Nosocomial transmission of measles among healthcare workers ...

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Europe’s leading journal on infectious disease epidemiolog y, prevention and control

Vol. 16 | Weekly issue 15 | 14 April 2011

Rapid communications Nosocomial transmission of measles among healthcare workers, Bulgaria, 2010 by R Komitova, A Kunchev, Z Mihneva, L Marinova

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Surveillance and outbreak reports National outbreak of Salmonella Enteritidis phage type 14b in England, September to December 2009: case–control study by K Janmohamed, D Zenner, C Little, C Lane, J Wain, A Charlett, B Adak, D Morgan

The proof of the pudding is in the eating: an outbreak of emetic syndrome after a kindergarten excursion, Berlin, Germany, December 2007

by GO Kamga Wambo, F Burckhardt, C Frank, P Hiller, H Wichmann-Schauer, I Zuschneid, J Hentschke, T Hitzbleck, M Contzen, M Suckau, K Stark

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Perspectives Public health crises: the development of a consensus document on their management in Spain

by T Rodrigo, JA Caylà, the Working Group of the Network of Public Health Research Centres (RCESP)

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Letters Influenza vaccine effectiveness, 2010/11

by A Steens, W van der Hoek, F Dijkstra, M van der Sande

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Rapid communications

Nosocomial transmission of measles among healthcare workers, Bulgaria, 2010 R Komitova ([email protected])1, A Kunchev2, Z Mihneva3, L Marinova3 1. University Hospital, Plovdiv, Bulgaria 2. Communicable Diseases Surveillance Department, Ministry of Health, Sofia, Bulgaria 3. National Centre of Infectious and Parasitic Diseases, Sofia, Bulgaria Citation style for this article: Komitova R, Kunchev A, Mihneva Z, Marinova L. Nosocomial transmission of measles among healthcare workers, Bulgaria, 2010. Euro Surveill. 2011;16(15):pii=19842. Available online: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19842 Article published on 14 April 2011

This report describes 326 cases of nosocomial transmission of measles with 286 cases among non-healthcare workers who acquired the disease in a hospital setting. Between October 2009 and April 2010, 40 healthcare workers from seven different regions in Bulgaria have contracted the disease. Measles is a potentially severe highly contagious disease. However, at least 98% of those receiving two doses of measles-mumps-rubella vaccine (MMR) are protected against the disease. Preliminary reports for 2010 show that there were more than 30,000 measles cases in the Member States of the European Union (EU) / European Economic Area (EEA) – the highest number of measles reported in Europe in more than 10 years [1]. The highest number of cases was reported in Bulgaria, followed by France, Italy and Germany [1]. Measles continues to spread in 2011 with more than 4,000 cases reported in the EU/EEA in January and February [1].

Outbreak overview

The current outbreak in Bulgaria started in March 2009 following an imported case of measles from Germany [2]. It has been the largest outbreak ever reported in Bulgaria since the large outbreak which occurred in 1976, only a few years after the immunisation schedule with one dose of monovalent measles-containing vaccine starting with the age of 10 months had been implemented in the country. The second dose was introduced at four years of age in 1982. In 1993 the first dose of monovalent measles-containing vaccine was replaced by the MMR vaccine. Since 2001 the twodose measles immunisation with MMR vaccine has been introduced with the first dose at 13 months and the second at 12 years of age [3]. In this outbreak, the total number of cases reached 24,253 during the two-year period, reached its peak in March 2010 and started gradually to subside in late summer [unpublished data]. Only a few cases were reported every week in September and October 2010 [3]. However, according to preliminary results, about 130 cases were notified in the first three months of 2

2011, some of them diagnosed in late December 2010 but notified in January 2011. This calls into question whether it is at all possible to control such a contagious disease in a short time and in the presence of many pockets of susceptible individuals. Of the 24,137 cases with full epidemiological and clinical data available, 3,917 (16.2%) were laboratoryconfirmed (measles IgM), 7,944 (32.9%) were epidemiologically linked and the remaining 12,276 (50.9%) were probable cases. The highest incidence rate was observed in children under one year of age (n=4,717; 6/100,000 population) who were not eligible for MMR vaccination. Despite the ongoing outbreak, the Bulgarian health authority did not change the recommendation regarding MMR vaccination, i.e. did not recommend the first dose to be given earlier, at the age of nine months. Of the 24,047 cases investigated, 89.3% belonged to the Roma ethnic community. The majority (86.8%) were hospitalised, mainly due to epidemiological considerations – patients from overcrowded households with poor living conditions and inadequate access to medical care. Twenty-four deaths were reported but no information on complications is available at the moment [4].

Transmission in medical settings

Transmission in medical settings was reported for 326 cases and the hospital was the most frequently reported setting. Of these 326 cases, 286 were not healthcare workers and acquired measles in hospital or primary care. By April 2010, 40 healthcare workers (HCWs) (0.16% of all measles cases) in seven different regions in Bulgaria have contracted the disease. Most of them occurred during the peak of the outbreak, in March 2010. The measles case definition in Bulgaria is based on the EU case definition [5]. Twenty-three cases were classified as confirmed (presence of measles-specific IgM antibodies) and 17 as probable (not tested). Laboratory tests of all but two were performed at the National Reference laboratory of measles, mumps and www.eurosurveillance.org

rubella in Sofia. Thirty-four cases occurred in hospitals and six in primary care. The mean age of the cases among HCWs was 38 years (range 24–48 years) and 28 of them were women. The largest group of measles cases among HCWs were physicians (n=19), followed by laboratory technicians (n=8), nurses (n=7), cleaning staff (n=4) and pharmacists (n=2). All but one are likely to have acquired the infection from patients and one physician from a colleague. Ten HCWs developed radiologically proven pneumonia and all recovered. Fifteen HCWs were hospitalised due to dehydration or pneumonia. According to their age, the majority of cases should have been vaccinated with at least one dose of measles-containing vaccine, as one dose measles immunisation was introduced in Bulgaria in 1969 and in 1972 it became part of the immunisation schedule in the whole country. Nevertheless, only one case had a vaccination record of two doses of measles-containing vaccine; the rest did not know their vaccination status. No secondary cases among other contact patients and family members were reported. Information about susceptibility status or post-exposure prophylaxis of the HCWs’ contacts was not available.

Control measures

Two supplementary MMR vaccination campaigns were implemented. The first one started on 27 April 2009 and targeted all individuals aged between 13 months and 30 years in the affected regions (Razgrad, Shumen, Silistra and Dobrich), who had not undergone the full vaccination with two doses. Later, in order to increase the vaccine coverage, a second campaign was directed towards those older than 30 years without documented measles vaccination [4]. These measures were not very effective maybe because they were not implemented simultaneously for all 28 regions in Bulgaria. On the other hand, a large number of cases might have received a supplementary vaccine dose when already infected with measles virus. Post-exposure immunoglobulin for people at risk for a severe form of the disease was not routinely given. The full analysis of the outbreak is still in progress.

Discussion

Measles among HCWs accounts for a relatively small proportion of the reported cases but is important because of the potential for transmission of the disease to susceptible colleagues (thereby disrupting healthcare service), high-risk patients such as pregnant women, immunocompromised individuals, and family members. They have a nearly 19-fold higher risk of acquiring measles than the general population [6]. Transmission among HCWs was also reported in France in 2010 [7,8]. The Advisory Committee on Immunization Practice in the United States of America recommends all healthcare personnel to have presumptive evidence of immunity (positive serological test results or written www.eurosurveillance.org

evidence of appropriate (two doses) immunisation to mumps, measles and rubella or being born before 1957). For unvaccinated persons born after 1957 who lack evidence of mumps, measles and/or rubella immunity or laboratory confirmation of the disease, healthcare facilities should recommend two doses of MMR vaccine during an outbreak of mumps or measles and one dose during an outbreak of rubella [9]. European countries in general should recommend measles vaccine for HCWs who do not have documented vaccination record or history of the disease. This outbreak highlights the need for further activities with respect to vaccinating non-immune HCWs. Moreover, it illustrates that a high rate of hospitalisation for measles poses a risk for nosocomial infections that may have a detrimental effect on certain immunocompromised or non-immune patients and HCWs. Therefore, strict hygiene measures are important to prevent the spread in hospital settings. The 40 cases of measles identified in HCWs in the course of this outbreak further highlights the need for such recommendations. Increased vaccine uptake among HCWs of other contagious diseases like varicella and influenza also needs to be considered in medical settings. Maintaining a high immunisation coverage and strengthening surveillance are essential if Europe is to meet the new elimination target of 2015. Acknowledgements The authors wish to thank the colleagues from Bulgarian regional inspectorates for public health protection and control for providing the epidemiological data.

References 1. European Centre for Disease Prevention and Control (ECDC). Epidemiological update on measles in EU/EEA. Stockholm:ECDC. 31 Mar 2011. Available from: http://www. ecdc.europa.eu/en/activities/sciadvice/Lists/ECDC%20 Reviews/ECDC_DispForm.aspx?List=512ff74f%2D77d4%2D4a d8%2Db6d6%2Dbf0f23083f30&ID=1046&Source=http%3A% 2F%2Fwww%2Eecdc%2Eeuropa%2Eeu%2Fen%2Factivities%2 Fsciadvice%2FLists%2FECDC%2520Reviews%2Fall%2520item s%2Easpx 2. Marinova L, Kojouharova M, Mihneva Z. An ongoing measles outbreak in Bulgaria, 2009. Euro Surveill. 2009;14(26):pii=19259. Available from: http://www. eurosurveillance.org/ViewArticle.aspx?ArticleId=19259 3. Marinova L, Muscat M, Mihneva Z, Kojouharova M. An update on an ongoing measles outbreak in Bulgaria, AprilNovember 2009. Euro Surveill. 2009;14(50):pii=19442. Available from: http://www.eurosurveillance.org/ViewArticle. aspx?ArticleId=19442 4. Marinova L, Kojouharova M, Mihneva Z. Measles outbreak in Bulgaria 2009-2010: causes and lesson learned. Pediatrics. 2011;51(1):38-42. Bulgarian. 5. Official Journal of the European Union 18.6.2008 L 159/65. COMMISSION DECISION of 28 April 2008 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 (reference number C(2008) 1589) 2008/427/ EC. Available from: http://eur-lex.europa.eu/LexUriServ/ LexUriServ.do?uri=OJ:L:2008:159:0046:0090:EN:PDF 6. Steingart KR, Thomas AR, Dykewicz CA, Redd SC. Transmission of measles virus in healthcare settings during a communitywide outbreak. Infect Control Hosp Epidemiol. 1999;20(2):115-9.

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7. Six C, Blanes de Canecaude J, Duponchel JL, Lafont E, Decoppet A, Travanut M, et al. Spotlight on measles 2010: Measles outbreak in the Provence-Alpes-Côte d’Azur region, France, January to November 2010 - substantial underreporting of cases. Euro Surveill. 2010;15(50):pii=19754. Available from: http://www.eurosurveillance.org/ViewArticle. aspx?ArticleId=19754 8. Botelho-Nevers E, Cassir N, Minodier P, Laporte R, Gautret P, Badiaga S, et al. Measles among healthcare workers: a potential for nosocomial outbreaks. Euro Surveill. 2011;16(2):pii=19764. Available from: http://www. eurosurveillance.org/ViewArticle.aspx?ArticleId=19764 9. Centers for Disease Control and Prevention (CDC). Advisory Committee on Immunization Practices (ACIP). ACIP Provisional Recommendations for Measles-Mumps-Rubella (MMR) ‘Evidence of Immunity’ Requirements for Healthcare Personnel. Atlanta:CDC. 24 Jun 2009. Available from: http://www.cdc. gov/vaccines/recs/provisional/downloads/mmr-evidenceimmunity-Aug2009-508.pdf

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Surveillance and outbreak reports

National outbreak of Salmonella Enteritidis phage type 14b in England, September to December 2009: case– control study K Janmohamed ([email protected])1, D Zenner1,2, C Little1, C Lane1, J Wain1, A Charlett1, B Adak1, D Morgan1 1. Health Protection Agency, Centre for Infections, London, United Kingdom 2. London School of Hygiene and Tropical Medicine, London, United Kingdom Citation style for this article: Janmohamed K, Zenner D, Little C, Lane C, Wain J, Charlett A, Adak B, Morgan D. National outbreak of Salmonella Enteritidis phage type 14b in England, September to December 2009: case–control study. Euro Surveill. 2011;16(15):pii=19840. Available online: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19840 Article published on 14 April 2011

We conducted an unmatched retrospective case–control study to investigate an upsurge of non-travelrelated sporadic cases of infection with Salmonella enterica subsp. enterica serotype Enteritidis phage type 14b with antimicrobial resistance to nalidixic acid and partial resistance to ciprofloxacin (S. Enteritidis PT 14b NxCpL) that was reported in England from 1 September to 31 December 2009. We analysed data from 63 cases and 108 controls to determine whether cases had the same sources of infection as those found through investigation of 16 concurrent local foodborne outbreaks in England and Wales. Multivariable logistic regression analysis adjusting for age and sex identified food consumption at restaurants serving Chinese or Thai cuisine (odds ratio (OR): 4.4; 95% CI: 1.3–14.8; p=0.02), egg consumed away from home (OR: 5.1; 95% CI: 1.3–21.2; p=0.02) and eating vegetarian foods away from home (OR: 14.6; 95% CI: 2.1–99; p=0.006) as significant risk factors for infection with S. Enteritidis PT 14b NxCpL . These findings concurred with those from the investigation of the16 outbreaks, which identified the same Salmonella strain in eggs from a specified source outside the United Kingdom. The findings led to a prohibition of imports from this source, in order to control the outbreak.

Introduction

Infection with Salmonella enterica subsp. enterica serotype Enteritidis (S. Enteritidis) remains an important public health problem in Europe and other parts of the world [1-4]. Outbreaks caused by Salmonella infection have been associated with a variety of foods; however, outbreaks caused by Salmonella Enteritidis infection are closely associated with eggs and egg products [2,5,6]. In September 2009, the Department of Gastrointestinal, Emerging and Zoonotic Infections at the Health Protection Agency (HPA) reported a marked upsurge in the number of non-travel-related human cases of infection with S. Enteritidis phage type (PT) 14b with resistance to nalidixic acid and partial resistance to ciprofloxacin (S. Enteritidis PT 14b NxCpL). Infectious diseases resulting from food poisoning are statutorily notifiable in England and Wales: cases are www.eurosurveillance.org

notified by registered medical practitioners and diagnostic laboratories to the HPA. In total, 572 cases of S. Enteritidis PT 14b NxCpL infection were reported between January and December 2009, compared with 141 in 2008. Between 1 September and 31 December 2009, there were 489 cases. There were 14 recognised, discrete local outbreaks of S. Enteritidis PT 14b NxCpL infection in England and two in Wales between August and December 2009 (HPA unpublished data). All but one of these outbreaks were linked to food-service premises; the remaining outbreak was linked to a residential care home for the elderly. The total number of reported cases associated with these outbreaks was 152: six were hospitalised and two deaths were reported. Preliminary investigations of these 16 outbreaks suggested putative links to infected eggs, with evidence of cross-contamination of S. Enteritidis PT 14b NxCpL to other foods, particularly ready-to-eat vegetarian foods. The outbreak strain was isolated from samples of eggs, egg mayonnaise, egg-fried rice, pooled liquid egg mix and work surfaces in the food-service premises investigated as part of the outbreak investigations. Eggs collected from these premises (five restaurants serving Chinese or Thai cuisine and two cafes) in seven of the outbreaks were from the same production establishment in Spain, as indicated by the stamp on the egg shells. We therefore conducted a case–control analysis to determine whether the likely source of infection in the apparently sporadic cases was the same as that for cases in the outbreaks. Before the upsurge in S. Enteritidis PT 14b NxCpL infections in September 2009, there had been other sustained increases in the incidence of S. Enteritidis non-PT4 infections in England and Wales between 2000 and 2004 [7,8]. Epidemiological and microbiological investigations and a case–control study of primary sporadic indigenous cases found that consumption of eggs from food prepared outside the home was associated with being a case. The investigations identified 5

eggs sourced from Spain used in the food-service sector as the main cause of the increase [1,2,7,8]. In the United Kingdom (UK), the predominant PT responsible for egg-borne S. Enteritidis infection had been PT 4 between 1992 and 2002 [5]. Following large epidemics of S. Enteritidis infection in the UK in the late 1980s, mainly due to PT 4, a decline in human S .Enteritidis PT 4 infection in England and Wales occurred from 1997, largely because of industry control programmes in the poultry sector, including vaccination of layer flocks [9]. Since 2000, egg-associated S. Enteritidis PTs other than PT 4 causing human infection have emerged, with the greatest increases occurring in S. Enteritidis PT 1and PT 14b-related infections [7]. Surveillance of salmonellosis from 1998 to 2003 also showed upsurges in S. Enteritidis non-PT4 infections in other European countries [1]. Between 1998 and 2003, the proportion of PT4 infections fell from 61.8% in 1998 to 32.1% in 2003, with a concomitant increase in S. Enteritidis non-PT4 infections (including PT1, 8, 14b and 21) in Austria, Germany, Spain, Denmark, Finland, England, Wales and Northern Ireland, Scotland, the Netherlands and Sweden [1]. Major upsurges are thought to be associated with substantive changes in market supply: during this time, eggs were imported from producers in EU Member States where there was a lack of vaccination of layer flocks against Salmonella or controlled food industry assurance schemes were not in place [1,10,11]. From 2000 to 2008, the mean incidence rate for S. Enteritidis PT 14b NxCpL gradually increased from 0.01 per 100,000 population in England to 0.4 per 100,000 population, respectively. In 2009, this rate more than doubled, to 1.1 per 100,000 population (HPA unpublished data). This evidence, along with the findings of the 16 foodborne outbreaks, was used to formulate a hypothesis that S. Enteritidis PT 14b NxCpL infection of cases who were not part of the outbreaks was associated with consumption of eggs outside the home, within five Table 1 Demographic characteristics of sporadic cases of Salmonella Enteritidis PT 14b NxCpL infection (n=63) and controls (n=108), England, October–December 2009 Characteristic

Number of cases

Number of controls

Sex Female

28

72

Male

35

36