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Reducing burden from respiratory infections in refugees and immigrants: a systematic review of interventions in OECD, EU, EEA and EU-applicant countries

BMC Infectious Diseases volume 21, Article number: 872 (2021) Cite this article

Abstract

Background

Respiratory diseases are a major reason for refugees and other immigrants seeking health care in countries of arrival. The burden of respiratory diseases in refugees is exacerbated by sometimes poor living conditions characterised by crowding in mass accommodations and basic living portals. The lack of synthesised evidence and guideline-relevant information to reduce morbidity and mortality from respiratory infections endangers this population.

Methods

A systematic review of all controlled and observational studies assessing interventions targeting the treatment, diagnosis and management of respiratory infections in refugees and immigrants in OECD, EU, EEA and EU-applicant countries published between 2000 and 2019 in MEDLINE, CINAHL, PSYNDEX and the Web of Science.

Results

Nine of 5779 identified unique records met our eligibility criteria. Seven studies reported an increase in vaccine coverage from 2 to 52% after educational multilingual interventions for respiratory-related childhood diseases (4 studies) and for influenza (5 studies). There was limited evidence in one study that hand sanitiser reduced rates of upper respiratory infections and when provided together with face masks also the rates of influenza-like-illness in a hard to reach migrant neighbourhood. In outbreak situations of vaccine-preventable diseases, secondary cases and outbreak hazards were reduced by general vaccination strategies early after arrival but not by serological testing after exposure (1 study). We identified evidence gaps regarding interventions assessing housing standards, reducing burden of bacterial pneumonia and implementation of operational standards in refugee care and reception centres.

Conclusions

Multilingual health literacy interventions should be considered to increase uptake of vaccinations in refugees and immigrants. Immediate vaccinations upon arrival at refugee housings may reduce secondary infections and outbreaks. Well-designed controlled studies on housing and operational standards in refugee and immigrant populations early after arrival as well as adequate ways to gain informed consent for early vaccinations in mass housings is required to inform guidelines.

Peer Review reports

Background

Worldwide, more than 60 million people were fleeing from war, violence, climate catastrophes, human rights violations and other circumstances at the end of 2017 [1]. Difficult living conditions, the context of having fled from hardship and cultural and language barriers can limit health care access and uptake, as well as result in missed opportunities for prevention, vaccination and treatment [2, 3].

Respiratory infections are a major reason why refugees and immigrants seek healthcare [4, 5]. There is agreement that refugees and asylum seekers are not a notable source of transmission of respiratory disease to the general population [5,6,7]. Refugees and asylum seekers often are exposed to difficult living and housing conditions in sometimes improvised camps, shelters, and reception centres especially during the period of travel after forced migration, but also during the first months after arrival. In some communities not only refugees but also other immigrants may experience similar conditions due to crowded households, missing financial resources, unsanitary housings, and a lack of hygiene. Whenever talking in general about this population we therefore use the term “refugees and immigrants’’. However, due to these difficult living and housing conditions refugees and immigrants are not only at higher risk of respiratory infections [8], but also at higher risk of critical illness from vaccine preventable diseases [9] than non-migrant populations. This makes respiratory tract-related infections and vaccine-preventable diseases particularly important health issues in this population [4, 4, 8, 10,11,12].

To our knowledge no specific guidelines on reducing the overall burden of respiratory infectious diseases in refugees and immigrants exists. Instead national guidelines mostly focus on vaccine-preventable diseases not always specifically mentioning refugees and immigrants. Also, there is little consensus across different guidelines on which strategies should be applied [13,14,15,16,17,18,19,20,21]. There is a lack of specific guidelines targeting the management of respiratory infections as well as guidelines specifically aiming on refugee and immigrant populations (see Table 1).

Table 1 National and international guidelines with recommendations regarding infectious diseases, including respiratory infectious diseases
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Several recent reviews have criticised national screening guidelines as too restrictive, focussed on single diseases [22] and failing to cover the targeted populations [4, 22, 23], failing to provide information on how to improve screening and treatment coverage and completion [23], and being insufficiently based on evidence and evidence synthesis [24] (see Table 2). Previous studies of refugee and immigrant populations have mainly been concerned with screening and treatment strategies, as well as the cost-effectiveness of tuberculosis prevention in immigrants from high to lower-incidence regions [25,26,27]. Despite prevalence assessments of disease spectrums in migrant and refugee health and evaluations of implemented screening strategies[4, 5, 8], effective strategies and recommendations to reduce the burden of respiratory infections are lacking [9, 24, 28,29,30]. Healthcare providers often have insufficient training and are confronted with specific ethical, institutional and cultural issues as well as unfamiliar spectrums of diseases and symptoms [31,32,33]. Overviews and syntheses of evidence regarding effective interventions in refugees and immigrants are scarce, especially in industrial nations [24, 34, 35]. Yet evidence is urgently needed to inform recommendations for treatment, diagnostics, screening and effective prevention of infectious diseases [22, 28] in national and international guidelines.

Table 2 Previous or ongoing systematic reviews regarding infectious diseases and respiratory infections in refugees and asylum seekers
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The objective of this systematic review is to collect and synthesize evidence on the effect of interventions to diagnose, treat and manage respiratory-tract infections in refugees and immigrants in OECD, EU, EEA and EU-applicant countries.

Methods

This review was carried out in accordance with the PRISMA Statement [36] and the Cochrane Handbook [37, 38]. (PROSPERO: CRD42018074338) [39]. A completed PRISMA checklist is provided as Additional file.

Eligibility for inclusion

We included controlled studies (including non-randomised intervention studies and longitudinal studies with pre-test/post-test designs) published between 1 January 2000 and 1 October 2019. Study populations were refugees [40], asylum seekers [40] or immigrant hard-to-reach populations (e.g. Sinti and Roma, sex workers, drug abusers, prisoners, homeless people and people living with HIV [29, 41]). As previously mentioned, we use the term ‘’refugees and immigrants’’ whenever talking about this population in general. Place of intervention was a member country of the OECD [42], the European Union [43, 44], the European Economic Area (EEA) [45] or an European Union applicant country [46] (For full list of included countries see Additional file 1). Included were interventions to reduce incidence, prevalence, mortality, delay to diagnosis and treatment and transmission from respiratory infections, including lower and upper respiratory infections of unknown aetiology, acute respiratory infections and respiratory infections with pathogens listed in the PICOS table (Table 3). Also included were interventions to improve vaccination coverage for respiratory-related vaccine-preventable diseases. We excluded interventions to reduce tuberculosis incidence due to the existence of several recently-published systematic reviews [25,26,27, 29, 41]. Studies with any type of individual- or group-level interventions were included: outbreak prevention, any type of vaccination campaign, health literacy interventions, pharmaceutical and non-pharmaceutical prevention and treatment strategies, housing interventions and local health care arrangements.

Table 3 PICOS table
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Outcomes were change in diseases incidence, prevalence or mortality, delay to diagnosis or treatment, transmission rates, number of secondary cases and vaccination coverage.

Search strategy, study selection and data collection

The database search was conducted following the Cochrane Collaboration guideline for systematic literature searches [47, 48]. The following databases were searched in June 2017. The search was updated in May 2018 and October 2019:

  • MEDLINE® using OvidSP (including: Ovid MEDLINE® Epub Ahead of Print, In-Process & Non-Indexed Citations, Ovid MEDLINE® Daily)

  • Web of Science by Clarivate Analytics using All Databases

  • CINAHL using EBSCOhost

  • PSYNDEX using EBSCOhost.

The search terms in the literature review included specific terms for respiratory infections, unspecific terms for infections and inflammation in general, terms for anatomic and topographic localisations, and terms for refugees and immigrants. The Medline® search was complemented by a Mesh Term search. The full search strategy can be found in Additional file 3.

References were screened by title and abstract by two reviewers (JFL and AB) independently, consensus was reached via consultation with a third reviewer (BL). For all selected abstracts full texts were obtained. We extracted information on study characteristics, study population, study design and outcome measures. In cases of incomplete or inconsistent data, authors were contacted.

Interrater agreement was calculated with kappa-statistics using the respective decisions whether to include or to exclude a study of the two reviewers J-F L and AB.

Our used data collection form is provided in Additional file 2.

After extraction, data was summarised and represented in tabular form by outcomes and outcome measures: Incidence rate, outbreak measures in number of secondary cases per exposed individual and vaccination coverage as percentage of being vaccinated. Further outcome measures were not found, i.e. mortality rate, delay to diagnosis and treatment. Whenever possible, we calculated risk or rate ratios comparing intervention and control groups to achieve better comparability.

Risk of bias assessment

Risk of bias assessment was carried out using the ROBINS-I tool for cohort-style non-randomised trials of interventions for all included non-randomised trials [49] and using RoB2.0 for all included randomised controlled trials [50]. Risk of bias across studies was evaluated for publication and language bias and following the GRADE recommendations in the range of outcome subgroups across studies [51,52,53,54,55].

Results

Study Selection and characteristics

After manual deduplication 5779 of 10,242 abstracts remained for screening. After title and abstract screening 105 full texts were assessed of which 9 studies were included in the review. Inter-reviewer reliability was high. The calculated kappa was = 1. While the actual decisions whether to include or exclude a study were the same in 100% of cases (kappa = 1), only in 96% the reasons for these decisions were the same. The PRISMA flowchart is displayed in Fig. 1.

Fig. 1
figure 1

Prisma Flow-Chart (separately uploaded)

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Results of individual studies

(See Table 4 and 5).

Table 4 Characteristics of included studies
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Table 5 Results of included studies
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While using the term ‘’refugees and immigrants’’ whenever talking in general about the targeted populations in this review we used the respective expression of the respective study when narrating the individual results.

Influenza vaccination/interest in vaccination informational campaigns

Three studies assessed influenza vaccination in hard-to-reach neighbourhoods in New York City with an immigrant proportion of more than 70% [56,57,58]. Each evaluated multilingual information campaigns in various forms such as comic strips, informational talks, and community events responding to common myths about vaccinations and advising on locations of free vaccination clinics. Three different outcomes have been measured. The interest in getting vaccinated against influenza [58] increased by 14% post-intervention compared to pre-intervention. The probability of a person vaccinated against influenza living in the same household as the respondent [56], increased by 10.2% pre-intervention compared to post-intervention. A randomised controlled study compared health literacy campaign with added non-pharmaceutical prevention strategies against influenza and upper respiratory infections [57]: one group (Group E) received only the informational campaign, another (Group 1) received additional alcohol-based hand sanitiser, and a third group (Group 2) received additional hand sanitiser and face masks. Influenza vaccination coverage improved in all groups after the intervention period by 19.7% in Group E, by 38.1% in Group 1 and by 21.1% in Group 2.

One study retrospectively evaluated the effect of the national vaccination campaigns against influenza in Spain in 2008/2009 and 2009/2010 [59]. There was no evidence of an increase in vaccination coverage in immigrants; the proportion of vaccinated immigrants increased insignificantly by 2.1% compared to the years before. We were unable to identify the main content of the campaign interventions. We found no official records of the interventions and received no answer to our requests for information.

In pregnant women of varying ethnicities in Seattle [60], influenza vaccination coverage increased by 27.2% post-intervention, which compares to data from the Pregnancy Risk Assessment Monitoring System (PRAMS) from separate studies [61,62,63,64,65]. The intervention in this study comprised three months of multi-language information and video material in the waiting room of a birth-clinic as well as personal talks and “flu-packs” consisting of face masks, hand sanitiser and thermometers [60].

Vaccination campaigns for respiratory tract-related childhood diseases

Three studies evaluated different vaccination campaigns for respiratory tract-related childhood diseases [66,67,68]. One compared the effectiveness of two consecutive mass vaccination campaigns of governmental and non-governmental organisations against 8 antigens in recently-arrived refugee children under 4 years of age fleeing from the Kosovo Crisis (1998/1999) in Macedonian refugee camps with high and low turnover [66], showing a benefit for more stable populations with less turnover: in a camp with high population turnover vaccination coverage rates dropped by 20% after the second campaign three weeks later, while in a stable population camp vaccination coverage stayed constant after both campaigns. Before the second mass vaccination weekly vaccination clinics were initiated in the respective camps.

In a second study the Ministry of Health in German reception centres implemented a vaccination campaign for MMR and DPPT which involved vaccine doses, informational material and interpreters to ensure informed consent in newly arrived refugees. The percentage of refugees with at least one vaccination increased by 26.8% compared to pre-intervention.

The third study evaluated the effect of the “keyperson’’ principle enhancing the effectiveness of a MMR vaccination campaign for children under 10 years of age [67]. Keypersons are defined as trained persons from similar living conditions and ethnicities. In this study, they assisted in a door-to-door vaccination campaign in German hard-to-reach and broad-spectrum immigrant neighbourhoods with refugee proportions of about 30%. The risk of receiving at least one dose of vaccination increased by 29%, while the risk of receiving two doses increased by 52%.

Outbreak prevention

In a Swiss interventional study, two varicella outbreak response strategies were evaluated in newly arrived refugees [69]. The first (”rapid’’) involved the isolation of index cases and serotesting and, if necessary, vaccination of people in the same housing facility. This was found to lower the proportion of infected persons from by 10% compared to an outbreak series in 2007 with no previously defined response strategy. The second (“general’’) response strategy involved the strict vaccination of all arriving refugees aged 15–39 years without a history of varicella, leading to no varicella infections in any refugee shelter.

URI/ILI/Influenza prevention

The previously-described randomised controlled trial by Larson et al. in hard-to-reach neighbourhoods also assessed rates of upper respiratory infections (URI), influenza and influenza-like illness (ILI) [57]. It was found that the URI rate/1000 person-weeks in the control group E (informational campaign only) was 35.38, in Group 1 (additional hand sanitiser) it was 29.06 and in Group 2 (hand sanitiser and face masks) it was 38.91. ILI rates/1000 person-weeks were 2.26 in Group E, 1.93 in Group 1, and 1.56 in Group 2. Influenza rates/1000 person-weeks were 0.52 in Group E, 0.60 in Group 1, and 0.49, 95% CI: 0.32–0.73 in Group 2.

Main evidence gaps

The main evidence gaps include a lack of data on housing arrangement standards, interventions to reduce rates of bacterial pneumonia, and evidence for the efficacy of operating standards in refugee and immigrant health care and reception centres (Table 6).

Table 6 Evidence gaps identified in this systematic review
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Risk of bias

(See Table 7).

Table 7 Risk of bias assessment of included studies
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The most important sources of bias among studies targeting vaccination coverage of respiratory tract-related infections were confounding bias in seven [56, 58,59,60, 66, 68, 70], reporting bias in six [56, 59, 60, 66, 68, 70] and bias due to the measurement of outcomes in 6 studies [56, 59, 60, 66, 68, 70]. The most important non reported confounding factors were length of travel in seven [56,57,58,59,60, 66, 68,69,70], period of stay in seven [56,57,58,59,60, 66, 70] and health literacy in seven studies [56, 58,59,60, 66,67,68]. The main source of bias among studies targeting prevention of upper respiratory tract infections, influenza-like illness, influenza and vaccination coverage for influenza was social desirability bias in three studies [56,57,58]. In two studies the risk of bias was rated as critical; one because of missing data [60], and the other mainly due to incorrect classification of interventions [59].

Across studies the heterogeneous outcome measures could be an important source of bias, especially among the studies on influenza vaccination uptake, as interest in being vaccinated [58] or the presence of a vaccinated person in a household [56] may not be valid measures of actual vaccination coverage [57, 60] in the examined population. Publication bias may also be an important source of bias, because with only two exceptions [57, 66], no negative intervention effect was described. Therefore, the findings regarding the overall effect of these interventions should be interpreted with caution [51] and evidence across all outcomes is evaluated as “low’’ following the GRADE approach.

Since the included studies have heterogeneous study designs, characteristics and outcome measures, no pooled analysis in the form of a meta-analysis was performed.

Discussion

Key results

In this systematic review of controlled studies, we collected evidence on interventions aiming to reduce morbidity or mortality from respiratory infections and to improve vaccination coverage among refugees and immigrants in hard-to-reach neighbourhoods. In six studies, we found evidence for the effectiveness of multilingual informational campaigns to increase the uptake of vaccination [56,57,58, 60, 67, 68].

There was limited evidence in one study that hand sanitiser reduced rates of upper respiratory infections and when provided together with face masks also the rates of influenza-like-illness in a hard to reach migrant neighbourhood [57].

To reduce secondary cases in outbreak situations, one study reported that in the case of vaccine-preventable diseases, general vaccination strategies implemented in refugees immediately after arrival have a large effect in reducing secondary cases. Evaluation of a positive history of infection or vaccination is sufficient, but serological testing after potential exposure is not necessary [69]. The hazard of outbreak situations is also lowered by this strategy. [69]

Evidence rarely reflected in international standards

Five informational campaigns assessed in this review integrated the cultural and educational background of the targeted population [56,57,58, 60, 67], either by recruiting keypersons supporting the campaign staff [67], or by directly addressing common cultural myths about vaccinations [57, 58]. The efficacy of this strategy is not currently reflected in national or international guidelines, but is congruent with evidence that informational campaigns, community und culturally-oriented health literacy interventions are effective in improving vaccination coverage in autochthonous populations [71,72,73].

Currently, only NICE recommends institutional health literacy interventions in immigrant populations, however these are not clearly defined. Other European guidelines for refugee and immigrant health care do not address this issue (Table 1).

European guidelines explicitly recommend against implementation of vaccination strategies at border crossings because informed consent is difficult to obtain [15]. However, a timely vaccination strategy has been shown to reduce the potential for outbreaks in particular for highly transmissible diseases [69]. Research is needed to determine the optimal strategies for obtaining informed consent in this situation [74,75,76].

No evidence could be found for interventions targeting housing facilities for refugees and immigrants, although they play an important role in the transmission and spreading of infectious diseases [15]. The effect of turn-over of refugees and immigrants on vaccination coverage in refugee camps shows that it is easier to implement vaccination campaigns during the first months after arrival in more stable camps, but this study did not investigate overall housing conditions or number of housing units [66]. We did not find any controlled studies of interventions to reduce morbidity and mortality from relevant severe respiratory diseases such as bacterial pneumonia or interventions affecting the latency to diagnosis in airway infections.

Limitations

Migration status was not always clear for all participants in the identified studies. While most of the studies indicated the ethnic or geographical origin of the participants [56,57,58, 60, 67], only two primarily represented refugee populations [66, 69]. However, interventions in the context of having fled from hardship, forced migration and life as a refugee are possibly presenting an important independent factor [5]. Countries of origin were not always clearly indicated, especially for Latin American and African populations. In addition, the heterogeneous outcome measures among the included studies made it difficult to obtain concrete effect estimates for refugee and immigrant populations. Some of the findings should be interpreted with caution due to methodological issues in several of the studies (see Table 7).

The countries of origin of refugees and immigrants have shifted in the last 10 years [77, 78], therefore we included a longer time-span to provide a broader overview and context in relation to refugee health.

Conclusions

Respiratory infections continue to be a major contributor to the poor health status of refugees and immigrants and currently interventions to lower this burden are not adequately reflected in national guidelines. This evidence synthesis shows that while there is some low-quality evidence for the effect and timing of multilingual vaccination campaigns that involve the community, there is little high-quality research on housing standards or operational standards needed to prevent respiratory infections in this population. Similar to other reviews of refugee and hard-to-reach populations for tuberculosis [29, 41], vaccine-preventable diseases [79] and respiratory infections [8], we conclude that it is important to follow community-involving principles in informational campaigns and that more controlled operational research is needed. New methods of ensuring informed consent for early vaccinations must also be established. This could allow immediate vaccinations upon arrival in order to reduce secondary infections in crowded living portals such as reception centres and mass housings. Also, for future research it is essential to indicate the political status of migrant study populations because the context of forced migration may present an important independent factor.

Availability of data and materials

Not applicable. Full search strategy in Additional file 3. Data extraction spreadsheet in Additional file 2. Our full extraction dataset will only be available on request.

Abbreviations

Tb:

Tuberculosis

VPD:

Vaccine preventable diseases

AMR:

Antimicrobial resistant pathogens

OECD:

Organisation for Economic Co-operation and Development

EU:

European Union

EEA:

European Economic Area

ILI:

Influenza-like-illness

URI:

Upper respiratory infections

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Acknowledgements

Part of the results of this systematic review have been presented as an oral session at the 29th ECCMID in Amsterdam (April 2019). As previously stated, this systematic review was updated afterwards in October 2019.

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Open Access funding enabled and organized by Projekt DEAL.

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Author notes

  1. Martin Boeker and Berit Lange contributed equally to this work

Authors and Affiliations

  1. Division of Infectious Diseases, Department of Medicine II, Medical Center and Faculty of Medicine, University of Freiburg, Hugstetter Straße 55, 79106, Freiburg im Breisgau, DE, Germany

    Jan-Frederic Lambert, Katarina Stete, Annabelle Bockey, Winfried Kern, Siegbert Rieg & Berit Lange

  2. Institute of Medical Biometry and Statistics, Faculty of Medicine and Medical Center, University of Freiburg, Freiburg im Breisgau, Germany

    Jan-Frederic Lambert, James Balmford & Martin Boeker

  3. Department of Epidemiology, Helmholtz Centre for Infection Research, Inhoffenstr.7, 38124, Braunschweig, DE, Germany

    Berit Lange

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Contributions

Idea: BL, KS, J-FL, MB. Conception and design: BL, MB, J-FL, KS. Data extraction and screening: J-FL, AB, BL. Interpretation of the findings: J-FL, BL, JB, WK, SR. First draft: J-FL, BL. Commented and revised first draft: MB, KS, AB, JB, SR, WK. All authors read and approved the final manuscript.

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Correspondence to Jan-Frederic Lambert.

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Supplementary Information

Additional file 1.

Included countries.

Additional file 2.

Data extraction spreadsheet.

Additional file 3.

Full search strategy.

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Lambert, JF., Stete, K., Balmford, J. et al. Reducing burden from respiratory infections in refugees and immigrants: a systematic review of interventions in OECD, EU, EEA and EU-applicant countries. BMC Infect Dis 21, 872 (2021). https://0-doi-org.brum.beds.ac.uk/10.1186/s12879-021-06474-0

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