Research

Original Investigation | ADOLESCENT AND YOUNG ADULT HEALTH

Impact of Tetanus Toxoid, Reduced Diphtheria Toxoid,

and Acellular Pertussis Vaccinations on Reported Pertussis
Cases Among Those 11 to 18 Years of Age in an Era of Waning
Pertussis Immunity
A Follow-up Analysis
Tami H. Skoff, MS; Stacey W. Martin, MSc

Editorial
IMPORTANCE There is accumulating literature on waning acellular pertussis vaccine–induced
immunity, confirming the results of studies assessing the duration of protection of pertussis
vaccines.

OBJECTIVE To evaluate the tetanus toxoid, reduced diphtheria toxoid, and acellular pertussis
(Tdap) vaccine’s effect over time among those 11 to 18 years old, while accounting for the
transition from whole-cell to acellular pertussis vaccines for the childhood primary series.

DESIGN, SETTING, AND PARTICIPANTS Extended, retrospective analysis of reported pertussis

cases between January 1, 1990, and December 31, 2014, in the United States. The analysis
included all nationally reported pertussis cases.

EXPOSURE US Tdap vaccination program and the transition from whole-cell to acellular
pertussis vaccines.

MAIN OUTCOMES AND MEASURES Rate ratios of reported pertussis incidence (defined as
incidence among 11- to 18-year-old individuals divided by the combined incidence in all other
age groups) modeled with segmented regression analysis and age-specific trends in reported
pertussis incidence over time.

RESULTS Between 1990 and 2014, 356 557 pertussis cases were reported in the United
States. Of those, 191 914 (53.8%) were female and 240 665 (67.5%) were white. Overall
incidence increased from 1.7 in 100 000 to 4.0 in 100 000 between 1990 and 2003, while
latter years were dominated by epidemic peaks. Incidence was highest among infants
younger than 1 year throughout the analysis period. Pertussis rates were comparable among
all other age groups until the late 2000s, when an increased burden of pertussis emerged
among children 1 to 10 years old, resulting in the second highest age-specific incidence. By
2014, 11- to 18-year-old individuals once again had the second highest incidence. While slope
coefficients from segmented regression analysis showed a positive impact of Tdap
immediately following introduction (slope, −0.4959; P < .001), a reversal in trends was
observed in 2010 when rates of disease among 11- to 18-year-old individuals increased at a
Author Affiliations: Meningitis and
faster rate than all other age groups combined (slope, 0.5727; P < .001). Vaccine Preventable Diseases Branch,
Division of Bacterial Diseases,
CONCLUSIONS AND RELEVANCE While the impact of Tdap among adolescents looked National Center for Immunization and
Respiratory Diseases, US Centers for
promising following vaccine introduction, our extended analysis found that trends in Disease Control and Prevention,
adolescent disease were abruptly reversed in 2010, corresponding directly to the aging of Atlanta, Georgia.
acellular pertussis–vaccinated cohorts. Despite the apparent limitations of Tdap, it remains Corresponding Author: Tami H.
the best prevention against disease in adolescents. Skoff, MS, Meningitis and Vaccine
Preventable Diseases Branch,
Division of Bacterial Diseases,
National Center for Immunization and
Respiratory Diseases, US Centers for
Disease Control and Prevention,
JAMA Pediatr. doi:10.1001/jamapediatrics.2015.4875 1600 Clifton Rd NE, MS C-25, Atlanta,
Published online March 28, 2016. GA 30329 (tlh9@cdc.gov).

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 Research Original Investigation
T
etanus toxoid, reduced diphtheria toxoid, and acellu-
lar pertussis (Tdap) vaccines were licensed in the United
States in 2005 for use as a booster dose among adoles-
cents and adults. The primary goal of Tdap vaccination was to
reduce the growing burden of disease among adolescents. Early
field evaluations conducted shortly after vaccine introduc-
tion revealed 66% to 78% effectiveness of Tdap among
adolescents,1-3 and vaccination coverage increased steadily in
the years following introduction. By 2014, Tdap coverage
among those aged 13 to 17 years reached 87.6% in the United
States.4 Shortly following the introduction of Tdap vaccines,
the effects of vaccination among the target adolescent age
group looked promising. Although elevated, reported rates of
pertussis among 11- to 18-year-old individuals decreased more
quickly than rates of disease among all other age groups in the
years immediately following Tdap introduction, suggesting that
the targeted use of Tdap reduced the burden of pertussis pref-
erentially in the adolescent age group.5
Despite high or increasing coverage with both Tdap and the
childhood pertussis vaccination series (diphtheria toxoid, teta-
nus toxoid, and acellular pertussis vaccine [DTaP]), the United
States has been experiencing a pertussis resurgence in recent
years, with notable changes in the epidemiology of disease. Since
the early 1990s, significant epidemics have been reported nation-
ally in the United States, with the largest postvaccine introduc-
tion peak in 2012, when more than 48 000 cases were reported
in the United States, the largest number of cases since the mid-
1950s. Many factors are likely contributing to the resurgence in
disease including changes in diagnostic testing and reporting, in-
creased awareness of pertussis among health care profession-
als and the general public, molecular evolution of the organism,
and, most importantly, waning of vaccine-induced immunity.
Although pertussis vaccines have demonstrated excellent short-
term effectiveness, the protection of both DTaP and Tdap wanes
quickly in the years following vaccination.6-8 This waning is con-
sistent with the epidemiological shift toward the emergence of
disease among recently vaccinated children and adolescents.
In the 5 years since our original analysis of the early im-
pact of Tdap,5 the landscape of pertussis epidemiology has
changed. Waning of vaccine-induced immunity from DTaP has
been well documented, particularly as cohorts of children who
received an acellular vaccine for all 5 doses of their childhood
series age.6,7,9 In light of these changes and findings, we sought
to update our previous analysis, looking at the impact of Tdap
among those 11 to 18 years of age by including 5 additional years
of data (2010-2014), allowing us to assess the effect of Tdap
among acellular-primed adolescent cohorts.
Methods
This analysis is an extension of our earlier retrospective analy-
sis of pertussis cases reported through the National Notifiable Dis-
eases Surveillance System.5 For this analysis, cases with a cough
onset date between January 1, 1990, and December 31, 2014, were
classified by state and local health departments according to the
Council of State and Territorial Epidemiologists case definition
for pertussis. Cases with a confirmed, probable, or unknown case
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Impact of Pertussis Vaccinations on Reported Cases in Adolescents
Key Points
Question Accounting for the transition from whole-cell to
acellular pertussis vaccines for the childhood primary series, what
is the effect of the tetanus toxoid, reduced diphtheria toxoid, and
acellular pertussis vaccine among cohorts of adolescents and
young adults over time?
Findings In this analysis of reported cases of pertussis in the
United States between 1990 and 2014, the tetanus toxoid,
reduced diphtheria toxoid, and acellular pertussis vaccines had an
impact among adolescents following its introduction in 2005,
there was a reversal in disease trends in 2010, when reported
pertussis incidence among adolescents began to increase at a
faster rate than disease among all other age groups.
Meaning Our findings are consistent with recent literature
suggesting a diminished effect of the tetanus toxoid, reduced
diphtheria toxoid, and acellular pertussis vaccine among acellular
pertussis vaccine–primed cohorts of adolescents.
status were included in the analysis. Because this was a retrospec-
tive analysis of nationally notifiable surveillance data, institu-
tional review board approval was not needed.
Cases were stratified by the following age groups for the
trend over time analysis: younger than 1 year, 1 to 10 years, 11
to 18 years, and 19 years and older. Overall and age-specific in-
cidence rates were calculated using cases reported through the
National Notifiable Diseases Surveillance System as numera-
tors and population estimates from the National Center for
Health Statistics as denominators (bridged-race, intercensal
population estimates were used for 1990-1999 and 2014 post-
censal vintage estimates for 2000-2014).
Segmented regression analysis was used to model rate ra-
tios of reported pertussis incidence (defined as incidence among
those aged 11 to 18 years divided by the combined incidence in
all other age groups), while accounting for temporal variability
in disease trends. For the model, the pre-Tdap period was de-
fined as 1990 to 2004 and the post-Tdap period as 2005 to 2014.
Additionally, we used 2010 as a second break point to model the
transition to acellular DTaP vaccines for the entire childhood se-
ries; by 2010, all 11-year-old children were born after the Advi-
sory Committee on Immunization Practices recommendation
in 1997 to administer DTaP for all 5 doses of the childhood se-
ries. Changes in proportions and risk ratios were used for the
comparison of proportions; P < .05 was considered statistically
significant.
Results
A total of 356 557 pertussis cases were reported through the
National Notifiable Diseases Surveillance System between
January 1, 1990, and December 31, 2014; 200 401 (56%) of the
cases occurred between 1990 and 2009. Case characteristics
are summarized in Table 1.
Between 1990 and 2003, the overall incidence of pertussis
increased gradually from 1.7 in 100 000 population to 4.0 in
100 000 (135% increase, P ≤ .001). Following this increase, the
latter years were dominated by prominent epidemic peaks in
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 Impact of Pertussis Vaccinations on Reported Cases in Adolescents Original Investigation Research

Table 1. Case Characteristics, 1990-2014

No. (%)
1990-2009 2010-2014 Total
Characteristic (n = 200 401) (n = 156 156) (N = 356 557)
Sex
Male 89 590 (44.7) 70 847 (45.4) 160 437 (45.0)
Female 107 732 (53.8) 84 182 (53.9) 191 914 (53.8)
Unknown 3079 (1.5) 1127 (0.7) 4206 (1.2)
Race
White 133 511 (66.6) 107 154 (68.6) 240 665 (67.5)
Black 10 153 (5.1) 6494 (4.2) 16 647 (4.7)
Other 7383 (3.7) 8184 (5.2) 15 567 (4.3)
Unknown 49 354 (24.6) 34 324 (22.0) 83 678 (23.5)
Ethnicity
Hispanic 21 858 (10.9) 25 308 (16.2) 47 166 (13.2)
Non-Hispanic 120 825 (60.3) 94 462 (60.5) 215 287 (60.4)
Unknown 57 718 (28.8) 36 386 (23.3) 94 104 (26.4)
Age group, y
<1 45 458 (22.7) 20 344 (13.0) 65 802 (18.5)
1-10 52 724 (26.3) 57 835 (37.1) 110 559 (31.0)
11-18 49 195 (24.6) 41 654 (26.7) 90 849 (25.5)
≥19 50 550 (25.2) 35 197 (22.5) 85 747 (24.0)
Unknown 2474 (1.2) 1126 (0.7) 3600 (1.0)
CSTE classification
Confirmed 133 254 (66.5) 122 075 (78.2) 255 329 (71.6)
Probable 53 532 (27.7) 33 776 (21.6) 87 308 (24.5)
Unknown 13 615 (6.8) 305 (0.2) 13 920 (3.9)
Outcome
Died 253 (0.1) 86 (0.1) 339 (0.1)
Survived 142 587 (71.2) 105 146 (67.3) 247 733 (69.5)
Abbreviation: CSTE, Council of State
Unknown 57 561 (28.7) 50 924 (32.6) 108 485 (30.4)
and Territorial Epidemiologists.

Figure 1. Overall Incidence of Reported Pertussis, 1990-2014

18

16

14
Cases per 100 000 Population

12

10

0
1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014
Year

The solid black line with circle markers indicates overall incidence of pertussis among all age groups combined.

2004 (8.8 in 100 000), 2005 (8.7 in 100 000), 2010 (8.9 in
100 000), and 2012 (15.4 in 100 000) (Figure 1). Additionally, the
number of reported cases during the trough in 2013 was higher
than the number of cases reported during the prior peak years
of 2004, 2005, and 2010 (Figure 1).
When stratified by age group, rates of disease were consis-
tently highest among infants younger than 1 year compared with
the other age groups, ranging from a low of 26.4 in 100 000 in
1991 to a high of 127.2 in 100 000 in 2012 (Figure 2). Pertussis
incidence remained comparable among the other age groups

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 Research Original Investigation Impact of Pertussis Vaccinations on Reported Cases in Adolescents

Figure 2. Incidence of Reported Pertussis by Age Group, 1990-2014

140

<1 y
120
1-10 y
11-18 y
Cases per 100 000 Population

100 ≥19 y

80

60

40

20

1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014
Year

Figure 3. Pertussis Incidence and Rate Ratios

A Pertussis incidence, 1990-2014

45

11-18 y
40
All other ages
35
Cases per 100 000 Population

30

25

20

15

10

0
1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014
Year

B Rate ratios of pertussis incidence, 1990-2014

5

Observed rate ratios

Expected rate ratios
4
Slope = —.4959,
P<.001
Rate Ratio (Incidence)

3
Slope = .5727,
Slope = .2917, P<.001
P<.001
2

0
1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014
Year

A, Pertussis incidence, 1990-2014. B, Rate ratios of pertussis incidence, 1990-2014. Vertical dashes represent the breakpoints in segmented regression analysis
(1990-2004 as the pretetanus toxoid, reduced diphtheria toxoid, and acellular pertussis [Tdap] period, 2005-2009 as the post-Tdap [whole-cell pertussis–primed]
period, and 2010-2014 as the post-Tdap [transition to fully acellular pertussis–primed] period).

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 Impact of Pertussis Vaccinations on Reported Cases in Adolescents Original Investigation Research

Table 2. Description of Adolescent Birth Cohorts and Their Corresponding Age, by Yeara

Age, y
Birth Cohort 2009 2009 2010 2010 2011 2011 2012 2012 2013 2013 2014 2014
1991b 17 18 18 19 19 20 20 21 21 22 22 23
1992c 16 17 17 18 18 19 19 20 20 21 21 22
1993c 15 16 16 17 17 18 18 19 19 20 20 21
1994c 14 15 15 16 16 17 17 18 18 19 19 20
1995c 13 14 14 15 15 16 16 17 17 18 18 19
1996c 12 13 13 14 14 15 15 16 16 17 17 18
1997c 11 12 12 13 13 14 14 15 15 16 16 17
1998d 10 11 11 12 12 13 13 14 14 15 15 16
1999d 9 10 10 11 11 12 12 13 13 14 14 15
2000d 8 9 9 10 10 11 11 12 12 13 13 14
2001d 7 8 8 9 9 10 10 11 11 12 12 13
2002d 6 7 7 8 8 9 9 10 10 11 11 12
2003d 5 6 6 7 7 8 8 9 9 10 10 11
2004d 4 5 5 6 6 7 7 8 8 9 9 10
a
Each calendar year includes 2 age groups to capture change in age over the vaccine only. For example, in 2012, all children younger than 14 years should
course of the year. In 1997, it was recommended that all 5 doses of the have received acellular vaccine for all 5 doses of their childhood pertussis
childhood pertussis vaccination series be replaced with acellular vaccines. series.
Therefore, all children below the 1997 row should have received the acellular b
Whole-cell vaccine only.
vaccine for the 5-dose childhood series, whereas the children above the 1997 c
Combination of whole-cell and acellular pertussis vaccines.
row would have either received a combination of whole-cell and acellular
d
pertussis vaccines (with whole-cell for the first 3 priming doses) or whole-cell Acellular vaccine only.

until the late 2000s, when an increased burden of pertussis
emerged among children 1 to 10 years; between 2007 and 2011,
children 1 to 10 years had 1 to 2 times higher incidence of reported
pertussis than adolescents 11 to 18 years. While incidence in-
creased dramatically across all age groups between 2011 and 2012,
the largest relative increases were observed among those aged
11 to 18 years (267.5%), followed by those aged 1 to 10 years
(156.8%). By 2014, a slight increase was observed among adoles-
cents 11 to 18 years of age, surpassing the rate of reported pertus-
sis among those aged 1 to 10 years (Figure 2).
As our previous analysis showed, prior to the introduc-
tion of Tdap in 2005, the incidence of pertussis among ado-
lescents aged 11 to 18 years increased gradually before reach-
ing a peak during the 2004 epidemic (slope, 0.2917; P < .001)
(Figure 3A). Following the peak, the incidence of pertussis came
down in all age groups but declined at a significantly faster rate
among adolescents than among all other age groups com-
bined (slope, −0.4959; P < .001) (Figure 3B). However, begin-
ning in 2010, this trend was reversed. Once again, the inci-
dence of disease among adolescents increased at a faster rate
than the other age groups, similar to what was observed prior
to the introduction of Tdap in the United States but at a much
steeper incline (slope, 0.5727; P < .001) (Figure 3B).
Discussion
Although Tdap had a positive impact among adolescents in the
4 years immediately following vaccine introduction, our ex-
tended analysis of data through 2014 revealed a reversal in dis-
ease trends in 2010, when reported pertussis incidence among
adolescents began to increase at a faster rate than disease among
all other age groups. Our extended analysis of additional years
of surveillance data supports the accumulating literature on wan-
ing of acellular vaccine–induced immunity and offers an addi-
tional perspective by confirming the results of published case-
control and cohort studies assessing the duration of protection
of pertussis vaccines. The United States transitioned from whole-
cell pertussis (wP) vaccines to acellular DTaP vaccines for the
childhood series during the 1990s; in 1992, the Advisory Com-
mittee on Immunization Practices recommended DTaP for the
fourth and fifth doses of the childhood series, given at 15 to 18
months and 4 to 6 years, respectively, and in 1997, further rec-
ommendations were made to transition the primary doses of the
series, given at 2, 4, and 6 months of age, to acellular pertussis
vaccine.10,11 By 2014, all cohorts of children younger than 16 years
should have received acellular vaccine for all 5 doses of the child-
hood series (Table 2). While our previous analysis showed a strong
impact of Tdap among the target adolescent age group, the analy-
sis only included data up through 2009, which captured adoles-
cent cohorts that had received greater than 1 wP dose for the child-
hood series. Data from the past few years have shown that Tdap
duration of protection wanes more quickly among adolescents
primed with DTaP than with wP formulations and that at least
a single dose of wP vaccine as part of the 5-dose childhood se-
ries, especially when administered as the first dose, results in
greater Tdap-induced protection.12-14 We observed an abrupt shift
in the direction of rate ratios in 2010, the very year that children
aged 11 years would have been the first cohort born after the 1997
transition from wP to acellular vaccines to have received acel-
lular vaccines for all doses of the childhood series.
There are many hypotheses surrounding the recent resur-
gence of pertussis in the United States and abroad. While wan-
ing immunity from acellular vaccines is thought to be a driving
factor, especially among school-aged children and adolescents,
the cause is likely multifactorial. Changes in diagnostic testing,

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 Research Original Investigation Impact of Pertussis Vaccinations on Reported Cases in Adolescents

surveillance, and reporting are likely playing a role in the resur-
gence. However, similar trends in diagnostic test use, with a tran-
sition away from culture to polymerase chain reaction, have been
observed across age groups.15 More importantly, changes in di-
agnostic tests and/or reporting do not explain the strong cohort
effect of increasing pertussis incidence that has been observed
among birth cohorts of acellular-primed adolescents.9,16 In recent
years, a rapid increase in pertactin-deficient Bordetella pertussis
strains has also been observed in the United States.17 Pertactin is
a key B pertussis antigen thought to be involved in bacterial ad-
hesion and is included in all acellular pertussis vaccines used in
the United States. Vaccine pressure combined with imperfect and
waning vaccine-induced immunity in children and adolescents
may have enabled evolution of the bacterium to allow for more
efficient transmission among highly vaccinated cohorts.
Given what our analysis and other publications have
shown, recommending Tdap for an additional dose among the
general population is unlikely to have a significant effect on
disease burden in the United States. With modest effective-
ness of Tdap vaccines and significant waning of protection
within 2 years of vaccine receipt, susceptible individuals will
continue to accumulate in the population. A 2016 cost-
effectiveness model looking at additional doses of Tdap among
a theoretical cohort of persons 11 to 30 years of age found that
the fraction of pertussis disease prevented never exceeded 10%
with an additional dose of Tdap administered at 16 or 21 years
of age.18 While more than 1 dose of Tdap may be considered
for high-risk populations pending licensure of additional doses,
for now, the Advisory Committee on Immunization Practices
recommends more than 1 dose of Tdap only among pregnant
women to provide direct protection through maternal anti-
body transfer to infants who are at increased risk for severe per-
tussis-related morbidity and mortality.19 Strategies such as early
detection and treatment of pertussis should be used in addi-
tion to vaccination to optimize the control of pertussis among
adolescents and reduce transmission within the general popu-
lation and to high-risk groups.
Conclusions
Pertussis vaccines continue to protect against severe disease
and death, offering major benefits to their recipients. There-
fore, maximizing current pertussis vaccination strategies re-
mains the best defense against disease in the short term until
pertussis vaccines with extended duration of immunity are de-
veloped and made available. Emphasis should be placed on en-
suring on-time pertussis vaccination and increasing Tdap cov-
erage among pregnant women to provide protection to infants,
those at highest risk for disease.

ARTICLE INFORMATION
Accepted for Publication: December 16, 2015.
Published Online: March 28, 2016.
doi:10.1001/jamapediatrics.2015.4875.
Author Contributions: Ms Skoff had full access to
all of the data in the study and takes responsibility
for the integrity of the data and the accuracy of the
data analysis.
Study concept and design: Both authors.
Acquisition, analysis, or interpretation of data: Both
authors.
Drafting of the manuscript: Both authors.
Critical revision of the manuscript for important
intellectual content: Both authors.
Statistical analysis: Both authors.
Administrative, technical, or material support: Skoff.
Study supervision: Martin.
Conflict of Interest Disclosures: None reported.
Disclaimer: The findings and conclusions in this
article are those of the authors and do not
necessarily represent the views of the Centers for
Disease Control and Prevention.
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