.6% through 2009, according to the NHIS [19]. If a strong inverse association was present between Tdap vaccination coverage and novelty of the published ACIP recommendation at the time of NIS-Adult interviews, a greater increase in coverage might be expected with time. Continued slow uptake of Tdap indicates that barriers described here still persist. At the time of the survey, pertussis could be identified as a vaccine-preventable disease by an estimated 3% of U.S. adults [28]. We found that specific awareness of Tdap was also low, among unvaccinated respondents. It is unlikely that high vaccination coverage among adults can be achieved without being preceded by an increased collective awareness of Tdap. Possessing at least a college level education and receiving a recent influenza vaccination were the only two factors significantly associated with Tdap vaccination status, and not surprisingly, these characteristics also were associated with vaccine awareness. Other factors associated with vaccine awareness, such as possessing medical insurance, employment in a healthcare setting, and non-Hispanic, white race/ethnicity did not appear to be significant predictors of Tdap uptake in 2007, but were estimated as such one year later according to results from the 2008 NHIS [29]. It is possible that collective awareness of pertussis as a vaccine-preventable disease has increased following outbreaks like California’s in 2010. Future research will be needed to determine the extent to which this is true at the national level, and whether these factors have resulted in increased vaccination-seeking behavior.

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Healthcare providers are a common source of vaccination information for patients [30,31]. However, respondents aware of Tdap were likely not informed by a healthcare provider, as many were not provided with a recommendation. Awareness of the vaccine was also not associated with a recent provider visit, as might be expected if providers were collectively recommending Tdap. Prior to the ACIP recommendation, primary care providers expressed favorable attitudes toward Tdap, and a willingness to recommend vaccination to their patients [30,32]. Our findings might indicate logistical barriers have hindered this in practice. A cross-sectional study conducted in 2009 showed that Tdap was not even stocked by 12% of family physicians and 24% of internists [33]; these proportions were likely higher at the time of NIS-Adult interviews. Observed differences in vaccine stocking behavior – a behavior that is highly predictive of a provider recommendation – between healthcare providers serving adolescent vs. adult populations may partially explain the profound discrepancy between recent Tdap vaccination coverage estimates of these respective populations (adolescents, 13–17 yrs [55.5%]; adults [6.6%]) [19,21,34]. While it was beyond the scope of this study to determine providers’ attitudes and behavior regarding adult Tdap vaccination, our results do underscore the importance of future research in this area. Despite these likely barriers to Tdap uptake, our results also clearly indicate that significant potential for increased vaccination coverage exists. As is the case for other ACIP-recommended adult vaccines [26–28], most participants were willing to be vaccinated with Tdap if recommended by a healthcare provider. Importantly, we found that adults with infant contact were more likely than others to express this willingness. These persons are among the most important candidates for Tdap vaccination, in order to protect against transmission to those infants not completely vaccinated with a primary pertussis series. Pertussis can be fatal among infants, and 10 died from the disease during the 2010 California outbreak alone [35]. Adults in contact with infants may be difficult to identify, especially for internists [30], but actively targeting these individuals in the pediatrician’s office [36], as well as in post-partum acute hospital settings [37], have shown some promise. A small proportion of respondents were unwilling to be vaccinated with Tdap. In contrast to other adult vaccines [28,38], our results do not show that vaccine safety concerns were a predominant factor. Over half of those unwilling to be vaccinated with Tdap either indicated that they did not feel at risk to contract pertussis, or that they would need more information in order to reconsider vaccination. These reasons are likely easier for healthcare providers to address than safety concerns, fear of needles and a general distrust of vaccines. Our results show that no respondent cited a low perceived risk of transmitting pertussis to susceptible contacts as a reason not to be vaccinated, which indicates that adults do not identify this as a potential impetus to be vaccinated. Those unwilling to receive a Tdap vaccination might be persuaded by a discussion with their healthcare provider that clearly addresses both the risk of contracting pertussis, as well as the risk of transmitting the disease to susceptible contacts [39–41]. 4.1. Limitations The findings of this study are subject to certain potential limitations. First, vaccination status was self-reported and may be subject to recall bias. Recall of tetanus vaccinations within the previous 10 years can be highly reliable, but potentially unreliable for those who did not receive a vaccination during this time [42]. Because survey interviews were conducted approximately two years after Tdap was licensed, it is plausible that Tdap recall was more accurate than what is traditionally observed for Td vaccination. Second, although comparable to other population-based telephone surveys with a similar scope [43–46], the response rate of the NIS-Adult was

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low (31%), which could have resulted in nonresponse bias. However, estimates were weighted to reflect differential probabilities of unit nonresponse, and demographic characteristics described here were similar to those of the 2007 NHIS [47]. While tetanus vaccination information was not available in NHIS 2007, Tdap vaccination coverage estimates from NHIS 2008 were in the expected ranges across levels of similar descriptive characteristics, given our findings [29]. Third, Tdap vaccination coverage was estimated after excluding many participants who had received a tetanus vaccination since 2005 but either reported that their provider did not inform them of the vaccine type (Td or Tdap), or that they could not recall the vaccine type. To quantify the upper bound of potential bias this may have introduced, a sensitivity analysis was conducted. Assuming that none, or alternatively, all of these excluded participants received Tdap, coverage ranged from 3.1 to 12.6%. Fourth, since NIS-Adult interviews were conducted in 2007, current barriers to Tdap vaccination may differ from results reported here; however, a cross-sectional study conducted through October, 2010 on localized California populations describes similar barriers to Tdap uptake [48]. Lastly, NIS-Adult excluded persons without landline telephones, including cellular phones, which may be a source of selection bias; however, differential probabilities of these characteristics were also weighted in the analyses. 5. Conclusion Our findings represent an early – and to our knowledge, the only available – snapshot of barriers to pertussis vaccination among U.S. adults. For at least two years after licensure, adults were largely not aware of Tdap, and not frequently being recommended Tdap vaccination by healthcare providers. Since the NIS-Adult was fielded, population-based Tdap vaccination coverage has increased by only an estimated 3.0 percentage points, which suggests that barriers described here still persist [19]. Nevertheless, the prospect of higher coverage remains encouraging, as most adults are willing to be vaccinated with Tdap if recommended by a provider. Those unwilling to be vaccinated might be amenable to vaccination after an informed discussion with their healthcare provider. Going forward, evidence-based recommendations for improving vaccination coverage among adults, in general, include reminder/recall systems and standing orders [49,50]. Acknowledgements Contributions: Mr. Miller had full access to all of the data in the study and takes responsibility for the integrity of the data and accuracy of the data analysis. All authors have approved the final manuscript. Miller, Kretsinger, Euler, Lu, and Ahmed contributed to study concept and design. Euler and Lu helped in the acquisition of the data and Miller and Ahmed in the analysis and interpretation of the data. Drafting of the manuscript was done by Miller and Statistical analysis by Miller and Ahmed. Ahmed and Euler supervised the study and along with Kretsinger and Lu lent administrative, technical or material support. All of them helped in critical revision of the manuscript. Financial disclosures: None reported. Conflict of interest: None reported. Funding/support: This work was funded by the US Centers for Disease Control and Prevention. Role of the sponsor: The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the funding agency. References [1] Lee GM, Lett S, Schauer S, LeBaron C, Murphy TV, Rusinak D, et al. Societal costs and morbidity of pertussis in adolescents and adults. Clin Infect Dis 2004;39(11):1572–80.

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