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Tuberculosis Screening Among Newly Arrived Asylum Seekers in Denmark
Tuberculosis Screening Among Newly Arrived Asylum Seekers in Denmark
Tuberculosis Screening Among Newly Arrived Asylum Seekers in Denmark
To cite this article: Kristina Langholz Kristensen, Marie Norredam, Sidse Graff Jensen, Niels
Seersholm, Marie Louise Jørgensen, Banoo Bakir Exsteen, Franziska Grundtvig Huber,
Ebbe Munk-Andersen, Troels Lillebaek & Pernille Ravn (2022) Tuberculosis screening
among newly arrived asylum seekers in Denmark, Infectious Diseases, 54:11, 819-827, DOI:
10.1080/23744235.2022.2106380
ORIGINAL ARTICLE
Kristina Langholz Kristensena,b, Marie Norredamc,d, Sidse Graff Jensene, Niels Seersholme,
Marie Louise Jørgensenb, Banoo Bakir Exsteend,f, Franziska Grundtvig Huberf, Ebbe Munk-Anderseng,
Troels Lillebaeka,h and Pernille Ravnf
a
International Reference Laboratory of Mycobacteriology, Statens Serum Institut, Copenhagen, Denmark; bDepartment of
Pulmonary- and Infectious Diseases, Nordsjaellands Hospital, Hilleroed, Denmark; cResearch Centre for Migration, Ethnicity and
Health, University of Copenhagen, Copenhagen, Denmark; dSection of Immigrant Medicine, Department of Infectious Diseases,
University Hospital Hvidovre, Hvidovre, Denmark; eDepartment of Internal Medicine, Section of Respiratory Diseases, Herlev and
Gentofte Hospital, University of Copenhagen, Hellerup, Denmark; fDepartment of Internal Medicine, Infectious Disease Section,
Herlev and Gentofte Hospital, University of Copenhagen, Hellerup, Denmark; gDanish Red Cross, Copenhagen, Denmark; hGlobal
Health Section, Department of Public Health, University of Copenhagen, Copenhagen, Denmark
ABSTRACT
Background: Tuberculosis (TB) screening programmes among asylum seekers tend to focus on chest radiography (CXR) for
early diagnosis, whereas knowledge on sputum examination is limited. We evaluated active TB screening using CXR and
sputum culture among asylum seekers arriving in Denmark. In addition, we assessed the coverage of a voluntary
health assessment.
Methods: Between 1 February 2017 and 31 March 2019, all newly arrived asylum seekers in Denmark 18 years from TB
high-incidence countries or risk groups, who attended a voluntary general health assessment, were offered active TB
screening with CXR and spot sputum examination. Sputum samples were examined by culture and smear microscopy.
Results: Coverage of the general health assessment was 65.1%. Among 1,154 referred for active TB screening, 923 (80.0%)
attended. Of these, 854 were screened by CXR and one case of active TB was identified equivalent to a yield of 0.12%.
Sputum samples were collected from 758 and one M. tuberculosis culture-positive TB case (also identified by CXR) was
identified, equivalent to a yield of 0.13%. No cases were found by sputum culture screening only. In addition, screening
found three cases of malignant disease.
Conclusion: We suggest that TB screening should focus on asylum seekers from TB high-incidence countries. Furthermore,
early health assessments should be of high priority to ensure migrant health.
Table 1. Characteristics of all asylum seekers arriving and their attendance in the voluntary health assess-
ment (n ¼ 3,446).
Total Attending Not attending
Total, n 3,446 2,244 1,202
Sex,a % (n)
Male 66.4 (2,288) 59.6 (1,338) 79.0 (950)
Female 33.6 (1,158) 40.4 (906) 21.0 (252)
Ageb 30 (24–37) 31 (25–40) 27 (21–33)
Region of origin,a,c % (n)
Eastern Europe and Central Asia 31.1 (1,071) 31.9 (716) 29.5 (355)
Middle East and North Africa 49.0 (1,689) 46.8 (1,051) 53.1 (638)
South- and Central America 2.1 (72) 2.1 (46) 2.2 (26)
South-East Asia 4.4 (152) 4.8 (108) 3.7 (44)
Sub-Saharan Africa 12.7 (437) 13.5 (304) 10.1 (133)
Western Europe and the United States 0.7 (25) 0.9 (19) 0.5 (6)
Country of origin,a,d % (n)
Afghanistan 4.1 (143) 4.3 (97) 3.8 (46)
Albania 3.3 (113) 3.4 (77) 3.0 (36)
Eritrea 2.7 (93) 3.1 (69) 2.0 (24)
Georgia 10.8 (371) 10.1 (227) 12.0 (144)
Iran 8.6 (297) 9.3 (209) 7.3 (88)
Iraq 5.7 (196) 5.3 (120) 6.3 (76)
Morocco 5.3 (182) 2.5 (56) 10.5 (126)
Nigeria 3.9 (133) 2.6 (58) 6.2 (75)
Statelessness 4.3 (149) 4.4 (98) 4.2 (51)
Syria 19.3 (664) 22.2 (499) 13.7 (165)
Ukraine 2.0 (70) 2.6 (59) 0.9 (11)
TB incidencee in country of origina/100,000, % (n)
0–49 55.0 (1,894) 57.4 (1,288) 50.4 (606)
50–99 23.2 (799) 22.8 (511) 34.5 (288)
100–199 13.4 (461) 10.7 (239) 7.9 (222)
200 8.5 (292) 9.2 (206) 7.2 (86)
a
Data are presented as % (n) unless otherwise stated.
b
Median (interquartile range).
c
Modified from regions used by the World Bank Group (https://data.worldbank.org/country).
d
Ten most common countries of origin among all newly arrived.
e
World Health Organization estimated incidence.
Figure 1. Flow chart of health assessment attendance and active tuberculosis screening.
Two (0.26%) sputum samples were smear-positive, were asymptomatic and had normal radiologic findings
but culture-negative. Both asylum seekers were asymp- i.e. no indication for treatment [20].
tomatic with normal CXR, and the samples were consid- CXR was abnormal in 47 (5.5%) asylum seekers
ered false-positive. Another two (0.26%) sputum samples (Figure 2). Of these, one was the active TB case #2, 15
were culture positive for non-tuberculous mycobacteria (31.9%) were considered to have had previous TB and
(M. abscessus and M. fortuitum). Both asylum seekers three (6.4%) were diagnosed with a malignant disease
INFECTIOUS DISEASES 823
assessment was 65.1% and TB screening attendance was higher (535/100,000 screened) than the incidence in
after the initial health assessment was as high as 80.0%. their countries of origin [31]. Mostly, they reached the
Yield of sputum and CXR screening was around 0.1%. In Italian coast over the Mediterranean Sea after waiting
addition, TB screening resulted in the diagnosis of three for transfer in Libya under precarious living conditions,
cases of malignant disease. Sputum culture screening all increasing the TB risk. In the present study, the pro-
did not identify additional TB cases. portion of asylum seekers arriving in Denmark from sub-
The yield of CXR screening was 0.12%. CXR-based Saharan Africa was considerably lower compared to ear-
screening has been used for identifying TB among asy- lier years, whereas a large proportion of migrants was
lum seekers in many studies and our findings are similar from Georgia. Most often, they travelled to Denmark by
to studies from neighbouring countries reporting screen- plane and did not experience the same migration
ing yields between 0.1% and 0.5% [21–25]; however, our related risk factors but were screened based on the high
study suggests that TB screening should focus on those MDR-TB risk in Georgia. However, the proportion of asy-
at high risk of TB to improve the yield of screening. lum seekers arriving in Denmark from Georgia was not
Screening among newly arrived asylum seekers in representative compared to earlier years. In 2018, the
Germany [21] and the Netherlands [24] reported slightly number of asylum seekers from Georgia who applied for
lower yields. In Germany and the Netherlands, all asylum asylum in Denmark was about four to five times higher
seekers were screened regardless of incidence in the than normal and the large majority was not recognized
country of origin. In Germany, most asylum seekers for refugee status [32].
screened were from Syria (42.0%), an intermediate-inci- Sputum culture screening identified one case of cul-
dence country, whereas in our study, Syrian asylum ture-positive TB. In another Danish study, where home-
seekers comprised < 1% of screened. Only few asylum less and socially marginalized individuals were screened
seekers in the German study were from TB high-inci- for TB with sputum culture regardless of symptoms,
dence countries, but these comprised nearly half of the 3.3% had culture-positive TB [15]. Twenty-two percen-
TB cases detected. tages of these did not have a CXR suggestive of TB and
One of the most important TB risk factors is incidence most were smear-negative, suggesting they were identi-
in the country of origin [26], which also affects the yield fied in an early and less infectious stage. To our know-
of screening [5,27–29]. In a study from Germany, the ledge, only one study using sputum screening among
overall yield was 82 per 100,000 screened, but country- asylum seekers in low-incidence countries has been pub-
specific yields ranged from 10 to 683 per 100,000 lished [17]. This study screened newly arrived asylum
screened in Iraqi and Somali asylum seekers, respectively seekers in Italy using a symptom-based approach. All
[29]. This indicates that incidence in country of origin were screened for TB symptoms and mainly symptom-
among the screened population of asylum seekers may atic individuals were screened by sputum analysis with
account for differences in yield, and that it may be more Gene Xpert MTB/RIF, smear microscopy and culture [17].
efficient to target TB screening towards asylum seekers Among 591 individuals, they found 3.0% had TB based
from TB high-incidence countries [30]. In our study, on at least one microbiologic laboratory test of which
62.0% were screened due to TB risk factors other than 1.9% were culture-positive. Potential reasons for the
originating from a high-incidence country. More than high yield in this study may be that asylum seekers
half were screened based on MDR-TB risk. In Denmark, were selected based on TB symptoms and that the
the risk of MDR-TB is very low, but because many asy- majority came from TB high burden Sub-Saharan Africa.
lum seekers arrive from Eastern European countries with Finding TB cases as early as possible is important to
higher risk of MDR-TB, this is a screenings criterion. reduce transmission, especially in high-risk populations
However, several of these countries have TB incidences such as asylum seekers and socially marginalized individ-
< 50/100,000 population, which would be expected to uals. In the Italian study [17], the Gene Xpert-based
lower the overall yield in screening. screening facilitated rapid TB diagnosis; however, two
Other factors affecting the differences in yield could cases were culture-positive only and would have been
be differences in migration routes and the conditions missed if using Gene X-pert only. The study did not
faced during migration such as overcrowding, imprison- report data on smear or CXR. In a population including
ment and lack of health care [1,7,8]. In a CXR-based more individuals from TB high-incidence countries, spu-
screening from Italy, the yield among asylum seekers tum culture screening may prove effective for early diag-
mainly from Western Africa (81.0%) screened at arrival nosis, or could potentially be offered to symptomatic
INFECTIOUS DISEASES 825
individuals. However, this cannot be answered from availability should be prioritized and provided to all asy-
our study. lum seekers as part of an early health assessment.
In voluntary screening programmes, an important In our study, CXR abnormalities were observed in
aspect is coverage [33]. The coverage of the health 5.5% of CXRs and three individuals had a malignant dis-
assessment in Denmark (65.1%) was slightly higher than ease. Due to the screening, the malignant diseases were
seen in a similar Swedish programme (50%) [34]. As a likely detected at an earlier stage potentially resulting in
result of implementing a new systematic TB screening in a better prognosis. A general concern is that migrants
Denmark during our study, there was an increased focus have more challenges accessing health care facilities
on health assessment attendance including health staff than host populations, which can cause health inequal-
education and encouragement to attend. Likely, this had ities [37,38]. Our study underlines the importance of
a positive effect on coverage. Still, one-third of asylum facilitating an early contact to the health care system for
seekers did not participate in the voluntary health newly arrived refugees to reduce barriers. Providing a
assessment. One reason may be that the time shortly general health assessment, including a CXR for TB high-
after arrival is stressful for asylum seekers e.g. settling in, risk groups, might be an opportunity to identify unmet
meetings with authorities, uncertainties etc., and the vol-
health needs and optimize health among newly arrived
untary health assessment may not be a priority. Another
refugees [39,40].
reason is logistics: In periods of pressure on the asylum
system fewer asylum seekers are offered screening at
the reception centre because they are rapidly housed
elsewhere with less rigorous offers of assessment. Also, Limitations
TB is often associated with stigma, which could keep The study has some limitations. Only one sputum sam-
migrants from attending both the health assessment ple was collected, which may have decreased sensitivity
and the TB screening due to mistrust, concerns that a [41]. Data on TB cases among asylum seekers arriving in
TB diagnose will affect the asylum application or a fear Denmark before February 2017 were not available.
of discrimination and deportation [33,35]. Thus, Therefore, we could not assess whether implementation
emphasis on patient-rights, confidentiality, and informa- of systematic screening increased TB detection or
tion on health benefits as well as encouragement to reduced diagnostic delay. Although asylum seekers were
attend needs to be prioritized. Interestingly, we saw
assessed clinically, symptoms were not systematically
large differences in attendance rates between national-
recorded, thus we could not assess a symptom-based
ities. Asylum seekers from Morocco and Nigeria had
approach. Thirty-five percent of asylum seekers did not
non-attendance rates between 60% and 70%, whereas
attend the health assessment and thus were not
the non-attendance for most other nationalities was
assessed for TB risk or clinically evaluated which could
around 30%. Morocco and Nigeria are considered TB
possibly underestimate morbidity among the
high-incidence countries [36], which could mean TB
study population.
cases in this group were potentially missed during the
study period. Unfortunately, we do not know the rea-
sons for not attending, but this is an important factor
for improving the health care reception of asylum Conclusion
seekers and should be further explored in future studies, Voluntary TB screening among asylum seekers is feasible
including perception of stigma among high-risk TB based on the high health assessment coverage we
groups. Additionally, easy access to screening should be achieved. However, the low yield of CXR and sputum
facilitated to improve screening adherence. In our study, screening in our study suggest focussing TB screening
CXR screening was not offered on-site, which probably on asylum seekers from TB high-incidence countries.
created a structural barrier [33].
Additionally, early health assessments should be of high
In this study, only asylum seekers referred for TB
priority to ensure migrant health.
screening were informed about symptoms of TB disease,
treatment free of charge, etc. Migrant status as an asy-
lum seeker or a refugee pose a risk factor for TB [26]. As
many TB cases develop years after arrival [6], raising Disclosure statement
awareness regarding TB, symptoms, and treatment No potential conflict of interest was reported by the author(s).
826 K. LANGHOLZ KRISTENSEN ET AL.
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