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Citation: Smyczy´nska, J.; Pawelak,
N.; Hilczer, M.; Łupi´nska, A.;
Lewi´nski, A.; Stawerska, R. The
Variability of Vitamin D
Concentrations in Short Children
with Short Stature from Central
Poland—The Effects of Insolation,
Supplementation, and COVID-19
Pandemic Isolation. Nutrients 2023,
15, 3629. https://doi.org/10.3390/
nu15163629
Academic Editor: Bruce W. Hollis
Received: 24 July 2023
Revised: 13 August 2023
Accepted: 16 August 2023
Published: 18 August 2023
Copyright: © 2023 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
nutrients
Article
The Variability of Vitamin D Concentrations in Short Children
with Short Stature from Central Poland—The Effects of
Insolation, Supplementation, and COVID-19 Pandemic
Isolation
Joanna Smyczy ´nska 1, * , Natalia Pawelak 2, Maciej Hilczer 2, Anna Łupi ´nska 2,3, Andrzej Lewi ´nski 2,4
and Renata Stawerska 2,3
1Department of Pediatrics, Diabetology, Endocrinology and Nephrology, Medical University of Lodz,
90-419 Lodz, Poland
2Department of Endocrinology and Metabolic Diseases, Polish Mother’s Memorial Hospital—Research
Institute in Lodz, 93-338 Lodz, Poland; pawelak.natalia@gmail.com (N.P.);
maciej.hilczer@umed.lodz.pl (M.H.); anna.lupinska@umed.lodz.pl (A.Ł.);
andrzej.lewinski@umed.lodz.pl (A.L.); renata.stawerska@umed.lodz.pl (R.S.)
3Department of Pediatric Endocrinology, Medical University of Lodz, 93-338 Lodz, Poland
4Department of Endocrinology and Metabolic Diseases, Medical University of Lodz, 93-338 Lodz, Poland
*Correspondence: joanna.smyczynska@umed.lodz.pl; Tel.: +48-42-617-77-87
Abstract:
The aim of the study was to investigate the effects of seasonal variability of insolation,
the implementation of new recommendations for vitamin D supplementation (2018), and the SARS-
CoV-2 pandemic lockdown (2020) on 25(OH)D concentrations in children from central Poland. The
retrospective analysis of variability of 25(OH)D concentrations during the last 8 years was performed
in a group of 1440 children with short stature, aged 3.0–18.0 years. Significant differences in 25(OH)D
concentrations were found between the periods from mid-2014 to mid-2018, from mid-2018 to mid-
2020, and from mid-2020 to mid-2022 (medians: 22.9, 26.0, and 29.9 ng/mL, respectively). Time
series models created on the grounds of data from 6 years of the pre-pandemic period and used
for prediction for the pandemic period explained over 80% of the seasonal variability of 25(OH)D
concentrations, with overprediction for the first year of the pandemic and underprediction for
the second year. A significant increase in 25(OH)D concentrations was observed both after the
introduction of new vitamin D supplementation guidelines and during the SARS-CoV-2 pandemic;
however, the scale of vitamin D deficiency and insufficiency was still too high. Time series models
are useful in analyzing the impact of health policy interventions and pandemic restrictions on the
seasonal variability of vitamin D concentrations.
Keywords: vitamin D; sun exposure; SARS-CoV-2 pandemic; lockdown; supplementation
1. Introduction
The main role of vitamin D is influencing the calcium-phosphate metabolism, and
its long-term deficiency is important in the pathogenesis of rickets in children and bone
mineralization disorders in adults. Apart from that, it has many other proven or highly
probable roles, including the regulation of the proliferation and differentiation of normal
and cancerous cells [
1
–
3
], reducing the risk of cardiovascular diseases [
4
] and of some
cancers, as well as the modulation of the immune system, including protective effects
against both autoimmune diseases and infections. Proper vitamin D levels reduce the risk
of viral infections, including the SARS-CoV-2 virus [5].
The primary source of vitamin D in humans is its synthesis in the skin, requiring suffi-
cient exposure to UVB radiation, the source of which is sunlight. However, it is insufficient
not only in our latitude but also in countries with higher insolation, at least during the
Nutrients 2023,15, 3629. https://doi.org/10.3390/nu15163629 https://www.mdpi.com/journal/nutrients
Nutrients 2023,15, 3629 2 of 13
autumn and winter [
6
–
9
]. Another important source of vitamin D is food products. Despite
the well-documented seasonality of serum 25(OH)D concentrations, it is difficult to directly
assess the amount of vitamin D provided by the sun or food; nevertheless, the scale of
vitamin D deficiency in central European countries is high [
10
]. As it has previously been
documented, vitamin D intake from food alone is insufficient to achieve adequate concentra-
tions in the human body, even in terms of abundant sunshine [
11
,
12
]. Hence, an additional
supply of vitamin D seems necessary. The solutions of this problem include direct vitamin
D supplementation and the fortification of food products with vitamin D [13,14].
Vitamin D is a group of fat-soluble prohormones which can be synthesized naturally
in the human body from 7-dehydrocholesterol to cholecalciferol (vitamin D3) that depends
on sunlight exposure or may be provided through the dietary supplementation of ergocal-
ciferol (vitamin D2) and vitamin D3. To achieve metabolic effects, vitamins D2 and D3 must
be converted into active forms through the hydroxylation reactions. The result of the first
hydroxylation in liver is calcifediol—25-hydroxyvitamin D [25(OH)D] that is subsequently
hydroxylated in kidneys to calcitriol—1,25-dihydroxyvitamin D [1,25(OH)2D]. Calcitriol
synthesis is limited by the accessibility of calcifediol, which is a substrate. A serum con-
centration of 25(OH)D is considered the main marker of vitamin D supply. The biological
effects of vitamin D are mediated by the vitamin D receptor (VDR). Current knowledge
concerning the sources of vitamin D in humans and the pleiotropic effects of this vitamin
has been summarized by Bouillon et al. [15].
To date, literature reviews indicate vitamin D deficiency in the general population
worldwide [
16
,
17
]. Its concentration depends on many components, such as age, sex, race,
latitude, and season [
18
]. Vitamin D has pleiotropic effects and, for this reason, correcting its
deficiency through proper supplementation is important for public health. Grant et al. [
19
],
in the 2022 narrative review, discussed which vitamin D concentrations were appropriate
for various health outcomes, such as cardiovascular diseases, hypertension, cancers, type 2
diabetes mellitus, and many others, which were the most common causes of death. Optimal
thresholds for the different effects of vitamin D ranged from 25 ng/mL to 60 ng/mL. In this
paper, a special section has been devoted to the importance of vitamin D for the course of
SARS-CoV-2 infections. The significance of vitamin D during the COVID-19 pandemic and
the pleiotropic effects of vitamin D have also been discussed during the fifth International
Conference “Vitamin D—Minimum, Maximum, Optimum”, held in Warsaw, Poland, in
October 2021 [20].
In Poland, the guidelines for vitamin D supplementation for Central Europe, published
in 2013 [
21
], were used for several years. This did not solve the problem of the high
prevalence of vitamin D deficiency in the Polish population. Chlebna-Sokół et al. [
22
], in
2016, found vitamin D deficiency in more than 70% of children referred to the hospital
for symptoms suggesting bone metabolism disorders. The study involved the entire
developmental period from neonates to 18 years of age. They also observed an increase in
the prevalence of vitamin D deficiency with age. A high incidence of insufficient vitamin D
concentrations together with their seasonal variability in children not suffering from the
symptoms typical for skeletal disorders, assessed in 2014–2018, was also reported in the
previous paper of our research group, published in 2019 [23].
In 2018, Rusi´nska et al. [
24
] published the guidelines for vitamin D supplementation
for the Polish population that were widely promoted among medical staff. According
to these recommendations, vitamin D should be supplemented in healthy children and
adolescents when its availability from natural sources is limited (due to insufficient sun
exposure and insufficient dietary supply). In addition, there were specific recommendations
for using a higher vitamin D dosage in the groups at risk of vitamin D deficiency. The
expected effect of implementing these recommendations should be an improvement in
vitamin D supply and reduced prevalence of vitamin D deficiency, especially in autumn
and winter.
Nutrients 2023,15, 3629 3 of 13
During the initial phase of the COVID-19 pandemic lockdown, the possibility of sun
exposure was restricted, which must have caused a reduction in vitamin D synthesis in
the skin during the spring and summer of 2020 at the population level. On the other hand,
during the SARS-CoV-2 pandemic, vitamin D supplementation has been recommended in
response to numerous reports of its effect on the prevention of viral infections [5,25–27].
The aim of the study was to assess the effects of:
1. the seasonal variability of insolation,
2. implementing new guidelines of vitamin D supplementation,
3.
the pandemic situation with limited sun exposure due to lockdown and strong recom-
mendations to increase vitamin D supplementation on serum 25(OH)D concentrations
in children.
2. Materials and Methods
The retrospective analysis included 1440 children (879 boys, 561 girls), aged
3.0–18.0 years
,
with short stature, i.e., height SDS below
−
2.0, according to Polish reference standards [
28
],
admitted to a single tertiary reference center in Poland, and diagnosed from January 2014
to the end of June 2022. In all children, 25(OH)D serum concentrations were measured on
the second day of hospitalization, fasting, in morning hours. None of the patients had rec-
ommended therapeutic doses of vitamin D; however, they could supplement this vitamin
as over the counter (OTC) medications and consume foods fortified with vitamin D. The
patients with disorders of thyroid function, pituitary hormone disorders (except for ones
with isolated growth hormone deficiency), disorders of adrenal function, hyperthyroidism
or uncompensated hypothyroidism, and any calcium-phosphorus imbalance and/or im-
paired PTH secretion, as well as those diagnosed with diseases that may influence vitamin
D supply (including coeliac disease, other malabsorption syndromes, anorexia nervosa,
and chronic kidney disease, etc.) were excluded from the study.
The concentrations of 25(OH)D in the serum were measured with electrochemilumi-
nescence binding assay (ECLIA), Roche, standardized against LC-MS/MS, with a range
of detection of 5.0–100.0 ng/mL. According to the current guidelines for the Polish pop-
ulation [
24
], vitamin D deficiency was defined as serum 25(OH)D concentrations below
20 ng/mL, suboptimal concentrations—20–30 ng/mL, optimal—30–50 ng/mL, high—50–
100 ng/mL, and toxic—over 100 ng/mL.
First, the patients were divided into four groups with low, suboptimal, optimal,
and high 25(OH)D concentrations. As only one child had a 25(OH)D concentration over
100.0 ng/mL, this patient was included in the subgroup with high vitamin D levels.
Next, all the patients were classified with respect to the year and season of hospi-
talization. In the guidelines of Rusi´nska et al. [
24
], published in May 2018, prophylactic
vitamin D supplementation is, in general, recommended for all children, apart from those
with sufficient sun exposure in the period from May to September, thus the effects of
the application of these rules should be noticeable from the third quarter of 2018. The
SARS-CoV-2 pandemic started in Poland in March 2020; however, its possible effects on
vitamin D supply seemed to be delayed, as median serum 25(OH)D concentrations in
the second quarter of 2020 and 2021 were very similar (22.5 ng/mL vs. 22.6 ng/mL). So,
25(OH)D concentrations were compared between the patients diagnosed from mid-2014
to mid-2018, from mid-2018 to mid-2020, and from mid-2020 to mid-2022, and the groups
were labelled as “Old Guidelines”, “New Guidelines”, and “Pandemic”, respectively. The
patients diagnosed in the first and second quarter of 2014 were excluded from this part of
the analysis. The selection for the analysis of full 4-year and 2-year periods allowed us to
avoid a bias related to the unequal representation of data collected in different seasons. For
the purpose of this study, it was assumed that the seasons corresponded to the appropriate
quarters of the year.
For statistical analysis, a Shapiro–Wilk test was used first for the assessment of the
distribution of serum 25(OH)D concentrations in the studied group and in particular
subgroups. Due to the lack of a normal distribution of 25(OH)D levels, a non-parametric
Nutrients 2023,15, 3629 4 of 13
Kruskal–Wallis test was applied for comparisons between particular groups, followed by a
post hoc Bonferroni–Dunn test, if applicable. Statistical significance was defined as p< 0.05.
The second part of the analysis involved creating models of the seasonal (quarterly)
variability of serum 25(OH)D concentrations based on time series regression, including the
data on insolation during the observation period and testing the effect of the SARS-CoV-2
pandemic. The onset of pandemic isolation was in March 2020, and many restrictions
of outdoor activities and online education lasted during 2021, while the vaccination of
children at least 12 years of age started in June 2021, and for those aged 5–11 years in
December 2021. So, it might be assumed that pandemic isolation could decrease the
sun exposure of Polish children from spring 2020 to the end of 2021. The first model
included data concerning median 25(OH)D concentrations from the last 6 years of the
pre-pandemic period (from spring 2014 to winter 2020) and was used for predictions of
25(OH)D concentrations in the pandemic period (starting from spring 2020). The second
model included additional data concerning insolation during the 3 months preceding the
measurements of serum 25(OH)D concentrations in particular children, as it had previously
been documented that vitamin D concentrations correlated with insolation in previous
months [
23
]. The information concerning the number of sunny hours in particular months
during the study period and 3 months before, starting from October 2013 to June 2022,
was obtained from the website of the Institute of Meteorology and Water Management
in Poland (https://klimat.imgw.pl/pl/climate-maps/#Sunshine/Monthly accessed on
27 April 2023). All the models were created in quarterly intervals that seemed to reflect
the seasonal variability of 25(OH)D concentrations (the creation of monthly models was
abandoned due to their low readability and a relatively low number of patients diagnosed
in some months). The assessment of the fit of model forecasts to real data was used to
estimate the impact of the analyzed interventions (the introduction of New Guidelines and
the SARS-CoV-2 pandemic) on serum 25(OH)D concentrations.
3. Results
As distributions of both serum 25(OH)D concentrations and of patients’ age were
different from normal distribution, both in the whole studied group and in particular
subgroups, median values and interquartile (25–75 centile) ranges are presented. In the
studied group, the median 25(OH)D concentration was 24.0 ng/mL, with an interquartile
range of 18.3–30.2 ng/mL. Only 25.1% of measured 25(OH)D values were within the
normal range, 41.9% were suboptimal, 32.0% confirmed vitamin D deficiency, and only
1.0% were high. In general, vitamin D concentrations were higher in younger children, with
significant differences in the patients’ age between the subgroup with low serum 25(OH)D
concentrations and all the remaining subgroups, as well as between the subgroups with
optimal and suboptimal 25(OH)D levels. The basic characteristics of the studied group and
of particular subgroups with respect to 25(OH)D concentration are presented in Table 1.
Table 1.
The number and age of patients in the whole studied group and in particular subgroups
with respect to serum 25(OH)D concentrations.
Group All Low Suboptimal Optimal High
No of patients
(boys/girls)
1440
(879/561)
461
(285/176)
604
(362/242)
361
(223/138)
14
(9/5)
Age [years] median
(lower-upper quartile)
10.0 11.1 a,b,c 10.3 a,d 8.6 b,d 10.6 c
(6.9–12.9) (8.5–13.6) (7.1–12.8) (5.5–12.0) (6.2–11.3)
Significant differences: a,b,d—p< 0.001, c—p< 0.05.
In the studied group, 25(OH)D concentrations were the highest in children assessed
from mid-2020 to mid-2022, and lowest in those assessed from mid-2014 to mid-2018. See
Table 2; for raw data see Figure 1.
Nutrients 2023,15, 3629 5 of 13
Table 2.
Comparison of serum 25(OH)D concentrations before and after the implementation of the
New Guidelines of vitamin D supplementation.
Group All
Mid-2014
to Mid-2018
(Old Guidelines)
Mid-2018
to Mid-2020
(New Guidelines)
Mid-2020
to Mid-2022
(Pandemic)
No of patients
(boys/girls)
1397
(854/543)
841
(501/340)
314
(195/119)
242
(158/84)
Age [years] median
(lower-upper quartile)
10.0
(7.0–12.9)
10.1
(7.1–13.1)
9.8
(6.8–12.6)
9.9
(7.0–12.7)
25(OH)D [ng/mL]
(lower-upper quartile)
24.2 22.9 a,b 26.0 a,c 29.9 b,c
(18.6–30.3) (17.3–28.7) (20.0–30.7) (21.3–34.3)
Significant differences: a,b,c—p< 0.05.
Nutrients2023,15,xFORPEERREVIEW5of13
Tab l e 2.Comparisonofserum25(OH)Dconcentrationsbeforeandaftertheimplementationofthe
NewGuidelinesofvitaminDsupplementation.
GroupAll
Mid-2014
toMid-2018
(OldGuidelines)
Mid-2018
toMid-2020
(NewGuidelines)
Mid-2020
toMid-2022
(Pandemic)
Noofpatients
(boys/girls)
1397
(854/543)
841
(501/340)
314
(195/119)
242
(158/84)
Age[years]median
(lower-upperquartile)
10.0
(7.0–12.9)
10.1
(7.1–13.1)
9.8
(6.8–12.6)
9.9
(7.0–12.7)
25(OH)D[ng/mL]
(lower-upperquartile)
24.222.9a,b26.0a,c29.9b,c
(18.6–30.3)(17.3–28.7)(20.0–30.7)(21.3–34.3)
Significantdifferences:a,b,c—p<0.05.
2014-01-01
2015-01-01
2016-01-01
2017-01-01
2018-01-01
2019-01-01
2020-01-01
2021-01-01
2022-01-01
time axis
0
20
40
60
80
100
120
25(OH)D [ng/ml]
Figure1.Serum25(OH)Dconcentrationsinparticularpatientsduringthestudyperiod.
Theseasonalvariabilityofserum25(OH)Dconcentrationsinparticularyearsand
seasonsisshowninFigure2.
Non-parametrictestsformultiplecomparisonsfollowedbyposthoccomparisons
showedthatalldifferencesinserum25(OH)Dconcentrationsbetweenthegroupsdiag-
nosedinparticulartimeperiods(i.e.,“OldGuidelines”,“NewGuidelines”,and“Pan-
demic”)weresignificant(p<0.05).Furthercomparisonsofserum25(OH)Dconcentrations
betweenthesegroups,forseasonsinparticular,alsodemonstratedsignificantdifferences
forwinter,spring,andautumn,butnotforsummer;seeFigure3.
Detaileddataonpreviousinsolationforparticularyearsandmonths,calculatedac-
cordingtothedailynumbersofsunnyhoursinthe3monthsprecedingtheassessmentof
serum25(OH)Dconcentration,areshowninTable3.Significantcorrelationsbetween
25(OH)Dconcentrationsandinsolationinpreviousmonthswereobserved,withthebest
onebeingbetweenthemedianserumconcentrationof25(OH)Dandthecumulativenum-
berofsunnyhoursduringtheprevious3months(r=0.695,p<0.05).
Figure 1. Serum 25(OH)D concentrations in particular patients during the study period.
The seasonal variability of serum 25(OH)D concentrations in particular years and
seasons is shown in Figure 2.
Non-parametric tests for multiple comparisons followed by post hoc comparisons
showed that all differences in serum 25(OH)D concentrations between the groups diagnosed
in particular time periods (i.e., “Old Guidelines”, “New Guidelines”, and “Pandemic”)
were significant (p< 0.05). Further comparisons of serum 25(OH)D concentrations between
these groups, for seasons in particular, also demonstrated significant differences for winter,
spring, and autumn, but not for summer; see Figure 3.
Detailed data on previous insolation for particular years and months, calculated
according to the daily numbers of sunny hours in the 3 months preceding the assessment
of serum 25(OH)D concentration, are shown in Table 3. Significant correlations between
25(OH)D concentrations and insolation in previous months were observed, with the best
one being between the median serum concentration of 25(OH)D and the cumulative number
of sunny hours during the previous 3 months (r = 0.695, p< 0.05).
Nutrients 2023,15, 3629 6 of 13
Nutrients2023,15,xFORPEERREVIEW6of13
I 2014
II 2014
III 2014
IV 2014
I 2015
II 2015
III 2015
IV 2015
I 2016
II 2016
III 2016
IV 2016
I 2017
II 2017
III 2017
IV 2017
I 2018
II 2018
III 2018
IV 2018
I 2019
II 2019
III 2019
IV 2019
I 2020
II 2020
III 2020
IV 2020
I 2021
II 2021
III 2021
IV 2021
I 2022
II 2022
time [years & quarters]
10
15
20
25
30
35
40
45
50
25(OH)D [ng/ml]
Upper quartile
Median
Lower quartile
Figure2.Variabilityofserum25(OH)Dconcentrationsinparticularyearsandseasonsduringthe
studyperiod.
Figure3.Serum25(OH)Dconcentrationsarepresentedasmedian(point),25–75centile(box),and
non-outlierrange(whiskers);significantdifferences:a,b,c,d—p<0.05.
Concentrationsofserum25(OH)Dinparticularseasonsbeforeandaftertheimple-
mentationoftheNewGuidelinesofvitaminDsupplementationandduringtheSARS-
CoV-2pandemic.
Figure 2.
Variability of serum 25(OH)D concentrations in particular years and seasons during the
study period.
Nutrients2023,15,xFORPEERREVIEW6of13
I 2014
II 2014
III 2014
IV 2014
I 2015
II 2015
III 2015
IV 2015
I 2016
II 2016
III 2016
IV 2016
I 2017
II 2017
III 2017
IV 2017
I 2018
II 2018
III 2018
IV 2018
I 2019
II 2019
III 2019
IV 2019
I 2020
II 2020
III 2020
IV 2020
I 2021
II 2021
III 2021
IV 2021
I 2022
II 2022
time [years & quarters]
10
15
20
25
30
35
40
45
50
25(OH)D [ng/ml]
Upper quartile
Median
Lower quartile
Figure2.Variabilityofserum25(OH)Dconcentrationsinparticularyearsandseasonsduringthe
studyperiod.
Figure3.Serum25(OH)Dconcentrationsarepresentedasmedian(point),25–75centile(box),and
non-outlierrange(whiskers);significantdifferences:a,b,c,d—p<0.05.
Concentrationsofserum25(OH)Dinparticularseasonsbeforeandaftertheimple-
mentationoftheNewGuidelinesofvitaminDsupplementationandduringtheSARS-
CoV-2pandemic.
Figure 3.
Serum 25(OH)D concentrations are presented as median (point), 25–75 centile (box), and
non-outlier range (whiskers); significant differences: a, b, c, d—p< 0.05.
Nutrients 2023,15, 3629 7 of 13
Table 3.
Previous insolation, calculated for the patients diagnosed in particular years and seasons as mean
number of sunny hours in the3 months preceding the assessment of serum 25(OH)D concentrations.
2014 2015 2016 2017 2018 2019 2020 2021 2022
Winter 2.4 1.6 2.2 2.0 1.7 2.1 2.2 1.8 2.1
Spring 5.0 4.3 4.3 4.3 5.5 4.2 5.3 4.5 5.6
Summer 6.8 8.0 8.5 7.9 9.0 8.6 8.0 8.2 -
Autumn 5.6 7.3 6.2 5.2 7.4 5.9 6.6 5.7 -
According to the data from https://klimat.imgw.pl/pl/climate-maps/#Sunshine/Monthly, accessed on
27 April 2023
.
Concentrations of serum 25(OH)D in particular seasons before and after the imple-
mentation of the New Guidelines of vitamin D supplementation and during the SARS-CoV-
2 pandemic.
Finally, the models of the seasonal variability of serum 25(OH)D concentrations were
created on the grounds of data from 6 years of the pre-pandemic period (from spring
2014 to winter 2020) and used for prediction for the pandemic period (from spring 2020
to mid-2022) in order to assess the influence of the SARS-CoV-2 pandemic on vitamin D
supply (i.e., to validate fitting the model to the pandemic situation). The first model of
median 25(OH)D concentrations in particular seasons (quarters) explained 84.0% of its
variability. The second model, including the additional variable “Previous Insolation” (see
Table 3), explained 88.6% of median 25(OH)D concentration variability. Interestingly, both
models overpredicted 25(OH)D concentrations in spring, summer, and autumn 2020, and
underpredicted in 2021 and the first two quarters of 2022; however, the differences between
real and forecasted values were insignificant. The model including the variable “Previous
Insolation” is presented in Figure 4. Implementing the detailed data on insolation added
less than 5% accuracy to the model based only on the seasonal variability of serum 25(OH)D
concentrations. It should also be noted that, during the whole study period, except for
summer 2021, the median values of 25(OH)D concentrations were below the normal range
(i.e., below 30 ng/mL).
Nutrients2023,15,xFORPEERREVIEW7of13
Tab l e3.Previousinsolation,calculatedforthepatientsdiagnosedinparticularyearsandseasons
asmeannumberofsunnyhoursinthe3monthsprecedingtheassessmentofserum25(OH)Dcon-
centrations.
201420152016201720182019202020212022
Winter2.41.62.22.01.72.12.21.82.1
Spring5.04.34.34.35.54.25.34.55.6
Summer6.88.08.57.99.08.68.08.2-
Autumn5.67.36.25.27.45.96.65.7-
Accordingtothedatafromhps://klimat.imgw.pl/pl/climate-maps/#Sunshine/Monthly,accessed
on27April2023.
Finally,themodelsoftheseasonalvariabilityofserum25(OH)Dconcentrationswere
createdonthegroundsofdatafrom6yearsofthepre-pandemicperiod(fromspring2014
towinter2020)andusedforpredictionforthepandemicperiod(fromspring2020tomid-
2022)inordertoassesstheinfluenceoftheSARS-CoV-2pandemiconvitaminDsupply
(i.e.,tovalidatefiingthemodeltothepandemicsituation).Thefirstmodelofmedian
25(OH)Dconcentrationsinparticularseasons(quarters)explained84.0%ofitsvariability.
Thesecondmodel,includingtheadditionalvariable“PreviousInsolation”(seeTable3),
explained88.6%ofmedian25(OH)Dconcentrationvariability.Interestingly,bothmodels
overpredicted25(OH)Dconcentrationsinspring,summer,andautumn2020,andunder-
predictedin2021andthefirsttwoquartersof2022;however,thedifferencesbetweenreal
andforecastedvalueswereinsignificant.Themodelincludingthevariable“PreviousIn-
solation”ispresentedinFigure4.Implementingthedetaileddataoninsolationadded
lessthan5%accuracytothemodelbasedonlyontheseasonalvariabilityofserum
25(OH)Dconcentrations.Itshouldalsobenotedthat,duringthewholestudyperiod,ex-
ceptforsummer2021,themedianvaluesof25(OH)Dconcentrationswerebelowthenor-
malrange(i.e.,below30ng/mL).
III 2014
IV 2014
I 2015
II 2015
III 2015
IV 2015
I 2016
II 2016
III 2016
IV 2016
I 2017
II 2017
III 2017
IV 2017
I 2018
II 2018
III 2018
IV 2018
I 2019
II 2019
III 2019
IV 2019
I 2020
II 2020
III 2020
IV 2020
I 2021
II 2021
III 2021
IV 2021
I 2022
II 2022
16
18
20
22
24
26
28
30
32
34
median 25(OH)D [ng/ml]
Pre-pandemic
Model w ith In solation
Pande m ic
Figure4.Modelofmedian25(OH)Dconcentrationsinthepre-pandemicperiodbasedonquarterly
seasonalityandpreviousinsolation,withtheforecastforthepandemicseasons.
Figure 4.
Model of median 25(OH)D concentrations in the pre-pandemic period based on quarterly
seasonality and previous insolation, with the forecast for the pandemic seasons.
Nutrients 2023,15, 3629 8 of 13
4. Discussion
In our study, a seasonal variability in vitamin D concentrations was confirmed, with
almost 75% incidence of suboptimal and low serum 25(OH)D concentrations during the
whole study period. Similar conclusions have been drawn from other papers published
in recent years. Mean serum 25(OH)D concentrations were higher during the summer–
autumn seasons compared to the winter–spring seasons [
12
,
29
–
32
]. The highest prevalence
of serum 25(OH)D below 20.0 ng/mL in Greek adults was found in the spring season,
precisely in March, by Dimakopoulos et al. [
33
]. Basi´nska-Lewandowska et al. [
34
] com-
pared only two seasons—spring and autumn—in Polish adults and obtained mean serum
25(OH)D concentrations at the levels of 18.1
±
7.37 ng/mL and 24.58
±
7.72 ng/mL, re-
spectively. Seasonal differences in the prevalence of vitamin D deficiency or sufficiency
observed in that study were highly significant.
During the first days of the COVID-19 pandemic, the authorities in many countries
imposed restrictions that included limiting going out of the house (a so-called lockdown).
One of the consequences of this situation was reduced sun exposure and, as a result, a
greater prevalence of vitamin D deficiency. Rustecka et al. [
35
] evaluated the effect of
staying home during the pandemic on vitamin D concentrations among Polish children.
They compared serum 25(OH)D concentrations between two groups of patients who had
blood samples taken either before the pandemic (January 2019 to February 2020) or during
the first pandemic year (March 2020 to February 2021). Among children over 1 year of
age, the mean vitamin D concentration was significantly lower during the pandemic than
in the pre-pandemic period (35
±
18 ng/mL and 31
±
14 ng/mL, respectively), while
in infants, serum 25(OH)D levels were normal. Moreover, season-dependent changes in
vitamin D levels were observed in the pre-lockdown period, while no such changes were
observed during the lockdown. In our study, the obtained serum 25(OH)D concentrations
are lower than those reported by Rustecka et al. [
35
], and we did not observed such a
decrease in 25(OH)D concentrations during the first year of the pandemic; however, a
direct comparison of the obtained results is difficult as we reported median 25(OH)D levels.
Nevertheless, serum 25(OH)D concentrations in 2020 were lower than those predicted in
the model based on the data from the pre-pandemic period, but they surpassed the forecast
since 2021.
Tsugawa et al. [
36
] provided a study conducted on young women in which they
measured 25(OH)D concentrations from May 2016 to June 2017 and in September 2020
(after lockdown due to COVID-19). They showed a significant difference in 25(OH)D levels
between the samples obtained in September 2016 and in September 2020 (
21.7 ±6.6 ng/mL
vs. 13.2
±
5.0 ng/mL). Additionally, serum 25(OH)D concentrations showed seasonal-
ity with the highest values in September. Similarly, in our study, the highest 25(OH)D
concentrations were observed each year in the summer season.
Jastrz˛ebska et al. [
37
] demonstrated changes in vitamin D concentrations among
24 young soccer players over the course of a year. The study started in September 2019 and
ended during the COVID-19 pandemic in August 2020. Significant differences in serum
25(OH)D concentrations between the seasons were reported, with the lowest concentrations
in autumn and winter, and during the home isolation period in spring 2020.
Lippi et al. [
38
] compared vitamin D concentrations in the outpatient population
before and after the first day of lockdown (10 March 2020). The results showed higher
vitamin D concentrations and a modest but lower likelihood of vitamin D deficiency in
the first 9 months of the pandemic (from 10 March 10 to 11 December 2020) than in the
same period of the previous 2 years. The authors linked the paradoxical rise in serum
25(OH)D concentrations at the start of the COVID-19 pandemic and during the consequent
lockdown to the higher proportion of males who were tested while compared to the same
period in the previous two years. In general, higher vitamin D concentrations in males
than in females have been confirmed in other studies [
11
,
27
,
30
], which may indeed offer an
explanation for these findings.
Nutrients 2023,15, 3629 9 of 13
Ferrari et al. [
39
] investigated vitamin D concentrations among patients in different
age groups in 2019 and 2020. In their study, serum 25(OH)D concentrations were higher
during the lockdown period than in the same period a year earlier. The authors did
not find a direct link between vitamin D concentrations and sun exposure, but indicated
that different variables, such as vitamin D supplementation, may have influenced this.
Conversely, Beyazgül et al. [
40
] reported a decrease in vitamin D in Turkish school-aged
children and adolescents in first year of the pandemic with respect to the pre-pandemic
period.
Li et al. [41]
observed significantly higher vitamin D levels in 2020 than in 2019. In
Chinese children, however, in February, March, and April 2020 vitamin D concentrations
were lower than in the same months of 2019. In our study, as in most other reports,
significantly higher 25(OH)D concentrations during the SARS-CoV-2 pandemic than in the
pre-pandemic period were observed. Moreover, seasonal variability related to differences
in sun exposure was an important variable in the created models of 25(OH)D levels.
In the context of the SARS-CoV-2 pandemic, very recent studies concerning the re-
lationships between solar activity or solar cycles and epidemics seem to be especially
interesting [
42
–
44
]. The direct effects of weather variables on SARS-CoV-2 transmission
have also been confirmed in studies conducted in different countries [
45
–
48
]. In the Spanish
population, a direct influence of higher insolation on a lower rate of COVID-19 spread has
been documented [
49
]. Even in Brazil, which is a tropical country in which the pandemic
onset was during the summer, high solar radiation presented to be the most important
climatic factor suppressing the spread of COVID-19 [
50
]. There are also suggestions that vi-
tamin D may be the link between these phenomena [
43
]. This hypothesis may be supported
to some extent by a very recent observation of Polish authors that the risk of COVID-19
infection was increased in subjects with severe 25(OH)D deficiency (below 12 ng/mL) [
51
].
These issues were not directly analyzed in our study; however, in the studied pop-
ulation of Polish children, the pandemic lockdown resulted in decreased sun exposure
which resulted in lower vitamin D concentrations with respect to the prediction based
on insolation.
In our study, seasonal differences in insolation turned out to be the variable that
explained 84% of the seasonal variability of serum 25(OH)D concentrations. In fact, we did
not assessed the individual dietary habits of our subjects and their possible seasonality;
however, there is some evidence from other studies that vitamin D intake from diet in
children is below the recommended level [
52
,
53
], even in terms of vitamin D fortification
school meal programs [
53
]. A study comparing Brazilian women living in different latitudes
showed an almost-twice-as-high basal serum 25(OH)D concentration in women living in
latitudes with high ultraviolet B (UVB) exposure (16
◦
S) than in those living in latitudes
“without UVB exposure” (51
◦
N), despite no difference in vitamin D intake from diet
between them and with similar 25(OH)D increase in terms of supplementation of 15
µ
g
cholecalciferol in both groups [
54
]. For our considerations, the studies on the population of
Canada, Alberta (the region located at a similar latitude as Poland) seem to be especially
important, documenting low vitamin D intake and high prevalence of its insufficiency
both in pregnant women and in children, with no significant difference in serum 25(OH)D
concentrations in 3-month-old infants measured in summer and in winter [
55
,
56
]. We have
not found studies indicating the seasonality of vitamin D intake in food, especially for
higher vitamin D content in the diet in summer with respect to winter, not only in Polish
children but also in other populations. Moreover, as in Poland vitamin D supplementation
in healthy children and adolescents has been recommended for October to April [
24
],
it seems that its seasonal application could only weaken the observed effects related
to insolation.
The consumption of dietary supplements has increased in recent years. Especially during
the COVID-19 pandemic, this related to vitamin D supplementation. This was most likely due
to emerging reports on the effect of vitamin D supplementation on reducing the risk of SARS-
CoV-2 infection, disease severity, and risk of death [
57
].
Pu´scion-Jakubik et al. [58]
conducted a
survey on the consumption of dietary supplements, particularly vitamin D and zinc, among
Nutrients 2023,15, 3629 10 of 13
Polish adults during the three waves of the COVID-19 pandemic. The results indicated that
the largest percentage of respondents used supplements containing vitamin D. In addition,
it was shown that the consumption of dietary supplements was significantly higher among
those with higher medical education, indicating a high awareness of the health-promoting
aspects of supplementation among this group.
Our study was not devoted directly to the assessment of vitamin D supplementation;
however, it documented a significant increase in serum 25(OH)D concentrations both after
the implementation of the New Guidelines of vitamin D supplementation in 2018 [
24
] and
during the SARS-CoV-2 pandemic. Nevertheless, the scale of vitamin D deficiency and
insufficiency is still too high and further efforts seem necessary to improve the vitamin D
supply. On the other hand, there is a need to prevent the cases of uncontrolled overdosing
of vitamin D. A very recent update of the guidelines for preventing and treating vitamin D
deficiency in Poland [
59
] includes recommended vitamin D dosing in different age groups
and in specific clinical situations (such as pregnancy and lactation, prematurity, overweight
and obesity, chronic diseases, and diets), together with the determination of maximum
doses of cholecalciferol in the general population by age for the prophylaxis of vitamin
D deficiency.
5. Conclusions
A significant increase in serum 25(OH)D concentrations has been observed after the
introduction of new vitamin D supplementation guidelines, which indicates the effective-
ness of the actions to implement these recommendations. A further increase in 25(OH)D
concentrations during the SARS-CoV-2 pandemic seems to be related to increased vitamin
D supply with the intention to reduce the risk of COVID-19 infection. Nevertheless, the
scale of vitamin D deficiency and insufficiency among children is still too high. Time series
models have proven to be useful in analyzing the impact of health policy interventions and
pandemic restrictions on the seasonal variability of vitamin D concentrations.
Author Contributions:
Conceptualization, J.S.; methodology, J.S.; validation, R.S., M.H. and A.L.;
formal analysis, J.S.; investigation, J.S., M.H., A.Ł. and R.S.; resources, N.P.; data curation, J.S. and
N.P.; writing—original draft preparation, J.S. and N.P.; writing—review and editing, M.H., A.Ł. and
R.S.; visualization, J.S.; supervision, R.S. and A.L. All authors have read and agreed to the published
version of the manuscript.
Funding:
The APC was funded by the Medical University of Lodz, Poland, from statutory funds
(503/1-090-05/503-11-001).
Institutional Review Board Statement:
This study was conducted in accordance with the Declara-
tion of Helsinki and approved by the Institutional Ethics Committee of Polish Mother’s Memorial
Hospital—Research Institute in Lodz, Poland.
Informed Consent Statement:
Informed consent was obtained from the parents of all subjects
involved in the study.
Data Availability Statement:
The data presented in this study are available on request from the
corresponding author.
Conflicts of Interest: The authors declare no conflict of interest.
References
1.
Samuel, S.; Sitrin, M.D. Vitamin D’s role in cell proliferation and differentiation. Nutr. Rev.
2008
,66 (Suppl. S2), S116–S124.
[CrossRef] [PubMed]
2.
Wasiewicz, T.; Piotrowska, A.; Wierzbicka, J.; Slominski, A.T.; Zmijewski, M.A. Antiproliferative activity of non-calcemic vitamin
D analogs on human melanoma lines in relation to VDR and PDIA3 receptors. Int. J. Mol. Sci.
2018
,19, 2583. [CrossRef] [PubMed]
3.
De Luca, P.; de Girolamo, L.; Orfei, C.P.; Viganò, M.; Cecchinato, R.; Brayda-Bruno, M.; Colombini, A. Vitamin D’s effect on
the proliferation and inflammation of human intervertebral disc cells in relation to the functional vitamin D receptor gene foki
polymorphism. Int. J. Mol. Sci. 2018,19, 2002. [CrossRef]
4. Norman, P.E.; Powell, J.T. Vitamin D and cardiovascular disease. Circ. Res. 2014,114, 379–393. [CrossRef]
Nutrients 2023,15, 3629 11 of 13
5.
Panfili, F.M.; Roversi, M.; D’Argenio, P.; Rossi, P.; Cappa, M.; Fintini, D. Possible role of vitamin D in COVID-19 infection in
pediatric population. J. Endocrinol. Investig. 2021,44, 27–35. [CrossRef] [PubMed]
6.
Cashman, K.D.; Dowling, K.G.; Škrabáková, Z.; Gonzalez-Gross, M.; Valtueña, J.; De Henauw, S.; Moreno, L.; Damsgaard, C.T.;
Michaelsen, K.F.; Mølgaard, C.; et al. Vitamin D deficiency in Europe: Pandemic? Am. J. Clin. Nutr.
2016
,103, 1033–1044.
[CrossRef]
7.
O’Neill, C.M.; Kazantzidis, A.; Ryan, M.J.; Barber, N.; Sempos, C.T.; Durazo-Arvizu, R.A.; Jorde, R.; Grimnes, G.; Eiriksdottir, G.;
Gudnason, V.; et al. Seasonal changes in vitamin D-effective UVB availability in Europe and associations with population serum
25-hydroxyvitamin D. Nutrients 2016,8, 553. [CrossRef]
8.
Vierucci, F.; Del Pistoia, M.; Fanos, M.; Erba, P.; Saggese, G. Prevalence of hypovitaminosis D and predictors of vitamin D status
in Italian healthy adolescents. Ital. J. Pediatr. 2014,40, 54. [CrossRef]
9.
Oliosa, P.R.; Oliosa, E.M.R.; de Oliveira Alvim, R.; Sartório, C.L.; dos Anjos Zaniqueli, D.; Mill, J.G. Association of sun exposure
and seasonality with vitamin D levels in Brazilian children and adolescents. Rev. Paul. Pediatr. 2023,41, e2021361. [CrossRef]
10.
Pludowski, P.; Grant, W.B.; Bhattoa, H.P.; Bayer, M.; Povoroznyuk, V.; Rudenka, E.; Ramanau, H.; Varbiro, S.; Rudenka, A.;
Karczmarewicz, E.; et al. Vitamin D status in central Europe. Int. J. Endocrinol. 2014,2014, 589587. [CrossRef]
11.
Kiely, M.; Black, L.J. Dietary strategies to maintain adequacy of circulating 25-hydroxyvitamin D concentrations. Scand. J. Clin.
Lab. Investig. 2012,72, 14–23.
12.
Manios, Y.; Moschonis, G.; Lambrinou, C.P.; Tsoutsoulopoulou, K.; Binou, P.; Karachaliou, A.; Breidenassel, C.; Gonzalez-Gross,
M.; Kiely, M.; Cashman, K.D. A systematic review of vitamin D status in southern European countries. Eur. J. Nutr.
2018
,57,
2001–2036. [CrossRef] [PubMed]
13.
Hayes, A.; Cashman, K.D. Food-based solutions for vitamin D deficiency: Putting policy into practice and the key role for
research. Proc. Nutr. Soc. 2017,76, 54–63. [CrossRef] [PubMed]
14.
Cashman, K.D. Vitamin D: Dietary requirements and food fortification as a means of helping achieve adequate vitamin D status.
J. Steroid Biochem. Mol. Biol. 2015,148, 19–26. [CrossRef] [PubMed]
15.
Bouillon, R.; Marcocci, C.; Carmeliet, G.; Bikle, D.; White, J.H.; Dawson-Hughes, B.; Lips, P.; Munns, C.F.; Lazaretti-Castro, M.;
Giustina, A.; et al. Skeletal and Extraskeletal Actions of Vitamin D: Current Evidence and Outstanding Questions. Endocr. Rev.
2019,40, 1109–1151. [CrossRef] [PubMed]
16.
Amrein, K.; Scherkl, M.; Hoffmann, M.; Neuwersch-Sommeregger, S.; Köstenberger, M.; Tmava Berisha, A.; Martucci, G.; Pilz, S.;
Malle, O. Vitamin D deficiency 2.0: An update on the current status worldwide. Eur. J. Clin. Nutr.
2020
,74, 1498–1513. [CrossRef]
17.
Holick, M.F. The vitamin D deficiency pandemic: Approaches for diagnosis, treatment and prevention. Rev. Endocr. Metab. Disord.
2017,18, 153–165. [CrossRef]
18.
Cashman, K.D. Vitamin D Deficiency: Defining, Prevalence, Causes, and Strategies of Addressing. Calcif. Tissue Int.
2020
,106,
14–29. [CrossRef]
19.
Grant, W.B.; Al Anouti, F.; Boucher, B.J.; Dursun, E.; Gezen-Ak, D.; Jude, E.B.; Karonova, T.; Pludowski, P. A Narrative Review of
the Evidence for Variations in Serum 25-Hydroxyvitamin D Concentration Thresholds for Optimal Health. Nutrients
2022
,14, 639.
[CrossRef]
20.
Płudowski, P. COVID-19 and Other Pleiotropic Actions of Vitamin D: Proceedings from the Fifth International Conference
“Vitamin D—Minimum, Maximum, Optimum” under the Auspices of the European Vitamin D Association (EVIDAS). Nutrients
2023,15, 2530. [CrossRef]
21.
Płudowski, P.; Karczmarewicz, E.; Bayer, M.; Carter, G.; Chlebna-Sokół, D.; Czech-Kowalska, J.; D˛ebski, R.; Desci, T.; Franek, E.;
Głuszko, P.; et al. Practical Guidelines for the Supplementation of Vitamin D and the Treatment of Deficits in Central Europe.
Endokrynol. Pol. 2013,64, 319–327. [CrossRef]
22.
Chlebna-Sokół, D.; Michałus, I.; Rusi´nska, A.; Łupi´nska, A.; Fijałkowski, B.; Andrzejewska, K.; Magsar Khuchit, B.; Porczy´nski,
M.; Woch, I.; Jo´nczyk, A.; et al. Evaluation of vitamin D levels in children hospitalized with symptoms suggesting metabolism
disorders in skeleton system. Pediatr. Endocrinol. 2016,15, 23–32. [CrossRef]
23.
Smyczy´nska, J.; Smyczy´nska, U.; Stawerska, R.; Domagalska-Nalewajek, H.; Lewi´nski, A.; Hilczer, M. Seasonality of vitamin D
concentrations and the incidence of vitamin D deficiency in children and adolescents from central Poland. Pediatr. Endocrinol.
Diabetes Metab. 2019,25, 54–59. [CrossRef] [PubMed]
24.
Rusi´nska, A.; Płudowski, P.; Walczak, M.; Borszewska-Kornacka, M.K.; Bossowski, A.; Chlebna-Sokół, D.; Czech-Kowalska, J.;
Dobrza´nska, A.; Franek, E.; Helwich, E.; et al. Vitamin D Supplementation Guidelines for General Population and Groups at
Risk of Vitamin D Deficiency in Poland—Recommendations of the Polish Society of Pediatric Endocrinology and Diabetes and
the Expert Panel With Participation of National Specialist Consultants and Representatives of Scientific Societies—2018 Update.
Front. Endocrinol. 2018,9, 246. [CrossRef]
25.
Mercola, J.; Grant, W.B.; Wagner, C.L. Evidence regarding vitamin D and risk of COVID-19 and its severity. Nutrients
2020
,12,
3361. [CrossRef] [PubMed]
26.
Chiodini, I.; Gatti, D.; Soranna, D.; Merlotti, D.; Mingiano, C.; Fassio, A.; Adami, G.; Falchetti, A.; Eller-Vainicher, C.; Rossini, M.;
et al. Vitamin D Status and SARS-CoV-2 Infection and COVID-19 Clinical Outcomes. Front. Public Health
2021
,9, 1–19. [CrossRef]
27.
Szarpak, L.; Rafique, Z.; Gasecka, A.; Chirico, F.; Gawel, W.; Hernik, J.; Kaminska, H.; Filipiak, K.J.; Jaguszewski, M.J.; Szarpak, Ł.
A systematic review and meta-analysis of effect of vitamin D levels on the incidence of COVID-19. Cardiol. J.
2021
,28, 647–654.
[CrossRef]
Nutrients 2023,15, 3629 12 of 13
28.
Palczewska, I.; Nied´zwiecka, Z. Indices of somatic development of children and adolescents in Warsaw. Med. Wieku Rozw.
2001
,
5(Suppl. S1), 17–118. (In Polish)
29.
Lin, L.; Ou, Q.; Lin, L.; Zhang, H.; Chen, K.; Chen, D.; Quan, H.; He, Y.; Fang, T. Low prevalence of vitamin D deficiency in adult
residents in Hainan, the tropical island province of China. Ann. Palliat. Med. 2021,10, 5580–6394. [CrossRef]
30.
Lee, J.; Woo, H.W.; Kim, J.; Shin, M.H.; Koh, I.; Choi, B.Y.; Kim, M.K. Independent and interactive associations of season, dietary
vitamin D, and vitamin D-related genetic variants with serum 25(OH)D in Korean adults aged 40 years or older. Endocr. J.
2021
,
68, 701–711. [CrossRef]
31.
Pott-Junior, H.; Luzeiro, C.; Senise, J.F.; Castelo, A. Association of seasonality and serum albumin concentration with Vitamin
D deficiency in subjects with chronic hepatitis C infection living in a sunny country. Public Health Nutr.
2020
,23, 1247–1253.
[CrossRef] [PubMed]
32.
Shen, M.; Li, Z.; Lv, D.; Yang, G.; Wu, R.; Pan, J.; Wang, S.; Li, Y.; Xu, S. Seasonal variation and correlation analysis of vitamin D
and parathyroid hormone in Hangzhou, Southeast China. J. Cell. Mol. Med. 2020,24, 7370–7377. [CrossRef] [PubMed]
33.
Dimakopoulos, I.; Magriplis, E.; Mitsopoulou, A.V.; Karageorgou, D.; Bakogianni, I.; Micha, R.; Michas, G.; Chourdakis, M.;
Ntouroupi, T.; Tsaniklidou, S.M.; et al. Association of serum vitamin D status with dietary intake and sun exposure in adults.
Clin. Nutr. ESPEN 2019,34, 23–31. [CrossRef]
34.
Basi´nska-Lewandowska, M.; Lewi´nski, A.; Horzelski, W.; Skowro´nska-Jó´zwiak, E. Effect of summer sunshine exposure on
vitamin D status in young and middle age Poles: Is 30 ng/ml vitamin D cut-off really suitable for the Polish population? Int. J.
Environ. Res. Public Health 2021,18, 8116. [CrossRef]
35.
Rustecka, A.; Maret, J.; Drab, A.; Leszczy´nska, M.; Tomaszewska, A.; Lipi´nska-Opałka, A.; B ˛edzichowska, A.; Kalicki, B.; Kubiak,
J.Z. The impact of COVID-19 pandemic during 2020–2021 on the vitamin D serum levels in the paediatric population in Warsaw,
Poland. Nutrients 2021,13, 1990. [CrossRef] [PubMed]
36.
Tsugawa, N.; Kuwabara, A.; Ogasawara, H.; Nishino, M.; Nakagawa, K.; Kamao, M.; Hasegawa, H.; Tanaka, K. Vitamin D Status
in Japanese Young Women in 2016–2017 and 2020: Seasonal Variation and the Effect of Lifestyle Including Changes Caused by
the COVID-19 Pandemic. J. Nutr. Sci. Vitaminol. 2022,68, 172–180. [CrossRef]
37.
Jastrz˛ebska, J.; Skalska, M.; Radzimi ´nski, Ł.; López-Sánchez, G.F.; Weiss, K.; Hill, L.; Knechtle, B. Changes of 25(OH)D Concen-
tration, Bone Resorption Markers and Physical Performance as an Effect of Sun Exposure, Supplementation of Vitamin D and
Lockdown among Young Soccer Players during a One-Year Training Season. Nutrients 2022,14, 521. [CrossRef]
38.
Lippi, G.; Ferrari, A.; Targher, G. Is COVID-19 lockdown associated with Vitamin D deficiency? Eur. J. Public Health
2021
,31,
278–279. [CrossRef]
39.
Ferrari, D.; Locatelli, M.; Faraldi, M.; Lombardi, G. Changes in 25-(OH) vitamin D levels during the SARS-CoV-2 outbreak:
Lockdown-related effects and first-to-second wave difference—An observational study from northern Italy. Biology
2021
,10, 237.
[CrossRef]
40.
Beyazgül, G.; Ba˘g, Ö.; Yurtseven, ˙
I.; Co¸skunol, F.; Ba¸ser, S.; Çiçek, D.; Kanbero˘glu, G.˙
I.; Çelik, F.; Nalbanto˘glu, Ö.; Özkan, B. How
Vitamin D Levels of Children Changed During COVID-19 Pandemic: A Comparison of Pre-pandemic and Pandemic Periods.
JCRPE J. Clin. Res. Pediatr. Endocrinol. 2022,14, 188–195. [CrossRef]
41.
Li, T.; Li, X.; Chen, N.; Yang, J.; Yang, J.; Bi, L. Influence of the COVID-19 pandemic on the vitamin D status of children: A
cross-sectional study. J. Med. Virol. 2023,95, e28438. [CrossRef] [PubMed]
42.
Chen, S.; Wei, Y.; Yue, X.; Xu, K.; Li, M.; Lin, W. Correlation analysis between the occurrence of epidemic in ancient China and
solar activity. Sci. China Earth Sci. 2023,66, 161–168. [CrossRef] [PubMed]
43.
Lee, K.C.; Kim, J.S.; Kwak, Y.S. Relation of pandemics with solar cycles through ozone, cloud seeds, and vitamin D. Environ. Sci.
Pollut. Res. 2022,30, 13827–13836. [CrossRef] [PubMed]
44.
Bell, T. Do solar cycles explain the emergence of COVID-19? Neutron count comparison between the solar minima of 2008–2009
and 2019–2020. Curr. Opin. Environ. Sci. Health 2022,26, 100333. [CrossRef]
45.
Fu, S.; Wang, B.; Zhou, J.; Xu, X.; Liu, J.; Ma, Y.; Li, L.; He, X.; Li, S.; Niu, J.; et al. Meteorological factors, governmental responses
and COVID-19: Evidence from four European countries. Environ. Res. 2021,194, 110596. [CrossRef]
46.
Xie, J.; Zhu, Y. Association between ambient temperature and COVID-19 infection in 122 cities from China. Sci. Total Environ.
2020,724, 138201. [CrossRef]
47.
Ahmadi, M.; Sharifi, A.; Dorosti, S.; Jafarzadeh Ghoushchi, S.; Ghanbari, N. Investigation of effective climatology parameters on
COVID-19 outbreak in Iran. Sci. Total Environ. 2020,729, 138705. [CrossRef]
48. ¸Sahin, M. Impact of weather on COVID-19 pandemic in Turkey. Sci. Total Environ. 2020,728, 138810. [CrossRef]
49.
LochéFernández-Ahúja, J.M.; Fernández Martínez, J.L. Effects of climate variables on the COVID-19 outbreak in Spain. Int. J.
Hyg. Environ. Health 2021,234, 113723. [CrossRef]
50.
Rosario, D.K.A.; Mutz, Y.S.; Bernardes, P.C.; Conte-Junior, C.A. Relationship between COVID-19 and weather: Case study in a
tropical country. Int. J. Hyg. Environ. Health 2020,229, 113587. [CrossRef]
51.
Basi´nska-Lewandowska, M.; Lewandowski, K.; Horzelski, W.; Lewi ´nski, A.; Skowro´nska-Jó´zwiak, E. Frequency of COVID-19
Infection as a Function of Vitamin D Levels. Nutrients 2023,15, 1581. [CrossRef]
52.
Borger, C.; Paolicelli, C.; Ritchie, L.; Whaley, S.E.; Dematteis, J.; Sun, B.; Zimmerman, T.P.; Reat, A.; Dixit-Joshi, S. Shifts in sources
of food but stable nutritional outcomes among children in the early months of the COVID-19 pandemic. Int. J. Environ. Res. Public
Health 2021,18, 12626. [CrossRef]
Nutrients 2023,15, 3629 13 of 13
53.
Calvo, M.S.; Whiting, S.J. Perspective: School Meal Programs Require Higher Vitamin D Fortification Levels in Milk Products and
Plant-Based Alternatives—Evidence from the National Health and Nutrition Examination Surveys (NHANES 2001–2018). Adv.
Nutr. 2022,13, 1440–1449. [CrossRef]
54.
Mendes, M.M.; Hart, K.H.; Williams, E.L.; Mendis, J.; Lanham-New, S.A.; Botelho, P.B. Vitamin D supplementation and sunlight
exposure on serum Vitamin D concentrations in 2 parallel, double-blind, randomized, placebo-controlled trials. J. Nutr.
2021
,151,
3137–3150. [CrossRef] [PubMed]
55.
Aghajafari, F.; Field, C.J.; Weinberg, A.R.; Letourneau, N. Both mother and infant require a vitamin D supplement to ensure that
infants’ vitamin D status meets current guidelines. Nutrients 2018,10, 429. [CrossRef] [PubMed]
56.
Letourneau, N.; Aghajafari, F.; Bell, R.C.; Deane, A.J.; Dewey, D.; Field, C.; Giesbrecht, G.; Kaplan, B.; Leung, B.; Ntanda, H. The
Alberta Pregnancy Outcomes and Nutrition (APrON) longitudinal study: Cohort profile and key findings from the first three
years. BMJ Open 2022,12, e047503. [CrossRef] [PubMed]
57.
Tomaszewska, A.; Rustecka, A.; Lipi ´nska-Opałka, A.; Piprek, R.P.; Kloc, M.; Kalicki, B.; Kubiak, J.Z. The Role of Vitamin D in
COVID-19 and the Impact of Pandemic Restrictions on Vitamin D Blood Content. Front. Pharmacol.
2022
,13, 836738. [CrossRef]
58.
Pu´scion-Jakubik, A.; Bielecka, J.; Grabia, M.; Mielech, A.; Markiewicz- ˙
Zukowska, R.; Mielcarek, K.; Moskwa, J.;
Naliwajko, S.K.
;
Soroczy´nska, J.; Gromkowska-K˛epka, K.J.; et al. Consumption of food supplements during the three COVID-19 waves in
Poland—Focus on zinc and vitamin D. Nutrients 2021,13, 3361. [CrossRef]
59.
Płudowski, P.; Kos-Kudła, B.; Walczak, M.; Fal, A.; Zozuli´nska-Ziółkiewicz, D.; Sieroszewski, P.; Peregud-Pogorzelski, J.;
Lauterbach, R.; Targowski, T.; Lewi´nski, A.; et al. Guidelines for Preventing and Treating Vitamin D Deficiency: A 2023 Update in
Poland. Nutrients 2023,15, 695. [CrossRef]
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