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Abstract
High rates of drug-resistant tuberculosis in Ukraine suggest screening is necessary to mitigate public health hazards for host populations. A pathway was implemented in Wales and data prospectively collected Between 8 April and 21 December 2022. Of 5425 Ukrainian arrivals, notifications were received by TB teams on 2395 (44%) of whom 1955 (82%) were screened. The refugees were young (median age 30, IQR 14–41), and predominantly female (66.1%). Interferon- gamma release assay (IGRA) tests were positive in 112 (6.5%). One Case of active tuberculosis was identified (0.05%). Our data supports European guidelines that routine screening of this population is not recommended, but we remain uncertain as to the risks of this population going forwards.
- Tuberculosis
- Infection Control
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Introduction
As of 10 January 2023, the war in Ukraine has resulted in 4.9 million Ukrainian refugees in Europe, including 1.5 million in Poland, 1 million in Germany and 155 000 in the UK.1 This upheaval has produced significant traumas for the Ukrainians involved, but also presents public health issues for the host nations. TB incidence rates in the Ukraine are moderately high at 71 (CI 47 to 100)/100,000,2 but of more concern is the fact that Ukraine has rifampicin-resistant TB (RR-TB) rates of 25 (CI 16 to 35)/100,000 with 24% of all new cases and 58% of those previously treated being multi-drug resistant (MDR-TB).3 Evidence suggests that the burden of drug resistant TB is higher in the east of the country4 and associated with HIV co-infection.3 5 In view of these facts, concerns were raised about the risk of housing refugees in host families without an adequate TB screening programme.
In England, routine screening including chest radiographs was recommended for those more than eleven years old,6 to identify those with pulmonary TB who could pose an infection risk to host families. By contrast, European Centre for Disease Control (ECDC) guidelines recommended screening only those in high risk groups.7 Wales implemented a more comprehensive screening programme utilising a digital implementation framework,8 which has been used successfully to implement a national COVID-19 guideline.9
Methods
Prospective observational study of Ukrainian refugees arriving in Wales from April until 21 December 2022.
Data collection
Data on Ukrainian arrivals to Wales were provided from the Home Office/Welsh Government Ukraine sponsorship Scheme. However, this did not include Ukrainians arriving through more informal routes such as the family settlement scheme.
Data collected on arrivals between 8 April and 21 December 2022 included; age, sex, date of arrival, the presence of symptoms suggestive of TB and the results of tests (chest radiograph, interferon-gamma release assays (IGRA) and mycobacterial culture sensitivities). All tests were labelled with a specific Ukrainian signifier to aid data collection. Chest radiographs were reported by radiology departments in each Health Board (HB). Data was inputted by TB screening teams in each HB onto an online data dashboard.
Guideline development and implementation
A TB screening guideline was developed by senior clinicians using a standard format (figure 1) and launched on April 8 2022. Briefly, the expectation was that screening would be undertaken by TB teams and/or welcome centres in each HB. All TB teams attended a webinar on the pathway which was also disseminated to primary care through a digital framework as previously described.9 The guideline was changed on 5 August to only screen children under 11 who were symptomatic or close contacts of active TB cases.
All Wales pathway for screening refugees at risk of drug resistant tuberculosis.
Outcomes
The primary outcome was identification of cases of active or latent tuberculosis.
Statistical analysis
Continuous variables are presented as median and inter-quartile range. Differences between ages were assessed using the Wilcoxon rank sum test. Differences between sexes were assessed using Fishers exact test. The confidence intervals for the age and sex specific rates used the Wilson method. All analyses were conducted in Stata 17.0.
Results
2395 cases were screened by the TB teams and data inputted into the online tool. 118 cases were excluded due to missing data on sex or age, leaving 2277. A further 322 cases were excluded as they did not record chest radiograph and IGRA data on those 11 or older, leaving 1955 cases for analysis (online supplemental figure). The majority of arrivals were women (1292, 66.1%), and most arrivals of both sexes were young (median age 30 IQR 14–41), table 1.
Supplemental material
Health Board, demographic and IGRA positive rates
There were 112 positive IGRA tests giving a latent TB rate of 6.5%. 96 IGRA tests were done in children under 11 before the guideline changed and only one of these was positive. Those with positive IGRA results were older (median age 40.5, IQR: 35–50) than those with a negative test (median age 33, IQR: 18–42), (p<0.001), and more likely to be male, 42% vs 31.7%, (p=0.03). There were quite different patterns of IGRA positive rates between the sexes with over a quarter of all males 50+testing positive, compared with just one in 20 females aged 50+ (figure 2). Overall, 93% (104/112) of IGRA positive cases were aged less than 65 and thus would potentially qualify for Latent TB treatment. One asymptomatic case had an abnormal chest radiograph and underwent bronchoscopy. Washings confirmed smear negative, fully sensitive mycobacterium tuberculosis. No other chest radiographs were reported as suggestive of tuberculosis.
Latent TB cases (IGRA+) by age and sex.
Discussion
We present the results of screening 1955 Ukrainian refugees for tuberculosis in Wales. The lack of data on precise arrival time or location, together with the fact that many arrived through informal routes highlights the difficulties of the screening process. It is of interest that the ECDC guidelines did not recommend routine screening of this population, although a number of European countries did in fact implement screening programmes.
The strengths of this study are; first, that we implemented a national screening pathway which all screening teams were familiar with. Second, to our knowledge, this is the first analysis of the outcomes of screening this population. The low rate of positive results with a single case of pulmonary TB who was of low infectivity supports the ECDC guidelines that routine screening is not recommended. It is of interest that those with Latent TB infection (LTBI) were significantly older and more often male, so our findings are likely to underestimate LTBI rates in the country as a whole as our population was predominantly female and young. Recent UK screening of refugees from Afghanistan found LTBI rates of 15% among adults.10
The major limitations of this study relate to the lack of precise data on arrivals. TB teams received notifications on 44% and screened 36% of all arrivals, highlighting significant missing data. However, comparison of the study population to the total arrivals data indicated no substantive demographic differences.11 Second, data on where in the Ukraine arrivals came from was not collected, so we cannot compare latent TB infection rates between the east and west of the country. Third, a large number of individuals aged over 11 (322) were excluded from the analysis due to failure to undergo an IGRA or chest radiograph. Lastly, the guideline was changed to no longer recommend screening asymptomatic children under 11 years, partly as a result of frequent refusals from parents to screen their children whom they believed were healthy. The low rates of positive IGRA tests in those under 11 who were screened (1/96) suggests that they were right.
While our results support the European guidelines that routine screening is not recommended, we remain uncertain of the risks for this population going forwards. The majority of TB cases have always been from the east of the country, and the trauma of war creates the perfect conditions for the spread of this disease. Moreover, the WHO goal of TB eradication will only be achieved by identifying and treating latent TB, ultimately necessitating screening of populations such as this.
Ethics statements
Patient consent for publication
Ethics approval
This work was performed as health Surveillance. Consideration of the Health Research Authority decision tool: https://www.hradecisiontools.org.uk/research/docs/DefiningResearchTable_Oct2022.pdf indicated that REC review was not required.
Acknowledgments
Welsh Government for supporting and coordinating the meetings between key stakeholders.
Supplementary materials
Supplementary Data
This web only file has been produced by the BMJ Publishing Group from an electronic file supplied by the author(s) and has not been edited for content.
Footnotes
Contributors SMB conceived the screening guideline and data collection tool and wrote the first draft of the paper with contributions from TDB. GD performed all of the statistical analysis and had substantial input into the key arguments. CD created the guideline and data tool and HS coordinated implementation of the guideline and data collection. GH and JS provided overall denominator data. All other co-authors were involved directly with both the screening process and with data acquisition across Wales and contributed to intellectual content. All authors critically revised and approved the final version.
Funding Welsh Government Funds the Respiratory Health Implementation Group (RHIG) who in turn fund the Institute for Clinical Science and Technology (ICST), who create and implement the digital innovations. There was no specific funding or grant for this work.
Competing interests None declared.
Provenance and peer review Not commissioned; externally peer reviewed.
Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.