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See corresponding editorial on page 273.

See corresponding CME exam on page 468.

High prevalence of vitamin D deficiency in pregnant non-Westernwomen in The Hague, Netherlands 1,2

Irene M van der Meer, Nasra S Karamali, A Joan P Boeke, Paul Lips, Barend JC Middelkoop, Irene Verhoeven, and Jan D Wuister

ABSTRACTBackground: Vitamin D deficiency is common in dark-skinnedpersons living in northern countries. Vitamin D deficiency duringpregnancy may have serious consequences for both mother andchild.Objective: The objective was to ascertain the prevalence of vitaminD deficiency in pregnant women of several ethnic backgrounds whowere living in The Hague, a large city in the Netherlands.Design: Midwives whose practice was visited by a large number of non-Western immigrants added the assessment of serum 25-hydroxyvitamin D [25(OH)D] to the standard blood test given towomen who visited the practice during week 12 of pregnancy. Sub-sequently, the Municipal Health Service collected additional datafrom the midwives files (June 2002 through March 2004): back-ground variables, use of tobacco or alcohol or drugs, and infectiousdiseases. The women were grouped ethnically as Western, Turkish,Moroccan, and other non-Western.Results: The vitamin D concentrations of 358 women were found inthe midwives files. Of these women, 29% were Western, 22% were

Turkish, and 19% were Moroccan. Mean serum 25(OH)D concen-trations in Turkish (15.2 12.1 nmol/L), Moroccan (20.113.5 nmol/L), and other non-Western women (26.3 25.9 nmol/L)were significantly ( P 0.001) lower than those in Western women(52.7 21.6 nmol/L). Serum 25(OH)D was below the detectionlimit in 22% of the Turkish women. The differences between ethnicgroups were not confounded by other determinants such as age,socioeconomic status, or parity.Conclusions: The prevalence of vitamin D deficiency in pregnantnon-Western women in the Netherlands is very high, and screeningshould be recommended. Am J Clin Nutr 2006;84:3503.

KEY WORDS Hypovitaminosis D, vitamin D deficiency, se-

rum 25-hydroxyvitamin D, pregnancy, ethnic groups, prevalence,women

INTRODUCTION

Vitamin D deficiency is common in dark-skinned personsliving in northern countries. Vitamin D 3 is produced in the skinafter exposuretosunlightor toartificialultraviolet light.Sunlightis less effective in producing vitamin D 3 in persons with darkerskin because theultraviolet light is absorbed by theskin pigment(1,2). Lowsunlight exposure,coveringof theskin, anda diet lowin vitamin D andcalcium may also contribute to lower vitamin D

concentrations in non-Western immigrants to northern countries(35). These risk factors affect both males and females of allages.

Vitamin D deficiency in pregnant women may affect thewomen as well as their unborn children. The deficiency couldlead to a high bone turnover, bone loss, osteomalacia, and hypo-vitaminosis D myopathy in the mother (6, 7). Most studies of vitamin D deficiency during pregnancy have shown negativeeffectson calciumhomeostasisandskeletalmineralizationof the(unborn) child, eg, the occurrence of congenital rickets, cranio-tabes, and lower bone mineral content (810). Effects on mater-nalweight gain, fetal growth, andbirth weight areconflictingandinconclusive (11). Some researchers hypothesize that low pre-natal andperinatal vitaminD concentrations affect the functionalcharacteristicsof varioustissuesof thebody(12, 13),which leadsto a greater risk in later life of multiple sclerosis, cancer, insulin-dependent diabetes mellitus, and schizophrenia.

To ensure adequate absorption of calcium by the fetus, theHealth Council of the Netherlands recommends a higher vitaminD intake for pregnant than for nonpregnant women (14). How-ever, several Dutch organizations (ie, those for midwives, gyne-cologists, andgeneral practitioners) state thatthere is insufficientevidence of a greater need in pregnant than in nonpregnantwomen (15). Many of the studies of vitamin D deficiency inpregnant women over the past 25 y found a high prevalence inpregnant non-Western women in countriesin various parts of theworld (1622). Information on the prevalence in pregnantwomen in the Netherlands is scarce but highly relevant, becausethe group at risk is large and growing: 43% of babies born in the4 largest Dutchcities in2002 were ofnon-Westernethnicity. Theaim of our study was to ascertain the prevalence of vitamin D

1 From the Municipal Health Service of The Hague, The Hague, Nether-lands (IMM, NSK, and BJCM); the Institute for Research in ExtramuralMedicine (EMGO) (PL and AJPB) and the Department of Endocrinology(PL), Vrije University Medical Centre Amsterdam, Amsterdam, Nether-lands; theDepartment of Public Healthand Primary Care, Leiden UniversityMedical Centre, Leiden, Netherlands (BJCM); the Femme Midwives Prac-tice, The Hague, Netherlands (IV); and the De Rubenshoek Primary HealthCare Centre, The Hague, Netherlands (JDW).

2 Reprints not available. Address correspondence to IM van der Meer,Gemeente Den Haag, Dienst OCW/EGG, Postbus 12 652, 2500 DP DenHaag, Netherlands. E-mail: i.vandermeer@ocw.denhaag.nl.

Received December 1, 2005.Accepted for publication March 8, 2006.

350 Am J Clin Nutr 2006;84:3503. Printed in USA. 2006 American Society for Nutrition

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deficiency in an early stage of pregnancy in women of differentethnic groups in The Hague.

SUBJECTS AND METHODS

Subjects

In June 2002, midwives whose practice was in a socioeco-nomically deprived neighborhood in The Hague decided to addthe assessment of serum 25-hydroxyvitaminD [25(OH)D]to thestandard blood tests given to pregnant women (with health in-surance) at their first antenatal visit. Serum 25(OH)D was mea-sured with a radioimmunoassay (Diasorin, Stillwater, MN) by alaboratory accredited by CCKL, the Dutchagency for laboratoryaccreditation. This test assesses 25-hydroxyvitamin D 2 and 25-hydroxyvitamin D 3 together, and, because theformer isabsentintheNetherlands, thisprotocolis identical in the Netherlandswiththe assessment of the latter. The intraassay and interassay CVswere 6%to7%and9% to11%, respectively. Thelower detectionlimit of the assay was 7 nmol/L.

Subsequently, the Municipal Health Service of The Haguecollected additional data from the files of the midwives (June2002 through March 2004): date of blood sample (ie, the seasonin which blood was drawn), self-reported ethnicity, age, postalcode, parity, smoking or alcohol or drug use, and infectiousdiseases. Ethnicity is relevant in relation to type of skin. Wesuspected that some women born in the Netherlands but withforeign parents may have described themselves as being Dutch.Therefore, we verified the subjects ethnicity by comparing itwith their family name at birth; we recoded the ethnicity in 15cases. Women were categorized into 4 broad ethnic groups:Western, Turkish, Moroccan, and other non-Western women.The postal code was used to assign a deprivation score, which isbased on income, percentage of unemployed inhabitants, and thequality of thehousing; a high deprivation score isassociated witha low socioeconomic status.

Statistical analysis

We calculated the mean 25(OH)D values by replacing theconcentrations that were under the detection limit (ie,

7 nmol/L) with concentrations of 3 nmol/L. Differences inmeans between Western and non-Western ethnic groups were

tested with ANOVA, and Dunnetts test was used to correct formultiple comparisons. Serum25(OH)D concentrations were log

transformedbecauseof lackof fitwiththe normalcurve. Becauseof unequal cell variances, this analysis was weighted by theinverse variances of the subgroups (23). Differences in percent-ages were tested by using logistic regression. All analyses wereperformed by using SPSS software (version 12.0.1, SPSS Inc,Chicago, IL).

RESULTS

In theperiod from June 2002 through March2004, 762womencame to the midwives practice in their 12th week of pregnancy.Of these women, vitamin D concentrations for 358 (47%) werefound in the files.

Of these 358 women, 29% were of Western (including indig-enous Dutch), 22%were of Turkish, and19%were of Moroccanorigin ( Table 1 ). Ages ranged from 17 to 42 y ( x

: 26.8 y).Thirty-one percent and 45% of the women lived in neighbor-hoods witha veryhigh anda highdeprivationscore, respectively.Forty-five percent of the women were primigravidae, and 29%werein their second pregnancy. Comparedwith thenon-Westernwomen, the Western women were significantly older, signifi-cantly fewerlived ina neighborhoodwith a veryhigh deprivationscore, and a greater proportion were primigravidae (the last itemwas not significant in comparison to Turkish women). No asso-ciation was found between the season of blood sampling and theethnic group.

Serum 25(OH)D concentrations were significantly associatedwith ethnic group ( Table 2 ). The highest 25(OH)D concentra-tionswere found inthe Western group,and thelowestwere foundin the Turkish group. Replacement of concentrations that wereunder the detection limit with values of either 0 or 6 nmol/Lresulted in almost identical means. In all non-Western groups,most of the subjects (Turkish, 84%; Moroccan, 81%; other non-Western women, 59%) had a vitamin D deficiency. Serum25(OH)D wasbelow thedetection limitof 7 nmol/Lin 22%of theTurkish women.

The mean serum 25(OH)D concentrations did not differ signifi-cantly between the seasons. We did not find a significant seasonalvariation even in the Western women, who had the lightest skin[25(OH)D 25nmol/L: JanuaryMarch, 6%; AprilJune, 10%;

TABLE 1Maternal characteristics by ethnic group

Age 1

Proportion with veryhigh deprivation

score 2 Primigravidae 2Tested Januarythrough March 2

n (%) % % %

Western (reference) 105 (29) 29.5 4.7 3 6 55 34

Turkish 79 (22) 24.3 4.74

534

48 33Moroccan 69 (19) 26.4 5.4 4 46 4 38 5 22Other non-Western 105 (29) 26.3 5.3 4 30 4 36 6 36Total 358 (100) 26.8 5.3 31 45 32

1 Means compared by using ANOVA and Dunnetts test.2 Means compared by using logistic regression.3 x

SD (all such values).4 P 0.001.5 P 0.05.6 P 0.01.

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JulySeptember, 4%; OctoberDecember, 12%). The relation be-tween vitamin D and ethnicity was not confounded by age, season,deprivationscoreoftheneighborhood,parity, smokingoralcoholor

drug use, or infectious diseases.

DISCUSSION

Mean serum 25(OH)D concentrations in women of Turkish,Moroccan, and other non-Western groups were significantlylower than those in the Western women. In all non-Westerngroups, most of the women had a vitamin D deficiency ie,serum 25(OH)D concentrations 25 nmol/L. This threshold isthe reference concentration of the analyzing laboratory and hasbeen debated in theliterature(7).However, there is no consensusabout the appropriate threshold; higher thresholds have beensuggested (2426). These differences in 25(OH)D concentra-

tions between ethnicgroupsmaybe causedby differences inskintype, skin covering (clothes), and the avoidance of direct sunexposure. However, information on these variables was notavailable.

The season of the blood sampling did not show a clear trend invitamin D concentrations. In the Netherlands (52 N), vitamin Dproduction in theskin takes place from April through September(27). We would therefore presume the serum 25(OH)D concen-trations in theJulySeptemberspan to be thehighestand those inthe JanuaryMarch span to be the lowest. However, our resultsdo not support this presumption, even in the Western womenie, those with the lightest skin.

Vitamin D concentrations were available for 47% of 762 eli-gible women. Possible reasons for this relatively low percentageare that the midwives did not 1) add the vitamin D test to thestandard blood test, 2) receive the results from the laboratory, or3) record the serum25(OH)D concentration in the medical files.We assume that this omission may have resulted in an underes-timationof meanvalues.Even if, in a hypotheticalsituation, noneof thewomen withan unknown serum concentrationof 25(OH)Dhad a vitamin D deficiency, 25% of the total population wouldstill bevitamin D deficient, andsucha situationwould bea majorproblem.

Some women came to the midwives practice during a latestage of their pregnancy, had already undergone the standardblood test given in another health-care setting, or both. Thesewomen probably are at higher risk of a vitamin D deficiency

because mostof themare non-Western.The inevitable exclusionof these women will have causedselection bias that is opposite tothe 3 above-mentioned possible reasons. In total, 260 pregnant

women came later than the12th wk of pregnancy, partlybecausethey came from a midwife or physician outside the participatingpractice.

Some other studies have been conducted at a similar latitude(20, 2830) and thus in a region with an intensity of sunlightsimilar to that in the area in the current study. The overall con-clusion in these studies was comparable: vitamin D deficiency iscommon among ethnic minorities in thecities studied(ie,Cardiff and London, United Kingdom), even early in pregnancy. Al-though the first of these studies was published in 1981, the cur-rent study indicates that the problem still has not been solved.

DietarysupplementsmaypreventvitaminD deficiencyduringpregnancy. The Health Council of the Netherlands recommends

a higher amount of vitamin D for pregnant than for nonpregnantwomen. Because of a lack of evidence, this recommendation isnot generally accepted (11, 15, 31). The current study shows,irrespective of this discussion, that special attention should bepaid to non-Western pregnant women in the Netherlands. Thisrecommendation is supportedby recent case historiesof convul-sion in thenewborns of non-Westernmothers in theNetherlands(32).Theseconvulsionswere dueto a vitaminD deficiency in themother during pregnancy.

If the pregnancy itself is not the cause of the vitamin D defi-ciency, it can be said that (preventive) campaigns should aim atall non-Western women, not only pregnant women. However,pregnant women are more easily reachable because of their reg-ular antenatal visits. In addition, the deficiency affects not onlythe mother, because the vitamin D status of the (unborn) child isdependent on the mother (33). There is no consensus about theadequate amount of vitamin D supplementation to prevent orcure a vitamin D deficiency (31, 34). A study by Cockburn et al(35) found that a dose of 400 IU/d for 4 mo resulted in 25(OH)Dconcentrations that were 3.8 nmol/L higher than baseline. How-ever, the baseline concentrations in the population in the currentstudy were lower than those of subjects in thestudyby Cockburnet al, and therefore a higher dose should be considered for oursubjects.

Ourestimation of thepercentageof vitamin Ddeficient preg-nant non-Western women is conservative. With thresholds 25nmol/L, the percentage may rise to almost 100%. Although not

TABLE 2Mean serum 25-hydroxyvitamin D [25(OH)D] concentrations in subjects and proportions of subjects with deficiency or with concentrations under thedetection limit

25(OH)D concentration 1 25(OH)D deficiency 2,3 25(OH)D under the detection limit 3,4

n (%) n (%)

Western (reference) ( n 105) 52.7 21.6 5 8 (8) 1 (1)Turkish ( n 79) 15.2 12.1 6 66 (84) 6 17 (22) 6

Moroccan ( n 69) 20.1 13.56

56 (81)6

3 (4)Other non-Western ( n 105) 26.3 25.9 6 62 (59) 6 9 (9) 7

1 Means compared by using ANOVA and Dunnetts test; vitamin D data were log transformed and weighted by inverse cell variances.2 Deficiency 25 nmol 25(OH)D/L.3 Means compared by using logistic regression.4 Under the detection limit 7 nmol 25(OH)D/L.5 x

SD (all such values).6 P 0.001.7 P 0.05.

352 VALTUENA ET AL

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all effects mentioned above are the proven result of a vitamin Ddeficiency,enough evidence exists forus to consider a vitamin Dconcentration 25 nmol/L as a deficiency. These deficienciesshouldbe diagnosedand cured,andtherefore we recommendthescreening of all pregnant non-Western women for vitamin Ddeficiency. The high prevalences found in this study, the size of the population groups at risk, and the consequences of inactionmake this screening and treatment necessary.

We gratefully acknowledge the statistical assistance of DL Knol.IMM, NSK, BJCM, IV, andJDWdesignedthe study; IMM, NSK, and IV

collected the data; IMM and NSK analyzed the data; BJCM supervised theanalysis of the data; and all authors were involved in writing the manuscript.None of the authors had a personal or financial conflict of interest.

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