Introduction

Vitamin D status has been found to be poor among nonwestern immigrant populations in European countries compared to indigenous European populations [1–4]. The lower serum 25(OH)D concentrations among nonwestern immigrants compared to indigenous European populations may lead to differences in health. Consequences of vitamin D deficiency include bone- and muscle-related symptoms (e.g., bone and muscle pain), decreased muscle strength, and diseases (e.g., rickets in children; osteomalacia in adults) [5, 6]. Other possible consequences are diabetes mellitus, infectious diseases, and cancer [7].

Direct sunlight stimulates the production of vitamin D in the skin from 7-dehydrocholesterol. Other sources of vitamin D include some natural foods (e.g., fatty fish), fortified foods (e.g., margarine), and supplements. The amount of vitamin D produced through exposure to UVB radiation depends on skin type: the darker the skin, the more sunlight is required to produce a given amount of vitamin D [8–10]. Nonwestern immigrants usually have darker skin than indigenous European subjects. Therefore, they have a higher risk of lower serum 25-hydroxyvitamin D (25(OH)D) concentrations when living at the same latitude.

The duration of UVB irradiation needed to produce a certain quantity of vitamin D in a particular skin surface depends on season, time of day, and geographical location [11]. The higher the latitude, the lower the UVB intensity, and the fewer months and hours per day during which vitamin D is produced. Most European countries are located at a higher latitude than the countries of origin of nonwestern immigrants.

The threshold for vitamin D deficiency should—ideally—be based on its consequences. However, most studies of the consequences of vitamin D deficiency have been performed among older western populations in Europe and North America, rather than among adult nonwestern immigrant populations in these countries. Another means of establishing a deficiency threshold is through the use of reference values within a population [12]. For that purpose, a comparison of the vitamin D status of nonwestern immigrant populations with the populations in their countries of origin might be more suitable than a comparison with the indigenous western populations. Our aim was to compare the vitamin D status of nonwestern immigrant populations with both the populations in their countries of origin and the populations in the country they migrated to. Additionally, we wanted to identify what determinants were mentioned to explain differences in vitamin D status between subgroups in the studied populations.

Methods

We performed literature searches in the “PubMed” and “Embase” databases. The search profile consisted of terms referring to vitamin D or vitamin D deficiency, prevalence or cross-sectional studies, and countries or ethnicity. The search was restricted to publications from 1990 onwards; about 1,000 were returned. Titles and abstracts were reviewed to identify studies on population-based mean serum 25(OH)D concentrations among Turkish, Moroccan, Indian, and sub-Sahara African populations in Europe, Turkey, Morocco, India, or sub-Sahara Africa. We accepted the definitions of ethnicity as used in the identified articles.

We extracted data for the Turkish, Moroccan, Indian, and sub-Sahara African populations and for the indigenous European populations if this group was included in the studies performed in Europe. From suitable publications, we extracted information about geographical location and season of data collection, age and gender of the study population, duration of pregnancy if applicable, number of subjects, mean serum 25(OH)D concentration with standard deviation, percentage of subjects with serum 25(OH)D <25 nmol/l, and determinants of serum 25(OH)D concentration. Specific characteristics of the study population which could influence the vitamin D status, such as clothing habits, were also extracted. Of identified intervention studies, we used only data from baseline measurements. Serum 25(OH)D concentrations presented in nanogram per milliliter or microgram per liter were transformed into nanomole per liter. Data variances presented as standard errors or 95% confidence intervals were converted to standard deviations. When either vitamin D status parameter (mean and % <25 nmol/l) was not presented, another measure for vitamin D status (such as median concentration or % below another threshold) was extracted.

Results

Prevalence

The identified studies on Turkish populations in Europe are presented in Table 1 and on Turkish populations in Turkey in Table 2. The vitamin D status was lower in the Turkish groups in Europe than in the indigenous European groups. Vitamin D status in the Turkish groups in Turkey varied widely. The subgroups with covering clothes had the lowest serum 25(OH)D concentrations (mean 10 nmol/l) [13, 14]. Turkish elderly living in their own homes (mean 158 nmol/l for males and 103 nmol/l for females) and Turkish unveiled adult women (mean 135 nmol/l)—all of whom were measured at the end of summer—had the highest serum 25(OH)D concentrations [15, 16].

Table 1 Studies among Turkish populations in Europe
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Table 2 Studies among Turkish populations in Turkey
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Studies on Moroccan populations in Europe are presented in Table 3. Table 4 presents the only study found on the vitamin D status of a Moroccan population in Morocco. As was the result among Turkish populations, the Moroccan populations in Europe had lower serum 25(OH)D concentrations than the indigenous European populations. The Moroccan adult women in Morocco, who were measured at the end of winter, had a mean serum 25(OH)D concentration of 45 nmol/l [17]. This was lower than the indigenous population in the Netherlands (median 67 nmol/l) and in Belgium (mean 49 nmol/l) [1, 3]. The Dutch and Belgian populations consisted of both men and women, and these were measured year-round, which might explain the difference.

Table 3 Studies among Moroccan populations in Europe
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Table 4 Studies among Moroccan populations in Morocco
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Studies on adult Indian (or South Asian) populations in Europe also found lower serum 25(OH)D concentrations in comparison to indigenous European populations (Table 5). Concerning pregnant women and children, we did not identify any studies which included an indigenous European population. The vitamin D status among various Indian populations in India differed (Table 6). Some populations with limited sunlight exposure, such as physicians and nurses (mean 8 nmol/l in winter and 18 nmol/l in summer) or Delhi-based males (mean 18 nmol/l) and females (mean 17 nmol/l) measured in winter, had low serum 25(OH)D concentrations, similar to Indian populations in Europe [18, 19]. Other, mainly rural, Indian adult populations in India had higher serum 25(OH)D concentrations [20, 21].

Table 5 Studies among Indian populations in Europe
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Table 6 Studies among Indian populations in India
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Sub-Saharan Africans in the Netherlands—consisting predominantly of Ghanaians and Somalis—had a median serum 25(OH)D concentration of 33 nmol/l (n = 57) [1]. Congolese immigrants in Belgium had a mean serum 25(OH)D concentration of 38 nmol/l (standard deviation (SD) of 14 nmol/l). We did not identify any studies on vitamin D status in Ghana, Somalia, or the Democratic Republic of Congo. Studies in sub-Saharan countries include a study in Cameroon, with a mean serum 25(OH)D concentration of 53 nmol/l (SD 19 nmol/l) among an older population (aged 60–86 years), a study on Nigerian children (6–35 months) with a mean serum 25(OH)D concentration of 64 nmol/l (sd 23 nmol/l), and a study on Gambian women aged 25 or older, with a mean serum 25(OH)D concentration between 73 nmol/l (SD 20 nmol/l) and 113 nmol/l (SD 27 nmol/l), varying with age [22–24].

In all studies performed in Europe where both groups were included, immigrant groups in European countries had significantly lower serum 25(OH)D concentrations than indigenous European groups [1–4, 25–32].

Determinants

In the last column of each table, the determinants for a lower 25(OH)D concentration are presented. As expected, many studies found a lower exposure to sunlight (e.g., behavior or season) [1–3, 13–18, 27, 32–38] or a restricted intake of vitamin D (via food or supplements) [1, 14, 17, 33, 39, 40], to be associated with a lower serum 25(OH)D concentration.

Neither gender nor age were unambiguously associated with the serum 25(OH)D concentration. Female gender was found to be a determinant for a low serum 25(OH)D concentration [2, 4, 15, 33, 35, 36, 41, 42], but not in all studies that compared males and females [3, 19, 20, 31, 41, 43]. Both a younger age [33] and an older age [15, 17] were associated with a lower serum 25(OH)D concentration.

Other determinants of lower serum 25(OH)D concentrations—explained by association with exposure to sunlight or dietary habits—are a lower socioeconomic position [34, 42], a shorter duration of education [33, 39], or a lower educational level [14], living in an urban environment [20, 21], and an earlier start time to the workday [44].

In newborn children, a mother’s lower serum 25(OH)D concentration was associated with a lower serum 25(OH)D concentration in the child [18, 45, 46].

Discussion

The vitamin D status of Turkish, Moroccan, Indian, and sub-Sahara African immigrant populations in Europe was poor compared to the indigenous European populations. The vitamin D states of studied populations in Turkey, Morocco, and India varied between concentrations similar to the immigrant populations in Europe (low) and concentrations similar to or higher than the European indigenous populations (high). Determinants of the serum 25(OH)D concentration included both sources of vitamin D: exposure to sunlight and intake of vitamin D.

Gender and age were each associated with serum 25(OH)D concentration in both directions. Differences according to gender and age group could be the result of biological differences but might also reflect behavioral differences; dress style (e.g., wearing a veil) is often mentioned as a reason for a higher prevalence of vitamin D deficiency among women than men. A lower serum 25(OH)D concentration among older participants can partly be the result of the lower capacity of the skin to produce vitamin D after exposure to sunlight. The study that found lower serum 25(OH)D concentrations at younger ages [33] might have had a study population that was too young to find an effect of a lower skin capacity (their mean age was below 40 years).

As the described studies were observational, not all determinants could be studied due to a lack of variation in the determinants. For instance, Sahu et al. described the dietary intake in rural India as remarkably monotonous from meal to meal, with a low consumption of dairy and foods containing reasonable amounts of vitamin D [36]. As a consequence, it is difficult to find an association between dietary intake and serum 25(OH)D.

The darker skin types of the immigrant populations are a suitable protection against the intensity and amount of sunlight in their countries of origin, while they are a risk factor for vitamin D deficiency in northerly European countries. The serum 25(OH)D concentrations of the populations in the country of origin may, therefore, indicate normal or reference concentrations. However, those populations may themselves be deficient or suffer from insufficient concentrations as a whole. Given that until recently, mankind lived and worked outside, the serum 25(OH)D concentrations of groups who currently spend much of their time outdoors might, therefore, be considered “normal” [47]. Serum 25(OH)D concentrations of rural populations, who are expected to have a greater exposure to sunlight as a result of their agricultural occupation than urban populations [20, 21], might be a more suitable indicator of normal concentrations than those of total populations.

The high (>100 nmol/l) serum 25(OH)D concentrations in subgroups of two Turkish studies, which were performed at the end of the summer, suggest a large impact of sunlight. As sun exposure does not lead to toxic vitamin D concentrations due to a feedback mechanism, these serum 25(OH)D concentrations are expected to be within the normal or reference range, which is an additional argument that the low serum 25(OH)D concentrations (found in immigrant populations) can be interpreted as a deficiency. Of course, assay differences might also explain part of the difference with other studies.

Symptomatic vitamin D deficiency is also suggested by the prevalence of rickets in Turkey, India, and some African countries [48–53]. The incidence of rickets in Eastern Turkey declined from 6.09% to 0.099% after a nationwide free vitamin D supplementation program [54]. Within European countries, rickets is not highly prevalent, but immigrant populations are groups at risk [55–57]. Additionally, although most nonwestern immigrant populations are younger than the indigenous European populations, cases of osteomalacia in nonwestern immigrants have been observed [58, 59]. Finch et al. found all but one case of osteomalacia within the vegetarian Asian group in England, the group with lowest vitamin D concentrations in their study [32]. Furthermore, osteoporotic and peripheral fractures were found in the vitamin-D-deficient subgroup in Morocco [17]. Erkal et al. found that 61% of the Turkish group (in Turkey) and 55% of the Turkish immigrant group in Germany complained of bone pain and/or nonspecific generalized muscle aches and pain, while it was 15% within the German group with higher serum 25(OH)D concentrations [2]. However, one should keep in mind that serum 25(OH)D is not the sole determinant of rickets; calcium intake is also important [48, 60, 61].

The comparison of serum 25(OH)D concentrations of the various populations in this article has some limitations.

First, several studies present the prevalence of vitamin D deficiency but have excluded individuals using drugs or medication known to affect bone metabolism, those recently treated for vitamin D deficiency, or those who used vitamin D supplements [1, 2, 4, 14–17, 19, 28, 35, 37, 41–43]. Medications that affect bone metabolism include, among others, vitamin D and calcium. One can argue whether the presented values represent the real prevalence in the respective populations when these individuals are excluded. However, we expect the number of excluded individuals to be small and, therefore, not of great influence on the prevalence. Furthermore, it implies that the prevalence is applicable for an apparently healthy population.

Second, the season of blood sampling varies, and this might account for a part of the observed differences between studies, because the intensity of sunlight and the amount of sunlight per day varies between seasons. These differences may be larger when studies in European countries are part of the comparison, because seasonal differences in sunlight are expected to be higher in countries at higher latitudes. For that reason, the time of year was mentioned in the tables.

Third, the comparison is hampered because the serum 25(OH)D assessment methods differ, which may influence differences between groups [62]. In addition, the level of accuracy of studies within Europe and in the country of origin might differ. However, although we could not adjust for this type of bias, we presume that the differences will not be systematic or large enough to substantially alter the conclusions.

Finally, in comparing the various populations, it is important to realize that the social conditions of the immigrants might not be the same as those of the original populations. The cultural habits (skin-covering clothes, sun exposure, diet) might also change after immigration, particularly among the second generation.

Serum 25(OH)D concentrations of nonwestern immigrants in Europe and of subgroups of Turkish, Moroccan, Indian, and sub-Saharan countries are low. Ways to increase the serum 25(OH)D concentration include increased exposure to sunlight and increased intake of products that contain vitamin D. The strategy to effectuate these increases will differ in the various countries and populations and should be the subject of further study. These studies should ideally include measures of health to support the need for this increase in serum 25(OH)D.