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Eurosurveillance, Volume 3, Issue 11, 01 November 1998
Surveillance report
ESEN : a comparison of vaccination programmes Part two : pertussis

Citation style for this article: Lévy-Bruhl D, Pebody RG, Osborne K, Veldhuijzen I, Valenciano M. ESEN : a comparison of vaccination programmes Part two : pertussis. Euro Surveill. 1998;3(11):pii=86. Available online:

Daniel Lévy-Bruhl (coordinator), RNSP/CIDEF, France
Richard Pebody, NPHI/EPIET, Finland
Irene Veldhuijzen, RIVM, Netherlands,
Marta Valenciano, RNSP/EPIET, France
Kate Osborne (ESEN Project Coordinator), CDSC, England and Wales

from data provided, on behalf of the ESEN project, by:

 Anne-Marie Plesner, SSI, Denmark
Mary Ramsay, CDSC, England and Wales
Wolfgang Vettermann / Doris Altmann, RKI, Germany
Stefania Salmaso, Christina Rota, ISS, Italy
Richard Pebody, NPHI, Finland
Martine Le Quellec Nathan, DGS / Nicole Guérin, CIDEF, France
Marina Conyn-van Spaendonck, RIVM, Netherlands
Patrick Olin, Victoria Romanus, SIIDC, Sweden


This article is the second of a series of three, which compare vaccination programmes, immunisation schedules, vaccine coverage, and the epidemiological impact of vaccination for diphtheria, pertussis, measles, mumps, and rubella in eight countries (Denmark, England and Wales, Germany, Italy, Finland, France, the Netherlands, and Sweden). This analysis has been undertaken within the European Union funded European Sero-Epidemiology Network (ESEN) project (1). This article presents the results for pertussis.


The first paper of the series, which dealt with diphtheria vaccination, described the methods used in the analysis and the characteristics of the immunisation programmes (2). Briefly, ESEN’s national coordinators completed or arranged completion of questionnaires about their countries’ immunisation programmes early in 1997. The responses were analysed by an international group.


Immunisation schedule and coverage

Different perceptions among the participating countries of the balance between the benefits and the risks of pertussis vaccination with whole cell vaccine have led to important variations in coverage reached and in attitudes towards new acellular vaccines. The countries can be divided into two groups on the basis of primary vaccination coverage over the past 15 years (table 1).

Table 1: Pertussis immunisation schedules and disease incidence according to coverage performances in the 8 participating countries


Group 1: High coverage

Group 2: low coverage





England and Wales




Coverage in past 15 years


» 100%

94 % - 96 %


86 % - 90 %*

from 41 % (1980)
to 94 % (1995)


12-15 % (1985) 8-71% (1991) **

< 5 % (1980-90)
< 50 % (1991-95)
³ 95 % (1996)

Type of vaccine






ac + Ge
ac + Wc

ac + Ge
ac + Wc


Age at 1st dose

3 m

2 m

3 m

3 m

2 m

3 m

3 m

3 m

No doses < 1 year









Total No of doses







3- 4


Difference in coverage
diphtheria - pertussis

0% 1% 1% 7- 12 %

15 % - 4 % (1975-80)
2% (1993-95)


> 90% (1980-90)
> 50 % (1991-95)
< 5 % (1996)

Incidence per 100 000 (years range)

< 10 (1970-95) †


1 - 3.5
(1989 - 93)

10 - 100
< 10

10 - 100
(1974 - 90)
< 10
(1991 - 95)


10 -50
(1970 - 94)

100 - 160
(1987 - 96)

% of cases over 10 years (years range)

63% (1995 - 96)


(1989 - 95)

15 - 20 %
(1980- 93)

5 - 10 %
(1974 - 89)
(1994 - 95)


< 20 %
(1974 - 91)

< 5 % (1994)

ND = Pas de données / No data
Ge = Vaccin à germes entiers / Wc = Whole cell vaccine
ac = acellulaire / acellular

* Basé sur le vaccin à germes entiers ( vaccin acellulaire depuis janvier 1997) / Based on whole cell vaccine (shift to acellular in January 1997)
** Dans sept régions sélectionnées d'Italie / In seven selected regions of Italy
*** Une cinquième dose de vaccin acellulaire est recommandée depuis 1998 pour les 11 - 13 ans / A fifth dose with an acellular vaccine was introduced in 1998 at 11-13 years

† Excepté 4 années épidémiques / Except 4 epidemic years

In group one, Finland, France, and the Netherlands have very high coverage (>95%). There are either no official contraindications (as in the Netherlands) or those that exist do not affect coverage. Consequently, the need for a change to acellular pertussis vaccine for primary immunisation has not been felt necessary.

Group one also includes Denmark and England and Wales. In Denmark, coverage with whole cell vaccine was high for the first dose (96% - 98%), but dropped to 87% - 90% by the third dose, perhaps because reactions to the first and second doses were thought to constitute a contraindication. Acellular pertussis vaccine completely replaced the use of whole cell vaccine in 1997. In England and Wales, where only the whole cell vaccine is used, coverage has increased steadily from 41% in 1980 to 94% in 1995.

In the second group, (Italy, Sweden, and Germany) coverage has remained, until recently, much lower. In Sweden the coverage fell dramatically from 90% in 1974 to below 5% in the 1980s. It increased in the early 1990s but remained under 50%. In 1996, the introduction of the acellular vaccine into the national immunisation schedule, was followed by a swift rise in coverage to over 95% (P. Olin, personal communication). In Italy, cluster surveys of voluntary pertussis vaccination in the 1970s and 1980s suggested that coverage for three doses was between 7.6% and 71%. Uptake has increased since the introduction of acellular vaccine in 1995, and is now estimated to be 88%. In Germany, routine immunisation with whole cell pertussis vaccine ceased in 1976. In 1991 it was again recommended for routine immunisation and, in 1995, an acellular pertussis preparation was also approved. No data are available on vaccine coverage.

The types of vaccine used differ, but there is little variation in primary vaccination schedules. Between two and four doses are given in the first year of life: most countries give three. The total number of doses varies between three and four. In all countries the maximum age at which children were offered the vaccine (until 1997) was 2 years.

Surveillance and epidemiology

Pertussis is a notifiable disease in all countries except Germany and France. Among those countries with routine surveillance, only Italy and England and Wales have case definitions that do not require laboratory confirmation. The data provided by the participating countries are likely to vary in reliability. Most countries could not assess the quality of their surveillance systems. One potential source of variation is a failure to diagnose the disease in older age groups. Therefore comparisons between countries should be made cautiously. No analysis could be made for Germany, because no surveillance data exist, or for France, where notification ceased in 1985 and a hospital based paediatric sentinel surveillance system was implemented in 1996.

Pertussis is still endemic in the two countries that have had very high vaccine coverage (above 95%) for many years and where annual morbidity data are available (Finland and the Netherlands). Their annual incidences are between one and five cases per 100 000 and epidemic cycles are still seen. Finland experienced two outbreaks in 1983 and 1990-1991, with rates higher than 12 cases per 100 000. In 1995 and 1996, 63% of cases were at least 10 years of age. In the Netherlands, peak incidences were noted in 1989 and 1994 (3.5 and 3.4/100 000, respectively). In 1996, however, a sudden larger than expected increase in the incidence of pertussis (27.3/100 000) occurred before it was due, according to the usual three and five year cycle. Infant cases (1 to 11 months of age) accounted for only 6% in 1996 compared with 20% in 1989-1995. A larger proportion of cases were children aged 5 years and over in 1996 (67%) than in 1989-1995 (55%). Greater awareness, changes in diagnostic practices, or a lower vaccine coverage could not explain the epidemic. It has been suggested that changes in the circulating strain of Bortella pertussis could have resulted in a mismatch with vaccine induced immunity (4). In France, where the disease was thought to have almost disappeared, a resurgence of pertussis has been suspected, based on a study carried out in 1993-1994 (5).

The high coverage category also includes Denmark and England and Wales. In Denmark, very large outbreaks occurred in 1976 and 1977 with rates exceeding 300/100 000, but the incidence has since declined to <20/100 000 in 1986 and <10/100 000 in 1992-1993, the last years for which data for the whole population are available. Since 1987, the three to four year epidemic cycle seems to have virtually disappeared. Between 15% and 20% of cases from 1980 to 1993 were over 10 years of age. Vaccine coverage in England and Wales declined dramatically in the 1970s because of concerns about the safety of the whole cell vaccine preparation. Two major epidemics in England and Wales peaked in 1978 and 1982 (at rates of 130/100 000). Since 1982, coverage has improved gradually, resulting in a proportional decrease in incidence. The size of peaks has gradually decreased and the interepidemic period has lengthened since 1990, when high vaccine coverage was achieved for the first time. The proportion of cases 10 years old or older, based on clinical surveillance, was between 5% and 10% from 1974 to 1989, but since 1990 has steadily increased to reach 16% in 1994-1995.

The uptake of pertussis vaccine in Italy is poor, and the incidence of the disease has not decreased. The four year cycles are well documented and the average incidence is 20/100 000. This is probably an underestimate, given the data from countries with much higher vaccine coverage. About 10% of cases are over 10 years of age. In Sweden, the annual reported incidence of culture confirmed cases of pertussis was less than 20/100 000 during the 1970s. After vaccination was discontinued in 1979, the incidence increased sharply to an annual rate of over 100/100 000 from the mid-1980s onwards.


The comparability of pertussis surveillance data is more questionable than for diphtheria as both the case definition and the accuracy of the surveillance data vary between countries. Nevertheless, we identified two different situations with regard to the level of control of the disease. Differences in vaccination schedules between countries for parameters such as age of completion of the first series and total number of doses/boosters are few and seem not to play an important role in differences in the current epidemiological profile of the disease. As for diphtheria, vaccine coverage in children seems to be the main factor that determines pertussis incidence. The history of pertussis vaccine coverage shows how varying perceptions by the public and health professionals of the value of vaccines and their safety can lead to very different decisions and levels of effectiveness of vaccination programmes (6). Even in countries where coverage has been very high for a long period, however, B. pertussis is still circulating and epidemics still occur. The proportion of cases over 10 years of age increases with coverage as shown by comparisons within and between countries. This is mainly because vaccine induced immunity is lost in older children in the absence of natural boosting with wild pertussis bacteria, whose circulation has fallen dramatically (7). In England and Wales the susceptibility in older cohorts could be also explained by lower coverage when they were scheduled to receive the vaccine. Unlike some other communicable diseases, the severity of pertussis decreases with increasing age of infection, although adult cases may be a reservoir for infants too young to have been protected by a full series of primary vaccinations (8). These factors have been used to call for a booster dose in older members of the population.

Concerns about the perceived risk of vaccine related adverse events associated with a whole cell booster (9), however, have led two of the group one countries to introduce or plan to introduce the acellular vaccine as a booster. In France, the 1998 immunisation schedule includes an acellular booster at 11 to 13 years and in the Netherlands, a trial starts in 1998 on the effect of a booster dose of acellular vaccine at 4 years of age. In addition, in Sweden, a study of a booster of acellular pertussis vaccine given at 4, 5, or 6 years of age is in progress.

In group two countries the age distribution of cases does not show a significant shift in infection towards older age groups. Thus increasing and maintaining the coverage of the primary series to over 95% seems to be the priority rather than introducing booster doses.

It is too early to assess the impact on the current incidence of the disease of the very recent introduction of acellular pertussis vaccine either in the primary series or as a booster dose. Preliminary data show, however, that in countries where the acellular vaccine for primary immunisation has been adopted, coverage of pertussis vaccine is increasing tremendously.


1. Osborne K, Weinberg J, Miller E, The European Sero-Epidemiological Network, Eurosurveillance 1997; 2: 29-31.

2. Lévy-Bruhl D, Pebody R, Veldhuijzen I, Valenciano M, Osborne K. ESEN: a comparison of vaccination programmes. Eurosurveillance 1998; 3: 93-6.

3. Salmaso S, Rota MC, Ciofi degli Atti ML, Anemona A, Tozzi AE, Kreidl P and ICONA working group. Preliminary results from ICONA: national survey on vaccination coverage. Ann Ig 1998; 10: 37-43

4. De Melker HE, Conyn-van Spaendonck MAE, Rümke HC, van Wijngaarden JK, Mooi FR, Schellekens JFP. Pertussis in the Netherlands: an outbreak despite high levels of immunization with whole-cell vaccine. Emerging Infectious Diseases 1997; 3: 175-8.

5. Baron S, Njamkepo E, Grimprel E, Begue P, Desenclos JC, Drucker J et al. Epidemiology of pertussis in French hospitals in 1993 and 1994: thirty years after a routine use of vaccination. Pediatr Infect Dis J 1998; 17: 412-18.

6. Gangarosa EJ, Galazka AM, Wolfe CR, Phillips LM, Gangarosa RE, Miller E, et al. Impact of anti-vaccine movements on pertussis control: the untold story. Lancet 1998; 351: 356-61.

7. Cherry JD. Historical review of pertussis and the classical vaccine. J Infect Dis 1996; 174: S259-63.

8. Wirsing von König CH, Postel-Multani S, Bock HL, Schmit HJ. Pertussis in adults: frequency of transmission after household exposure. Lancet, 1995; 346:1326-9.

9. Linnemann CC, Ramundo N, Ferlstein PH, Minton SD. Use of pertussis vaccine in an epidemic involving hospital staff. Lancet 1975; 540-3.

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