The global incidence of
pertussis declined to very low level with the advent of whole-cell
pertussis (wP) vaccines by the 1970s. However, in the 1990s, safety
concerns prompted a switch from wP to acellular-pertussis (aP) vaccines
in most of the developed countries. Since 2009, large outbreaks of
pertussis are regularly reported from many industrialized countries
employing aP vaccines despite having very high vaccination coverage
[1-10]. Outbreaks have also been reported from countries using wP
vaccines like the one reported recently from Khairpur District of Sindh
province of Pakistan . However, another study from Pakistan
conducted between 2005 and 2009 found that B. parapertussis was
responsible for the pertussis outbreak against which the wP vaccines had
shown little efficacy .
Reasons for Resurgence
There are multiple factors responsible for the recent
resurgence of pertussis in industrialized countries. They include
enhanced awareness, increased public health reporting, introduction of
more sensitive tools like polymerase chain reaction (PCR) for diagnosing
infection, suboptimal efficacy of aP vaccines, and the potential
antigenic drift in circulating pertussis strains [8, 13-15]. But the
major concern is the lower efficacy of aP vaccines than wP vaccines
[8,15]. Many reasons for apparent decreased efficacy of aP have been
proposed, including observer bias in initial trials, reduced antigenic
stimulation in aP, and mutation of Bordetella pertussis .
Antigenic shifts in circulating Bordetella pertussis strains 
or the different immune responses from acellular and whole-cell priming
 have also been proposed as probable reasons. Another hypothesis
states that the lesser protection provided by aP may be due to linked
epitope suppression when the initial exposure locks in the immune
response to certain epitopes and inhibits response to other linked
epitopes on subsequent exposures .
Duration of Protection
Waning of protective immunity is noted with both wP
and aP vaccines , and also after acquisition of immunity after
natural infection. According to studies that provide the longest period
of evaluation, the protection accorded by wP vaccines wanes by 50% over
a period of 6-12 years [20-22]. Whereas little is known about the
duration of protection following aP vaccination in developing countries,
many studies in industrialized world documented faster waning with aP
vaccines and showed that protection waned after 4-12 years [25-28]. A
recent case-control study investigated Kaiser Permanente Northern
California outbreak in US and concluded that protection after aP (DTaP)
vaccine waned substantially after administration of the 5th dose, and
the odds of acquiring pertussis increased by an average of 42% per year
after the fifth dose of DTaP . The researchers found a lower
incidence of PCR confirmed pertussis in children aged 12-15 years who
had received wP vaccine as infant than in 8-11 years who had received
all 5-doses of aP vaccine in their primary immunization series .
Similar conclusions were reached by another set of researches from North
America . They found vaccine effectiveness of aP vaccines as 41%,
24%, and 79% for children aged 2-7 years, 8-12 years, 13-18 years,
respectively and concluded that the current schedule of aP vaccine was
insufficient to prevent outbreaks of pertussis . Misegades et al.
studied the California outbreak in 15 counties and noticed progressive
incremental decline in estimated vaccine effectiveness each year after
the final dose of aP vaccine .
Choice of Vaccines: Whole Cell Versus Acellular Pertussis Vaccines
Several randomized trials (Web Table I)
conducted in the 1990s compared the efficacy of aP vaccines with wP
vaccines. At least five trials found that wP vaccines had greater
efficacy than aP vaccines . Many later trials have also hinted that
the efficacy of the aP vaccine may not be as robust as reported in the
initial studies [30-32]. Studies after the recent outbreaks in US, UK
and Australia have now concluded that the change from wP to aP vaccines
contributed to the increase in perutussis cases [33-35]. Recent data
from US and Australia have suggested reduced durability of
vaccine-induced immunity after the aP vaccination in comparison to wP
vaccines [28, 29]. World over, the experts now believe that aP vaccines
may be less effective than previously believed when contrasted with wP
vaccines [30, 33, 34].
Witt et al.  studied 263, 496 persons in
age group of 8-20 years in US province of Kaiser Permanente (KP) and
concluded that a vaccination schedule that contained all aP vaccine
series was significantly less effective and durable than one that
contained the traditional wP vaccine. There was a markedly increased
risk of disease with the use of former. Addition of a 6th dose of
pertussis vaccine (Tdap) though mitigated, but not completely eliminated
this risk. They found receipt of 1 or more wP doses markedly augmented
the durability of immunity from subsequent aP doses . The superior
priming with wP vaccines in comparison to aP vaccine was also confirmed
by two different studies from Australia  and US . Sheridan and
colleagues in Australia have found a 3-fold higher rate of pertussis in
the aP recipients 10 years after primary vaccination during both
pre-epidemic and outbreak periods . Another study conducted by Liko
et al.  among children born during the 1997–1999 transition
periods (from wP to aP) in Oregon state of US documented significantly
higher rates of the disease in those who underwent priming with aP
rather than wP vaccine. These findings suggest that priming with wP is
more effective at sustained prevention of pertussis disease than aP
Hence, the current evidence is tilted heavily in
favor of wP vaccines as far as effectiveness of the pertussis vaccines
is concerned. However, the industrialized world would not take the risk
of reverting to wP vaccines considering the low acceptance of these
vaccines by the public in the past. Few middle income group countries
sitting on the fence and on the verge of shifting to acellular products
would like to wait further till a better alternative is available.
Preference of a Particular Acellular Vaccine Product
There is no consensus so far on the antigenic
composition of an ideal aP vaccine [36-38]. Currently available aP
vaccines in India include 5-component vaccines, 3-component vaccines,
and a 2-component combination vaccine  (Table 1). The
exact contribution of the different aP antigens in according protection
is not clear. The currently available aP vaccines should be regarded as
different and unique products because of the presence of different
components in different concentrations, and with different degree of
adsorption to different adjuvants, individual antigens derived from
different strains of B. pertussis, and purified by different
methods . This heterogeneity in production of different aP vaccines
explains why direct comparison of protective efficacy of different aP
vaccines in human is not possible.
Table I Composition of Available Acellular Pertussis Vaccines (in combination) Brands in India
Pertussis Toxoid (PT)
Filamentous Haemagglutinin (FHA)
Fimbriae Types 2 and 3 (FIM)
* A combination of acellular pertussis, IPV and Hib
vaccines; ** Tdap vaccines.
Nevertheless, different researches have studied the
impact of number of components in an aP vaccine on relative protective
efficacy of different aP products. In a recent retrospective study in US
following a huge outbreak of pertussis in California , the
researchers found that 5-component aP vaccine had an estimated efficacy
of 88.7% (95% CI, 79.4%-93.8%) . According to a systematic review
involving 49 RCTs , aP vaccines containing 3 or more components had
much higher absolute efficacy (80-84%) than those containing only 1 and
2 components (67-70%). A Cochrane review by Zhang et al.  of
6 aP vaccine efficacy trials and 52 safety trials concluded that the
efficacy of multi-component (
3) aP vaccines over mono-or bi-component aP vaccines.
Vaccination of Adolescents and Adults
Pertussis in adolescents and adults is responsible
for considerable morbidity in these age groups and also serves as a
reservoir for disease transmission to unvaccinated/partially vaccinated
young infants . Several developed countries have instituted routine
booster immunization of adolescents and adults with standard quantity
tetanus toxoid and reduced quantity diphtheria and aP vaccine (Tdap)
instead of Td in their national immunization programs . The IAP has
also recommended only a single one-time dose of Tdap to adolescents aged
10-12 years of age . The US Advisory Committee on Immunization
Practices (ACIP) recommended routine administration of Tdap booster for
adolescents in 2005, the vaccine coverage still remains low, with only
56% of adolescents and 8.2% of adults vaccinated in 2012 . There is
no data on the coverage of Tdap in adolescents and adults in India since
it is being used exclusively in private health sector.
Objectives and rationale of adolescents and adult
pertussis vaccination: There are two main objectives- first, to
protect vaccinated persons against pertussis, and second, to reduce the
reservoir of pertussis in the population at large and thereby
potentially decrease exposure of persons at increased risk for
complicated infection (e.g., infants). However, adequate evidence is
lacking to support the recommendation of adding booster doses in these
age groups in order to achieve the primary goal of reducing severe
pertussis in infants . Repeat doses of Tdap at 5 or 10 years
interval in adolescents and adults have also failed to confer lifelong
Efficacy and effectiveness of Tdap: Wei, et al.
 evaluated effectiveness of Tdap booster among adolescents in the
Virgin Islands in 2007, and found effectiveness of 61.3% (95% CI:
52.5–90.2) and 68.3% (95% CI: -126.4–95.6) against probable and
laboratory-confirmed pertussis, respectively . However, a recently
conducted unpublished trial reported that Tdap was modestly effective
[vaccine effectiveness: 55.2% (95% CI 44.1-64.1%] at preventing
PCR-confirmed pertussis among Kaiser Permanente Northern California
(KPNC) adolescents and adults. According to a summary presented at ACIP
February 2013 meeting, the Tdap effectiveness was noticed ranging from
66 % to 78% in field observational studies. The preliminary data suggest
effectiveness wanes within 3-4 years among aP vaccine recipients and
there was no evidence of herd immunity.
Maternal Immunization-A Promising Strategy to Prevent
In 2006, the ACIP recommended a dose of Tdap to
pregnant women immediately postpartum and all other close contacts of
infants aged <12 months to reduce the risk for transmission of pertussis
to infants . However, immunization of adolescents and adults, and
postpartum administration of Tdap failed to have appreciable impact on
laboratory-confirmed pertussis in very young infants [36,44]. Several
strategies like maternal immunization including pregnant women,
cocooning, neonatal immunization, have been proposed to reduce the
burden of pertussis in those infants too young to have been immunized.
Amongst all these strategies, immunization during pregnancy appears to
be most effective strategy to have the most impact on infantile
pertussis, especially during the first few weeks after birth . The
effective transplacental transmission of maternal pertussis antibodies
would protect the infant against pertussis during the first months of
life. Though the transplacentally acquired antibodies may be detectable
at least up to first few weeks of life (at 6–8 weeks), the age at which
the first pertussis-containing vaccine is due, the concentration of
antibodies required for protection against pertussis in newborns is not
known . In 2011, the ACIP recommended a dose of Tdap to all pregnant
women after 20 weeks gestation to provide protection for both the mother
and her newborn during the infant’s earliest weeks of life .
Immunization of Pregnant Women
There are few concerns that need to be addressed
before this practice becomes universal.
Titers and duration of the maternal antibodies:
According to CDC, 80–100% of women immunized with wP vaccine during
pregnancy had considerable increases in agglutinin antibodies .
Limited data suggest that aP vaccine given to pregnant women will result
in significantly increased antibody concentrations in newborns, but the
duration of the maternal antibodies and the potential requirement for
booster doses with subsequent pregnancies has not been sufficiently
explored . However, according to a recent report  the newborns
born to mothers who received Tdap during pregnancy had significantly
higher antibody titers to diphtheria toxin (P <0.001), tetanus
toxin (P = 0.004), PT (P <0.001), FHA (P = .0002),
PRN (P <0.0001) and fimbriae type 2/3 (P <0.001) when
compared with newborns born to unimmunized mothers . ACIP has now
recommended Tdap vaccination in every pregnancy .
Decreased immune response of primary series of
pertussis vaccines: There is a concern that high concentrations of
maternal antibodies may interfere with proper take of pertussis vaccines
during primary immunization . Earlier studies have demonstrated that
infant immune responses to aP vaccines were not affected by preexisting
antibodies against PT, but interference was seen with the wP vaccine
[49,50]. A recent study by Hardy-Fairbanks et al. 
demonstrated that infants whose mothers had received Tdap vaccine during
pregnancy had higher pertussis antibody concentrations between birth and
the first vaccine dose than the cohort whose mothers did not receive the
vaccine. After primary series of aP vaccines, the antibody
concentrations to pertussis antigens were lower in the Tdap group (0.7-
to 0.8-fold lower), except for fimbriae types 2 and 3 (1.5-fold
greater). However, the antibody concentrations to pertussis antigens
before and after booster dose were comparable. The researchers concluded
that though after the primary pertussis vaccine series, there was some
blunting of the response to the infant series, children did develop
adequate antibodies by the end of the series . The results of this
study is quite reassuring and adds evidence to support the practice of
vaccinating pregnant mothers to protect their children against pertussis,
however, more studies with larger sample size are needed. Nevertheless,
vaccination of pregnant women has a good likelihood of preventing
pertussis in very young infants, without the risk of just increasing it
at a later age. So, the strategy of vaccinating pregnant women may be
Safety of Tdap during pregnancy: Although there
are limited safety data on Tdap administration in pregnant women, the
existing Tdap safety data from the CDC, US FDA and the pharmaceutical
pregnancy registries do not indicate any adverse safety effect . In
the past, even 3-6 doses of wP vaccines were administered during single
pregnancy in 5 different clinical trials conducted in US and no serious
untoward local or systemic reactions were noted. There was no adverse
pregnancy outcome .
Other Strategies to Prevent Infant Pertussis
‘Cocooning’: ‘Cocooning’ and neonatal
immunization are the two other notable strategies to prevent pertussis
in very young infants. Though there is no conclusive evidence in favor
of cocooning strategy, the available data indicate that a decreased risk
of infection in newborns can be achieved with the immunization of all
family members who could have a strict contact with a newborn. Cost and
logistical barriers to widespread implementation of this strategy appear
to be major limitations .
Neonatal immunization: Neonatal
vaccination seems to be an attractive strategy for protecting neonates
and young infants, but the vaccine administered at birth would need to
be only acellular vaccine and not the combination DTaP. There is concern
that administration of aP vaccine at birth could lead to the generation
of an excessive Th2 immune response with a decreased Th1 response .
Further, it was observed that, the newborn dose of aP (as DTaP) had
suppressing effect on the immune responses to subsequent doses of DTaP
and other co-administered vaccines [54, 55].
Current status of Pertussis Vaccination and Disease Epidemiology in
Pertussis continues to be a serious public health
problem in India. There is passive reporting of whooping cough cases
from the public sector, the data is maintained by the Government of
India and also shared with WHO. In India, the incidence of pertussis
declined sharply after launch of Universal of Immunization Program
(UIP). Prior to UIP, India reported 200,932 cases and 106 deaths in the
year 1970 with a mortality rate of <0.001%. During the year 1987, the
reported incidence was about 163,000 cases which came down to 40, 508 in
2010 and 39, 091 in 2011 reflecting a decline of about 75% . Andhra
Pradesh, Madhya Pradesh, Jharkhand, West Bengal, and Bihar reported the
maximum cases in 2010. In 2010 only 6 and in 2011 a total of 11 deaths
were reported . However, the reliability and quality of the data is
questionable. A large number of cases go unreported, and many non-pertussis
cases are reported and clubbed under the head of ‘whooping cough’ cases.
Hence, the available figures lack specificity. The actual number may be
high considering that the coverage with three doses of DTP vaccine in
infancy was 71.5% and only 41.4% children in the age group of 18-23
months had received first DTP booster . The data on pertussis
disease and infection in adolescents and adults is sorely lacking.
Further, there is no data on Bordetella pertussis infection rates
in the community.
India is employing only wP vaccines in their national
immunization program since the adoption of Expanded Program of
Immunization (EPI) in 1978. Though aP vaccines are also licensed and
available, they are mainly prescribed by the private sector and coverage
is still miniscule. Private health sector is responsible for offering
vaccination to only 9% of the population in India (57). According to
most recent estimates, the national coverage of 3 doses of DPT is 71.3%
amongst children aged 12-23 months whereas first booster immunization of
DTP is only 41.4 % amongst 18-23 months old children . Surprisingly,
despite low coverage figures, there is poor documentation of large scale
outbreaks of pertussis in the country unlike the recent large scale
outbreaks reported in many developed countries [1-7]. Either many large
scale outbreaks are totally ignored and go unreported or wP vaccines are
providing adequate protection. There are two scenarios of pertussis
epidemiology in a given population based on coverage of pertussis
vaccine. Since the overall coverage is not very high, pertussis in major
parts of the country continues mainly to be a problem of young children.
However, many states having very good immunization rates behave like
developed countries with high coverage in pediatric age group with
resultant more frequent disease in adolescents and adults.
Regarding the safety of wP vaccines, there is still
no report of higher rates of serious adverse effects of following
immunization (AEFIs), and public acceptance of the vaccine is still not
a serious concern. The resistance amongst the community and adverse
publicity of the wP vaccines, were the main reasons why developed
countries discontinued vaccination with wP vaccines and switched to more
safer aP vaccines. These are the reasons why they will not be reverting
to older product in future also despite the reports of poor performance
of aP vaccines.
IAP Position on Pertussis vaccination
Recommendations for public health: IAP believes
that pertussis is a highly prevalent pediatric illness having
significant morbidity and mortality in the country. Though reliable data
on exact burden and incidence of pertussis in the country are scarce,
and laboratory confirmation is not readily available, pertussis is
widespread. Immune protection, both natural and vaccine-induced, is not
long lasting. All the available figures are based on rough estimates of
pertussis-like illnesses. There is an urgent need of an effective
surveillance to evaluate both the burden of infection and the impact of
immunization. The Academy unambiguously supports the current
immunization policy of employing only wP vaccines (in form of DTwP) in
UIP because of its proven efficacy, safety, adequate public acceptance,
and absence of documentation of significant waning.
Recommendations for individual use: Since there
is scarcity of data on vaccine efficacies of both wP and aP vaccines in
India and other developing countries, most of the recommendations of the
academy in regard to pertussis vaccination are based on the experience
gained and data obtained from the use of these vaccines in
industrialized countries. However, the continuous decline in reported
pertussis cases in last few decades has demonstrated good effectiveness
of wP vaccine (of whatever quality) in India. There is no data on the
effectiveness of aP vaccines in India.
Primary immunization: The primary infant series
should ideally be completed with 3 doses of wP vaccines. Vaccination
must start at 6 weeks. Acellular pertussis (aP) vaccines should be
avoided for the primary series of infant vaccination. The aP vaccine
combinations should also be avoided for the primary series. However, the
aP vaccines may be preferred to wP vaccines in children with history of
severe adverse effects after previous dose/s of wP vaccines or children
with neurologic disorders, if resources permit. The parents should be
counseled about the probable efficacy related disadvantages of using aP
vaccines for the primary series. The schedule is same as with wP (DTwP)
vaccines. Like DTwP vaccines, DTaP vaccines must not be used in children
7 years or older because of increased reactogenicity. The
contraindications are the same for both the vaccines.
There is no data on either the efficacy/effectiveness
of individual wP product or comparative evaluation of different
available wP combinations in the Indian market. Few brands in India have
achieved WHO prequalification, but not all the products have uniformly
attained it. IAP urges the government of India to undertake studies on
the quality of available wP and aP vaccines in Indian market. The
national regulatory authority (NRA) must set indigenous national
guidelines to manufacture and market different pertussis vaccines in the
The recommendation on the use of wP vaccine in
primary immunization series is based on the experience with wP vaccines
in India and on demonstration of faster waning with aP vaccines in
comparison to wP vaccines and superior priming with wP vaccines than aP
vaccines in studies conducted in the industrialized countries after
recent resurgence of pertussis in many of these countries using aP
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