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Mycobacterium Tuberculosis Cases, Europe Isabelle Devaux, Kristin Kremer, Herre Heersma, and Dick Van Soolingen

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Mycobacterium Tuberculosis Cases, Europe Isabelle Devaux, Kristin Kremer, Herre Heersma, and Dick Van Soolingen RESEARCH Clusters of Multidrug-Resistant Mycobacterium tuberculosis Cases, Europe Isabelle Devaux, Kristin Kremer, Herre Heersma, and Dick Van Soolingen Molecular surveillance of multidrug-resistant tuberculo- treatment regimens (4). Recently, public health awareness sis (MDR TB) was implemented in Europe as case reporting about MDR TB has been reenforced by the occurrence of in 2005. For all new MDR TB cases detected from January extensively drug-resistant (XDR) TB outbreaks associated 2003 through June 2007, countries reported case-based with HIV, particularly in South Africa (5,6). Surveillance epidemiologic data and DNA fingerprint patterns of MDR TB of drug resistance, based on annual case reporting of drug strains when available. International clusters were detected susceptibility tests, has been ongoing in Europe since 1998 and analyzed. From 2003 through mid-2007 in Europe, 2,494 cases of MDR TB were reported from 24 European and includes annual reporting of MDR TB cases after the countries. Epidemiologic and molecular data were linked for start of treatment (7). In the 1990s, molecular methods be- 593 (39%) cases, and 672 insertion sequence 6110 DNA came available and have allowed researchers to study is- fingerprint patterns were reported from 19 countries. Of sues in the epidemiology of TB (8). Strains of the Myco- these patterns, 288 (43%) belonged to 18 European clus- bacterium tuberculosis Beijing genotype, which constitute ters; 7 clusters (242/288 cases, 84%) were characterized a group of genetically closely related strains (9), have been by strains of the Beijing genotype family, including the larg- associated with high levels of drug resistance in countries est cluster (175/288 cases, 61%). Both clustering and the of the former Soviet Union (FSU), including Latvia (10) Beijing genotype were associated with strains originating and Estonia (11); these strains have been of low prevalence in eastern European countries. Molecular cluster detection (6%–7%) in Western Europe (12). contributes to identification of transmission profile, risk fac- Public health officials are concerned about possible tors, and control measures. emergence and transmission of MDR TB strains across Europe (cross-border migration), but no system is in place revalence of multidrug-resistant tuberculosis (MDR to identify whether MDR TB strains are shared (clustered) PTB), i.e., TB resistant to at least rifampin and isoniazid, among European countries. Risk factors for possible clus- is increasing, particularly in some areas of Europe (1). From tering have yet to be determined. When the drug resistance 1999 through 2002, the median prevalence of MDR TB in surveillance project began, data on MDR TB cases were new case-patients was at critical levels (>6.5%) in specific reported in aggregated format at the European level and regions of the world, including the Baltic states and other could not be linked to molecular data identified from in- eastern European countries (2). In 2004, the Russian Feder- dividual MDR TB cases. Also, a need existed to further ation, China, and India accounted for 62% of the estimated identify the association between Beijing genotype strains global MDR TB cases (3). The increases in prevalence and or M. tuberculosis strains of other genotypes and MDR TB incidence of MDR TB are most likely caused by inadequate in Europe. Molecular surveillance of MDR TB was developed in Author affiliations: European Centre for Disease Prevention and Europe in recent years, first, in a pilot phase as part of the Control, Stockholm, Sweden (I. Devaux); and National Institute for European Concerted Action on Tuberculosis project and, Public Health and the Environment, Bilthoven, the Netherlands (K. prospectively, since 2005, with the MDR TB project pre- Kremer, H. Heersma, D. Van Soolingen) sented in this paper (13). The objectives of this project were DOI: 10.3201/eid1507.080994 to identify molecular clusters of MDR TB cases reported in 1052 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 15, No. 7, July 2009 Clusters of MDR TB Cases, Europe >1 European country, to describe epidemiologic risk fac- resented supranational reference laboratories of the World tors associated with MDR TB cases, and to initiate cluster Health Organization and the International Union against investigations at the national level to prevent cross-border Tuberculosis and Lung Disease and participated in the transmission. yearly proficiency testing for isoniazid, rifampin, strepto- In this article, based on surveillance data, we describe mycin, and ethambutol (15,16), or laboratories had their the main epidemiologic and demographic characteristics of external quality assurance conducted by such a reference MDR TB cases reported from January 2003 through June laboratory. For 1 country, drug susceptibility testing was 2007 in 24 European countries. We also describe character- performed in a laboratory abroad. More details (e.g., on istics of the main European clusters and identify risk fac- drug susceptibility test methods) can be found in the 2006 tors for clustering and association with the Beijing strain of EuroTB report (17). M. tuberculosis. European cluster information was communicated by the RIVM (Bilthoven, the Netherlands) to EuroTB on a Materials and Methods quarterly basis. The final database was maintained by Eu- roTB and included 3 sections: A) demographic and clinical Data Collection and Management variables, B) cluster information on the basis of molecular In 2005, all 53 countries of the World Health Organi- patterns at the country level, and C) European cluster in- zation’s European region were invited to participate in the formation. Data from sections A and B were matched ac- MDR TB surveillance project by Euro TB and the National cording to a patient code; data from sections B and C were Institute for Public Health and the Environment (RIVM). matched using the strain code attributed at the national Countries were encouraged to provide both epidemiolog- level. ic and genotyping data on MDR TB cases reported since January 1, 2003. However, countries that could provide Analysis of Genotyping Data only epidemiologic data were also included in the surveil- IS6110 RFLP was the recommended genotyping lance project. National surveillance institutions sent quar- method (18) to report IS6110 RFLP patterns to RIVM. For terly updates of individual and anonymous data on MDR most countries, genotyping was performed locally; for 2 TB cases reported since 2003 to EuroTB, according to a countries, genotyping was performed at RIVM. A Euro- standardized data file specification (www.eurotb.org/mdr_ pean cluster was defined as >2 MDR TB cases with M. tu- tb_surveillance/pdf/DFS_NSI_short.pdf). Each patient had berculosis isolates that shared identical IS6110 RFLP pat- a unique record identifier by country. Common definitions terns in >2 countries (18). A national cluster included cases of variables were used by participating countries, including diagnosed in a single country. Determination of a national demographic, clinical, and genotyping information. In 18 cluster (a cluster including MDR TB cases diagnosed in countries, the country of origin was defined as the coun- 1 participating country) could be based on 3 typing meth- try of birth. Because of confidentiality constraints, country ods: IS6110 RFLP typing (18), spoligotyping (19), and/or of birth was not reported for some countries. Country of typing that used mycobacterial interspersed repetitive units citizenship was used to qualify the origin of patients for 2 with variable numbers of tandem repeats (20). countries. Either country of birth or country of citizenship In each laboratory, quality control of the molecular was used in 3 countries, and information on geographic typing practices and computer-assisted analysis was in- origin was unavailable in 1 country. A patient had to be cluded as described in the standardized methods (14). The reported again (with a new identifier) when a new MDRM. DNA fingerprint patterns of MDR TB strains received at tuberculosis isolate was obtained >24 months after the pre- the RIVM were submitted to the molecular database man- viously reported MDR TB isolate. However, the possibility aged by the RIVM (MDRTBase) by using the Bionumerics of a case being reported twice in the same country or in 2 software (Applied Maths), and the database manager per- countries was low. formed a quality check. The IS6110 RFLP patterns newly National laboratories sent insertion sequence (IS) added to the MDRTBase were then compared with all other 6110 restriction fragment length polymorphism (RFLP) patterns stored in this database. The MDR TB strains were patterns from available MDR TB strains collected since classified as clustered (included in a European cluster) or 2003 to the RIVM every 3 months, either as a Bionumerics “unique” (not included in a European cluster). In addition bundle (Applied Maths, Sint-Maartens-Latem, Belgium) to specifying European cluster reports, the database man- or as a scanned image (14). To be included in the project, ager also specified strains belonging to the Beijing geno- laboratories had to perform drug susceptibility testing and type family of M. tuberculosis by compariing them with the participate in an international quality assurance program. 19 reference RFLP patterns of Beijing strains described by For quality assurance, either participating laboratories rep- Kremer et al. (21). Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 15, No. 7,
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