C. S. B. Lambregts-van Weezenbeek,* M. M. G. G. Sebek,* P. J. H. J. van Gerven,* G. de Vries, S. Verver,* N. A. Kalisvaart,* D.

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1 INT J TUBERC LUNG DIS 7(12):S463 S IUATLD Tuberculosis contact investigation and DNA fingerprint surveillance in The Netherlands: 6 years experience with nation-wide cluster feedback and cluster monitoring C. S. B. Lambregts-van Weezenbeek,* M. M. G. G. Sebek,* P. J. H. J. van Gerven,* G. de Vries, S. Verver,* N. A. Kalisvaart,* D. van Soolingen * Royal Netherlands Tuberculosis Association (KNCV), The Hague, Municipal Health Service, Rotterdam, National Institute of Public Health and the Environment (RIVM) Bilthoven, The Netherlands SUMMARY SETTING: The Netherlands, OBJECTIVES: To describe the contribution of 6 years of nationwide DNA fingerprint surveillance to tuberculosis control in general and to conventional contact investigations in particular. DESIGN: All Mycobacterium tuberculosis cultures are subjected to standardised IS6110-based RFLP typing, and clustered cases are systematically reported to the regional TB services involved (cluster feedback). Standardised questionnaires are used to collect information on contact investigations and epidemiological links (epi links) at regional level. Revision of the questionnaires for the period allows comparison of epi linking before and after cluster feedback. RESULTS: Among 2206 clustered cases, 462 (21%) epi links were expected before the RFLP result, whereas an additional 540 (24%) epi links were established after cluster feedback. Epi links based on documented exposure increased by 35%, from 357 to 550 (P 0.001). Only 1% of contact investigations were extended, however, and relatively few additional persons with active or latent tuberculosis were diagnosed. Reasons for the limited impact on contact investigation outcome were 1) contact took place 1 7 years previously (51%), 2) documented contact involved a subsequent case in the cluster (21%), 3) casual contact (15.5%) and 4) different region (9%). Five per cent of epi links established by contact investigation were contradicted by RFLP data. Epi links were more frequently documented in Dutch (41%) than non-dutch cases (19%, OR 3.0; 95%CI ). Cluster monitoring permitted: 1) identification of transmission chains that could not be detected by contact investigations, 2) development and evaluation of targeted interventions, and 3) identification of professional failures and poor programme performance. CONCLUSIONS: RFLP surveillance forms the bridge between conventional contact investigation and other forms of targeted active case finding. Combining both complementary strategies in a comprehensive approach to systematic outbreak monitoring and management allows countries in the elimination phase of the disease to better target and evaluate TB control interventions. KEY WORDS: RFLP; contact tracing/investigations; TB control; risk group CONVENTIONAL contact investigation aims at the identification and treatment of recently infected tuberculosis contacts and secondary cases to break the chain of transmission. In an ideal situation, the number of secondary cases is limited by rapid and complete contact investigation. However, in reality, most countries in the elimination phase of tuberculosis face diagnostic delay and concentration of tuberculosis in hard-to-reach risk groups. These characteristics interfere with both the timeliness and coverage of contact investigations. The consequences of late and incomplete contact investigations hamper the elimination of tuberculosis in low-prevalence countries. Diagnostic delays in The Netherlands resulted in large micro-epidemics which could have been prevented if latent tuberculosis infection (LTBI) had been detected and treated in time. 1 8 Low coverage of relevant contacts, for example when source cases migrate or are reluctant or unable to adequately identify their contacts, results in ongoing transmission in specific populations such as (illegal) immigrants, drug addicts and the homeless. In addition, we will have to accept that conventional contact investigation has intrinsic limitations, as it cannot cover all casual contacts. Conventional contact investigation studies in the past and more recent DNA fingerprint studies have confirmed that some effective transmitters only need very short casual contact to infect others As a result, secondary cases Correspondence to: C S B Lambregts-van Weezenbeek, Royal Netherlands Tuberculosis Association (KNCV), P O Box 146, The Hague, CC 2501, The Netherlands. Tel: ( 31) Fax: ( 31) lambregtsk@kncvtbc.nl

2 S464 The International Journal of Tuberculosis and Lung Disease will develop even in settings with optimal contact investigation. Systematic DNA fingerprint surveillance identifies these secondary cases and reveals the natural limitations of contact investigation and poor contact investigation performance. It permits us to delve beneath the surface of previously unidentified outbreaks and uncontrolled transmission, and is therefore complementary to the conventional stone in the pond approach of concentric circles of contact investigation. 13 Combining both strategies in systematic outbreak monitoring and management allows a comprehensive assessment of the dynamics of the tuberculosis epidemic and targeted interventions. However, in contrast to conventional contact investigation, DNA fingerprint surveillance does not measure recent transmission but transmission resulting in culture-confirmed tuberculosis which may have occurred many years ago. Second, DNA fingerprint clusters among immigrants may be related to transmission in the countries of origin rather than in the country where the DNA fingerprint surveillance is implemented. This paper combines descriptive and analytic components. In the latter, the contribution of 6 years of systematic DNA fingerprinting surveillance to conventional contact investigation is assessed by 1) comparing the ability of regional tuberculosis (TB) staff to determine epidemiological links before and after cluster feedback and 2) the number of additional LTBI and secondary cases detected. This is to our knowledge the first time that the impact of a long period of nationwide cluster feedback on conventional contact investigation is described. The descriptive part summarises our experiences with cluster monitoring and cluster management. As such the paper is illustrative of the integrated approach in The Netherlands. METHODS Table 1 Background information, TB control situation in The Netherlands, 2000 Overall tuberculosis incidence 8.9/ Incidence among the Dutch 3.4/ Percentage of patients with foreign nationality among all cases 63% Contribution of active case finding to overall case finding 23% Conventional contact investigations 9% Screening risk groups 14% The Netherlands is covered by a network of public health TB services staffed by 35 specialised TB doctors and 65 TB nurses. These services are responsible for conventional contact investigation and guidance of all TB patients throughout treatment, regardless of whether they are diagnosed in the public or the private sector. This public-private collaboration has existed for many decades. The conventional contact investigation strategy is based on the stone in the pond principle, in which the decision to extend conventional contact investigation is based on the prevalence of infection among investigated contacts with different levels of exposure. 13 The structure of the network allows for inter-regional contact investigation collaboration. Relevant background information on the Dutch TB control situation is summarised in Table 1. Since 1993, all Mycobacterium tuberculosis isolates in The Netherlands have been subjected to standardized IS6110-based restriction fragment length polymorphism (RFLP) typing, and all RFLP patterns are stored in the national RFLP library. 14 Strains harbouring fewer than five IS6110 copies are subjected to sub-typing by use of the polymorphic guanine-cytosinerich sequence (PGRS) as a probe. 15,16 Computer-assisted analysis of RFLP patterns is done using GelCompar software. 17,18 Fingerprint patterns of newly diagnosed patients are compared with those in the Dutch RFLP library. Clusters are defined as groups of patients having isolates with fully identical RFLP patterns (same number of IS6110 copies and PGRS copies at identical band positions). Since 1995, the National RFLP Project Nurse has routinely reported all new cluster links (new case in cluster) to the regional TB nurse(s) involved. This is known as cluster feedback. After receiving this information the nurses explore whether an epidemiological (epi) link between the clustered patients was or can be established. 19 The epi link is considered documented when the exposure is confirmed by the patient(s) involved, or assumed (considered likely) if the patients have visited the same place at the same time (without being aware of each other s presence). The regional nurses report their findings to the project nurse, using a standardised questionnaire comprising patient characteristics and contact investigation information (including the effect of cluster feedback on contact investigation). In 1997, a revised questionnaire was introduced, to allow epi linking before and after cluster feedback to be compared. Since then regional nurses have systematically reported whether they had documented or assumed an epi link before they received the cluster feedback. The whole system of systematic cluster feedback and subsequent collection of data through questionnaires was not introduced as a research project but as a programme routine, based on the voluntary collaboration of the regional TB services. Data analysis of the completed questionnaires is done at the national level using SPSS (SPSS Inc, Chicago, IL). It is important to note that the database involved does not contain any information on patients with a unique RFLP pattern. The evolution of clusters is monitored at both national and regional level for characteristics such as

3 Contact investigation and DNA fingerprinting in The Netherlands S465 size, geographical spread and risk profiles. The linkage of this information to the National TB Register (at national level) and regional conventional contact investigation findings is used for a wide range of research activities and the development of targeted risk group interventions. RESULTS TB control information Table 1 describes background information on TB control in The Netherlands. Results obtained from the questionnaires In the period , 3954 (45%) of 8726 TB patients reported to the regional TB nurses in The Netherlands were part of an RFLP cluster. These clustered patients are the subject of this report. A total of 3602 (91%) completed questionnaires were returned. The revised questionnaire, introduced in 1997, was distributed for 2450 cases and was completed for 2206 (90%) patients. During this period ( ), the TB services reported that an epi link was documented in 28% of the 3602 clustered cases with completed questionnaires, a link was assumed in 17%, and no link at all could be identified in 55% (Table 2). Epi links were more frequently documented in Dutch than non- Dutch cases (odds ratio [OR] 3.0; 95% confidence interval [CI] ). In contrast, epi links were more often assumed in foreigners. Overall, non-dutch cases were less likely to have some degree of epi link than Dutch cases (OR 1.64; 95%CI ). Epi linking before and after cluster feedback is compared in Table 3. An epi link was expected before the DNA fingerprint results became available in only 462 (21%) of the 2206 clustered cases who completed the revised questionnaire. After cluster feedback, an epi link was documented (confirmed exposure) in 25%, assumed (likely exposure) in 20% and not established in 55% of clustered cases. Therefore, the positive predictive value of RFLP match for epi link is In 5% (21/462), an expected epi link (established based on contact investigation) was not confirmed by RFLP (the patient was part of another RFLP cluster). Table 2 Epidemiological linking of the 3602 clustered cases with completed questionnaires in relation to nationality, The Netherlands, Epidemiological link after RFLP Dutch (n 1078) Nationality of clustered case Non-Dutch (n 1905) Unknown (n 619) Total (n 3602) No link 534 (50) 1176 (62) 269 (43) 1979 (55) Documented 437 (41) 353 (19) 217 (35) 1007 (28) Assumed 106 (10) 375 (20) 131 (21) 612 (17) No info (0.1) RFLP restriction fragment length polymorphism. Table 3 Epidemiological linking before and after cluster feedback for all clustered cases diagnosed in the period Epidemiological link after RFLP No (n 1744) Epidemiological link before RFLP Yes (n 462) Total (n 2206) No link 1203 (69) 21 (5) 1224 (55) Documented 193 (11) 357 (77) 550 (25) Assumed 347 (20) 84 (18) 431 (20) No info 1 1 RFLP restriction fragment length polymorphism. Overall, in 31% ( /1744) of clustered cases without any epi link before RFLP, an epi link (either assumed or documented) was established after RFLP. Among all 550 documented epi links, 35% (193/ 550) were only identified after cluster feedback. Cluster feedback significantly improved the identification of documented epi links (McNemar s test comparing expectations before and documented links after: P 0.001). A case by case analysis of this group of 193 additional documented epi links shows that reasons for not expecting an epi link before cluster feedback included the following: 1) contact took place 1 7 years before (51%); 2) the patient involved was the (satellite) source of a subsequent case in the cluster, but had no previous links in the cluster (21%); 3) casual contact (16%); 4) different region (9%); and 5) the patient developed TB after passing conventional contact investigation examinations (2%) (Table 4). Despite the improved understanding of transmission routes, the impact of 5 years of systematic cluster feedback on contact investigation organisation and outcome is limited. Of a total of 3602 clustered patients, 34 (0.9%) contact investigations were reopened or extended, resulting in the detection of 71 contacts with LTBI and 12 cases of smear-negative TB. Table 4 Reasons for not expecting epidemiological links in 193 patients for whom epidemiological links were proven after RFLP cluster feedback Reason Dutch Non- Nationality Dutch unknown Total Transmission 1 7 years previously (51) Source of later case in cluster (21) Casual contact (16) Transmission in another 4 region (9) Developed TB after contact investigation (2) Other reason (0) Total (100) RFLP restriction fragment length polymorphism.

4 S466 The International Journal of Tuberculosis and Lung Disease Figure 1 Example of DNA fingerprinting quarterly report. DNA fingerprint clusters with growth in the final quarter of 2001 and total cluster size 5, The Netherlands. Systematic outbreak monitoring & management Figure 1 shows how the risk profiles and the evolution of large clusters over time are monitored at the national level, whereas in Figure 2 the geographical spread of some clusters is shown. Quarterly reports as in Figure 1 are distributed to all TB services, whereas information on geographical spread is used to determine the need for supra-regional collaboration and assistance. Besides the close monitoring (and subsequent targeted interventions) of large clusters, small clusters may also provide valuable information for policy makers at the national level. Four case scenarios are provided to illustrate the usefulness of genotyping in the Netherlands. Case scenario 1 RFLP surveillance revealed a link between a patient with multidrug-resistant tuberculosis in a referral hospital and a fatal case of miliary tuberculosis in another part of the country 2 years later. The analysis of this

5 Contact investigation and DNA fingerprinting in The Netherlands Figure 2 S467 Geographical spread of some large clusters in The Netherlands. incident, which would not have been detected without cluster feedback, revealed several procedural (infection control) and professional (contact investigation, treatment) deficiencies and led to targeted action at ministerial and institutional level.20 never have been identified without cluster feedback. Analysis of the incident resulted in postgraduate training locally and revision and strengthening of infection control procedures (National Project Nurse and regional TB doctor, personal communications). Case scenario 2 For all health care workers reported with active tuberculosis in the period , it was determined whether 1) they were part of a cluster, 2) epi and RFLP link existed for either transmission at work or in the private environment, and 3) they had worked abroad. All proven work-related infections were analysed in detail and compliance with infection control and treatment guidelines was assessed (article in preparation).21 At a regional level, cluster surveillance in combination with contact investigation resulted in identification of risk groups, risk situations and poor practice among professionals. Case scenario 4 Contact investigation in a large city, involving a homeless index case with schizophrenia and several local homeless shelters, uncovered seven secondary cases. However, RFLP surveillance showed that none of these fingerprint patterns clustered with the contact investigation source case. Instead, they matched the patterns seen in two other large clusters involving drug addicts and homeless patients. This finding heavily modified further contact investigation planning and local TB control policies (De Vries G, article submitted). Case scenario 3 The analysis of a RFLP cluster of five seemingly unrelated cases revealed how a serious failure to diagnose TB in an 80-year-old hospitalised patient resulted in active TB in two health care workers, an 80-year-old contact and a casual contact. Because of the time span between casual exposure and breakdown to active tuberculosis, the links between these patients would DISCUSSION To our knowledge, this is the first study quantifying the impact of nationwide systematic cluster feedback on conventional contact investigation in general and on epi linking before and after cluster feedback in particular. Cluster feedback was introduced to improve, 1) the understanding of tuberculosis transmission, and 2) the results of conventional contact investigation. We show that in The Netherlands the first assumption is true, but the latter is not.

6 S468 The International Journal of Tuberculosis and Lung Disease Cluster feedback resulted in a significant increase (21 45%) of epi links at the regional level. However, comparable with what was reported by Braden et al. for Arkansas, 22 55% of clustered cases could not be epi linked. In The Netherlands this is most probably due to remote transmission, transmission in the country of origin of immigrants and, to a lesser extent, to casual transmission. Our study showed that epidemiological links that could be documented after cluster feedback had originally been missed because transmission took place a long time ago or involved migration and/or casual exposure. This also explains why contact investigations were rarely extended or reopened after cluster feedback and few additional cases and LTBI were diagnosed. However, in settings with relatively poor contact investigation performance, DNA fingerprinting surveillance may be of help in identifying deficiencies in the conventional contact investigations and evaluating ways to strengthen them. The question remains whether it is useful to obtain RFLP results for cases that are already epidemiologically linked before RFLP results became available. Three reasons are provided by TB departments to claim that it is. First, 5% of expected epidemiological links proved to be of no relevance, and in some of these cases contact investigation could be limited instead of expanded. Second, RFLP proof of an expected/ suspected epi link may provide relevant information about the period of infectiousness of the index case. Third, RFLP evidence can be used by the TB department to document professional failure and to convince the professionals and policy makers involved of the need to take appropriate action. Another interesting finding is that the proportion of documented epidemiological links is significantly lower in patients of non-dutch nationality. This may be due to the majority having been infected in their country of origin (sharing the same country-specific RFLP patterns). However, attempts to document epi links in non-dutch cases may also be frustrated by frequent migration of asylum seekers within The Netherlands, language problems or reluctance to cooperate with contact investigations (especially in the case of illegal immigrants). Our finding that a high proportion of clustered cases cannot be epidemiologically linked was also reported in other settings, 23,24 as was our observation that DNA fingerprinting results in improved understanding of TB transmission in general and the (missed) opportunities and limitations of contact investigation in particular. 9,24 30 Based on the previous discussion on RFLP and contact investigation, we conclude that both the RFLP-related increase in new epidemiological links and the RFLP confirmation of expected epi links provide the TB services with a continuous evaluation of their contact investigation performance. As such, RFLP surveillance also functions as an important training mechanism, especially for new, inexperienced TB nurses in a country during the elimination phase of the disease. However, as mentioned in the introduction, probably the most valuable contribution of RFLP surveillance begins where conventional contact investigation ends. Systematic RFLP surveillance shows what happens beyond the contact investigation ripples in the pond. The role and relevance of RFLP surveillance in detecting unsuspected transmission has been reported in many settings. 23,28,31 34 However, the Dutch situation is unique due to the nationwide coverage and the continuous utilisation during 10 years of systematic DNA fingerprint surveillance. Monitoring the quantitative and qualitative evolution of clusters over time, at both regional and national level, has become an integral part of TB control in The Netherlands and has led to targeted interventions and strengthening of existing control measures. Moreover, RFLP surveillance offers opportunities to monitor the effects of new control policies, as has been reported in other settings. 35 For example, the coverage and effect of targeted interventions can be assessed by monitoring the size and composition of those particular clusters. 36 On a smaller scale, the efforts made by TB nurses to document and analyse the links between clustered patients have resulted in a significant number of welldocumented cases of professional failure to adequately diagnose, treat and manage patients and contacts. 20 Comparable findings have been published in other countries Especially in hospitals and prisons where links between inhabitants are vague and related cases may be diagnosed with long periods in between, RFLP reveals what otherwise would not have been detected. Last, but not least, RFLP surveillance allows for systematic detection and reduction of laboratory cross contamination. 42 A thorough systematic assessment of the validity of the information as collected in the questionnaires has never been done. However, the voluntary compliance ( 90%) with completing the questionnaire, the intense and frequent communication between the National Project Nurse and regional nurses about details of the clusters, and the intensive relation between TB nurses and patients throughout the course of treatment, support our assessment of good validity. CONCLUSIONS In the specific Dutch situation, characterised by its specialised TB control network and long history of intensive contact investigation, the contribution of 6 years of systematic nationwide DNA fingerprinting surveillance to contact investigation seems limited, with only a few additional persons with LTBI or active disease being detected as a result. This finding

7 Contact investigation and DNA fingerprinting in The Netherlands S469 most probably reflects the high standard of routine contact investigation activities in the Netherlands. Our experience with cluster monitoring shows that DNA fingerprinting surveillance should be regarded as a complementary strategy, which starts where conventional contact investigation ends. As such, DNA fingerprint surveillance forms the bridge between conventional contact tracing and other forms of targeted active case finding. Combining both strategies in a comprehensive approach to systematic outbreak monitoring and management allows countries in the elimination phase of the disease to address the control problems in risk groups and settings for tuberculosis and to monitor the effects of targeted interventions. Furthermore, systematic DNA fingerprint surveillance has proved a powerful tool to detect professional and institutional deficiencies and to convince professionals and policy makers to take appropriate action. We therefore conclude that the public health resources (approximately annually) required to continue RFLP surveillance and systematic cluster feedback are well spent. Acknowledgements We would like to thank all Municipal Health Services for already 8 years of voluntary collaboration in the countrywide RFLP surveillance, as well as the Netherlands Ministry of Health for their financial support for this surveillance project. References 1 De Bliek J H. Gedetailleerde gegevens betreffende contactonderzoek i.v.m. een bijna-explosie in Leersum. Tegen de Tuberculose 1985; 81: Bangma P, De Bliek J H. Rapportage van een explosie in het district Utrecht zomer 1983 aan de hand van het model Werkwijze bij groepsinfecties. Tegen de Tuberculose 1984; 80: Groenhuis D J J. 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Molecular cloning of a highly repeated element from Mycobacterium tuberculosis and its use as an epidemiological tool. J Clin Microbiol 1992; 30: Heersma H F, Kremer K, van Embden J D A. Computer analysis of RFLP patterns of Mycobacterium tuberculosis, chap 29. In: Parish T, Stoker N G, eds. Methods in molecular biology. Vol 101. Totowa, NJ: Humana Press, Van Soolingen D, Qian L, De Haas P E W, et al. Predominance of a single genotype of Mycobacterium tuberculosis in countries of East Asia. J Clin Microbiol. 1995; 33: Šebek M. DNA fingerprinting and contact investigation. Int J Tuberc Lung Dis 2000; 4 (Suppl 1): S45 S Lambregts-van Weezenbeek C S B, Keizer S T, Šebek M M G G, Schepp-Beelen J C H M, van der Loo C J. Transmissie van multiresistente tuberculose in een Nederlands Ziekenhuis. Ned Tijdschr Geneeskd 1996; 140: De Vries G. 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8 S470 The International Journal of Tuberculosis and Lung Disease outbreak of tuberculosis among members of a highly mobile social network: implications for tuberculosis elimination. Int J Tuberc Lung Dis 2000; 4: Dobbs K G, Lok K H, Bruce F, Mulcahy D, Benjamin W H, Dunlap N E. Value of Mycobacterium tuberculosis fingerprinting as a tool in a rural state surveillance program. Chest 2001; 120: Klovdahl A S, Graviss E A, Yaganehdoost A, et al. Networks and tuberculosis: an undetected community outbreak involving public places. Soc Sci Med 2001; 52: Centers for Disease Control and Prevention. HIV-related tuberculosis in a transgender network Baltimore, Maryland, and New York City area, MMWR 2000; 49: Jasmer R M, Hahn J A, Small P M, et al. A molecular epidemiologic analysis of tuberculosis trends in San Francisco, Ann Intern Med 1999; 130: Verver S, Van Soolingen D, Borgdorff M W. Effect of screening of immigrants on tuberculosis transmission. Int J Tuberc Dis 2002; 6: Diaz R, Gomez R I, Garcia N, Valdivia J A, van Soolingen D. Molecular epidemiological study on transmission of tuberculosis in a hospital for mentally handicapped patients in Havana, Cuba. J Hosp Infect 2001; 49: Jereb J A, Burwen D R, Dooley S W, et al. Nosocomial outbreak of tuberculosis in a renal transplant unit: application of a new technique for restriction fragment length polymorphism analysis of Mycobacterium tuberculosis isolates. J Infect Dis 1993; 168: Breathnach A S, de Ruiter A, Holdsworth G M, et al. An outbreak of multi-drug resistant tuberculosis in a London teaching hospital. J Hosp Infect 1998; 39: Hannan M M, Peres H, Maltez F, et al. Investigation and control of a large outbreak of multi-drug resistant tuberculosis at a central Lisbon hospital. J Hosp Infect 2001; 47: Michele T M, Cronin W A, Graham N M, et al. Transmission of Mycobacterium tuberculosis by a fiberoptic bronchoscope. Identification by DNA fingerprinting. JAMA 1997; 278: de Boer A S, Blommerde B, de Haas P E W, et al. False-positive Mycobacterium tuberculosis cultures in 44 laboratories in The Netherlands (1993 to 2000): incidence, risk factors and consequences. J Clin Microbiol 2002; 40:

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