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Tuberculosis in newly arrived asylum seekers: A prospective 12 month surveillance study at Friedland, Germany Volker Meier a , Tanja Artelt b , Stefanie Cierpiol c , Johannes Gossner c , Simone Scheithauer b,∗ a
Department of Hospital Hygiene, Evangelisches Krankenhaus Goettingen-Weende, Goettingen, Germany Infection Control and Infectious Diseases, University Medicine Goettingen, University Hospital Goettingen, Germany c Department of Radiology, Evangelisches Krankenhaus Goettingen-Weende, Goettingen, Germany b
a r t i c l e
i n f o
Article history: Received 13 May 2016 Received in revised form 25 July 2016 Accepted 25 July 2016 Keywords: Asylum seeker Migrant Public health Refugee Screening Surveillance
a b s t r a c t Purpose: In the European Union tuberculosis prevalence-rates are among the lowest in the world. The prevalence of active tuberculosis in migrant populations has to be analyzed to get valid data on the risk of tuberculosis and for the decision of screening activities. Methods: Therefore, we prospectively quantified the risk of active tuberculosis among asylum seekers at time of arrival. Investigation was performed as regular part of the admission screenings for people arriving at Friedland, Germany, a primary major receiving center during one year. Results: In 11.773 newly arrived asylum seekers 16 X-ray investigations gave the suspicion of active tuberculosis, thereof 11 cases could be verified by culture, thereof 9 cases were classified as microscopically positive. These data translate into rates of 136 per 100.000 suspected cases, 93 per 100.000 verified cases, and finally 76 per 100.000 infectious cases, respectively. Prevalence was higher in asylum seekers coming from Eritrea and Russia compared to the main origins of current migration Syria, Afghanistan, Iraq, Iran, and Lebanon. One case of MDR-tuberculosis could be detected in a migrant from Russia. Conclusions: Prevalence rates of tuberculosis in newly arrived asylum seekers are higher than in native European populations. Rates seem to reflect the prevalence in the home countries. X-ray investigation during first examination may help identifying people needing further tests for detecting infectious tuberculosis and therefore may prevent transmission. However due to the low prevalence rates screening procedures have to be reviewed. © 2016 Elsevier GmbH. All rights reserved.
1. Introduction With respect to communicable diseases migrants and the current asylum seeker phase do not represent a major threat to European countries (Lee et al., 2013; Infectious diseases of specific relevance to newly arrived migrants in the EU/EEA, 2015; World Health Organization, 2015). However, there is a group of infectious diseases occurring more often in the asylum seekers home countries and therefore may occur more often after migration in some European countries, e.g. Germany (Infectious diseases of specific relevance to newly arrived migrants in the EU/EEA, 2015). Even more, the risk for migrants suffering from communicable diseases may increase due to the energy-sapping getaway and due to the
∗ Corresponding author at: Zentralabteilung Krankenhaushygiene und Infektiologie, Universitätsmedizin Goettingen, Robert Koch Strasse 40, Germany. E-mail address:
[email protected] (S. Scheithauer).
current overcrowding resulting in compromised hygiene and sanitation arrangements. During an estimation of the world health organization (WHO) there are 13.7 million prevalent cases of tuberculosis and 0.5 million of cases of multi drug resistance tuberculosis worldwide (World Health Organization, 2015). Incidence rates of tuberculosis have been fallen in Germany and other European countries during the last decades reaching the level of seldom diseases with an actual number of 5.3 per 100.000 inhabitants in Germany, respectively (European Centre for Disease Prevention and Control/WHO Regional Office for Europe and Control/WHO Regional Office for Europe, 2014). As tuberculosis infections are transmissible and can affect especially low-prevalence populations across countries their identification and control may be criticality important for their global epidemiology (European Centre for Disease Prevention and Control, 2010). The displacement of people from areas with high endemic rates of this infectious disease may increase the national incidence rates accordingly (Riley, 2007). Infection con-
http://dx.doi.org/10.1016/j.ijheh.2016.07.018 1438-4639/© 2016 Elsevier GmbH. All rights reserved.
Please cite this article in press as: Meier, V., et al., Tuberculosis in newly arrived asylum seekers: A prospective 12 month surveillance study at Friedland, Germany. Int. J. Hyg. Environ. Health (2016), http://dx.doi.org/10.1016/j.ijheh.2016.07.018
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trol measures are importantly needed to lower transmission rates and therefore strongly recommended in cases with positive smear microscopy and therefore infectious tuberculosis (Jensen et al., 2005). Early diagnosing of this situation is the cornerstone in effective infection prevention strategies (European Centre for Disease Prevention and Control, 2010; Jensen et al., 2005). Although there is up to now no evidence that imported tuberculosis can increase the incidence rates nationwide the actual waves in migration and the increase migrants worldwide raises concern regarding this issue (Dasgupta and Menzies, 2005; Coker et al., 2006; Hargreaves et al., 2009). Therefore the ministry of health in Germany decided to screen every newly arrived asylum seeker during the first physical examination by X-ray investigation for active tuberculosis exceptionally children below 16 years and pregnant women. In additional early diagnosis is also important for the individual patient benefiting from early professional therapy preventing complications and severe courses of illness. To quantify the risk of active tuberculosis in this population, we analyzed all screening results at near time of arrival. Results may help defining the additional risk more precisely. Finally, the need of infection prevention strategies could be better assessed. Actually, in Germany every ingoing asylum seeker has to tolerate a physical examination including a X-ray investigation of the lung. This strategy has been renewed in the context of the current migrant fluxes. Prevalence of active tuberculosis and even microscopically positive and thus infective tuberculosis in this population is not well known and gave rice to concerns in the home population. Therefore we prospectively investigated the prevalence and the infectivity status in the actual newly arriving asylum seekers at Friedland during one year.
2. Methods 2.1. Study design Prospective descriptive epidemiological study.
2.1.1. Study site, population and sampling During 01.11.2014 and the 30.10.2015 all newly arrived asylum seekers at Friedland, a major primary center in northern Germany and being sent to the first physical examination to the Evangelisches Krankenhaus Weende, Goettingen, representing one of three centers for admission screening, were enrolled. Exclusion criteria were: age younger 16 years and pregnancy—as reasons against X-ray investigation. Thus, in total we have an overview on the complete year of migrants arriving at this part of Germany. Due to the fact that each newly arrived asylum seekers has to agree by national rights in physical examination as well as X-ray investigation there is no other dropout rate. Admission screening should be performed at least during the first six weeks after arrival in Germany and includes a brief anamnesis, a physical examination with focus on transmissible diseases and a X-ray investigation oft the lung with the idea of detection tuberculosis. The origin of migrants can only be clearly determined by broad anamnesis with translator, thus we estimated the origin according to the information by Friedland. For all newly arrived asylum seekers having X-rays suspicious for tuberculosis we deeply investigated the origin and characterized all these asylum seekers in detail including age, nation, medical history, clinical symptoms during the last 6 months, previous tuberculosis, previous therapy for tuberculosis, and finally deeper characterization of the X-ray findings. Analyses were performed each day of the week (Monday to Friday). Investigators for physical examination as well as for radiological investigation did not change during the study period.
eritrea about 1 % Tuberculosis posive paents N=5
serbia/croaa/ monte negro about 1 % pakistan about 1 % Tuberculosis posive paents N=2
iran about 8 %
former soviet union countries about 1 % Tuberculosis posive paents N=3
syria about 42 % Tuberculosis posive paents N=1 afghanistan about 15%
iraq about 15 % lebanon about 8 %
libya about 1%
Fig. 1. Home countries and tuberculosis cases.
2.1.2. Data collection and analysis Collected data include beyond the physical examination and the X-ray investigation a medical history, clinical symptoms indicative for tuberculosis and in case of suspected tuberculosis a preparation of sputum or broncheoalveolar lavage for microscopy, possible previous diagnosis, and in each positive case tuberculosis cultures, respectively. In all cases tuberculosis was suspected the people were separated and investigated in hospital further. X-rays were evaluated by two radiologists for the presence of signs indicative for tuberculosis as well as for other deviations from normal X-rays. Data aggregation was performed by a medical senior physician. Cumulative interpretation was done by all previously named people and an infectious diseases consultant and microbiologist. For statistics Graph Pad Quick Calc was used in the current version. Since the investigations followed a national law and data represent epidemiological findings, no ethics approval was obtained. All processes were carried out in compliance with the Helsinki Declaration. 3. Results 3.1. Prevalence of tuberculosis During 01.11.2014 and 31.10.2015 total of 11.773 newly arrived asylum seekers were investigated. In 75 cases the X-ray investigation showed abnormal findings; for further characterization see Fig. 1. In 16 cases tuberculosis was suspected, that translates in a suspicion rate of 136 per 100.000 people (Fig. 1). Thereof in 11 cases tuberculosis could be confirmed by cultural detection of mycobacterium tuberculosis translating into 93 per 100.000 people, respectively. In 9 of these 11 cases (82%) the patients could be identified rapidly since the smear already showed positive microscopy in the Ziehl Neelsen staining, indicative for mycobacteria, which translates into a microscopical positive prevalence rate of 76 per 100.000 people for highly infectious tuberculosis. In one case a MDR-tuberculosis could be confirmed. This patient came from Russia and had been treated several years ago for tuberculosis. All people with a culture proven tuberculosis infection were initially diagnosed by screening, none of them through (self-) referral (Table 1). The rate of suspected tuberculosis cases did not differ
Please cite this article in press as: Meier, V., et al., Tuberculosis in newly arrived asylum seekers: A prospective 12 month surveillance study at Friedland, Germany. Int. J. Hyg. Environ. Health (2016), http://dx.doi.org/10.1016/j.ijheh.2016.07.018
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N (x-ray)
3
N (suspected tuberculosis)
1600
4
1400
3
1200
1000
800
2
600
400
1
200
0
0 Nov 14
Dec 14
Jan 15
Feb 15
Mar 15
Apr 15
May 15
X-ray investigations (left axis)
Jun 15
Jul 15
Aug 15
Sep 15
Oct 15
tuberculosis (right axis)
Fig. 2. Number of X-ray investigations and number of suspected tuberculosis from X-ray finding according month.
N 18 16 14 12 10 8 6 4
cardial abnormalities
scars
atelectasis
pleura callus
non-specific infiltrates focal
non-specific infiltrates interstitiell
non-specific focal lesions
predominant hili
increased lymph nodes
pleural effusion
0
suspected tuberculosis
2
Fig. 3. Abnormal X-rays, stratified according findings (NX-ray = 75).
Table 1 Characteristic of patients with active tuberculosis.
3.2. Socio-demographic characteristics
Tuberculosis positive patients Age (y) Known history for active tuberculosis History of “pneumonia” (+/− tuberculosis) Clinical symptoms indicative for tuberculosis
31.2 SD:12.6 2/11 (18%) 3/11 (27%) 4/11 (36%)
overtime in the study period and went in parallel with the number of investigations performed (Fig. 2). Beyond tuberculosis in cases relevant other diagnosis could be suggested by X-ray screening (Fig. 3), e.g. 16 out of 75 showed nonspecific focal lesions of the lungs, 14 cardiac abnormalities.
The number of primary investigations of newly arrived asylum seekers during the investigation period started with 600 investigations per month and ended up with about 1300 investigations per month, respectively. The acquisition of exact personal data and sozio-demographic characteristics of the newly arrived asylum seekers is known to be difficult. Reasons for this are missing or incomplete personal documents and distinct language barriers. This is particularly true on data on home country, escape route, age and family situation of the asylum seekers. The estimated distribution of home countries is shown in Fig. 3 and based on information calculated by the officials of the primary base camp Friedland. Five patients with active tuberculosis come from Eritrea, 3 from former soviet union countries, 2 from Pakistan and 1 from Syira. None case
Please cite this article in press as: Meier, V., et al., Tuberculosis in newly arrived asylum seekers: A prospective 12 month surveillance study at Friedland, Germany. Int. J. Hyg. Environ. Health (2016), http://dx.doi.org/10.1016/j.ijheh.2016.07.018
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of tuberculosis was identified in asylum seekers from Lebanon, Iraq, Iran, Afghanistan. The probability of being diagnosed with tuberculosis seems to depend on home countries. The mean age of tuberculosis positive migrants was 31.2 y (SD:12.6) which did not significantly differ to the mean age of all newly arrived migrants enrolled with 31.0 y (Table 1)
4. Discussion Population mobility across the world is becoming a major determinant of infectious disease epidemiology (World Health Organization, 2015). The relationship existing between international migration and tuberculosis control has been intensively studied by a report of the European task force from the international union against tuberculosis in WHO in 1994 (Infectious diseases of specific relevance to newly arrived migrants in the EU/EEA, 2015; Arshad et al., 2010). In additional the effectiveness of different tuberculosis control strategies has been investigated by Dasgupta et coworkers. As a result of our investigations we defined a rate of 93 tuberculosis cases per 100.000 asylum seekers, which is about 17.5 times greater than the prevalence in the general population in Germany with 5.3 cases per 100.000 inhabitants. Compared to previous analysis performed before 2010 these rates are in line with the previous results; our rates are on the lower limit several years ago (European Centre for Disease Prevention and Control/WHO Regional Office for Europe and Control/WHO Regional Office for Europe, 2014; Dasgupta and Menzies, 2005; Coker et al., 2006; Hargreaves et al., 2009; Arshad et al., 2010). Especially for refugees previous investigations detected up to 10-times higher prevalence rates (Arshad et al., 2010). One possible explanation for this may be the different home countries of the refugees and the migrants which have different prevalence or burden of tuberculosis. If the detected active infections are the result of a new infection or a reactivation of a latent tuberculosis during migration remain unclear. During our study most of the people came from Syria, where the health care system has been highly developed several years ago, resulting in a declining trend of the number of reported tuberculosis cases. This reflects, that only one patient coming from Syria showed active tuberculosis. In other words the newly arrived asylum seekers coming from Syria seem not to increase rate of active tuberculosis in the migrant population. Nevertheless, this situation might change as a consequence of the ongoing conflict. Only a few people came from Eritrea, Serbia, Croatia and Montenegro and the former Soviet Union countries. However, about one half of active tuberculosis cases (5 out of 11) were detected in patients from Eritrea. X-ray investigation allone is not able to detect latent tuberculosis, which poses a risk of progress to active tuberculosis due to migration. The value of the radiological screening might be overestimated. Moreover, there are ethical concerns about mandatory X-ray investigation. Our results give rise to discuss about a changing of the general screening strategy including all asylum seekers or should be used different procedures depending on the home countries. To quit the general screening for tuberculosis for people from Syria might be a viewpoint for further discussion. More data from other asylum seeker centers are needed to confirm our findings on the different risks depending on the home countries for a possibly more selective screening procedure. Another procedure to reduce the screening activities could be an individual anamnesis giving hints for active tuberculosis. In our investigated population only 2 of 11 people knew or wanted to talk about their previous active tuberculosis. In addition, clinical signs indicative for tuberculosis seldom occurred, in our study population in only one third of patients. This finding
may be explained by language and communication barriers and/or the fear of telling negative events. This is even more important on the individual patient level, since due to admission screening these people can immediately get the right therapy and thus may prevent prolonged illness and complications. Moreover, beyond tuberculosis additional medically relevant diagnoses could be suggested by X-ray investigation, thus leading to a better medical supply. On the other hand active screening for tuberculosis seems to be a useful tool, since the prevalence of active tuberculosis in this population exceeded the prevalence in the native population in Germany several times. However, the risk of transmission in migrant communities tends to stay within that community and the risk for the native population seems to be small (Kamper-Jorgensen et al., 2012). Special emphasis should be given to asylum seekers from home countries with high risk of highly resistance tuberculosis (MDR). In one of the 11 patients a MDR-strain could be detected. This patient came from Russia and has been treated 5 years ago for tuberculosis with not remembered medication for an unknown duration. By now this tuberculosis was resistant against all four first line substances. This finding is of general interest, because early detection of these cases is of great importance in controlling the spread of extensively resistant tuberculosis. Cost-effectiveness calculation of screening was beyond the aim of this study. Nevertheless, the small number of detected patients with active tuberculosis compared to the high number of X-ray investigations performed, may raise concern for cost-effectiveness. 5. Limitations Single centre design; pre-dominance of certain home countries; open questions concerning i. screening for extrapulmonary tuberculosis;.ii. screening in pregnant women; screening in children; iii screening by other technigques, e.g. interferon gamma release assay; iiii cost-effectiveness calculation; iiiii ethical concerns. 6. Conclusions Active tuberculosis in the asylum seekers population in Friedland is about 17.5 times more prevalent than in the native German population. However, newly arrived asylum seekers do not represent a high risk for tuberculosis. The prevalence seems to depend on the home countries. The risk of tuberculosis in asylum seekers from Syria the dominating population in Friedland, is very low. More data are needed for the decision on a home country specific procedure for reductions of screening and the burden of the asylum seekers. Including X-ray investigation in migrant arrival screening seems to be of great importance in controlling this disease. Due to early detection of infective cases immediate exposition control and infection control measures can be initiated in order to prevent cross transmission and finally an increase in tuberculosis in Europe. This is even more important in case of MDR tuberculosis. From the individual point of view initial investigation including X-ray investigation is of importance, too. Several diseases needing therapy could be detected at an early stage. Conflicts of interest The authors declare that they have no conflict of interest. Transparency declaration Nothing to declare.
Please cite this article in press as: Meier, V., et al., Tuberculosis in newly arrived asylum seekers: A prospective 12 month surveillance study at Friedland, Germany. Int. J. Hyg. Environ. Health (2016), http://dx.doi.org/10.1016/j.ijheh.2016.07.018
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The manuscript or parts of the manuscript have not been published and are not currently under consideration for publication. Authors’ contribution VM: data arrangement and calculation. TA: assistance in data arrangement and writing. SC: radiological analysis and interpretation. JG: radiological analysis and interpretation. SS: design of the study; preparation of the manuscript. All authors have approved the current version of the manuscript. Acknowledgements We are grateful to microbiological examinations with the team of the Institute of Medical Microbiology at the University Hospital, Göttingen, especially Prof. Dr. med. Dr. rer nat. Helmut Eiffert and Ortrud Zimmermann. References Arshad, S., Bavan, L., Gajari, K., Paget, S.N., Baussano, I., 2010. Active screening at entry for tuberculosis among new immigrants: a systematic review and meta-analysis. Eur. Respir. J. 35 (6), 1336–1345.
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