An ongoing measles outbreak in Bulgaria, 2009.

Abstract

After seven years without indigenous transmission of measles in Bulgaria, an increasing number of cases have been reported since 15 April 2009. By 19 June, the total number of notifications reached 84. To date, 64 were confirmed as measles cases and 15 cases, for whom laboratory results are pending, have been classified as probable. The present measles outbreak affects mostly the Roma population living in the north-eastern part of the country. The most affected age groups are young children below 1 year of age and children 1 to 9 years of age. An immunisation campaign was started in the affected administrative regions, targeting all persons from 13 months to 30 years of age who had not received the complete two-dose MMR vaccination.

Full text

Page 1

EUROPEAN CENTRE FOR
DISEASE PREVENTION
AND CONTROL
Volume 14, Issue 26 - 2 July 2009
Rapid communications
An ongoing measles outbreak in Bulgaria, 2009
by L Marinova, M Kojouharova, Z Mihneva
2
Plague outbreak in the Libyan Arab Jamahiriya
by A Tarantola, T Mollet, J Gueguen, P Barboza, E Bertherat
5
PModelling of the influenza A(H1N1)v outbreak in Mexico City, April-May 2009, with control sanitary measures
by G Cruz-Pacheco, L Duran, L Esteva, AA Minzoni, M López-Cervantes, P Panayotaros, A Ahued Ortega, I Villaseñor Ruíz
8
The emerging influenza pandemic: estimating the case fatality ratio
by N Wilson, MG Baker
11
Research articles
StatFlu - a static modelling tool for pandemic influenza hospital load for decision makers
by M Camitz
15
News
ECDC guidance on chlamydia control in Europe: next steps
by MJ van de Laar , J Fontaine
22

Page 2

2 EUROSURVEILLANCE Vol. 14 · Issue 26 · 2 July 2009 · www.eurosurveillance.org
Rapid communications
An ongoi ng m eAsles outbreAk i n bu lgAriA, 2009
L Marinova (lmarinova@ncipd.org)1, M Kojouharova1, Z Mihneva1
1. National Centre of Infectious and Parasitic Diseases, Sofia, Bulgaria
After seven years without indigenous transmission of measles in
Bulgaria, an increasing number of cases have been reported since
15 April 2009. By 19 June, the total number of notifications
reached 84. To date, 64 were confirmed as measles cases and 15
cases, for whom laboratory results are pending, have been classified
as probable. The present measles outbreak affects mostly the Roma
population living in the north-eastern part of the country. The most
affected age groups are young children below 1 year of age and
children 1 to 9 years of age. An immunisation campaign was started
in the affected administrative regions, targeting all persons from
13 months to 30 years of age who had not received the complete
two-dose MMR vaccination.
Introduction
Measles has been a notifiable disease in Bulgaria since 1921.
National case-based notification was initiated in 2004 and the
European Union (EU) case definition and case classification have
been adopted since 2005 [1,2]. The Bulgarian National program
for elimination of measles and congenital rubella infection (2005-
2010) was approved by the Council of Ministries of Republic of
Bulgaria in 2005 [3].
Measles immunisation was introduced in Bulgaria in 1969
[4] and in 1972 it became universal. Until 1982 the routine
vaccination included one dose measles vaccine administered at
≥10 months of age. During the period 1983-1992 a two-dose
schedule using monovalent measles vaccine was applied, firstly at
12 months and 4 years of age, and later at 12 and 24 months of
age. In 1993, the measles, mumps, rubella (MMR) vaccine was
introduced into the national vaccination schedule. Until 2000,
the routine measles immunisation consisted of the first dose with
MMR vaccine given at 13 months of age and the second dose
with monovalent measles vaccine at 12 years of age. Since 2001
a routine two-dose immunisation with MMR vaccine has been
implemented, administered at 13 months and 12 years of age.
According to the official data, collected by the National Center of
Health Information, the vaccine coverage in Bulgaria with MMR
is high (Table).
The last indigenous cases of measles in Bulgaria were reported
in 2001 [5]. From 2002 to 2008 only six measles cases have been
registered, all of them imported: three from China (2005); one from
Ukraine (2006); one from Germany (2007) and one from United
Kingdom (2008) [6,7].
Ta b l e
National immunisation coverage with measles, mumps,
rubella (MMR) vaccine, Bulgaria, 2005-2008
MMR dose2005200620072008
First dose (13 months) 96.2%95.7%96.0%95.9%
Second dose (12 years)92.4%93.3%94.0%94.3%
F i g u r e 1
Number of probable and confirmed measles cases reported in Bulgaria between 15 April and 19 June 2009, by date of
notification (n=79)
11
4
33
111
2
11111
2
3
2
8
1
5
1
3
7
2
5
1
22
1
3
1
6
11
0
05.04
1
2
3
4
5
6
7
8
9
15.04
21.04
23.04
25.0427.04
29.04
05.05
08.05
12.05
16.05
21.0525.05 27.05
31.05
01.06
03.06
06.06
08.0610.06
12.0614.06
16.06
18.06
Date
Number of cases

Page 3

EUROSURVEILLANCE Vol. 14 · Issue 26 · 2 July 2009 · www.eurosurveillance.org
3
Outbreak description
After seven years without indigenous transmission of measles in
Bulgaria, an increasing number of cases have been reported since
15 April 2009 (Figure 1).
By 19 June, the total number of notifications reached 84.
Of these, five were discarded (one patient who presented with a
rash 10 days after MMR vaccination was considered as a case of
adverse events following immunisation (AEFI), and four suspected
cases tested IgM-negative). Of the remaining 79, to date, 64
were confirmed as measles cases (61 laboratory-confirmed by the
National Reference Laboratory for Measles, Mumps and Rubella in
Sofia, and three having clinical symptoms and an epidemiological
link with laboratory-confirmed cases); the remaining 15 cases
for whom laboratory results are pending, have been classified as
probable.
The epidemiological investigation demonstrated that the
index case was imported in March from Germany. The patient, a
24-year-old man, became ill on 12 March, four days after arrival
from Hamburg, where he works. The initial symptoms included
high fever, cough, runny nose, malaise and rash, developed three
days later. The clinical presentation was compatible with measles
and fulfilled the clinical criteria of measles. The patient was not
hospitalised but consulted an infectious diseases specialist. A
serum sample was tested and the case was classified as confirmed
by the National Reference Laboratory and notified as an imported
case (included in Figure 1).
The subsequent three measles cases occurred among his close
contacts (family members). They were laboratory-confirmed by the
National Reference Laboratory in Sofia. The samples were then
sent to the WHO Regional Reference Laboratory (RRL) for Measles
and Rubella in Berlin for reconfirmation and measles virus (MV)
genotyping. The nucleotide sequences of the variable part of measles
virus N gene (450 nt) derived from these three cases were identical
and classified as genotype D4. Their sequence is represented by
the official WHO name MVs/Shumen.BGR/15.09/1(D4). Later on
samples collected from four further cases in epi-week 21 were
sent to the RRL Berlin. The sequences derived from these cases
(represented by MVs/Silistra.BGR/21.09/1[D4]) were identical
to MVs/Shumen.BGR/15.09/1[D4] demonstrating that the seven
analysed cases belonged to a single chain of MV transmission.
The same genetic variant of MV was previously detected during an
outbreak observed between January and June 2009 in northern
Germany. This confirms the assumption that the Bulgarian index
case was imported from Hamburg. Outbreaks due to the introduction
of imported MV (D6, D4 and B3) into the hard-to-reach populations
were recently reported also from other European countries [8]. The
strain name MVs/Shumen.BUL/15.09(D4) was included in the
WHO/EURO CISID database. [Information in this paragraph was
kindly provided by Dr Annette Mankertz and Dr Sabine Santibanez
from the Robert Koch-Institut, Berlin, Germany].*
All 78 cases following the index case occurred as a result of
local transmission and were shown to be epidemiologically linked.
The present measles outbreak affects mostly the Roma
population living in the north-eastern part of the country – in
Razgrad, Shumen, Silistra and Dobrich regions (Figure 2). This
population is characterised by large families living together and
frequently moving from one place to another, looking for seasonal
work in Bulgaria as well as abroad. Until now, several family clusters
have been registered among this group.
The outbreak affects both genders almost equally, with male
to female ratio 30/49. The most affected age groups are young
children below 1 year of age (non-immunised because of the
young age) and children 1 to 9 years of age, who are eligible to
immunisation.
Because of the crowded households and poor living conditions
of affected Roma families a large proportion of cases (51 of 79,
64.5%) were hospitalised. Complications were observed in 46.8%
of cases (37/79): 33 cases developed pneumonia and four cases
had abdominal disorders with diarrhea and acute abdominal pain.
The immunisation status of all reported 79 measles cases is
shown in Figure 3.
Considering the age of cases, 68 of the total of 79 measles
cases should have been immunised with at least one dose of
measles vaccine. However, in the majority of cases (n=43,
54.4%) the vaccination status was unknown because of the lack
of documentation. Twenty-two cases were known not to have been
vaccinated (including 11 below the age of one year). Only seven
cases (10.3%) have received one dose and another seven (10.3%)
F i g u r e 3
Distribution of reported measles cases by immunisation
status and age group, Bulgaria, April-June 2009 (n=79)
7
10
2
66
7
4
1
11
7
1
1
1
1
1
1
1
1
1
2
2
1
2
1
1
0
2
4
6
8
10
12
14
16
18
under 1
1-4
5-9
10-14
15-19
Age groups
20-24
25-29
30-34
35-39
40+
Number of measles cases
unknown immunisation status
0 doses
1 dose
2 doses
F i g u r e 2
Measles cases spread by regions, Bulgaria, April-June 2009
(n=79)

Page 4

4 EUROSURVEILLANCE Vol. 14 · Issue 26 · 2 July 2009 · www.eurosurveillance.org
both doses of the measles vaccine. Of note is that among those
immunised with two doses, three cases received the second dose
during the catch-up campaign organised in response to the outbreak
in May 2009, and it is most likely that they were harbouring
a measles infection in the incubation period during that time,
because soon after the immunisation, they fell ill with measles.
Control measures
The outbreak and the investigations are still ongoing, and
therefore the data presented are preliminary. The public health
authorities expect more cases to occur, especially among the Roma
population.
The control measures are in progress: the Bulgarian Ministry of
Health issued a press release regarding the situation and future
immunisation and surveillance activities. General practitioners and
other medical staff were requested to pay special attention to rash/
fever symptoms and to strengthen routine immunisation of children
aged 13 months (first dose) and 12 years (second dose) by directly
reaching the parents and explaining the benefits of vaccination.
An immunisation campaign was started on 27 April in the
affected administrative regions, targeting all persons from 13
months to 30 years of age who had not received the complete
two-dose MMR vaccination. The MMR vaccine is supplied by the
Ministry of Health and is offered free of charge through the routine
immunisation services (family doctors) and special outreach teams.
These supplementary immunisation activities are still ongoing.
Discussion and conclusions
Despite the high national immunisation coverage with MMR
vaccine, the current measles outbreak clearly demonstrates the
existence of pockets of non-immunised population, here specifically
the Roma population. A quick risk assessment made by the
epidemiologists investigating the outbreak concluded that the
minority groups and living in closed communities as described
above are at higher risk of measles infection and should be offered
a supplementary measles immunisation.
In recent years, similar outbreaks, affecting unvaccinated
groups, have been reported in a number of European countries,
however, it seemed that the epidemic did not spread to the eastern
part of Europe. During 2008, a total of 7,821 measles cases were
reported to the EUVAC.NET, and most of them (90%) were from
six countries: Switzerland, Italy, the United Kingdom, Germany,
France and Austria [9-12].
Acknowledgements
We thank Dr Annette Mankertz and Dr Sabine Santibanez (Robert Koch-
Institut, Berlin, Germany) for the prompt investigation and identification
of the origin of Bulgarian measles strains. We thank all colleagues
from the Bulgarian regional inspectorates for public health prevention
and control in Razgrad, Shumen, Silistra and Dobrich for providing
essential epidemiological data.
*Authors’ correction:
On request of the authors, the paragraph on genotyping results was
modified and a figure was deleted from the article after the publication.
This change was made on 9 July 2009.
References
1. Commission decision of 19 March 2002 laying down case definitions for
reporting communicable diseases to the Community network under Decision
No 2119/98/EC of the European Parliament and of the Council (2002/253/EC),
Official Journal of the European Communities 03.04.2002. Available from:
http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2002:086:0044:00
62:EN:PDF
2. Ministry of Health of Bulgaria. [Ordinance 21/18.07.2005 on the procedure for
registration, notification and reporting of communicable diseases]. State
Gazette. 2005;62. [In Bulgarian]. Available from: http://www.mh.government.
bg/Articles.aspx?lang=bg-BG&pageid=391&categoryid=314&articleid=552
3. Ministry of Health of Bulgaria. [National program for elimination of
measles and congenital rubella infection (2005-2010)]. [In Bulgarian].
Available from: http://www.mh.government.bg/Articles.aspx?lang=bg-
BG&pageid=411&categoryid=780
4. Mihailov A, Mihneva Z. Specific immunoprophylaxis for measles in Bulgaria.
Information Journal NCIPD. 2004.6:36-40. [In Bulgarian].
5. Gacheva N, Kojouharova M, Vladimirova N, Novkirishki V, Kurchativa A, Voynova
V, et al. [Acute infectious diseases in Bulgaria in 2001. Analysis of the
main epidemiological indicators]. Information Journal NCIPD. 2002;40(5). [In
Bulgarian].
6. Kojouharova M, Vladimirova N, Kurchativa A, Marinova L, Mehandjieva V,
Stoeva M, et al. [Acute infectious diseases in Bulgaria in 2005-2006 (main
epidemiological indicators)]. Information Journal NCIPD. 2008.51(4-5). [In
Bulgarian].
7. Kojouharova M, Kurchativa A, Vladimirova N, Marinova L, Parmakova K, Georgieva
T, et al. [Acute infectious diseases in Bulgaria in 2007 (main epidemiological
indicators)]. Information Journal NCIPD. 2008;40(6). [In Bulgarian].
8. Muller CP. From protection to elimination of measles: what do we learn
from molecular epidemiology? WHO-EURO Reference Center for M/R WHO
Collaborative Center for Measles National Avian Influenza Surveillance Lab.
Available from: http://ec.europa.eu/eahc/documents/news/technical_meetings/
From_protection_to_elimination_measles.pdf
9. Bernard H, Fischer R, Wildner M. Ongoing measles outbreak in southern
Bavaria, Germany. Euro Surveill. 2008;13(1):pii=8002. Available from: http://
www.eurosurveillance.org/ViewArticle.aspx?ArticleId=8002
10. EUVAC.NET Measles surveillance annual report 2008. EUVAC.NET, Statens Serum
Institut. 2009. Available from: http://www.euvac.net/graphics/euvac/pdf/
annual_2008.pdf
11. Muscat M, Bang H, Wohlfahrt J, Glismann S, Mølbak K, EUVAC.NET group. Measles
in Europe: an epidemiological assessment. Lancet. 2009;373(9661):383-9.
12. Pfaff G, Mezger B, Santibanez S, Hoffmann U, Maassen S, Wagner U, et al.
Measles in south-west Germany imported from Switzerland - a preliminary
outbreak description. Euro Surveill. 2008;13(8): pii 8044. Available from: http://
www.eurosurveillance.org/ViewArticle.aspx?ArticleId=8044
This article was published on 2 July 2009.
Citation style for this article: Marinova L, Kojouharova M, Mihneva Z. An ongoing
measles outbreak in Bulgaria, 2009. Euro Surveill. 2009;14(26):pii=19259. Available
online: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19259

Page 5

EUROSURVEILLANCE Vol. 14 · Issue 26 · 2 July 2009 · www.eurosurveillance.org
5
Rapid communications
Plag u e outbreak i n th e li byan arab Jamah i riya
A Tarantola (a.tarantola@invs.sante.fr)1, T Mollet2, J Gueguen1, P Barboza1, E Bertherat3
1. Département international et tropical (International and Tropical Department), Institut de Veille Sanitaire (InVS, French
Institute for Public Health Surveillance), Saint-Maurice, France
2. European Centre for Disease Prevention and Control, Stockholm, Sweden
3. World Health Organization, Geneva, Switzerland
Plague is circulating regularly in localised areas worldwide, causing
sporadic cases outside Africa and remains endemic or causes
limited outbreaks in some African countries. Furthermore, some
notable outbreaks have been reported in Asia in the last 20 years.
A limited outbreak with five cases has recently been notified by the
health authorities of the Libyan Arab Jamahiriya.
Introduction
Plague is a zoonosis caused by the bacillus Yersinia pestis. This
disease may have caused over 200 million deaths in the history of
humanity [1]. The disease is principally transmitted from animal
to animal by fleas. Humans usually become infected through the
bite of an infected flea (mainly Xenopsylla cheopis). The occurrence
of bubonic plague cases is therefore the result of the presence of
fleas, rodents and humans in a given place at a given time.
Since the first description of what may have been a plague
outbreak in 430 BC in Ancient Greece [2], the plague has spread
worldwide during the course of several pandemic waves. Between
1998 and 2008, more than 23,278 cases were reported including
2,116 fatalities (case fatality ratio, CFR, of approximately 9%) in
11 countries [3]. Over 95% of the 23,278 cases, however, were
reported in Africa with well-identified endemic plague foci (mainly
in three countries: Madagascar, the Democratic Republic of Congo
[DRC] and Tanzania).
The bubonic plague is the most common form of the disease
(93% of plague cases in Madagascar [4] and 81% of plague cases in
the United States (US) [5]. Without adequate treatment, the case-
fatality rate of bubonic plague ranges from 50 to 90%. Bubonic
plague does not give rise to direct human-to-human transmission.
Pulmonary plague is not the most frequent form of the disease
(3% of the plague cases in the US, 8% in DRC, sometimes
more frequent in outbreaks with sustained human-to-human
transmission), but is deadly in almost all cases in absence of
adequate and timely treatment. This clinical presentation may give
rise to human-to-human transmission through droplet transmission.
Ta b l e
Reported human plague cases/outbreaks since January 1945
CountryYearLocationConfirmed or probable casesDeaths
Morocco
No cases reported since 1945
1945 Countrywide, mainly around Marrakech811 ND
Algeria
No cases reported
from 1950 to 2003
1945-1946Oran121
1945Algiers5 ND
1946-1950Countrywide8ND
2003Kahelia (Tafraoui, Oran)181
2008Laghouat43
Tunisia
No cases reported since 1945
1944-1945Bizerte/Ferryville3427
Libya
No cases reported from 1984 to 2009
1972Nofilia183
1976-1977Tobruk3012
1984Tobruk9ND
2009Betnane (Tobruk)121
Egypt
No cases reported since 1947
1945Port-Said, Suez, Ismailia218ND
1946Port-Saïd, Suez, Ismailia, Damietta66ND
1946-1947Alexandria14539
Source: Department of international and tropical diseases, Institut de Veille Sanitaire (DIT-InVS) based on numerous reports and the literature