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Home Eurosurveillance Weekly Release  2005: Volume 10/ Issue 33 Article 4
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Eurosurveillance, Volume 10, Issue 33, 18 August 2005

Citation style for this article: Grilc E, Pirnat N. Pertussis outbreak in recently vaccinated children in a kindergarten in Ljubljana during a resurgence in pertussis incidence. Euro Surveill. 2005;10(33):pii=2779. Available online:

Pertussis outbreak in recently vaccinated children in a kindergarten in Ljubljana during a resurgence in pertussis incidence

Eva Grilc ( and Nina Pirnat, Institute of Public Health, Ljubljana, Republic of Slovenia

Pertussis (whooping cough) is a mandatorily notifiable disease in Slovenia and since 1959, there has been an active national immunisation programmme. Since the start of this programme, the annual number of notified cases has fallen sharply [1]. Children are vaccinated (DTP (acellular)-Hib) with three doses at one to three month intervals, starting at the age of three months, with a booster one year after the third dose. Slovenia started to import acellular pertussis vaccine in 1997, and acellular vaccine has been used exclusively since 1999.

Table 1. Notified cases of whooping cough* from 1998 to 2002 in Slovenia

Year 1998 1999 2000 2001 2002 2003 2004
Number of notifications of pertussis in Slovenia 25 23 34 77 30 182 113
Morbidity / 100 000 inhabitants 1.2 1.1 1.7 3.8 1.5 30.2 18.7

Table 2. Notified cases of whooping cough* in the Ljubljana health region in years 1998 to 2004

Year 1998 1999 2000 2001 2002 2003 2004
Number of notifications of pertussis in the Ljubljana health region 6 0 10 23 3 44 46
Morbidity / 100 000 inhabitants 1.0 0 1.7 3.8 0.5 7.3 7.6

The Ljubljana health region has about 600 000 inhabitants (about one third of the entire Slovene population).

Outbreak of pertussis in a Ljubljana kindergarten, August 2004
The Institute of Public Health of Ljubljana was notified of a case of pertussis in a 16 month old boy, on 31 August 2004. The boy had received three doses of pertussis vaccination in the 12 months before becoming ill. The diagnosis was laboratory confirmed (RT-PCR and culture isolation).

A diagnosis of pertussis in the mother of the infant was also laboratory confirmed (IgM > 40,2 IE/ml, IgG > 500 IE/ml, Ig A 22.6 IE/ml). She had been fully immunised against pertussis in childhood. She worked in a prison where she had many contacts. There was no information about a possible source of infection.

The boy (index case), attended a kindergarten in Ljubljana. Four days after his onset of illness, another case of pertussis was confirmed (RT-PCR and isolation in culture) in the same group of children. The second case, also a boy, had been in close contact with the index case.

Epidemiological and clinical investigations revealed that at least three of the 12 children in the same kindergarten group as the index case had pertussis symptoms. Another six children in the same group had acute respiratory infection symptoms. All nine suspected cases were also laboratory tested (RT-PCR), but the results were negative. The children in the kindergarten group were between one and two years old. All the children had been immunised with three doses of DTP(acellular)-HiB. Less than a year had passed since the last immunisation. Children in other groups in the kindergarten were healthy, as were the teachers and parents of the ill children.
Control measures
All children in the same kindergarten group as the index case were given antibiotics (azithromycin), as were the children who were family contacts of the children with symptoms characteristic of pertussis. The kindergarten was thoroughly cleaned and disinfected.

Whooping cough is highly infectious, and before vaccination was introduced, almost all children became infected [2]. However, vaccination does not prevent the infection or asymptomatic carriage, and immunity wanes after vaccination. In recent years in the United States and Europe (for example, the Netherlands) pertussis in adolescents and young adults has been diagnosed more frequently [3].

The reason for a small outbreak of pertussis remains unclear. The cases were in young children who had been vaccinated according to the national vaccination programme. The occurrence of smaller outbreaks of whooping cough is not unexpected; what is unexpected is an outbreak in children who had all been vaccinated against the disease with acelullar vaccine less than one year previously.
Some hypotheses for this apparent vaccine failure are:

  • antigenic shift so that the circulating strains and vaccination strains of Bordetella pertussis diverge and vaccine efficacy is reduced
  • other factors, alone or in combination

To investigate the first hypothesis, B. pertussis strains that have been collected in Slovenia in recent years, should be characterised by sequencing surface protein genes. Changes in circulating B. pertussis have been reported in the Netherlands [2] and Australia [4]. The extent to which bacterial polymorphisms affect vaccine efficacy probably depends on the vaccine used [2], on the proportion of polymorphic bacteria in the human population, and other factors. Further studies are required to assess the effect of the antigen changes on the efficacy of pertussis vaccines.

Paediatricians and general practitioners should be aware of the possibility of pertussis occurrence in both children and adults. Continued surveillance of Bordetella strains/genome is very important..

Footnote: *Case definition used for pertussis notification in Slovenia:

A case is defined as a person with:

• either cough continuing for at least two weeks or cough in paroxysms;
• or paroxysms of coughing without intervening inhalation that are followed by a characteristic crowing or high pitched inspiratory whoop;
• or paroxysms of coughing followed by vomiting;
• or a cough with no other reason [1].

The laboratory criteria are:

• demonstration of a specific pertussis antibody response in absence of recent vaccination;
• detection of nucleic acid;
• isolation of Bordetella pertussis from a clinical specimen.

A possible case is one that meets the clinical case definition;
A probable case is one that meets the clinical case definition and has epidemiological link;
A confirmed case is one that is laboratory confirmed.

  1. Kraigher A. Analiza izvajanja imunizacijskega programa in drugih ukrepov za varstvo prebivalstva pred nalezljivimi boleznimi v Sloveniji v letu 2003 [Analysis of Active Immunization Programme and other Measures Against Infectious Diseases in Year 2003]. Ljubljana:Inštitut za varovanje zdravja republike Slovenije; 2004. [in Slovene]
  2. Mooi FR, Loo IHM, King A. Adaptation of Bordetella pertussis to Vaccination: A Cause for its Reemergence? Emerg Inf Dis 2001; 7(3): 526-528. (
  3. De Melker HE, Conyn-van Spaendonck MA, Rumke HC, van Wijngaarden JK, Mooi FR, Schellekens JF. Pertussis in The Netherlands: an outbreak despite high levels of immunization with whole-cell vaccine. Emerg Infect Dis 1997;3(2):175-178. (
  4. Poynten M, McIntyre PB, Mooi FR, Heuvelman KJ, Gilbert GL. Temporal trends in circulating Bordetella pertussis strains in Australia. Epidemiol Infect 2004; 132(2): 185-193.

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