Announcements
On 6 June 2017, the World Health Organization (WHO) published updates to its ‘Essential Medicines List’ (EML). Read more here.

Eurosurveillance is on the updated list of the Directory of Open Access Journals and in the SHERPA/RoMEO database. Read more here.

Follow Eurosurveillance on Twitter: @Eurosurveillanc


In this issue


Home Eurosurveillance Edition  2017: Volume 22/ Issue 23 Article 2
Back to Table of Contents
Previous Download (pdf)
Next

Eurosurveillance, Volume 22, Issue 23, 08 June 2017
Rapid communication
George, Valente, Augusto, Silva, Pereira, Fernandes, Palminha, Aguiar, Martins, Santos, Valente, Calé, Leça, and Nogueira: Measles outbreak after 12 years without endemic transmission, Portugal, February to May 2017

+ Author affiliations


Citation style for this article: George F, Valente J, Augusto GF, Silva AJ, Pereira N, Fernandes T, Palminha P, Aguiar BA, Martins A, Santos E, Valente P, Calé E, Leça A, Nogueira PJ. Measles outbreak after 12 years without endemic transmission, Portugal, February to May 2017. Euro Surveill. 2017;22(23):pii=30548. DOI: http://dx.doi.org/10.2807/1560-7917.ES.2017.22.23.30548

Received:30 May 2017; Accepted:08 June 2017


We describe a measles outbreak that started in February 2017, with 28 confirmed cases, as at 31 May. The investigation is ongoing and we present here preliminary findings and the implemented control measures. After the identification of the first measles case, a contingency plan at the Directorate-General of Health (Direção-Geral da Saúde, DGS) was implemented, following the Portuguese National Programme for Measles Elimination (Programa Nacional de Eliminação do Sarampo, PNES) [1]. This report is based on data extracted on 31 May from the National System for Epidemiological Surveillance (Sistema Nacional de Vigilância Epidemiológica, SINAVE), which is an integrated clinical and laboratory system of mandatory notification.

Vaccination against measles is included in the national immunisation programme (Programa Nacional de Vacinação, PNV) since 1974 and is available for free. This outbreak occurs after a 12-year period without endemic measles transmission in Portugal, which led the World Health Organization (WHO) Regional Office for Europe to certify measles as eliminated in the country in 2015 and 2016 [2]. In Portugal, measles is a mandatory notifiable disease since 1987 and, within the scope of the PNES [1], any suspected measles case notified is investigated thoroughly.

Immunity against measles is high in Portugal. The National Serological Survey conducted in 2001–02 showed a proportion of immune individuals above 93.4% in all age groups [3]. Preliminary results from the latest survey (2015–16), show that this trend of high immunity was maintained (data not shown).

Case definition

The measles case definition used during this outbreak was based on the European Commission case definition [4]. Measles cases were defined as possible, probable or confirmed, depending on clinical, epidemiological and laboratory criteria.

A possible case was any person who met clinical criteria i.e. fever, maculopapular rash, and any of cough/coryza/conjunctivitis; a probable case was any person who met clinical criteria and had an epidemiological link to a confirmed case; a confirmed case was any possible case with laboratory evidence of infection with measles virus i.e. detection of viral RNA in a biological sample and/or a positive IgM result in serum, determined by the WHO-certified national reference laboratory for measles and rubella (National Institute of Health – Instituto Nacional de Saúde Doutor Ricardo Jorge, INSA) [5].

Following the WHO criteria [6], cases were discarded when clinical, epidemiological or laboratory criteria were not met, taking into account vaccination history and risk of measles infection in the community or abroad.

Outbreak description

As at 31 May, 156 measles cases were notified in Portugal in 2017. In the outbreak reported here, 28 cases were confirmed, seven were classified as possible, three cases were under investigation and 117 cases were discarded. Additionally, one confirmed imported measles case was identified in the north health region, which was an isolated case with no epidemiological or genotypic links to the cases in the outbreak described here.

All possible measles cases notified were investigated and control measures were promptly implemented in order to contain transmission. This report focuses on the description of confirmed cases in Algarve and Lisbon and the Tagus Valley (Lisboa e Vale do Tejo, LVT), two health regions which are not in close proximity (Figure 1).

Figure 1

Incidence rate of confirmed measles cases per 100,000 population by health region, Portugal, 23 February–31 May 2017 (n = 28 confirmed cases)

/images/dynamic/articles/22812/17-00347-f1

Map developed by GeoSaúde (http://www.geosaude.dgs.pt/).

Source: Direção-Geral da Saúde, Sistema Nacional de Vigilância Epidemiológica.

The distribution of cases over time is described in the epidemic curve (Figure 2).

Figure 2

Confirmed measles cases by week of rash onset, Portugal, 23 February–31 May 2017 (n = 28)

/images/dynamic/articles/22812/17-00347-f2

LVT: Lisboa e Vale do Tejo (Lisbon and the Tagus Valley).

Source: Direção-Geral da Saúde, Sistema Nacional de Vigilância Epidemiológica.

Algarve health region

The first measles case was notified to health authorities on 30 March (rash onset on 21 March), and was from the Algarve health region, a touristic region with tourists mainly from other European countries. Local and regional public health teams immediately initiated epidemiological investigations that led to the retrospective identification of three additional cases, with prior disease onset. Overall, this transmission chain comprised seven confirmed cases (Figure 1, 2). The earliest case had rash onset on 23 February and the latest had rash onset on 8 April. No further confirmed cases were identified in Algarve. Five of these cases acquired measles in a healthcare setting, including two healthcare workers; five cases (4 infants aged under 1 year and 1 adult) were hospitalised. To date, no epidemiological link has been found between this cluster and other cases reported in Portugal or abroad.

Lisbon and the Tagus Valley health region

The first case identified in the LVT health region was reported by a paediatrician from Cascais Hospital to the Regional Department of Public Health and the DGS on 6 April (rash onset on 30 March). Twenty-one cases were confirmed in LVT health region, with the earliest case having had rash onset on 17 March. This case was identified due to the epidemiological investigation of the first notified case in this region. The last confirmed case in the LVT region had developed rash on 13 May and no further measles cases were confirmed. The transmission chain in the LVT region is under investigation, with epidemiological links already identified between most cases. Eleven cases were healthcare workers. In the LVT region, seven cases were hospitalised, and one death has occurred in an unvaccinated teenager.

Characteristics of cases

Most confirmed measles cases (n = 19) occurred in adults (≥  18 years), two cases were adolescents (10–18 years), and seven cases occurred in children (< 10 years) (Figure 3).

Figure 3

Confirmed measles cases by age group, Portugal, 23 February–31 May 2017 (n = 28)

/images/dynamic/articles/22812/17-00347-f3

Of note, 13 cases occurred in healthcare workers (Table). Of the 28 cases, 16 had not been previously vaccinated; while the remaining cases had documented evidence of one (4 cases) or two or more doses (8 cases, including 1 case vaccinated with 3 doses, the first one between 6 and 12 months of age) of a measles vaccine, either single or combined (Table).

Table

Characteristics of confirmed measles cases, Portugal, 23 February–31 May 2017 (n = 28)

Characteristic Total (n = 28)
Sex
Male             12            
Female 16
Occupation
Physicians 5
Nurses 5
Other healthcare workers 3
Other occupation / NA 15
Vaccination status
2 or more doses 8
1 dose 4
Not vaccinated 16

NA: not applicable.

Among the unvaccinated cases, five were infants under 1 year of age and thus too young to be vaccinated, one case was 13 months old, two were adolescents, and the remaining eight cases were in adults (Figure 3). Thirteen cases were healthcare workers, of which three were unvaccinated.

Laboratory investigation

Laboratory investigation was carried out by INSA. A variety of samples were used to confirm or discard a measles case: serum, oral fluids or throat swabs, or urine. Measles cases were confirmed by positive IgM, detection of measles nucleic acid or isolation of measles virus.

Genotype B3 was identified in 14 cases from Algarve and LVT health regions, identical to the genotype detected in other outbreaks in Europe in 2017 e.g. in Belgium, Italy and the United Kingdom [7,8]. Genotyping of the remaining 14 confirmed cases is still ongoing.

Control measures

Following the increasing number of measles cases reported in several European countries in early 2017, DGS issued a warning to healthcare services, followed by recommendations and guidelines about diagnosis, early detection and response to measles cases, within the scope of the PNES [1].

In Portugal, when a suspected measles case is identified by health services, the physician is requested to fill in an electronic notification form at the SINAVE, and an email alert is simultaneously generated for local, regional and national public health authorities. Likewise, INSA also notifies DGS of all requests for measles tests, and notifies results electronically through SINAVE. Additionally, local public health units must inform immediately by phone and/or email regional and national public health authorities.

In this outbreak, all reported suspected measles cases were investigated and control measures were promptly implemented in order to contain transmission. While transmission could be prevented for imported case identified in the north health region, cases in Algarve and LVT had already generated transmission chains by the time they were reported.

Local public health teams undertook extensive contact tracing for all measles cases. Furthermore, surveillance and control measures included: immediate isolation of suspected cases, verification of immunisation status of close contacts, and administration of prophylactic immunoglobulin or measles-mumps-rubella (MMR) vaccine.

Epidemiological investigations and isolation of cases was complemented with broader public health measures, that included: (i) dissemination of key documents – posters about measles clinical picture, guidelines, epidemiological bulletins, and background materials for healthcare services – to support prevention and control measures [9-12]; (ii) creation of a specific section on measles on the DGS website [13], together with emails to inform healthcare professionals and schools; (iii) raising public awareness about the importance of vaccination through numerous reports in the media; (iv) enhancing vaccination, especially in children < 18 years and in healthcare workers, according to the PNV and PNES guidelines.

Discussion

As at 31 May, 28 laboratory-confirmed measles cases were identified in Portugal in 2017. Transmission occurred in three different settings: household, community and healthcare services. Besides interviewing patients, hospital staff and family members, public health authorities had to liaise with airline companies and foreign public health authorities, as one confirmed case travelled abroad during the incubation period.

This measles outbreak in a country with high levels of reported vaccination coverage and immunity [3,14] represents a challenge for the Portuguese public health authorities. In contrast with many European countries, Portugal records high uptake of MMR vaccine. However, immunity gaps persist, with vulnerable population pockets [3,14,15]. We found a relatively large proportion of measles cases in vaccinated individuals and this has also been reported in other outbreaks [16-18]. This situation is expected in highly vaccinated communities and might be explained by the fact that MMR is not 100% effective, with around 7.5% and 5.0% non-respondents to the first and second doses, respectively [19].

Mass immunisation campaigns against measles took place in Portugal between 1973 and 1977. In 1974, the single measles vaccine was introduced in the PNV for children aged 12–15 months, and in 1987 the combined MMR. Since 1990, two doses of MMR vaccine are recommended for children. Since 2017, the recommended schedule is at 12 months and 5 years of age [20]. Two doses are also recommended for healthcare professionals, and one dose for adults born in or after 1970 without previous measles history [20]. Portugal has achieved sustained immunisation coverage against measles, above 95% for one and two doses in < 18-year-olds [21]. Measles immunity in older age groups was above 93% in 2002 [3].

Some delay between disease onset and notification in the early measles cases in Algarve and LVT could be explained by the fact that physicians might not have considered measles as the first diagnosis. This is very likely in a country without endemic measles transmission for more than a decade. After the first notifications, public health teams retrospectively investigated all potential measles cases, leading to the identification of four additional cases that had not been notified timely. The outbreak however made physicians more aware of the measles diagnosis and subsequent cases were notified timely.

The accumulation of measles-susceptible population pockets in a context of increasing number of outbreaks in European countries since 2016 [22,23] could have contributed to this outbreak in our country. Thus, possible links between these cases and other outbreaks in Europe are under investigation. The outbreak has increased national awareness and knowledge about measles diagnosis and epidemiological investigations, enhanced vaccination activities at the local level, and also motivated demand for vaccination from the general population and healthcare workers. The high and increasing number of notified possible measles cases being discarded in the course of this outbreak, increases confidence about its control. The last confirmed measles case in this outbreak was notified in the LVT health region on 14 May (rash onset on 13 May). No further confirmed cases linked to this case have been notified to date.


Acknowledgements

The authors wish to thank all members of local public health units, regional public health departments who are involved in investigation and control measures in this outbreak. Special thanks go also to all doctors, nurses and other healthcare professionals in hospitals and primary care units who have assisted with control measures, as well as all patients and their families who promptly cooperated in the epidemiological investigations.

Conflict of interest

None declared.

Authors’ contributions

FG directed and AJS and PJN coordinated the investigations of the outbreak. GFA, JV, BAA, AM, NP, TF, PV and AL contributed to data collection, case information and data analysis. JV and GFA drafted the manuscript, with contribution by NP, TF, PV and AL. NP, TF, PP, ES, PV, AL and EC were involved in revising the manuscript. All authors reviewed and approved the final version.


References

  1. Republic of Portugal – Directorate-General of Health (DGS). Programa Nacional para a Eliminação do Sarampo [National Programme for Measles Elimination]. Lisbon: DGS; Mar 2013. Portuguese. Available from: https://www.dgs.pt/documentos-e-publicacoes/programa-nacional-de-eliminacao-do-sarampo-jpg.aspx

  2. World Health Organization (WHO) Regional Office for Europe. 4th Meeting of the European Regional Verification Commission for Measles and Rubella Elimination (RVC). Copenhagen: WHO; 2016. Available from: http://www.euro.who.int/__data/assets/pdf_file/0011/304958/4th-RVC-meeting-report.pdf?ua=1

  3. Republic of Portugal – Directorate-General of Health (DGS). Avaliação do programa nacional de vacinação e melhoria do seu custo-efetividade: 2.° inquérito serológico nacional: Portugal Continental 2001-2002. [Evaluation of the National Immunisation Programme and improvement of its cost-efectiveness: 2nd National Serological Survey – Continental Portugal 2001-2002]. Lisbon: DGS; 2004. Portuguese. Available from: www.dgs.pt/ficheiros-de-upload-1/2-inquerito-serologico-nacional-livro-pdf.aspx

  4. European Commission. Commission Implementing Decision of 8 August 2012 amending Decision 2002/253/EC 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. Luxembourg: Publications Office of the European Union. L262 Sep 27, 2012. Available from: http://eur-lex.europa.eu/legal-content/EN/TXT/?uri=OJ%3AL%3A2012%3A262%3ATOC

  5. Republic of Portugal. Directorate-General of Health (DGS). Despacho N.° 15385-A/2016 [Dispatch No. 15385-A/2016]. In Diário da República, Serie II; 21 Dec 2016. Portuguese. Available from: https://dre.pt/home/-/dre/105574339/details/maximized?serie=II&dreId=105574337

  6. World Health Organization (WHO). Eliminating Measles and rubella - Framework for the verification process in the WHO European Region 2014. Copenhagen: WHO; 2014. Available from: http://www.euro.who.int/__data/assets/pdf_file/0009/247356/Eliminating-measles-and-rubella-Framework-for-the-verification-process-in-the-WHO-European-Region.pdf

  7. Grammens T, Schirvel C, Leenen S, Shodu N, Hutse V, Mendes da Costa E,  et al.  Ongoing measles outbreak in Wallonia, Belgium, December 2016 to March 2017: characteristics and challenges. Euro Surveill. 2017;22(17):30524. DOI: 10.2807/1560-7917.ES.2017.22.17.30524 PMID: 28488998

  8. World Health Organization (WHO). Measles Nucleotide Surveillance (MeaNS) Database. Geneva: WHO. [Accessed 5 Jun 2017]. Available from: http://www.hpa-bioinformatics.org.uk/Measles/Public/Web_Front/main.php

  9. Republic of Portugal – Ministry of Education and Ministry of Health. Despacho N.o 3668-A/2017 [Dispatch No. 3668-A/2017]. In Diário da República, II Serie 28 Apr 2017. Portuguese. Available from: https://dre.pt/application/file/a/106955144

  10. Republic of Portugal – Directorate-General of Health (DGS). Sarampo: Procedimentos em Unidades de Saúde. [Measles: Procedures in Healthcare Units]. Lisbon: DGS. Apr 2017; Normative Document No. 4/2017. Portuguese. Available from: http://www.dgs.pt/saude-publica1/sarampo.aspx

  11. Republic of Portugal – Directorate-General of Health (DGS). Sarampo. Informações à Comunidade Educativa [Measles. Informations to Schools]. Lisbon: DGS; Apr 2017. Guideline No. 6/2017. Portuguese. Available from: https://www.dgs.pt/directrizes-da-dgs/orientacoes-e-circulares-informativas/orientacao-n0062017-de-19042017-.aspx

  12. Republic of Portugal – Directorate-General of Health (DGS). Sarampo. Medidas Especiais [Measles. Special Measures]. Lisbon: DGS; Apr 2017. Guideline No. 7/2017. Portuguese. Available from: www.dgs.pt/directrizes-da-dgs/orientacoes-e-circulares-informativas/orientacao-n0072017-de-20042017-pdf.aspx

  13. Republic of Portugal – Directorate-General of Health (DGS). Sarampo. [Measles]. Lisbon: DGS. [Accessed 5 Jun 2017]. Portuguese. Available from: http://www.dgs.pt/saude-publica1/sarampo.aspx

  14. World Health Organization (WHO). WHO vaccine-preventable diseases: monitoring system. Geneva: WHO. [Accessed 5 Jun 2017]. Available from: http://apps.who.int/immunization_monitoring/globalsummary

  15. Republic of Portugal – Administration of the Lisbon and the Tagus Valley Health Region (ARSLVT). Perfil de Saúde. [Health Profile]. Lisbon: ARSLVT; 2015. Portuguese. Available from: http://www1.arslvt.min-saude.pt/Documents/ARS_Perfil%20de%20Saude_Final.pdf

  16. Hahné SJ, Nic Lochlainn LM, van Burgel ND, Kerkhof J, Sane J, Yap KB,  et al.  Measles Outbreak Among Previously Immunized Healthcare Workers, the Netherlands, 2014. J Infect Dis. 2016;214(12):1980-6. DOI: 10.1093/infdis/jiw480 PMID: 27923955

  17. Muscat M, Marinova L, Mankertz A, Gatcheva N, Mihneva Z, Santibanez S,  et al.  The measles outbreak in Bulgaria, 2009-2011: An epidemiological assessment and lessons learnt. Euro Surveill. 2016;21(9):30152. DOI: 10.2807/1560-7917.ES.2016.21.9.30152 PMID: 26967661

  18. Moghadam M, Afsarkazerooni P, Ebrahimi M, Soltani M, Razmpoor A, Pirasteh E,  et al.  Measles outbreak in South of Iran, where vaccine coverage was high: a case-series study. Iran J Public Health. 2014;43(3):375-80.PMID: 25988100

  19. World Health Organization. Measles vaccines: WHO position paper – April 2017.Wkly Epidemiol Rec. 2017;92(17):205-27.PMID: 28459148

  20. Republic of Portugal – Directorate-General of Health (DGS). Programa Nacional de Vacinação 2017. [National Immunisation Programme 2017]. Lisbon: DGS; 2016. Portuguese. Available from: https://www.dgs.pt/documentos-e-publicacoes/programa-nacional-de-vacinacao-2017-pdf.aspx

  21. Republic of Portugal. Directorate-General of Health (DGS), Directorate of Disease Prevention and Health Promotion. Programa Nacional de Vacinação. Boletins de Vacinação N.° 1, 6-8, 10. [National immunisation programme. Vaccination Bulletins No. 1, 6-8, 10]. Lisbon: DGS; [Accessed 7 Jun 2017]. Portuguese. Available from: https://www.dgs.pt/paginas-de-sistema/saude-de-a-a-z/programa-nacional-de-vacinacao/relatorios-e-publicacoes.aspx

  22. European Centre for Disease Prevention and Control (ECDC). Communicable Disease Threats Report. Week 19, 7-13 May 2017. Stockholm: ECDC; May 2017. Available from: http://ecdc.europa.eu/en/publications/Publications/Communicable-disease-threats-report-13-may-2017.pdf

  23. European Centre for Disease Prevention and Control (ECDC). Measles and rubella monitoring, January 2017 - Disease surveillance data: 1 January 2016 – 31 December 2016. Stockholm: ECDC; 2017. Available from: http://ecdc.europa.eu/en/publications/Publications/measles%20-rubella-monitoring-170424.pdf



Back to Table of Contents
Previous Download (pdf)
Next

The publisher’s policy on data collection and use of cookies.

Disclaimer: The opinions expressed by authors contributing to Eurosurveillance do not necessarily reflect the opinions of the European Centre for Disease Prevention and Control (ECDC) or the editorial team or the institutions with which the authors are affiliated. Neither ECDC nor any person acting on behalf of ECDC is responsible for the use that might be made of the information in this journal. The information provided on the Eurosurveillance site is designed to support, not replace, the relationship that exists between a patient/site visitor and his/her physician. Our website does not host any form of commercial advertisement. Except where otherwise stated, all manuscripts published after 1 January 2016 will be published under the Creative Commons Attribution (CC BY) licence. You are free to share and adapt the material, but you must give appropriate credit, provide a link to the licence, and indicate if changes were made. You may do so in any reasonable manner, but not in any way that suggests the licensor endorses you or your use.

Eurosurveillance [ISSN] - ©2007-2016. All rights reserved
 

This website is certified by Health On the Net Foundation. Click to verify. This site complies with the HONcode standard for trustworthy health information:
verify here.