Oral Health Status among Migrants from Middle- and Low-Income Countries to Europe: A Systematic Review

Introduction. Economic inequality, political instability and globalization have contributed to the constant growth of the migration phenomenon in recent years. In particular, a total of 4.2 million people migrated to Europe during 2019 and most of them settled in Germany, France and Italy. Objectives. The objective of this study was to conduct a systematic review of studies analyzing the oral health condition among migrants from middle- and low-income countries to Europe and assessing the eventual association between their sociodemographic and socioeconomic characteristics and oral health status. Materials and Methods. A systematic review was conducted in PubMed, Cochrane Library, Scopus and Science Direct databases. After titles, abstracts and full-text examination, only 27 articles were selected on the basis of inclusion criteria and consequently included for quality assessments and data extraction. Results. Most of the studies reported a higher prevalence of caries experience, a poorer periodontal health and more difficulties in accessing dentalcare services among migrant groups compared with the non-migrant population. Inequalities were mostly associated with ethnic background, economic condition and social grade. Conclusion. Our review demonstrates the lack of dental health among migrants, underlining that their cultural beliefs and their social and economic living conditions could influence their oral health.


Introduction
According to the 2017 International Migration Report, the number of international migrants reached 220 million in 2010 and 258 million in 2017, showing a continuous growth in recent years [1]. Migrants represent 3.5% of the world's population (updated to 2019) and India has the highest number of individuals living abroad [2]. Europe, Asia and Northern America host two thirds of international migrants, mainly originating from middle-and low-income countries [3,4]. In particular, a total of 4.2 million people immigrated to one of the European Union (EU) Member States during 2019 (30% of who comes from non-EU countries). In the same year, the largest total number of immigrants was reported by Germany, followed by Spain, France and Italy [5]. The reasons that prompt people to move are known: economic inequality, political instability, increased globalization [6], and it has been demonstrated that immigration status is one of the main determinant in health disparities [7][8][9]. Several factors contribute to defining migrants as vulnerable subjects: health risks before, during and after migration, different disease 1.
What are the oral health conditions among migrants from middle-and low-income countries to Europe? 2.
Considering the sociodemographic (ethnic background) and socioeconomic characteristics (income, social grade, professional status) of migrants, is there an association between these variables and migrants oral health status?
Clinical Question (PICO) • P: A sample of migrants from middle-and low-income countries to Europe • I: Analysis of the oral health condition, oral health habits, attitude towards oral health and use of dentalcare services • C: Association between oral health condition, oral health habits, attitude to-wards oral health and use of dentalcare services and sociodemographic/socioeconomic characteristics • O: Presence of dental caries, periodontal status, need for dental treatment, self-reported oral health, oral health habits, oral hygiene practices, impact of the oral health on life quality

Protocol and Registration
Methods and inclusion criteria were selected following the PRISMA statement [32], since it provides a suitable protocol for systematic reviews.

Eligibility Criteria
Inclusion and Exclusion criteria All the items concerning the oral health status in a population of migrants from middle and low-income countries to Europe were selected and included in our research. Pa-per selection was based on the following inclusion criteria: o The selected population sample had to include subjects identified as migrants o Studies which assessed the social fragility of the migrants' selected subjects, by analyzing their socioeconomic characteristics (education level/professional status/money income/social class) or by identifying them as refugees or asylum seekers o Articles which reported quantitative or qualitative data about the oral health status of the migrants included participants o Papers written in English Reviews and case reports were not selected and studies published before 2010 were excluded from our review, in order to collect the most recent data available in the literature.

Electronic Search
The databases of PubMed, Cochraine Library, Science Direct and Scopus were used to conduct electronic research, selecting relevant articles (published from 2010 to date) concerning the oral health status of migrants from middle-and low-income countries to Europe. Only articles written in the English language were considered, but no restrictions were imposed with regard to the age range of the participants and to the oral health evaluation methodology. Both items with or without non-immigrant (native) population control group were included. The keywords, with the Boolean term "AND", used for the electronic search in each database were "oral health status", "migrants", "oral health inequalities", and "migration to Europe".

Study Selection and Data Collection Process
Eligible articles were selected following the inclusion and exclusion criteria mentioned above by two independent reviewers, who analyzed the titles, abstracts and full text of all the articles that were found during the electronic search. Disagreements between reviewers were resolved by consensus. Data collection was performed by one researcher, who extracted from each article the following information: (a) design of the study (cross-sectional, prospective/retrospective longitudinal), (b) European country in which the study was conducted (Finland, Germany, Greece, Italy, Netherlands, Norway, Spain, Sweden and UK), (c) participants' sociodemographic characteristics (age, gender, country of origin, religious affiliation, place of residence), (d) participants' socioeconomic status (education level, social class, marital status, monthly net income, professional status), (e) methodology used for the oral health evaluation (clinical indices/parameters, self-reported questionnaires or oral interviews); (f) quantitative/qualitative data about the oral health condition of the included subjects (dental caries, periodontal status, oral health habits, oral hygiene practices, impact of the oral health on life quality) were also extracted and used as outcome measures (means and percentages). Furthermore, the researcher collected information regarding the (g) association between the oral health parameters and the sociodemographic (ethnic background) and socioeconomic (income, social grade, professional status) characteristics of the migrant population sample, reporting them as descriptive outcomes.

Critical Appraisal
The JBI Critical Appraisal Tool [33] was used in order to evaluate the methodological quality of the included items (Tables 1-4) and to determine the risk of bias in their design, conduct and analysis. The JBI for case-control studies judges each study based on nine items: (1) target population, (2) participants selection methods, (3) sample size, (4) description of study subjects and setting, (5) response rate of participants, (6) diagnostic methods, (7) standardized and reliable way of measurements, (8) statistical analysis, (9) management of the participants' response rate. Cohort studies are investigated by the same tool based on 11 items: (1) population recruitment, (2,3) exposure, (4,5) confounding factors, (6,7) outcome, (8,9,10) follow-up, (11) statistical analysis. Authors indicate for each item "yes", "no", "unclear", "not applicable" and finally giving an overall appraisal.   Most of the cross-sectional studies included an appropriate sample to address the target population, sampled participants in an appropriate way, choose an adequate sample size and described subjects and settings in detail [34][35][36][37][38][39][40][41][42][44][45][46][48][49][50][51][52][53][54][55]. Only two articles [43,47] did not select an adequate sample size and one research [43] did not describe subjects in detail. None of the included items indicated the response rate, except for two articles [35,43]. Only three of the selected research papers did not provide appropriate statistical analysis [43,47,48], while all the studies used standardized and reliable methodologies for condition identification and measurement. The exposure measurements were similar for both exposed and unexposed group and statistical analysis was appropriate in all the included cohort studies [56][57][58], but confounding factors were not identified in any of these articles.

Study Selection and Characteristics
During the electronic search on PubMed, Cochrane Library, Scopus and Science Direct databases, a total of 681 articles were found. After duplication removal, 646 items were identified and consequently subjected to titles, abstracts and full-texts examination. Only 25 items (22 cross-sectional, 1 prospective longitudinal and 2 retrospective longitudinal) were selected on the basis of inclusion criteria and included for quality assessment and data extraction: 184 studies were not selected based on the publication date (prior to 2010), 72 citations were not included after analyzing titles, 391 after reading abstracts and fulltexts (absence of sociodemographic/socioeconomic status assessment, non-representative sample size, quantitative/qualitative data about oral health not re-ported) and 1 study was excluded because it was written in German language. The flow chart of publication assessment is showed in Figure 1.
The list of the included studies is presented in Tables 5-7. For each item, several information were reported: author, publication date, country in which the research was conducted, study design, number and age range of the included mi-grants (MI) subjects, investigation method used for sociodemographic (SDS) and socioeconomic status (SES) assessment, clinical and qualitative oral health parameters evaluated, statistical test used to establish the association between the oral health and the SDS/SES of the selected subjects (Table 8).            [36] • Use of dental care services (NICE guidelines) Home interview with a structured questionnaire Arora et al. 2017 [37] • Use of dental care services • Self-reported oral health ADHS 2009 model [61] Dujister et al. 2015 [39] • Parents' dental health efficacy • Dental health-related Locus of control (Loc) Validate questionnaire by Pine et al.
Erdsiek et al. 2017 [40] • Use of dental check-ups in the 12c months prior to the interview (dichotomous variable) Secondary analysis from the cross-sectional telephone survey "German Health Update 2010" by Robert Koch Institute [65] Freiberg et al. 2020 [56] • Dental healthcare utilization      [50] Oral questionnaire proposed by the WHO [72] / Pearson correlation between oral health and children's age /  Our review included in total 138,607 participants, of which 26,277 were MI and 112,330 were non-migrants (NMI). Country of origin of MI subjects were Africa, Asia, Central and South America and Eastern Europe. The following sociodemographic characteristics of each MI participant were reported: age, gender, religious affiliation and country of origin. Socioeconomic status was also investigated on the basis of education level, social class, marital status, monthly net income, and professional status.
The oral health condition of the selected sample was analyzed using different parameters. The main oral pathologies evaluated by performing clinical oral examination were: Questionnaires, face to face interview and phone interviews were conducted in order to investigate self-reported oral health, use of dental care services, oral hygiene habits and oral health related quality of life (OHRQoL). Due to the heterogeneity of methodologies used for the oral health condition assessment, results were reported in descriptive way.

Results of Individual Studies
Quantitative data about the oral health of the MI population sample are reported in Tables 9 and 10. Results grouped by single country are presented in Tables 11-15. DMFT/dmft Index was the most used parameter to assess the presence of dental caries [34,35,38,[41][42][43][44]46,50,52].            The DMFT of MI and NMI in the research by Aarabi et al. [34] were equal to 24.8 ± 3.9 and 23.4 ± 4.6, respectively (p value 0.093): the number of missing teeth (M) was similar in both groups, while the number of decayed teeth (D) was on average three times higher in MI subjects. After adjusting for gender, age, monthly net income and education, the number of decayed teeth in MI was higher than NMI. The higher values of API and PBI in MI group (API = 55.3 ± 32.3, p value 0.002; PBI = 46.3 ± 21.1, p value 0.016) demonstrate that the latter had a poorer oral hygiene compared with the native control group (API = 33.0 ± 28.2, p value 0.002; PBI = 30.5 ± 4.5, p value 0.016).
Delgado-Angulo et al. [38] associated the DMFT Index with ethnicity, nativity status and socio-economic position (SEP): Black and Asian MI had lower DMFT than White British and ethnic differences in DMFT remained significant after adjusting for SEP measures. Among MI, the higher the age of arrival and the longer the residence in the UK, the greater the DMFT (adjusted RR: 1.03 and 1.04 per additional year).
The number of decayed and filled teeth in MI children in the study by Ferrazzano et al. [41] were significantly higher (2.49 ± 1.98 and 0.56 ±1.10, p value < 0001) than those in NMI children (1.16 ± 1.35 and 0.38 ± 1.98, p value < 0001) also after adjusting for the educational level of the mothers. The unmet restorative treatment needs (UTN) in native children were lower compared to MI children (68.4% and 86.3% respectively).
Higher odds ratio of caries prevalence was found to be associated with higher age, immigrant background (OR = 2. 65-4.40) and with living in lower income areas (OR = 1.34-1.72) in the article by Gatou et al. [42].
The mean DMFT of the 102 MI included by Goetz et al. [43] was equal to 6.89 ± 5.5 and only 13.7% of the refugees had a healthy dentition.
Høyvik et al. [44] registered a mean DMFT of 10.7 ± 6.8 in MI from the Middle East and of 5.7 ± 4.3 in African refugees. After adjusting for age, gender, origin and level of education, DMFT scores remained higher in Middle East subjects.
Jacobsson et al. [45] analyzed the oral health status of 154 MI and 585 native Swedish participants aged 3, 5, 10 and 15 years in 1993 and 2003: the Plaque indices (PLI) and the Gingival indices (GI) were higher in all age groups among MI group, compared to the NMI one, except the 15-year-olds. Both in 1993 and 2009, significantly less 3 and 5 year-olds in the MI group were caries-free compared with native subjects of the same age. Julihn et al. (2010) [57] selected a cohort of 15538 adolescents aged 13 years (14,160 NMI, 1378 MI) and followed them until they were 19 years of age. The authors showed that MI adolescents with foreign-born parents had statistically significantly more caries compared to NMI adolescents with both parents born in Sweden. The same research recorded a higher DMFSa increment in MI adolescents with 1 or more parents born abroad (53.9) compared to NMI individuals with both Swedish parents (34.7). After adjusting for sociodemographic and socioeconomic confounders (age at migration, maternal/paternal birth region, maternal/paternal education level, marital status, family income, social welfare allowance), the study found out that subjects from Eastern Europe had a higher risk of developing approximal caries lesions during the follow-up period compared to NMI participants (OR = 1.44 (1.12-1.85)).
In 2021 Julihn et al. [58] followed a sample of 3 year-old children until they were 7 years of age, demonstrating that children with both NMI parents (born in Sweden) had a lower caries experience at 3 and 7 years of age (0.1 ± 0.6 and 0.5 ± 1.3 respectively) than children with MI parents. The risk of caries experience at age 7 years was adjusted for household income level and, with regards to the lowest income, OR (CI 95%) of children with both parents born in Sweden was equal to 1.49 (1.37-1.63), OR of children with parents from high-medium-low human development countries (according to Human Development Index, HDI) resulted to be 2.89 (1.64-5.09), 1.69 (1.31-2.17) and 1.90 (1.14-3.15) respectively.
Solyman et al. [52] analyzed the oral health of refugees from Syria and Iraq living in Germany (aged 18-60 years), reporting a mean DMFT = 6.38 ± 5.058 and demonstrating that DMFT score was significantly associated with age and with education level ((Regression Coefficient −0.019, p value 0.037). This study also reported that 79% of the selected participants had bacterial plaque in all six sextants and that 60% of them presented calculus in at least three sextants.
According to Wigen et al. [55], a 5-year-old children in Norway had a higher risk of developing caries into dentine if they had one or both parents of non-western origin (OR = 4.8) and one (OR = 2.1) or both parents (OR = 3.0) with low education.
Results about the use of dentalcare services by MI and NMI were contradictory: two thirds of the MI population included by Aarabi et al. [34] showed difficulties in accessing dental care because of costs and language barriers, presenting a poorer oral hygiene than NMI group; a greater dental services utilization (in United Kingdom) was observed by Al-Haboubi et al. [36] among Asian subjects compared to White and Black individuals. The same authors underlined that access to dental services decreased in lower social classes. On the contrary, Asian and Black participants of the article by Arora et al. [37] declared that they attended dental clinics only if they suffered symptoms (unlike White British people) and their oral hygiene practices, after adjusting for age, sex, education level, household tenure and other confounders, were poorer than the NMI population. Likewise, asylum seekers in Germany selected by Freiberg et al. [56] visited dentists only because of localized and non-localized pain. According to the research by Erdsiek et al. [40], MI adults presented lower socioeconomic status and lower utilization of dental check-ups than NMI individuals. A generally poor oral health was also recorded by Høyvik et al. [44] in refugees from Middle East and Africa to Norway, half of which had oral impacts on daily performances.
Mattila et al. [47] evaluated the utilization of dental care services among MI and asylum seekers in Finland and found that the latter (100%) were significantly less satisfied with access to dental treatment and the quality of treatment than MI (18%). In total, 48% and 11% of the MI and asylum seekers groups, respectively, were aware of caries prevention methods, and none of the asylum seekers knew how to prevent gingival bleeding, while 7% of the MI did.
MI and NMI children in Spain between 3 and 14 years old were compared by Portero de la Cruz et al. [49]: 51.78% and 35.43% of MI and NMI children did not use dental services for over a year respectively. According to socioeconomic and demographic variables, lower social classes and 3-6-year-olds were less likely to use regular dental check-ups.
Dental hygiene was practiced once per day by 44.1% of the refugees studied by Goetz et al. [43] and only 4.9% of them visited dental clinics twice per year during childhood.
Agudelo-Suárez et al. [35]. and Van Meljeren-van Lunteren et al. [56] assessed the OHRQoL of MI population in Spain and Netherlands, respectively. Surinamese and Turkish children showed significant lower OHRQoL than native Dutch children, after adjusting for age, gender of children, caries experience, family income and education level of the mother. On the contrary, the MI group in the Spanish study reported a general low impact of oral health on quality of life.
Mustafa et al. [48] investigated toothbrushing-related perceptions of parents living in Norway with MI background and found that 40% of parents have knowledge about caries as a common disease among children and that 80% of them are aware of the importance of toothbrushing in primary teeth. Moreover, it was demonstrated that oral attitudes were more favorable among MI who had lived in Norway for more than 6 years.
Dujister et al. [39] studied the association existing between parental and family-related factors and childhood dental caries in Moroccan, Turkish and Dutch children. Lower social class was significantly associated with more external locus of control (LoC), poorer parental oral hygiene practices and lower dental self-efficacy and, moreover, Moroccan and Turkish parents presented a more external LoC compared to native Dutch parents.

Discussion
Our review aimed to assess the oral health status, oral health habits and use of dentalcare services among migrant population from middle-and low-income countries to Europe. Data collected in our review highlighted, in general, a higher prevalence of dental caries [34,42,45,46,51,57,58] and a poorer periodontal condition [34,42,45,51] in MI population compared with NMI groups. The impact of inequalities in terms of socioeconomic status have been largely studied in literature [74]. The research conducted in Sweden in 2006 [75] hypothesized and demonstrated that the low socioeconomic status could limit access to dentalcare services, contributing to the social inequalities in oral health. Consequently, if socioeconomic position is linked to health status, it can be stated that inequalities in socioeconomic position could be associated to ethnic inequalities in health [76]. Borrel et al. (USA) [77] examined the relationship between individual and socioeconomic characteristics and periodontal disease and highlighted that low income and low education level were associated with severe periodontitis among Whites and African Americans.
The MI population studied by Aarabi et al. [34] (coming from East Europe, Africa, Asia and South America) had a lower socioeconomic status, a worse oral health and higher treatment needs compare to NMI individuals.
Similarly, 38% of the participants (White British/Irish, Black and Asian) included in the research by Al-Haboubi et al. [36] belonged to the lowest social grade (semi-and unskilled manual workers, state pensioners, casual or lowest-grade workers, unemployed with state benefits only): the authors assessed that dental services use decreased with decreasing social grade.
Erdsiek et al. [40] found a lower access to dentalcare services in Germany among MI, 53.8% and 17.8% of whom had a middle and low socioeconomic status respectively. Authors confirmed that having a higher socioeconomic status was associated with greater use of dental prevention.
The review by Scheppers et al. [78] investigated the potential barriers and factors that could interfere with the access to health services among ethnic minorities: low education, social and socioeconomic status, ethnic background, lack of financial resources and family/social support, cultural perception about symptoms, differences in health beliefs, language skills and unawareness of service availability.
For instance, Portero de la Cruz et al. [49] attributed the disparities in the utilization of dentalcare between MI and native Spanish group to the cultural differences regarding the way families seek dental health care and to the lack of information about health benefits.
Gatou et al. [42] estimated that children's ethnic background was the most strongly affecting risk factor for all the oral health parameters investigated in the study and reported that this relation became stronger when adjusted for independent variables, such as areabased income.
The higher caries prevalence proper of the MI group in the research by Ferrazzano et al. [41] was associated with language difficulties and inequalities in access to information and to health services.
Marcenes et al. [46] examined the inequalities in oral health between Whites, Blacks and Asians living in the most deprived boroughs in the Inner North East London: preschool children from Bangladesh and Pakistan presented a higher level of caries than White children (British, Eastern European), but, on the contrary, Indian children showed a lower level of caries than White children and Black individuals had similar dental health to Whites. Data obtained in this research confirmed the information provided by other authors, underlining that African countries experience a lower caries level than the United Kingdom [79].
Our review included thirteen articles analyzing the oral heath in children/adolescents with age ranging from 0 to 19 years old [39,42,45,46,[48][49][50][51][53][54][55]57,58]. Almost all the studies [39,42,45,46,49,51,54,55] recorded a better oral condition in native children of the control groups compared to the MI groups. Only Mustafa et al. [47] assessed a good knowledge about the importance of oral hygiene among MI parents, showing that they had on average favorable attitudes, subjective norms and strong perception of behavioral control in relation to child tooth brushing.
The oral hygiene practices and behaviors of parents has a direct influence on their children's oral health [80]. According to the socialization theory, family represents the primary socializing agent for children and, consequently, it is easy to explain why the latter adopt oral health-related habits [48]. Mothers and fathers with a foreign background are characterized by different cultures and tradition [45], migrating from their country of origin and facing several social and economic problems: this type of conditions may affect the general health of their children [78]. Julihn et al. [58] supported this theory, demonstrating that the social context of MI families from medium-and low-human development countries could be considered unfavorable for children's oral health. Furthermore, Al-Haj Ali et al. [81] determined the risk factors associated with the presence of ECC among preschool children in eastern Saudi Arabia: mother's occupation, carer's smoking status and feeding practices.
The data about the lack of good oral health among refugees included in five of the selected items [43,44,50,52] are in line with other studies published in literature, which reported a high prevalence of dental caries, periodontal diseases and poor oral hygiene [82][83][84][85]. Refugees left their country of origin because of fear of persecution and/or could not return because they were exposed to persecutory events; they migrate to other countries carrying around weighty problems, facing racism, homelessness, economic and language difficulties [86]. In such condition, since refugees have to face more pressing problems than oral health, they show a tendency to under-utilize dental services [87,88].
This review highlighted, in agreement with the literature, that oral health is one of the greatest unmet health needs of migrants [89]. Since oral health strongly influences quality of life, training and education programs about oral health prevention should be implemented [90], considering individuals' attitudes, capabilities, beliefs and cultural/ethnic background [91].

Strengths and Limitations of the Study
Our study not only provides an overview of the oral health conditions of migrants in Europe, but also analyzed the association between the prevalence of oral pathologies and risk factors of the target population. After performing a critical appraisal, we recorded that most of the selected papers presented a very high quality with regards to sample selection, reliability of measurement methodologies and statistical analysis. However, the included articles used different methods to determine oral health status and as a consequence, the results were presented in a descriptive way. In fact, due to this heterogeneity, it was not possible to provide an appropriate statistical analysis. Furthermore, the selected items conducted their research in different European countries, presenting different social security systems and social conditions. For this reason, we considered this systematic review as an initial analysis that should be followed by another study investigating the oral health status of migrants in a single host country or countries with similar social conditions.

Conclusions
This systematic review reported a poorer oral condition in MI subjects from middleand low-income countries to Europe. Oral health parameters were analyzed in association with ethnicity and socioeconomic status: it was demonstrated that foreign background, low income and social grade could be considered as risk factors for having a worse dental health.
The creation of prevention programs becomes of primary concern, aiming at strengthening oral health knowledge and practices among the MI population. Funding: This research was funded by University of Ferrara, 44121 Ferrara, Italy; research grant 8/2021, titled "Dental caries prevention and screening among socially vulnerable subjects with difficult access to care".