Vitamin D Fortification of Fluid Milk Products and Their Contribution to Vitamin D Intake and Vitamin D Status in Observational Studies—A Review

Abstract

Fluid milk products are systematically, either mandatorily or voluntarily, fortified with vitamin D in some countries but their overall contribution to vitamin D intake and status worldwide is not fully understood. We searched the PubMed database to evaluate the contribution of vitamin D-fortified fluid milk products (regular milk and fermented products) to vitamin D intake and serum or plasma 25-hydroxyvitamin D (25(OH)D) status in observational studies during 1993–2017. Twenty studies provided data on 25(OH)D status (n = 19,744), and 22 provided data on vitamin D intake (n = 99,023). Studies showed positive associations between the consumption of vitamin D-fortified milk and 25(OH)D status in different population groups. In countries with a national vitamin D fortification policy covering various fluid milk products (Finland, Canada, United States), milk products contributed 28–63% to vitamin D intake, while in countries without a fortification policy, or when the fortification covered only some dairy products (Sweden, Norway), the contribution was much lower or negligible. To conclude, based on the reviewed observational studies, vitamin D-fortified fluid milk products contribute to vitamin D intake and 25(OH)D status. However, their impact on vitamin D intake at the population level depends on whether vitamin D fortification is systematic and policy-based.

Full text

nutrients
Review
Vitamin D Fortification of Fluid Milk Products and
Their Contribution to Vitamin D Intake and Vitamin
D Status in Observational Studies—A Review
Suvi T. Itkonen * ID , Maijaliisa Erkkola ID and Christel J. E. Lamberg-Allardt ID
Department of Food and Nutrition, P.O. Box 66, 00014 University of Helsinki, 00790 Helsinki, Finland;
maijaliisa.erkkola@helsinki.fi (M.E.); christel.lamberg-allardt@helsinki.fi (C.J.E.L.-A.)
*Correspondence: suvi.itkonen@helsinki.fi; Tel.: +358-44-356-1209
Received: 25 June 2018; Accepted: 7 August 2018; Published: 9 August 2018


Abstract:
Fluid milk products are systematically, either mandatorily or voluntarily, fortified with
vitamin D in some countries but their overall contribution to vitamin D intake and status worldwide
is not fully understood. We searched the PubMed database to evaluate the contribution of vitamin
D-fortified fluid milk products (regular milk and fermented products) to vitamin D intake and
serum or plasma 25-hydroxyvitamin D (25(OH)D) status in observational studies during 1993–2017.
Twenty studies provided data on 25(OH)D status (n= 19,744), and 22 provided data on vitamin
D intake (n= 99,023). Studies showed positive associations between the consumption of vitamin
D-fortified milk and 25(OH)D status in different population groups. In countries with a national
vitamin D fortification policy covering various fluid milk products (Finland, Canada, United States),
milk products contributed 28–63% to vitamin D intake, while in countries without a fortification policy,
or when the fortification covered only some dairy products (Sweden, Norway), the contribution
was much lower or negligible. To conclude, based on the reviewed observational studies, vitamin
D-fortified fluid milk products contribute to vitamin D intake and 25(OH)D status. However, their
impact on vitamin D intake at the population level depends on whether vitamin D fortification is
systematic and policy-based.
Keywords:
dairy; vitamin D; vitamin D-fortified milk; vitamin D intake; vitamin D fortification;
25-hydroxyvitamin D
1. Introduction
Vitamin D plays an important role in bone health, being necessary for calcium absorption [
1
].
Low vitamin D status in terms of low serum 25-hydroxyvitamin D (S-25(OH)D) concentration has
also been linked to the increased risk of some common chronic diseases, such as type 2 diabetes or
cardiovascular disease [
2
]. In Northern latitudes, especially in the wintertime, ultraviolet B (UVB)
radiation is too low for dermal synthesis of vitamin D [
3
]. As there are only a few natural vitamin
D-rich foods, such as fish, egg yolk, and some wild mushrooms [
1
], some countries, particularly
populations at high latitudes, have initiated national policies of fortifying certain foods with vitamin
D to prevent vitamin D deficiency. Usually these vitamin D-fortified products are low-fat milk, fat
spreads, breakfast cereals, and certain baby foods [
4
,
5
]. To better cover different population groups
with differing food habits, a wider vitamin D fortification of different products instead of concentrating
on only a few staple foods has been suggested [5].
To our knowledge, a portion of milk products are systematically, either mandatorily or voluntarily,
fortified with vitamin D only in Finland, Norway, Sweden, Canada, and United States (Table 1) [
6
–
12
].
In Finland, the recommended fortification level of all fluid milks except some organic products
Nutrients 2018,10, 1054; doi:10.3390/nu10081054 www.mdpi.com/journal/nutrients

Nutrients 2018,10, 1054 2 of 19
is currently 1
µ
g/100 g, but some products with a concentration of 2
µ
g/100 g are available on
the market [
6
,
7
]. The fortification is voluntary, but all manufacturers unanimously follow the
recommendations. In Norway, only one type of milk is recommended to be fortified with vitamin D at
a concentration of 0.4
µ
g/100 g [
8
]. Sweden recently doubled the fortification levels of fluid milks to
1
µ
g/100 g and extended the mandatory fortification to cover all fluid milk products with <3% fat [
9
,
10
].
Health Canada has also proposed increasing the mandatory vitamin D fortification of fluid milks from
around 1
µ
g/100 g to 2
µ
g/100 g as a consequence of the inadequate vitamin D intake among the
population [
11
]. In the United States, fluid milks can be fortified with vitamin D by around 1
µ
g/100 g;
the fortification is not mandate at the federal level, but most states mandate fortification [
12
]. In other
countries, such as United Kingdom, Ireland, Spain, and Australia, the fortification is not systematic,
but there is a varying number of vitamin D-fortified milk products available [
13
–
17
]. However, data on
their proportion to the total amount of dairy products in different countries is not easily accessed due
to fluctuations in the market. This causes a knowledge gap on the prevalence of vitamin D fortified
fluid milks and their contribution to vitamin D intake worldwide.
In the latest updated systematic review and meta-analysis on the effects of vitamin D fortification
in randomised controlled trials (RCT), 12 of the 16 included studies used different milk products,
such as fluid milk or milk powder, as a carrier of vitamin D [
18
]. Four of these studies used vitamin
D-fortified milk and two used vitamin D-fortified yoghurt drinks. All of the studies showed the
efficacy of the studied milk products to increase the S-25(OH)D concentration or decrease the decline in
S-25(OH)D status during the wintertime relative to the control group [
19
–
24
]. Further, in Finland, the
vitamin D fortification of fluid milks has been shown to improve the S-25(OH)D status independently
among regular milk users after extensive changes in the national vitamin D fortification policy in an
11-year follow-up study [25].
The aim of this review was to investigate the contribution of vitamin D-fortified fluid milk
products (regular milk and fermented products, such as sour milk and yoghurt) (i) to vitamin D intake;
and (ii) to vitamin D status (25(OH)D concentration in plasma or serum in observational studies with
a special focus on differences possibly caused by different vitamin D fortification policies.

Nutrients 2018,10, 1054 3 of 19
Table 1. Countries with a vitamin D fortification policy of fluid milk products.
Country Vitamin D-Fortified Milk Products Type of Fortification Added Amount of Vitamin D New Proposed Amounts of Vitamin D
Finland [6,7]
fluid milk products (milk, yoghurt, sourmilk) *
voluntary 1 µg/100 g na
Norway [8] extra low-fat milk (also lactose free) voluntary 0.4 µg/100 g na
Sweden [9,10] low-fat milk (max 1.5% fat) mandatory 0.38–0.50 µg/100 g 0.95–1.10 µg/100 g for milk <3% fat
0.75–1.10
µ
g/100 g for fermented milk <3% fat
Canada [11] milk mandatory 0.825–1.125 µg/100 g 2 µg/100 g
United States [12]fluid milk (also acidified milk and cultured
milk), yoghurt voluntary ‡1.05 µg/100 g for milk
2.225 µg/100 g for yoghurt §na
* In regard to organic milk products, it is mandatory to add 1
µ
g/100 g vitamin D to homogenized fat-free milk (not allowed on other organic milk products).
‡
for milk products, only
evaporated and non-fat dry milk are mandatorily fortified. §maximum amount; na = not applicable.

Nutrients 2018,10, 1054 4 of 19
2. Materials and Methods
2.1. Data Sources and Search Strategy
The literature search was done in the PubMed database at the end of December 2017. The search
terms were the following combination of keywords: “vitamin D” [MeSH Terms] OR “vitamin D” [All
Fields] OR “ergocalciferols” [MeSH Terms] OR “ergocalciferols” [All Fields]) AND (dairy [All Fields]
OR (“milk, human” [MeSH Terms] OR (“milk” [All Fields] AND “human” [All Fields]) OR “human
milk” [All Fields] OR “milk” [All Fields] OR “milk” [MeSH Terms])) AND (fortification [All Fields] OR
fortified [All Fields]”. We limited the search to articles that had the search terms in their title, abstract
or among keywords. The data search was restricted to the last 25 years from 1993 to 2017.
2.2. Eligibility and Study Selection
Two independent authors reviewed the titles and abstracts of all identified studies and selected
observational studies that reported either vitamin D intake or 25(OH)D status in plasma or serum
for full-text screening. Among the full-texts, the eligibility of the articles was screened using the
following exclusion criteria: full-text in a language other than English, studies with disease outcomes,
participants/patient groups with diagnosed diseases, participants aged less than one year, studies in
which the contribution of growing up milks (special products marketed for 1 to 3-year-olds) could not
be separated from that of other fluid milks, RCTs, and reviews. In addition, nationally representative
study reports in local languages other than English were searched to cover vitamin D intake data from
all countries with vitamin D fortification policy of fluid milks.
2.3. Data Extraction
The following information was extracted from eligible studies: first author’s name, publication
year, country, number and age range of subjects, dietary assessment method, total and/or dietary
vitamin D intake (vitamin D intake studies), vitamin D intake from milk (vitamin D intake studies),
contribution of milk to vitamin D intake (vitamin D intake studies), latitude (25(OH)D studies),
season that blood was drawn (25(OH)D studies), 25(OH)D assay method and quality control of assay
(25(OH)D studies), and 25(OH)D concentrations (25(OH)D studies). The results were stratified by the
population groups as follows: “children and adolescents” (vitamin D and 25(OH)D studies), “pregnant
women and mother-child pairs” (25(OH)D studies), and “adults, elderly, and all age groups” (vitamin
D and 25(OH)D studies). In addition, the results were reported by country. In some cases, the results
were stratified by supplement use or other factors, depending on the original study design. In 25(OH)D
studies, the role of vitamin D-fortified milk on vitamin D status was examined as a determinant of
vitamin D status or as a comparison of the 25(OH)D status between low or non-users of vitamin
D-fortified milk and more frequent users. If the contribution of milk to total vitamin D intake was not
provided, it was calculated from the reported total intake and vice versa. International units were
converted to micrograms, and 25(OH)D concentrations in ng/ml were converted to nmol/L. In this
study, we referred to the Institute of Medicine threshold for S-25(OH)D status, where
≤
30 nmol/L is
vitamin D deficient, 30–49.9 nmol/L is insufficient, and ≥50 nmol/L is sufficient [26].
3. Results
Figure 1shows the literature search and study selection process. We found 337 articles that were
published between 1993 and 2017, and their titles and abstracts were scanned. Fifty-one full-text
review papers were selected. Of these, two were unavailable and the corresponding author could not
be reached, and 15 were not relevant to the research questions. Thus, 34 papers were included in the
review process. Of these, 20 provided data on the 25(OH)D status, and 20 provided data on vitamin
D intake. Additionally, intake data in national surveys covering countries with a fluid milk vitamin
D fortification policy that were not covered in the PubMed search (Norway, Sweden) were explored.
One Norwegian [
27
] and one Swedish report [
28
] in local language were found and were included

Nutrients 2018,10, 1054 5 of 19
to provide data on vitamin D intake and the contribution of milk in those countries. Nationally
representative data from other countries with a vitamin D fortification policy were already found in
the literature search.
Nutrients 2018, 10, x FOR PEER REVIEW 5 of 19
representative data from other countries with a vitamin D fortification policy were already found in
the literature search.
Figure 1. Literature search and study selection process.
3.1. Contribution of Vitamin D-Fortified Milk to Vitamin D Intakes
For this review, 22 observational studies reported data on the contribution of vitamin D-fortified
milk to vitamin D intake including 99,023 subjects (Table 2). Data from the following countries were
provided: United States (6 studies), Canada (4), Finland (4), Ireland (2), Australia (1), Norway (1),
Spain (1), Sweden (1), and United Kingdom (1). Additionally, one study provided data from both the
United States and Canada. Various methods to assess vitamin D intake were used: food records (8
studies), 24 h recalls (7), food frequency questionnaires (FFQ) (4), one-week diet history (1),
household food diary (1), and both FFQ and food records (1).
Figure 1. Literature search and study selection process.
3.1. Contribution of Vitamin D-Fortified Milk to Vitamin D Intakes
For this review, 22 observational studies reported data on the contribution of vitamin D-fortified
milk to vitamin D intake including 99,023 subjects (Table 2). Data from the following countries were
provided: United States (6 studies), Canada (4), Finland (4), Ireland (2), Australia (1), Norway (1), Spain
(1), Sweden (1), and United Kingdom (1). Additionally, one study provided data from both the United

Nutrients 2018,10, 1054 6 of 19
States and Canada. Various methods to assess vitamin D intake were used: food records (8 studies),
24 h recalls (7), food frequency questionnaires (FFQ) (4), one-week diet history (1), household food
diary (1), and both FFQ and food records (1).
3.1.1. Children and Adolescents
In the studies of Irish and British children and adolescents, the total vitamin D intakes were
2.8–3.5
µ
g/day and dietary intakes were 1.6–2.6
µ
g/day [
13
–
15
]. Fortified milks provided 0.4
µ
g/day
or less vitamin D [
13
–
15
]. It is notable that the consumption of vitamin D-fortified milk was not
common; in the study of Black et al. [
13
], only 4–5% of subjects consumed vitamin D-fortified milk. In
contrast, in countries with policy-based vitamin D fortification, i.e., in the United States, Canada, and
Finland, the mean dietary vitamin D intakes in children were 4.4–5.9
µ
g/day, and 2.3–3.3
µ
g/day of
that originated from milk products, covering more than half of the total dietary intake [29–32].
3.1.2. Adults and the Elderly, and Studies Including All Age Groups
In Spain and Australia, some of the fluid milks on the market are fortified with vitamin D and
studies conducted in these countries among the adult population showed that the contribution of milk
to total vitamin D intake was 15–18%, with total intakes being 3.5 and 4.4
µ
g/day, respectively [
16
,
17
].
In a Canadian population-based study among adults, the total vitamin D intake was shown to be
5.6
µ
g/day among females and 4.8
µ
g/day among males, and milk contributed 48% of the total
vitamin D intake among females and 63% among males [
33
]. In other large American and Canadian
population-based studies covering all age groups, 1.9–2.9
µ
g of vitamin D ingested per day originated
from milk, while mean total vitamin D intakes ranged from 4.2 to 9.8
µ
g/day and dietary intakes
from 3.9 to 7.0
µ
g/day, milk contributing 44–49% of the vitamin D intake [
33
–
37
]. In a smaller study
carried out among the adult population in the United States as well in a Canadian study on Inuit and
Inuvialuit women, vitamin D intakes were similar to those found in the larger studies; however, the
contribution of milk to vitamin D intake was slightly lower, 31–43% [
38
,
39
]. In line with the newer
studies, in two studies carried out among elderly people in the United States that were published
in the 1990s, half of the vitamin D intake originated from milk [
40
,
41
]. The recent representative
population-based study in Finland [
25
] showed that 34% of dietary vitamin D intake originated
from vitamin D-fortified fluid milk products which is similar to the proportion observed in the latest
National FINDIET Study—28–39%, varying between age and sex groups [
42
]. Dietary vitamin D
intakes in the study of
Jääskeläinen et al
. were the highest among all of the studies included in this
review: 14
µ
g/day among men and 12
µ
g/day among women [
25
]. Data on the contributions of milk
to vitamin D intake in other Nordic European countries following the implementation of a national
vitamin D fortification policy have also been provided. The latest Norwegian national dietary survey
reported that extra-skimmed milk, the only vitamin D-fortified milk in Norway, provided 4% of dietary
vitamin D intake, with the mean dietary vitamin D intake being 6
µ
g/day [
27
]. Despite the wider milk
fortification policy in Sweden, only 12% of dietary vitamin D intake originated from milk products in
the Swedish national survey, with the mean dietary vitamin D intake being 7 µg/day [28].

Nutrients 2018,10, 1054 7 of 19
Table 2. Studies on the contribution of milk to total or dietary vitamin D intake.
Reference Country Study
Population
Dietary Assessment
Method
Total/Dietary Vitamin D
Intake (µg/day)
SD
(or SEM *)
Vitamin D Intake from
(fortified) Fluid Milk or
Related Products (µg/day)
SD
Contribution of
(Fortified) Milk to Total
or Dietary Vitamin D
Intake (%)
Children and adolescents
Black et al.
(2014) [13]Ireland
594 children,
5–12 years and
441 teenagers,
13–17 years
7-day (semi-)
weighted food record
Total/dietary intake
5–8 years: 2.8/1.9
9–12 years: 2.8/2.2
13–17 years: 3.2/2.6
2.4/1.1
2.1/1.3
2.5/1.8
Fortified milk: 0.1
Milk and yoghurt: 0.3–0.4 na
Total intake
Fortified milk: 2–3%
Milk and yoghurt:
10–13%
Cole et al.
(2010) [29]
United
States
290 children,
1–5 years 3-day food record Dietary intake: 4.4 3.0 Fortified milk: 2.7 †na Dietary intake
Fortified milk: 62%
Cribb et al.
(2015) [14]
United
Kingdom
755 children,
1.5 years and
3.5 years
3-day food diary
Dietary intake
1.5 years: 1.6
3.5 years: 1.8
1.5
1.4
Yoghurt, cheese and milk
1.5 years: 0.035
µ
g/MJ/day
3.5 years: 0.023
µ
g/MJ/day
0.02
µ
g/MJ/day
0.02
µ
g/MJ/day
Dietary intake
Yoghurt, cheese and milk
1.5 years: 9%
3.5 years: 6%
Hennessy et al.
(2016) [15]Ireland 500 children,
1–4 years
4-day weighted
food diary
Total intake
All subjects: 3.5
Fortified food consumers: 3.2
3.7
2.7
Fortified milk
All subjects: 0.1
Fortified food
consumers: 0.1
na
Total intake
All subjects: 2%
Fortified food consumers,
supplement non-users:
13%
Mark et al.
(2011) [30]Canada 159 children,
8–11 years 3×24 h recalls Total/dietary intake: 6.6/5.6 4.3/3.5 Milk: 3.3 †na Total/dietary intake
Milk: 49/58%
Piirainen et al.
(2007) [32]Finland 36 children,
4 years 4-day food record Total/dietary intake: 7.9/4.5 6.3–9.6/
3.8–5.1 §2.3 2.0–2.6 §Total intake
Milk: 54%
Soininen et al.
(2016) [31]Finland 374 children,
6–8 years 4-day food record Total/dietary intake: 7.7/5.9 na/2.1 Fluid milk: 2.9
All milk products: 3.1
1.5
1.4
Total/dietary intake
Fluid milk: 38/49%
All milk products:
40/52%
Adults and the elderly
Amcoff et al.
(2012) [28]Sweden 1797 adults,
18–80 years 4-day food diary
Dietary intake
Women: 6.4
Men: 7.6
4.2/5.4 na na Dietary intake
Milk products: 12%
Gonzalez-
Rodriguez et al.
(2013) [16]
Spain 418 adults,
18–60 years 24 h recall Total/dietary intake: 3.5/3.2 4.0/3.8 Dairy products: 0.5 †na Total/dietary intake
Dairy products: 15/17%

Nutrients 2018,10, 1054 8 of 19
Table 2. Cont.
Reference Country Study
Population
Dietary Assessment
Method
Total/Dietary Vitamin D
Intake (µg/day)
SD
(or SEM *)
Vitamin D Intake from
(fortified) Fluid Milk or
Related Products (µg/day)
SD
Contribution of
(Fortified) Milk to Total
or Dietary Vitamin D
Intake (%)
Holm Totland
et al. (2012) [27]Norway 1787 adults,
18–70 years 24 h recall
Total/dietary intake
Women: 10/4.9
Men: 12/6.7
na/4.3
na/5.7
na na
Dietary intake
Vitamin D fortified
extra-skimmed milk: 4%
Jayaratne et al.
(2013) [17]Australia 785 adults,
≥31 years FFQ Total intake: 4.4 4.0
Dairy and related products
including margarine: 1.9 †
Milk: 0.8 †
Yoghurt: 0.3 †
na
na
na
Total intake
Dairy and related
products including
margarine: 43%
Milk: 18%
Yoghurt: 6%
Jääskeläinen
et al. (2017) [25]Finland 3635 adults,
≥30 years FFQ
Dietary intake
Men: 14
Women: 12 14–15 §
11–12 §na na Dietary intake
Fluid milk products: 34%
Kinyamu et al.
(1998) [41]
United
States
376 elderly
women,
65–77 years
7-day food record
Total intake
Supplement non-users: 3.5
Supplement users: 13.4
2.2
2.0
Milk
Supplement non-users: 2.0
Supplement users: 1.8
1.6
1.5
Total intake
Milk: 51%
Kolahdooz et al.
(2013) [38]Canada
203 Inuit and
Inuvialuit
women,
19–44 years
FFQ
All subjects: 6.0 ‡
Traditional food eaters: 7.1 ‡
Non-traditional food
eaters: 4.9 ‡
6.3
5.3
3.2
Dairy group (milk, yoghurt,
cheese and eggs)
Traditional food eaters: 2.2
Non-traditional food
eaters: 1.9
na
na
Dairy group (milk,
yoghurt, cheese and eggs)
Traditional food eaters:
31% ‡
Non-traditional food
eaters: 39% ‡
Levy et al.
(2015) [39]
United
States
743 adults,
20–65 years one week diet history
Total intake
Winter season: 4.5
Summer season: 4.3
4.0
3.2
Dairy products
Winter season: 1.9
Summer season: 1.9
2.5
3.8
Dietary intake
Winter season: 43%
Summer season: 41%
Moore et al.
(2014) [37]
United
States
9719 adults,
≥19 years 24 h recall Total/dietary intake
8.6/4.4 0.3/0.1 *
Milk and milk drinks: 1.7 †
Fortified milk and milk
products: 1.9 †
na
na
Total/dietary intake
Milk and milk drinks:
20/39%
Fortified milk and milk
products: 22/44%
O’Dowd et al.
(1993) [41]
United
States
109 elderly,
>60 years
FFQ or 3-day
dietary record
Total/dietary intake
All subjects: 9.5/
Supplement non-users: 7.3
5.1/2.5 Fortified milk
All subjects: 4.7 1.9 Total intake
Fortified milk: 50%

Nutrients 2018,10, 1054 9 of 19
Table 2. Cont.
Reference Country Study
Population
Dietary Assessment
Method
Total/Dietary Vitamin D
Intake (µg/day)
SD
(or SEM *)
Vitamin D Intake from
(fortified) Fluid Milk or
Related Products (µg/day)
SD
Contribution of
(Fortified) Milk to Total
or Dietary Vitamin D
Intake (%)
Poliquin et al.
(2009) [33]Canada 9425 adults,
≥25 years
interview-administered
semi-quantitative
FFQ
Total intake from milk and
supplements
Women: 5.6
Men: 4.8 5.9
5.5
Milk
Women: 2.7
Men: 3.0
2.9
3.5
Total intake from milk
and supplements
Women: 48%
Men: 63%
Raulio et al.
(2017) [42]Finland 1295 adults,
25–64 years 24 h recall
Total intake
Women: all women: 17.5
Supplement non-users: 8.6
Supplement users: 24.7
Men: all men: 17.3
Supplement non-users: 11.2
Supplement users: 29.5
15.4
6.2
16.8
17.0
7.5
23.1
na na
Dietary intake
Milk: 28–39%, depending
on age and sex
All ages
Hill et al.
(2012) [36]
United
States and
Canada
7837 US and
4025 Canadian
citizens,
≥2 years
7- to 14-day
household food diary
Total intake
United States: 4.4
Canada: 4.2
0.03 *
0.5 *
Milk
United States: 2.0
Canada: 1.9
na
na
Total intake
Milk: 44% in both
countries
Moore et al.
(2004) [34]
United
States
18931 subjects,
>1 years 24 h recall
Total/dietary intake:
5.3–9.8/3.9–7.0
depending on age and sex
na na na Dietary intake
Dairy products: 45–47%
Vatanparast
et al. (2010) [35]Canada 34789 subjects,
>1 years 24 h recall Dietary intake: 6.2 0.1 * Milk products: 2.9 na Dietary intake
Milk products: 49%
FFQ, food frequency questionnaire; na, not applicable; * SE(M), standard error (of mean);
†
calculated from the proportion of milk contribution;
‡
unclear whether total or dietary vitamin
D intake (3% supplement users); §95% confidence interval.

Nutrients 2018,10, 1054 10 of 19
3.2. Associations Between Consumption of Vitamin D-Fortified Milk and 25(OH)D Status
Twenty observational studies included in this review investigated associations between the
consumption of vitamin D-fortified milk and 25(OH)D status (n= 19,744) (Table 3). Data from the
following countries were provided: United States (5 studies), Canada (4), Finland (3), Sweden (2),
Egypt (1), Ireland (1), Jordan (1), Norway (1), Spain (1), and Thailand (1). Various methods were
used to assess 25(OH)D concentrations: different immunoassays (13 studies), LC-MS/MS (5) and
competitive binding assays (2). Milk consumption was assessed by either a questionnaire (8 studies),
FFQ (5), food records (4), 24 h recall (1), one-week diet history (1) or by both FFQ and food records (1).
3.2.1. Children and Adolescents
Among Egyptian children aged 9–11 years (n= 200), those who consumed vitamin D-fortified
milk less than once a day had a significantly higher risk of vitamin D insufficiency (S-25(OH)D <
50 nmol/L) than those who consumed more milk [
43
]. In Jordan, children who consumed vitamin
D-fortified fresh milk had higher S-25(OH)D concentrations than those who consumed unfortified
milk (53 nmol/L vs. 43 nmol/L) (n= 93) [
44
]. These two studies did not provide data on the amounts
of consumed milk. In Finland, higher consumption of vitamin D-fortified milk was associated with
higher S-25(OH)D concentrations among children aged 6–8 years (n= 374) [
31
]. Children who drank
at least 450 g/day of vitamin D-fortified milk had a 72–74% lower risk of having S-25(OH)D below
50 nmol/L than those who drank less than 300 g/day (adjusted for age and sex). However, another
study on 10-year-old Finnish children (n= 171) found no association between vitamin D-fortified milk
consumption frequency and S-25(OH)D status, but among those children with a history of cow’s milk
allergy (an indicator of milk avoidance), consumption of vitamin D-fortified milk as well as S-25(OH)D
concentrations were lower than among their peers without allergy history [
45
]. Nevertheless, vitamin
D supplement use was very common in this population (60% daily users), and thus was one important
determinant of their vitamin D status [45].
A Canadian study in 1–6-year-old children (n= 2468) showed that children who drank only
non-cow’s milk (i.e. vegetable-based milk alternatives or goat’s milk) were more than two-fold likely
to have an S-25(OH)D concentration <50 nmol/L relative to children who drank cow’s milk, which is
mandatorily fortified in Canada (odds ratio 2.7, 95% CI 1.6–4.7) [
46
]. In another sample of Canadian
children aged 8–11 years with a daily mean of 1.3 vitamin D-fortified milk servings (n= 159), one daily
serving of milk contributed to a 2.9 nmol/L increase in plasma 25(OH)D concentration [
30
]. Further,
among 2270 children aged 3–18 years in Canada, those consuming vitamin D-fortified milk daily were
more likely to have sufficient S-25(OH)D concentration (
≥
50 nmol/L) than those who drank milk
less frequently (odds ratio 2.4, 95% CI 1.7–3.3) [
47
,
48
]. A Spanish study in 9–13-year-old children
(n= 102) showed that the number of daily dairy servings (mean 2.3 servings) was associated with
the S-25(OH)D status [
49
]. Those who consumed
≥
2.5 servings of milk daily had higher S-25(OH)D
concentrations than those who did not (53 nmol/L vs. 46 nmol/L) [
49
]. In Sweden, fortified lean
milk consumption (mean 230 g/day) correlated with S-25(OH)D status in a group of 13-year-old
children (n= 165) [
50
]. Among 15–18-year-old adolescents in Norway (n= 890), the use of vitamin
D-fortified milk was significantly associated with S-25(OH)D status in a multivariate model in boys,
but not in girls [
51
]. Boys who were frequent milk consumers had higher S-25(OH)D concentrations
than infrequent consumers, but this was not seen among girls, and no milk consumption data was
provided [51].
3.2.2. Pregnant Women and Mother-Child Pairs
Two studies carried out in pregnant women in Thailand and Finland also showed an association
between vitamin D-fortified milk and vitamin D status [
52
,
53
]. Among Thai women (n= 120), the
consumption of multivitamin-fortified milk containing vitamin D was higher among those with
vitamin D sufficiency (S-25(OH)D concentration > 50 nmol/L) in the third trimester than among those

Nutrients 2018,10, 1054 11 of 19
with insufficiency [
52
]. Consumption of multivitamin-fortified milk was associated with an increase in
S-25(OH)D concentration between the first and third trimester. The mean multivitamin-fortified milk
consumption was 1.0 daily serving in the first trimester and 1.4 servings in the third trimester. In a
multivariate analysis, non-consumption of multivitamin-fortified milk was an independent predictor
of vitamin D deficiency [
52
]. In a study carried out in 584 mother-child pairs in Finland, modifiers of
umbilical cord blood (UCB) 25(OH)D status were studied [
53
]. The maternal dietary pattern “dairy
and sandwich”, including vitamin D-fortified milk and margarines, positively contributed to child
UCB 25(OH)D status in mother-child pairs in whom an increase was seen in 25(OH)D concentration
when comparing maternal 25(OH)D status in early pregnancy with UCB 25(OH)D status, but not in
those in whom no increase was seen [
53
]. Among Jordanian women, no differences in S-25(OH)D
concentration were seen among those who consumed vitamin D-fortified milk relative to those who
consumed unfortified milk (26 nmol/L vs. 27 nmol/L) [
44
]. However, their vitamin D status was
much worse than that of their children, whose vitamin D status was better if vitamin D-fortified milk
was consumed [44].
3.2.3. Adults, the Elderly, and All Age Groups
Among adults aged 20–65 years in the United States (n= 743), the use of vitamin D-fortified milk
was a significant predictor of S-25(OH)D status in the wintertime, but not in the summertime [
39
].
In an elderly American population aged >65 years (n= 376) [
41
], S-25(OH)D status correlated with
milk calcium intake from vitamin D-fortified milk (an indicator of milk consumption). Among those
who did not use vitamin D supplements, milk calcium was the main determinant of S-25(OH)D
status; however, this was not the case among vitamin D supplement users. Among adult (
≥
18 years)
Arab-American women (n= 87), vitamin D-fortified milk was not an independent determinant of
S-25(OH)D status, but their milk consumption was minimal, and S-25(OH)D concentrations were
extremely low [
54
]. In the Canadian National Survey consisting of a population aged 6–79 years
(
n= 5306
), those who consumed vitamin D-fortified milk once a day or more had higher S-25(OH)D
concentrations than those with consumption of less than once a day [
55
]. People who consumed milk
more than once a day had a mean S-25(OH)D concentration of 75 nmol/L, while the corresponding
mean among those who consumed milk less than once a day was 63 nmol/L. In a Swedish study
on elderly women aged >60 years (
n= 116
), consumption of vitamin D-fortified reduced-fat dairy
correlated with S-25(OH)D status, and the intake of two daily portions of fortified milk (300 g) was
associated with a 6.2 nmol/L increment in S-25(OH)D concentration in a multiple linear regression
model [
56
]. Further, in an Irish study of three large cohorts of elderly subjects (n= 1233, n= 1895,
n= 1316
), vitamin D-fortified milk consumption predicted a higher S-25(OH)D concentration in two of
the three cohorts [57].

Nutrients 2018,10, 1054 12 of 19
Table 3. Studies in which the contribution of vitamin D-fortified milk to serum or plasma 25-hydroxyvitamin D status was evaluated.
Reference Country
(Latitude)
Season Blood
Drawn Study Population
25(OH)D Assay Method
(Quality Control of Assay:
Certificate; CV% <15%)
Dietary
Assessment
Method
Serum or Plasma
25(OH)D nmol/L
Mean (or Median *)
SD (or IQR †or
95% CI ‡or SE §)
Children and
adolescents
Abu Shady et al.
(2016) [43]Egypt (31◦N) April, May 200 children,
9–11 years
Quantitative enzyme
immunoassay
(na; na)
Questionnaire 41 14
Barman et al.
(2015) [50]Sweden (63◦N) All 165 children,
13 years
LC-MS/MS
(na; na) FFQ 51 14
Cole et al. (2010) [
29
]
United States (33◦
N) All 290 children,
1–5 years
LC-MS/MS
(na; na) 3-day food record 65 19
Lee et al. (2014) [46] Canada (43◦N) All 2468 children,
1–6 years
Diasorin LIAISON
(na; yes except inter CV%
17.4% at high concentrations)
Questionnaire 80 * 66–99 †
Mark et al.
(2011) [30]Canada (45◦N) All 159 children,
8–11 years
IDS radioimmunoassay
(na; yes) 3×24 h recalls Winter/spring: 50
Summer/autumn: 58
10
15
Munasinghe et al.
(2017) [47,48]
Canada (various
latitudes) All 2270 children,
3–18 years
Diasorin LIAISON
(na; yes) FFQ 62 56–69 ‡
Rodríguez–Rodríguez
et al. (2011) [49]Spain (40◦N) February 102 children,
9–13 years
Chemiluminescence
(na; na)
3-day weighted
food diary 50 16
Rosendahl et al.
(2017) [45]Finland (60◦N) January–June 171 children,
10 years
Roche Diagnostics
immunocheminuminescence
(na; na)
FFQ 73 22
Soininen et al.
(2016) [31]Finland (62◦N) All but July 374 children,
6–8 years
Diasorin LIAISON
(na; yes) 4-day food record 69 24
Öberg et al.
(2014) [51]Norway (69◦N) September–April 890 children,
15–18 years
LC–MS/MS
(DEQAS; yes) Questionnaire Boys: 41
Girls: 54
21
23
Pregnant women and mother-child pairs
Charatcharoenwitthaya
et al. (2013) [52]Thailand (14◦N)
Winter season:
72%, rainy season:
28%
120 pregnant women,
18–40 years
LC–MS/MS MassCrom
(na; yes)
Interviewed
questionnaire
1st trimester: 61
2nd trimester: 84
3rd trimester: 90
17
20
22
Gharaibeh et al.
(2009) [44]Jordan (31◦N) June and July
93 children (4–5 years)
and mothers (mean age
34 years) dyads
IDS ELISA
(na; na) Questionnaire Mothers: 26
Children: 56
10
20

Nutrients 2018,10, 1054 13 of 19
Table 3. Cont.
Reference Country
(Latitude)
Season Blood
Drawn Study Population
25(OH)D Assay Method
(Quality Control of Assay:
Certificate; CV% <15%)
Dietary
Assessment
Method
Serum or Plasma
25(OH)D nmol/L
Mean (or Median *)
SD (or IQR †or
95% CI ‡or SE §)
Hauta–alus et al.
(2017) [53]Finland (60◦N) All 584 newborns and
mothers (18–43 years)
IDS–iSYS
(DEQAS; yes) FFQ Mothers: 89
Cord blood: 88
19
22
Adults and the
elderly
Burgaz et al.
(2007) [56]Sweden (60◦N) January–March 116 elderly women,
61–86 years
IDS EIA
(na; yes) FFQ 69 23
Hobbs et al.
(2009) [54]
United States (42◦
N) April 87 women,
≥18 years
Diasorin LIAISON
(na; na) Questionnaire
Unveiled subjects: 21 *
Veiled supplement
users: 17 *
Veiled supplement
non-users: 10 *
14–34 †
10–29 †
5–17 †
Kinyamu et al.
(1998) [41]
United States (41◦
N) All 376 elderly women,
65–77 years
Competitive binding assay
(na; yes) 7-day food record
Supplement
non-users: 74
Supplement users: 88
23
28
Levy et al.
(2015) [39]
United States
(various latitudes)
February–April
and
August–October
743 adults,
20–65 years
Diasorin LIAISON
(College of American
Pathology; na)
One week diet
history
Summer: 101
Winter: 93
42
39
McCarroll et al.
(2015) [57]Ireland (52◦N) All
3 cohorts (1233, 1895,
1316) of elderly subjects,
>60 years
LC–MS
(DEQAS; yes) Questionnaire
Supplement
non-users: 46/61/68
Supplement users:
67/83/74
24/32/23
27/27/30
O’Dowd et al.
(1993) [40]
United States (41◦
N) January–May 109 elderly,
>60 years
Competitive binding assay
(na; yes)
FFQ or 3-day
dietary record
All subjects: 45
Supplement
non-users: 40
Supplement users: 65
2§
2§
3§
All ages
Langlois et al.
(2010) [55]
Canada (various
latitudes) All 5306 subjects,
6–79 years
Diasorin Liaison
(DEQAS; yes)
Interviewed
questionnaire
All subjects 68
April–October 70
November–March 64
65–70 ‡
66–74 ‡
60–68 ‡
CI, confidence interval; CV coefficient of variation; DEQAS, Vitamin D External Quality Assessment Scheme; EIA enzyme immunoassay; ELISA enzyme linked immunosorbent assay; FFQ,
food frequency questionnaire; IQR interquartile range; LC-MS/MS liquid chromatography-tandem mass spectrometry; SE standard error; 25(OH)D, 25-hydroxyvitamin D. * Median;
†IQR; ‡95% CI; §SE.

Nutrients 2018,10, 1054 14 of 19
4. Discussion
Based on these observational studies on vitamin D intake and vitamin D-fortified milk
consumption, it seems that in countries with wide vitamin D fortification policies (Finland, Canada,
United States), the total vitamin D intake as well as the contribution of milk to total vitamin D intake is
higher than in the countries without fortification policies (Ireland, United Kingdom, Spain, Australia).
It is notable that in Norway and Sweden, where some of the fluid milks are fortified with vitamin D
amounts lower than in Finland, Canada, or United States, the contribution of fluid milk to vitamin D
intake was shown to be as low as 4% and 12%, respectively, compared with around 50% in the other
fortification policy countries.
Concerning the vitamin D status, we observed that the consumption of vitamin D-fortified
milk was positively associated with 25(OH)D status in almost all studies included in this review
within heterogeneous population groups, independent of country-specific vitamin D-fortification
policies. Even though the consumed amounts of milk varied, the associations between milk and
25(OH)D status were seen also at fairly low consumption levels. Further, the association was seen
in different population groups: children (with the exception of 10-year old Finns), teenagers (except
in Norwegian girls), adults (except in Arab-American women), pregnant women, and the elderly.
This mostly positive association between vitamin D-fortified milk consumption and vitamin D status
was supported by a recent standardized representative population-based study in Finland, where the
vitamin D fortification policy of fluid milks, in particular, was shown to be successful in improving
vitamin D status in the Finnish population [
25
]. It would be useful to have systematic follow-up
data from the other countries with vitamin D fortification policies, as the present evidence is based
mainly on the Finnish follow-up study. Vatanparast et al. [
35
] stated that despite vitamin D fortification
being mandatory in Canada, the vitamin D intakes are inadequate and recently, Canada implemented
new guidelines to increase the fortification levels [
11
]. Sweden has also extended their vitamin D
fortification policy [
10
]; thus, in the following years there is an opportunity to evaluate the effects of
vitamin D fortification at the population level also in those countries.
4.1. Limitations of the Study
The studies included in this review were carried out in populations of differing size, age, and
gender in numerous countries and at a range of latitudes with different levels of UVB exposure.
Different assay methods for 25(OH)D analysis have been used, increasing the heterogeneity of the
studies [58], and not all studies have provided quality control data. LC-MS/MS, which is considered
the golden standard and reference method in 25(OH)D assays [
58
], was used in 25% of the reviewed
studies. However, as our aim was to investigate the associations between the consumption of vitamin
D fortified milk and 25(OH)D status, the differences among the assays probably do not mitigate the
power of the overall conclusions, as the trends in 25(OH)D concentrations usually remain similar
independent of the analysis method used [59]. Of greater importance is that most studies considered
the variability of 25(OH)D concentrations between seasons and took the samples at a time when
UVB availability is low or over a short time period or adjusted the data for the season [
39
,
56
]. Also,
the dietary assessment methods used in the studies varied and the validity of the methods was not
described in all papers. Some used validated FFQs [
25
,
47
] and some only used questionnaires on
milk consumption [
43
,
46
]. Moreover, the portion sizes used were not defined in all studies. The
consumed amounts of milk and the vitamin D contents differed, as did the confounding factors
used in statistical analyses. The representativeness of the samples was not described in most of the
studies, but representative data from national health surveys in the United States, Canada, Sweden,
Norway, and Finland were included when describing the contributions of fluid milk to vitamin D
intake [
25
,
27
,
28
,
33
–
35
,
37
]. We only searched data from PubMed, and some studies might have been
missed in our limited literature search. However, these are probably studies that have not taken a stand
on vitamin D fortification of fluid milks as such, and therefore, have not emphasized it in the abstracts

Nutrients 2018,10, 1054 15 of 19
or in the keywords. Nevertheless, publication bias may have occurred, as some studies that found no
association between vitamin D-fortified milk and vitamin D status may not have been published.
4.2. Future Perspectives in Vitamin D Fortification
Vitamin D fortification of foodstuffs has proven to be a suitable vehicle to increase vitamin D intake
at the population level [
5
], and the present review shows that vitamin D-fortified fluid milk products
contribute to both vitamin D intake and 25(OH)D status. Cashman and Kiely [
5
], however, stated that
the fortification of fluid milks may not be enough. Thus, country-specific staple foods should be chosen
as optimal vitamin D carriers based on the results of simulation studies. Also, the biofortification of
foodstuffs should be considered [
5
]. In many countries without a current fortification policy, the option
of systematic vitamin D fortification of food is under consideration, and simulation studies have been
carried out in recent years. A study using Swedish, British, and Dutch data, for instance, showed that
increased fortification of fluid milk to the level currently used in Finland (
1µg/100 g
) and fortification
of margarines to 15
µ
g/100 g would substantially increase vitamin D intake [
60
]. Another study based
on British data [
61
] revealed that the best option would be the fortification of wheat flour with vitamin
D, this being a more efficient option to increase S-25(OH)D concentration than milk alone or combined
fortification of milk and wheat flour. In Germany, the effects of fortification on the seasonal variation
of S-25(OH)D concentrations were simulated, but milk was not considered to be a good carrier of
vitamin D [
62
]. Simulation studies in Irish and British children showed that the fortification of cow’s
milk would improve vitamin D intake [
14
,
63
]. Further, an Australian simulation demonstrated that
with vitamin D fortification of all milk and breakfast cereals, vitamin D intake would increase almost
two-fold [
17
]. These studies reflect the interest in widening the fortification policies. However, the
results of the above-described simulation studies show that fortification of milk products may not be
the most effective option in all countries.
5. Conclusions
The reviewed studies indicated that in countries with a national vitamin D fortification policy for
fluid milks at a level of around 1
µ
g/100 g, such as Finland, United States, and Canada, milk products
contribute substantially to vitamin D intake, while in countries without a fortification policy or with
only a few milk products being mandatorily fortified, the contribution is low. Studies carried out
at different latitudes among different population groups have also shown that the consumption of
vitamin D-fortified milk is associated with a higher 25(OH)D concentration. Based on the reviewed
observational studies, vitamin D fortification of milk is an effective vehicle in improving vitamin
D intake and 25(OH)D status in populations with adequate average milk consumption. However,
other food sources, natural or fortified, as well as national recommendations on the use of vitamin D
supplements should not be overlooked when planning national nutrition policies to ensure adequate
vitamin D intake.
Author Contributions:
Conceptualization: S.T.I., M.E. and C.J.E.L.-A.; Methods: S.T.I. and C.J.E.L.-A.; Data search:
S.T.I.; Study Selection: S.T.I. and C.J.E.L.-A.; Data Extraction: S.T.I.; Writing—Original Draft Preparation: S.T.I.;
Writing—Review & Editing: S.T.I., M.E. and C.J.E.L.-A.; Project Administration: S.T.I.; Funding Acquisition: S.T.I.
Funding: This research was funded by [Foundation for Nutrition Research].
Conflicts of Interest:
The authors declare no conflict of interest. The funders had no role in the design of the
study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, and in the decision to
publish the results.
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