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Vaccine
Safety > Research
Impact of Anti-Vaccine Movements on
Pertussis Control: The Untold Story
As published in Lancet, January 1998; 351(9099): 356-361.
| Authors: |
REJ
Gangarosa, AM Galazka, CR Wolfe, LM Phillips, RE Gangarosa, E Miller and RT Chen. |
ABSTRACT
To assess the impact of anti-vaccine movements that targeted pertussis
whole-cell vaccines, we compared pertussis incidence in countries where high coverage with
diphtheria-tetanus-pertussis vaccines (DTP) was maintained (Hungary, the former East
Germany, Poland, and the United States) with countries where immunization was disrupted by
anti-vaccine movements (Sweden, Japan, the United Kingdom, The Russian Federation,
Ireland, Italy, the former West Germany, and Australia). Pertussis incidence was 10
to 100 times lower in countries where high vaccine coverage was maintained than in
countries where immunization programs were compromised by anti-vaccine movements.
Comparisons of neighboring countries with high and low vaccine coverage further underscore
the efficacy of these vaccines. Given the safety and cost-effectiveness of
whole-cell pertussis vaccines, our study shows that, far from being obsolete, these
vaccines continue to have an important role in global immunization.
INTRODUCTION
Of the vaccine-preventable diseases, pertussis rivals measles and neonatal
tetanus in importance and severity among young children in the developing world. Millions
of cases and hundreds of thousands of deaths occur each year. Complications are common:
pneumonia in 15% of infants under 6 months of age, and severe neurological sequelae
in 0.1 to 4.0% of patients. Pertussis is an exhausting illness that often lasts months
(1). Because the disease is so serious and so difficult to treat, prevention is paramount.
Whole-cell vaccines, whether monovalent or in
diphtheria- tetanus-pertussis
(DTP), have been important in the control of pertussis (1). The decrease in pertussis
incidence resulting from vaccination may have created the impression that pertussis was
becoming milder and more scarce owing to medical and social development (2,3). As
pertussis became rarer, attention shifted from the disease to the adverse events- often
unrelated- that sometimes follow vaccination (4). In several countries, publicity
surrounding such adverse events gave rise to movements opposed to whole-cell pertussis
vaccination. This paper describes these anti-vaccine movements, their impact on pertussis
control, and the future role of whole-cell pertussis vaccines.
METHODS
We searched the literature, studied English translations of contemporary
news stories, and analyzed country-specific incidence of pertussis , whole-cell vaccine
coverage, and vaccination schedules from data compiled by the United States Centers for
Disease Control and Prevention (CDC), and by the World Health Organization (WHO). We also
studied books and other publications intended for lay audiences written by advocates
against vaccination. From available relevant data, we compared the pertussis experiences
of two groups of countries.
Group I includes countries in which use of whole-cell pertussis vaccine
(in DTP) has lasted decades- e.g., Hungary, the former East Germany, Poland, and the
United States (US). These countries have provided comprehensive DTP coverage with little
or no interruption by anti-vaccine movements.
Group II includes countries in which peer-reviewed publications documented
that anti-vaccine movements affected pertussis-control programs. We defined opposition to
whole-cell pertussis vaccines as activities of groups that actively or passively opposed
use of the vaccines. Sweden, Japan, the United Kingdom (UK), and The Russian Federation
had active opposition to whole-cell vaccines — that is, well-organized movements that
sought to stop their use by means of news stories, television interviews, lectures,
popular articles, books, and other writings. Distraught parents whose children suffered
adverse events blamed on whole-cell pertussis vaccination featured prominently. Some
outspoken medical authorities became leaders in these movements.
Italy, the former West Germany, Ireland, and Australia had less organized,
passive movements against whole-cell
pertussis vaccines, in which health-care providers withheld vaccines because of safety
concerns. Religious groups that oppose vaccination have been most prominent in passive
movements against the vaccines. Parents concerned about vaccine safety did not feature
prominently in passive movements. Characteristics of active and passive movements often
overlap. Practitioners and followers of natural, alternative and chiropractic medicine,
and homeopathy, have been prominent in both active and passive anti-vaccine movements.
We used country-specific incidences reported to WHO to compare
pertussis-vaccination experiences. The numerator is number of cases, the denominator is
per 100,000 of the total population. These data underestimate true incidence: pertussis is
underdiagnosed, especially without classic whoop and paroxysmal cough; laboratory
capabilities vary substantially; cultures are rarely undertaken for cases not
admitted to hospital; reporting systems are usually passive; and surveillance efficiency
varies from country to country. Although not quantitatively precise, surveillance data
show overall trends and patterns (1,5) .
FINDINGS
Group I: Countries with Sustained Use of Whole-Cell Pertussis Vaccines
HUNGARY- Hungary’s pertussis-control program has been exemplary (6) .
Surveillance, including mandatory reporting, began in 1931. Immunization with whole-cell
pertussis vaccine has continued without interruption since 1955. Vaccine coverage with
three primary and two booster doses has been nearly 100%. Reported incidences fell from
more than 100 per 100,000 in the prevaccine era to less than one per 100,000 after
vaccination, where they have remained for almost 30 years (figure 1).
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THE FORMER EAST
GERMANY- Germany before unification provides striking
contrast in pertussis experiences. The former West Germany adopted a non-compulsory
vaccination policy, resulting in low coverage. The former East Germany, however, achieved
control (figure 1) by requiring vaccination to consist of three primary doses and a single
booster dose of DTP. Thus, in 1989 DTP coverage in the former East Germany was 95%. The
country had only one to two cases per 100,000 during 1980-1990, whereas the former West
Germany had an incidence well over 100 times higher (7).
POLAND- Since 1960, pertussis has been controlled in Poland by means of a
schedule of three primary doses and a single booster dose, resulting in more than 95%
coverage. Reported incidence fell from 100-200 per 100,000 in the prevaccine era to
about one per 100,000 after vaccination (figure 1).
UNITED STATES- Pertussis has been controlled in the US, though there has
been an upward trend in incidence since 1981 (figure 1). Concerns over safety of
whole-cell pertussis vaccine peaked in the early 1980s after the television program
"Vaccine Roulette" and publication of the book A Shot in the Dark (8).
These gave rise to a movement against whole-cell vaccines, instigated several lawsuits
against vaccine manufacturers, substantially increased vaccine prices, and caused some
companies to stop production of the vaccines (4). Nevertheless, several developments
have favored pertussis control. Vaccines manufactured in the US have generally been highly
efficacious (9,10). Pediatric and primary-care organizations have strongly advocated
vaccination. School-entry immunization requirements further contributed to 90-95% DTP
coverage at primary- school entry. A strong infrastructure promotes vaccination,
surveillance of adverse events, and, since 1988, compensation for post-vaccination
injuries (4, 11).
Group II: Countries with Pertussis-Control Programs Affected by Active
or Passive Movements Against Whole-Cell Vaccines.
This group initially had varying success in controlling pertussis- first
with monovalent whole-cell vaccine and subsequently with DTP. Reported incidence exceeded
100 per 100,000 in the late 1940s and early 1950s, when vaccination programs began.
Coverage accelerated during the 1960s, reaching roughly 80% during the 1970s. The
consequent fall in reported incidence, ranging from ten-fold to 100-fold, set the stage
for movements against whole-cell pertussis vaccines.
SWEDEN- Pertussis vaccination began in the 1950s. A substantial drop in
incidence followed. In 1967, an influential medical leader, Justus Ström, claimed that
pertussis had become a milder disease owing to economic, social, and medical progress;
this claim led him to question the need for pertussis vaccines (2). By 1975, Swedish
pediatricians had lost confidence in the vaccine as the incidence of pertussis increased.
Some cases occurred in immunized children, and some neurological events were blamed on the
vaccine. DTP coverage decreased rapidly from 90% in 1974 to 12% in 1979 (12). In 1979, the
Swedish medical society abandoned whole-cell pertussis vaccine and decided to wait for a
new, safer, more effective vaccine- a strategy that was soon adopted as national policy.
During 1980-1983, annual incidence for children aged 0-4 years increased to 3370 per
100,000 (12), with rates of serious complications approaching global rates (1). In
subsequent years, Sweden reported more than 10,000 cases annually with an incidence
exceeding 100 per 100,000, comparable to rates reported in some developing countries
(figure 2) (1).
JAPAN- Vaccination against pertussis began in 1947. By 1974, there were
few cases and no deaths (13). During a national debate about adverse events resulting from
smallpox vaccine, news reports of neurological reactions after DTP vaccination gave rise
to Japan’s movement against whole-cell pertussis vaccines. Activists alarmed the
public with "unbalanced arguments concerning vaccine risks" and claimed that
"vaccination would no longer be needed" because "there was practically no
more pertussis in the community" (14). The national debate effectively created
"a social problem" (15). In response, the Okayama Prefectural Medical
Association switched from DTP to diphtheria-tetanus vaccine (DT) only. After two infants
died within 24 hours of receiving DTP, the Ministry of Health and Welfare eliminated
whole-cell pertussis vaccine altogether. They later allowed it only for children older
than two years. Pertussis coverage for infants fell from nearly 80% in 1974 to 10% in 1976
(13). A pertussis epidemic occurred in 1979 with more than 13,000 cases and 41 deaths.
Japan began replacing whole-cell with acellular pertussis vaccines in 1981, and striking
fall in pertussis incidence followed (figure 2).
UK- After a 1974 report, ascribing 36 neurological reactions to whole-cell
pertussis vaccine (16), persistent television and press coverage interrupted a successful
vaccination program (figure 2). A prominent public health academic, Dr. Gordon Stewart,
claimed that the protective effect of the vaccine was marginal and did not outweigh its
danger (3). Others reached opposite conclusions based on the fall in pertussis incidence
after introduction of the vaccine in the 1950s (17). Although health authorities resisted
pressure to withdraw the vaccine, loss of confidence in it led to a sharp reduction in
coverage. Pertussis epidemics followed (figure 2). Confidence was restored after
publication of a national reassessment of vaccine efficacy that showed "outstanding
value in preventing serious disease" (18). Provision of financial incentives for
general practitioners who achieved the target of vaccine coverage contributed to the
recovery (19) . Disease incidence declined dramatically, and
has since been low (figure 2).
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THE RUSSIAN
FEDERATION- The Soviet Union assigned high priority to
compulsory immunization, thereby achieving control of vaccine-preventable diseases,
including pertussis. The anti-government bias of Perestroika gave rise to an active
anti-vaccine movement that targeted DTP. Inspired by the virologist Galina
Chervonskaya,
the mass media initiated an active campaign to discredit vaccination. Another prominent
physician, A. V. Pichnohkov, asserted that the vaccine would cause leukemia and was
"stressful" for the child’s system. Chervonskaya, Pichnohkov, and other
pediatricians have propounded an excessive list of contraindications, specifying more than
50 diagnoses in which DTP vaccine should not be given. A series of "unbalanced
statements" about the dangers and ineffectiveness of vaccines were featured in
medical journals, on radio, on television, and in the popular press. Parents and
physicians lost confidence in vaccines, and chose not to immunize children. DTP coverage
fell by 30%, setting the stage for diphtheria and pertussis epidemics (20). Along with
perhaps the largest postwar diphtheria outbreak, The Russian Federation has reported one
of the highest incidences of pertussis in the developed world (figure 2).
IRELAND- Ireland’s vaccination program initially lowered pertussis
incidence from 79 per 100,000 in 1955 to about 10 per 100,000 in the mid 1970s. The trend
reversed in the mid-1970s with opposition to whole-cell pertussis vaccine in the UK (21).
Vaccine coverage fell from more than 60% in the early 1970s to 30% after 1976. Epidemics
occurred in 1985 and 1989. In 1990, only 65% of infants had received three primary doses.
Incidence remained higher than 10 per 100,000 through 1993 (figure 3).
ITALY- Binkin and colleagues (22) studied pertussis in Italy (figure 3)
using a national vaccination-coverage survey done in 1985, sales data from vaccine
manufacturers, and Italy’s infectious-diseases surveillance system. Fewer than 40% of
children under five years were vaccinated, and about 25% had experienced clinical
pertussis by the age of five years. Among children younger than one year, one in 14 was
admitted to the hospital for pertussis, and one in 850 of these admissions died. The
reported annual incidence between 1980 and 1989 was 22 times higher than in the US. A
seroepidemiological study of pertussis by Stroffolini and colleagues confirmed "a
great exposure of children" and "extremely low" vaccine coverage in Palermo
(23). In a 1991 telephone survey
(22), Binkin found that pediatricians’ attitudes about whole-cell pertussis vaccine
varied widely. In some regions only 20% of pediatricians recommended DTP, compared with
100% in other regions. By contrast, another survey showed that mothers accepted the
vaccine- 87% perceived pertussis as a dangerous disease, 69% were aware that the vaccine
was available, 90% believed that the vaccine was protective, and 87% said they would
accept their pediatricians’ advice on vaccination. Binkin reported that the
factors that gave rise to Italy’s pertussis dilemma were the attitudes, knowledge,
and practices of physician providers (22). In 1995, only 50% of children in Italy had
received three primary doses and a single booster as part of their routine schedule.
AUSTRALIA- Australia controlled pertussis during the 1970s, with an
incidence rate as low as 1 per 100,000 (figure 3). However, confidence in the vaccine
waned when news was received from the UK about alleged neurological reactions associated
with the vaccine (24). In a postal survey from the early 1990s, McIntryre and Nolan found
that up to 58% of randomly selected vaccine providers would give DT when DTP was indicated
(25). In 1993, Lester and Nolan warned that "geographically clustered populations of
children who have inadequate pertussis protection could promote epidemic outbreaks"
(25). A large outbreak with more than 5000 cases occurred in 1994 (figure 3).
Dr. Viera
Scheibner, Australia’s prominent opponent of whole-cell
pertussis vaccines, claims that these vaccines are ineffective and "constitute an
assault on the immune system". Her 1996 book has been marketed as "the most well
documented evidence against vaccines to be found anywhere in the world" (26).
THE FORMER WEST
GERMANY- The contrast between the former West Germany and
East Germany provides perhaps the most striking example of the national danger of
anti-vaccine movements. Finger and colleagues analyzed
vaccination histories and incidence of pertussis among West German children at school
entrance (7). Coverage with whole-cell pertussis vaccine was fairly constant at 11.0% and
11.2% for children born in 1976 or in 1983, respectively. Pertussis was reported from 35%
(1976) and 37% (1983) of these children. The authors estimated that incidence in West
Germany was 180 per 100,000 during this period. They attributed the high incidence to
health-care providers who believed the disease to be a "normal" childhood
illness.
Contrasting Experiences of Neighboring Countries with High and Low DTP
Protection, 1985-1995.
The efficacy of whole-cell vaccine is also evident in the comparison of
experiences in adjacent countries with different DTP protection- measured by the
percentage of infants covered and the number of primary and booster doses in immunization
schedules. Without complete information, we assume a generally uniform whole-cell vaccine
efficacy with the exception of reported anomalies (27)- e.g., low efficacy in Canada (28)
and in a 1996 field trial in Europe (29) . Higher vaccine coverage in Norway, Portugal,
Hungary and the US corresponded to a pertussis incidence 10 to 100 times smaller than in
each country's respective lower-protective neighbor-i.e., Sweden, Spain, Greece, and
Canada (figure 4). The most striking comparison, between the former West Germany and East
Germany, cannot be quantified because pertussis was not reportable in West Germany.
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DISCUSSION:
Our findings provide strong evidence of a causal relation between
movements against whole-cell pertussis vaccine and pertussis epidemics, based on
Hill’s criteria (30): strength of association (e.g., incidence ratios
exceeding 100 to 1, Sweden vs. Norway; 150 to 20 comparing peak incidence for Sweden in
1990 during antivaccine era vs. Sweden in 1972 with highest whole-cell vaccine coverage);
consistency of findings under different surveillance systems, time periods, and
populations; specificity of infection affecting primarily unvaccinated or undervaccinated
individuals; temporal relation (epidemics follow cessation of vaccination and recede with
resumed vaccine coverage); biological gradient (dose-response effect seen- e.g., in
incidence vs. vaccine coverage in the UK, 1963-95); plausibility that vaccination is
protective, that herd immunity suppresses transmission, and that successful
disease-control encourages complacency (4); coherence of evidence- i.e., no conflict with
the natural history of pertussis; and experimental evidence plus analogy- e.g.,
smallpox eradication, in which high vaccine coverage prevents disease through mass
vaccination and surveillance containment strategies.
This study shows overall trends, though not a precise comparison of
reported incidence, since practices of pertussis diagnosis and surveillance differ
according to country (1). A policy against whole-cell pertussis vaccination had a
qualitatively similar adverse impact in Sweden, Japan, the UK, The Russian Federation,
Ireland, Italy, the former West Germany, and Australia. Conversely, sustained vaccination
has controlled pertussis in Hungary, Poland, the former East Germany, and the US. A
dose-response relation is evident: extremes of vaccination coverage (e.g., Hungary vs.
Sweden) spanned reported incidence of 10 to 100 times, whereas smaller differences in
coverage or efficacy (e.g., US vs. Canada) showed intermediate effects.
Anti-vaccine advocates do not mention, minimize, or deny the consequences
of compromised immunization programs (8,26). This article documents those
consequences. Cases among children deprived of vaccine may have exceeded hundreds of
thousands, and disease-related clinical complications (e.g., pneumonia,
encephalopathy,
and seizures) may have numbered tens of thousands. Anti-vaccine movements have had
some beneficial effects. Their call for safer vaccines underscored the need for
acellular vaccines against pertussis, and their efforts have encouraged surveillance of
adverse events and the development of vaccine-injury compensation programs.
Our findings also corroborate Fine and Clarkson’s analysis (31) that
once high vaccine uptake and herd immunity are attained, perceived vaccine risks tend to
deter individuals from being vaccinated. The result is a lowering of vaccine uptake,
contrary to the community’s common interest maintaining high numbers of immunized
individuals. What follows is a "tragedy of the commons" -- a loss of confidence
in vaccine and a resurgence of disease (32). These tragedies were abetted by anti-vaccine
advocates through unbalanced news media accounts of perceived vaccine risks (33). Some of
these advocates have been prominent figures in science and medicine (2,3,26,34). They have
argued that vaccines compromise the immune system, inappropriately questioned vaccine
efficacy when sporadic cases occurred in immunized children (35), advocated a long list of
unwarranted contraindications to vaccination, warned that adverse events to the vaccine
might be more common than reported, and attributed "disappearance" of pertussis
to social and medical developments rather than vaccination. These messages undermined
confidence in whole-cell pertussis vaccines, and, though discredited in the medical
literature, are still commonly cited in anti-vaccine literature (8,26).
Severe side-effects of whole-cell pertussis vaccines are so rare that they
defy measurement. The American Academy of Pediatrics, the US’s National Vaccine
Advisory Committee, and the Advisory Committee on Immunization Practices, concur that
whole-cell pertussis vaccine is not a proven cause of brain damage, sudden infant death
syndrome (SIDS), infantile spasms, or Reye’s syndrome (36,37). Anaphylactic reactions
to DTP components are exceedingly rare. In the US, lawsuits have favored plaintiffs
alleging complications related to whole-cell pertussis vaccination, but the High Court of
the UK ruled that a causal link had not been proven (38). Mild local and systemic
reactions (fever, fussiness, drowsiness, and brief loss of appetite) are fairly common
with the vaccine, whereas moderate reactions (long periods of crying, sometimes with an
unusually high pitch, limpness, and pallor) are rare.
Since acellular vaccines cause fewer side-effects (9,27,29) some developed
countries (e.g., the US) plan to switch to such vaccines after using up existing supplies
of whole-cell pertussis vaccine. However, use of whole-cell pertussis vaccines in the UK
will probably continue pending studies of acellular pertussis vaccine's relative efficacy,
reactivity, and compatibility with Haemophilus influenzae type-B vaccine (39).
The choice between whole-cell and acellular pertussis vaccines involves trade-offs between
safety, efficacy, practicality, and cost. In addition to fewer mild or moderate reactions,
acellular vaccine could interrupt disease transmission by means of its potential use in
adolescents and adults. However, the best acellular vaccines may not provide protection
equal to that of the best whole-cell vaccines (27). Replacement of whole-cell pertussis
vaccines with acellular vaccines might conceivably lead to less effective control at
substantially higher costs. Despite the advantages of acellular vaccines, we believe that
lower costs and better protection are compelling reasons for use of whole-cell pertussis
vaccines to continue in many countries, particularly those with limited resources (40).
Scientists and physicians who choose acellular vaccine for their country have a
special responsibility to strengthen their surveillance to monitor disease impact, costs,
and rare adverse events-information that will guide others in the future.
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Whereas our study focused on morbidity following anti-vaccine movements
against whole-cell vaccines, other reports indicate that pertussis mortality also
increased. Excess sudden postperinatal deaths were inversely related to vaccination
coverage during pertussis outbreaks in several observational studies and in two ecological
studies--one in the UK (41) and the other in Scandinavia (42).
TABLES
AND FIGURES
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