International Journal of Clinical Medicine, 2012, 3, 400-406
http://dx.doi.org/10.4236/ijcm.2012.35075 Published Online September 2012 (http://www.SciRP.org/journal/ijcm) 1
The Relationship between Bone Mineral Density and
Dietary Intake in Moroccan Children with Juvenile
Idiopathic Arthritis
A. Hassani1, S. Rostom1, D. El Badri1, I. Bouaadi1, A. Barakat2, B . Chk i r at2, K. Elkari3, R. Bahiri1,
B. Amine1, N. Hajjaj-Hassouni1
1Department of Rheumatology, El Eyachi Hospital, University Hospital of Rabat-Sale, Sale, Morocco; 2Department of Pediatrics,
Hospital of Children, University Hospital of Rabat-Sale, Rabat, Morocco; 3Department of Nutrition, Faculty of Science of Kenitra,
University Ibn Tofaïl, Kenitra, Morocco.
Received May 30th, 2012; revised June 30th, 2012; accepted July 25th, 2012
ABSTRACT
Background and Objective: The aim of this study was to evaluate the association between dietary intake and bone
mineral density in children with juvenile idiopathic arthritis (JIA). Methods: A cross-sectional study carried out in
Morocco between May 2010 and June 2011, covering out patients with JIA. The characteristics of patients were col-
lected. The nutritional status was assessed by a food questionnaire including data of food intake during 7 consecutive
days using 24-hour dietary recall. Food intake was quantified using the software Bilnut (Bilnut version 2.01, 1991).
Bone mineral density (BMD in g/cm2) was measured by DXA method (X-ray absorptiometry) on a Lunar Prodigy. Re-
sults: The study consisted of 33 pa tients with JIA (4 - 16 years old). The median age of patients was 10.4 ± 4.3 years.
Median disease duration was 2 (1 - 4.5) years. The group of patients with low dietary intake of proteins was associated
with low BMD (p = 0.03). Low BMD was related with low intake of magnesium (p = 0.007) and vitamin C (p = 0.04)
in children aged between 4 and 9 years. Low intake of vitamin E and folate was associated with high BMD in the other
range of children (p < 0.001). Conclusion: This study suggests that low intake of protein and of some micronutrients
(magnesium, vitamin C, vitamin E and folate) in fluence bone mass in children with JIA. Prospective studies with a lar-
ger number of patients seem to be necessary in order to confirm our findings.
Keywords: Juvenile Idiopathic Arthritis; Macronutrients; Vitamins; Trace Elements; Bone Mineral Density
1. Background
Osteoporosis is currently estimated to be a major health
threat [1]. It’s defined by a disease characterized by loss
of bone masse, accompanied by microarchitectural dete-
rioration of bone tissue, which leads to an unacceptable
increase in the risk of fracture [2]. About 90% of total
adult mass is accrued by age 20, and a signification pro-
portion of this is archived during puberty alone [3].
Juvenile idiopathic arthritis (AJI) is one of the com-
monest rheumatic diseases of children [4]. In one hand,
several studies demonstrate reduced bone mineral density
(BMD) in children with JIA [5,6]. In the other hand, JI A
is often associated with poor nutritional status [7]. Nu tri-
tion is a key factor, not only for bone growth, but also for
its mineralization [5]. The acq uisition of adequate miner-
alization during childhood has proven to be a key event
in the prevention of osteoporosis in adults [8]. Recent
studies on various dietary components have shown that
there is some correlation between their daily food intake
and the genesis of osteoporosis and its fracture complica-
tions [9]. An inadequate nutrition (especially intake of
macronutrients, trace elements and vitamins), can be as-
sociated with an increase in bone remodeling leading to
significant loss of bone and an increase fracture risk [10].
There are few studies available in the literature assessing
the relation sheep between dietary intake and bone min-
eral density in children. In addition, there are no studies
in a Moroccan popu lation that evaluate the same subject.
The aim of this study was to assess the relationship be-
tween the dietary intake and bone mineral density in
Moroccan children and adolescents with JIA.
2. Materials and Methods
2.1. Data Collection
*The authors declare that they have no conflicts of interest concerning
this article. It was a cross sectional study of children with JIA over a

The Relationship between Bone Mineral Density and Dietary Intake in Moroccan
Children with Juvenile Idiopathic Arthritis 401
period of 13 months (between May 2010 and June 2011)
at the department of rheumatology of El Eyachi Univer-
sity hospital and department of pediatrics of university
hospital of children of Rabat-Sale. Informed consent was
obtained by parents from all subjects and the study was
approved by ethics committee of our university hospital.
The diagnosis of JIA was based on the criteria of the
International League of Association for Rheumatology
(ILAR) [11]. Patients were recruited in consultation or
during hospitalization. We excluded patients with any
other chronic disease (endocrinal, neurological, cardiac,
and renal) that affect bone metabolism. The disease and
patients characteristics considered as explanatory meas-
ures were: age (year), gender, diagnosis (JIA subtype),
disease duration (years), disease activity was assessed
using a visual analogical scale (VAS), functional disabil-
ity was determined by using the Moroccan version of
Childhood Health Assessment Questionnaire (CHAQ)
[12], number of tender joints, number of swollen joints
and the erythrocyte sedimentation rate (ESR). Treatment
with NSAIDs, corticosteroid and d isease modifying anti-
rheumatic drugs (DMARDs) was determined.
2.2. BMD Assessment
All BMD measurements were obtained with the same
DXA instrument (Lunar Prodigy; GE Lunar, Madison,
WI). BMD (g/cm²) was measured in the lumbar spine
(L1-L4) and total body. The lumbar spine and the total
body BMD values were transformed into Z scores by
comparing them with age- and sex-specific reference
values for this equipment [13,14]. According to the In-
ternational Society for Clinical Densitometry recom-
mendations osteoporosis was defined as a Z-score less
than 2 with a fracture history. Low BMD was defined as
a Z-score less than 2 without a significant fracture history
[15].
2.3. Dietary Evaluation
Nutrient intake was determined using the 24 hour diet
recall during 7 consecutive days [16]. The food ques-
tionnaire had two parts; the first identified all foods con-
sumed during the day previous to the interview; the sec-
ond part; specified food frequency to appreciate food
eating habits. Two nutritionists analyzed the food dietary
to quantify the food consumed from the recorded infor-
mation. Nutrient intake was analyzed by software bilnut
(Bilnut version 2.01, 1991), validated and standardized.
The dietary intake of macro and micronutrients were
assessed against the recommended dietary allowances
(RDA) [17]. The analysis of micronutrients was made
according to the age (group between 4 years and 9 years
and group between 10 years to 16 years). We con sidered
that 50% to 60% as the appropriate percentage of calories
from carbohydrates, between 10% and 15% the percent-
age related to proteins and between 25% to 30% the per-
centage of lipids [7].
2.4. Anthropometric Measures
Weight (kg) and height (m) were measured according to
the recommendation of the World Health Organization
(WHO). The results of the BMI (Kg/m2) were compared
with refe r e n c e values o f H a mmer et al. [18,19].
2.5. Statistics
Analysis was carried out using the statistical p ackage for
the social sciences (SPSS) version 16.0. Data for patients
were presented as mean ± standard deviation or median
(IQ) for continuous variables and as frequencies and
percentage for categorical variables. For dietary intake of
macronutrients, we are divided patients on 3 groups, low,
normal and high dietary intake, and we used one way
Anova test to compare values of BMD (g/cm2) between
the 3 groups. As regards micronutrient intake, Student’s
t-test for independent samples was used to compare val-
ues of BMD (g/cm2) between two groups: with low and
with normal dietary intake of micronutrients. Signifi-
cance level was p value less than 0.05.
3. Results
Thirty three patients where included in this study. The
mean age of our patients was 10.4 ± 4.35. 54.5% of our
patients were males. The median disease duration was
equal to 2 (1 - 4.5) years. Eleven patients (33.3%) had a
low BMD in lumbar spine, and nine (27%) in total body,
and no patient had an osteoporosis. Demographic and
clinical characteristics of patients are described in Table
1. We found that patients with JIA had an excessive in-
take of proteins, carbohydrates and lipids in 30.3%,
63.6% and 54.5% of the cases respectively. Moreover all
patients had a low consumption of micronutrients.
Low intake of proteins was associated with a low
BMD (p = 0.03) (Table 2). No difference was observed
between dietary intake of glucids and lipids, and BMD
(Table 2).
Daily mean intake of micronutrients show that low
dietary intake of vitamin C was associated with an in-
crease on BMD (p = 0.04) and low dietary intake of
magnesium was associated with decreased BMD (p <
0.0001) in children aged between 4 and 9 years (Table 3).
Low intake of vitamin E and folate was associated with
increased BMD in children between 10 and 16 years (p <
0.001) (Table 4).

The Relationship between Bone Mineral Density and Dietary Intake in Moroccan
Children with Juvenile Idiopathic Arthritis
402
4. Discussion
In our study, we show that low dietary intake of proteins
was associated to reduce bone density. It has been sug-
gested that dietary protein intake may be a risk factor for
Table 1. Clinical characteristics of patients.
Characteristics AJI (n = 33)
Age (year)1 10.45 ± 4.35
Sex males2 18 (54.5)
DAS28 ESR1 5.30 ± 1.10
Disease duration (year)3 2 [1 - 4.5]
Visual analogical scale (0 - 10)3 20 [10 - 50]
CHAQ score (0 - 3)³ 0.5 [0 - 1.6]
JIA clinical subtypes2
Oligoarticular 9 [27 - 3]
Polyarticular 16 [48 - 5]
Systemic 8 [24 - 2]
Nutritional status2
Underweight 9 (27.3)
Normal 16 (48.5)
Obesity 8 (24.2)
BMD lumber spine (g/cm2)3 0.6 [0.1 - 1]
BMD total body (g/cm2)3 0.7 [0.3 - 1.1]
Z score lumber spine < –22 11 (33.3)
Z score total body < –22 9 (27.3)
NSAID2 (yes) 26 (78.7)
DMARDs2 (yes) 17 (51.6)
Oral corticosteroid2 (yes) 14 (42.4)
DAS28 = disease activity score; CHAQ = Childhood Health Assessment
Questionnaire; JIA = juvenile idiopathic arthritis; BMD = bone mineral
density; NSAID = non-steroidal inflammatory drugs; DMARDs: Dis-
ease-Modifying Anti-Rheumatic Drugs. 1Mean ± S.D.; 2Number and per-
centage; 3Median and IQR.
osteoporosis, especially in childhood, and high-protein
diets are associated with increased bone loss [5]. Two
mechanisms are discussed. The protein metabolism is
accompanied by a significant production of amino acids
that can promote osteoclast function and bone resump-
tion. Also, protein intake may be involved indirectly in
the genesis of osteopo rosis by altering the metabolis m of
insulin like growth factor (IGF)-I [20,21].
Zhang Q. et al., found that higher protein intake, espe-
cially from animal foods, appeared to have a negative
effect on bone mass accrual in pubertal girls, which is
different with our data [22]. In the study of Vatanparast
H, they found that protein intake has a beneficial effect
on bone mass of young adult females when calcium in-
take is adequate; protein, in the absence of sufficient cal-
cium, does not confer as much benefit to bone [23]. In
the longitudinal study including 560 women aged be-
tween 14 and 40 years, they suggest that a higher protein
intake does not have an adverse effect on bone, and low
intake on vegetal protein is associated with a less bone
mass, [24].
Moreover, many scientists have examined the rela-
tionship between types of protein and urinary calcium
excretion, and found that animal protein was associated
with increased urinary calcium excretion, soy protein
was not. There is sufficient evidence suggesting soy
isoflavones may have potential benefits for bone, but a
relationship has not been established between the con-
sumption of ipriflavone and maintenance of bone mineral
density [25].
These studies were conducted in healthy subjects,
while our population is made of children with chronic
inflammatory arthritis and who take corticosteroids wh ich
could lower their bone mineral density and subsequent
can may explain our results.
In our study, we found that dietary intake of glucids
and lipids were not associated with bone mass. Epidemi-
Table 2. Association between daily macronutrients intake and BMD in children with JIA.
BMD (g/cm²) Lumber spine p Total body p
Low 0.510 ± 0.155 0.735 ± 0.049
Normal 0.833 ± 0.192 0.840 ± 0.134
Proteins (% of energy)
High 0.627 ± 0.230
0.03
0.246 ± 0.205
0.2
Low 0.619 ± 0.260 0.726 ± 0.179
Normal 0.714 ± 0.242 0.785 ± 0.239
Glucids (% of energy)
High 0.733 ± 0.193
0.4
0.826 ± 0.112
0.4
Low 0.723 ± 0.180 0.752 ± 0.179
Normal 0.710 ± 0.323 0.908 ± 0.202 Lipids (% of energy)
High 0.652 ± 0.245
0.7
0.749± 0.147
0.2
BMD: bone mineral density; JIA: juvenile idiopathic arthritis. Values are the mean ± SD; p, descriptive level of one way Anova. Low dietary intake of proteins
was associated with low BMD in lumber spine.

The Relationship between Bone Mineral Density and Dietary Intake in Moroccan
Children with Juvenile Idiopathic Arthritis 403
Table 3. Association between daily micronutrients intake and BMD in children with JIA aged between 4 and 9 years.
BMD (g/cm²) Lumber spine p Total body p
Calcium (mg)
Low 0.552 ± 0.209 0.720 ± 0.068
Normal 0.600 ± 0.001 0.7 0.650 ± 0.070 0.2
Phosphorus (mg)
Low 0.574 ± 0.223 0.713 ± 0.085
Normal 0.522 ± 0.093 0.6 0.705 ± 0.010 0.8
Magnesium (mg)
Low 0.100 ± 0.000 0.700 ± 0.000
Normal 0.594 ± 0.146 0.007 0.711 ± 0.073 0.8
Fer (mg)
Low 0.563 ± 0.234 0.725 ± 0.079
Normal 0.552 ± 0.104 0.9 0.684 ± 0.047 0.3
Zinc (mg)
Low 0.587 ± 0.261 0.727 ± 0.091
Normal 0.531 ± 0.103 0.6 0.694 ± 0.044 0.4
Vitamin B1 (mg)
Low 0.574 ± 0.223 0.723 ± 0.075
Normal 0.522 ± 0.093 0.6 0.680 ± 0.054 0.3
Vitamin C (mg)
Low 0.562 ± 0.234 0.738 ± 0.064
Normal 0.530 ± 0.100 0.9 0.634 ± 0.052 0.04
Vitamin E (mg)
Low 0.563 ± 0.200 0.711 ± 0.073
Normal 0.500 ± 0.001 0.7 0.700 ± 0.001 0.8
Folate (µg)
Low 0.560 ± 0.208 0.720 ± 0.068
Normal 0.550 ± 0.070 0.9 0.650 ± 0.070 0.2
BMD: bone mineral density; JIA: juvenile idiopathic arthritis. Values are the mean ± SD; p, descriptive level of Student’s t-test. Low intake of magnesium and
vitamin C was associated with decreased BMD in lumber spine, and increased BMD in total body respectively.
Table 4. Association between daily micronutrients intake and BMD in children with JIA aged between 10 and 16 years.
BMD (g/cm²) Lumber spine p Total body p
Calcium (mg)
Low 0.805 ± 0.250 0.761 ± 0.229
Normal 0.800 ± 0.001 0.9 0.900 ± 0.001 0.5
Phosphorus (mg)
Low 0.805 ± 0.250 0.761 ± 0.229
Normal 0.800 ± 0.001 0.9 0.900 ± 0.001 0.5
Magnesium (mg)
Low 0.773 ± 0.245 0.753 ± 0.241
Normal 0.973 ± 0.180 0.2 0.876 ± 0.040 0.4
Fer (mg)
Low 0.784 ± 0.241 0.758 ± 0.234
Normal 0.980 ± 0.254 0.3 0.900 ± 0.001 0.4
Zinc (mg)
Low 0.773 ± 0.245 0.753 ± 0.241
Normal 0.973±0.180
0.2 0.876 ± 0.040 0.4
Vitamin B1 (mg)
Low 0.805 ± 0.250 0.766 ± 0.229
Normal 0.800 ± 0.001 0.6 0.900 ± 0.001 0.8
Vitamin C (mg)
Low 0.829 ± 0.222 0.789 ± 0.228
Normal 0.600 ± 0.424 0.2 0.630 ± 0.190 0.3
Vitamin E (mg)
Low 0.805 ± 0.243 0.761 ± 0.229
Normal 0.500 ± 0.001 <0.001 0.600 ± 0.001 <0.001
Folate (µg)
Low 0.805 ± 0.243 0.789 ± 0.228
Normal 0.500 ± 0.001 <0.001 0.600 ± 0.001 <0.001
BMD: bone mineral densit y; JIA: juvenile idiopathic arthri t is. Values are the mean ± S D; p, descriptive level of S tudent’s t - t est. Low dietary intake of vitamin E
and folats was associated with high BMD in both lumber spine a n d to t al body.

The Relationship between Bone Mineral Density and Dietary Intake in Moroccan
Children with Juvenile Idiopathic Arthritis
404
ological data indicate that high-fat diets, especially those
rich in saturated fatty acids, may contribute to reduced
bone density and increased fracture risk, in older as well
as younger people [26]. One oth er study that assessed the
relation of dietary fat to hip bone mineral density (BMD)
in men and women indicated that BMD is negatively
associated with saturated fat intake [27]. Several studies
have shown the importance of individual fatty acids in
enterocyte membrane dynamics, Vitamin D3 activity,
and prostaglandin formation, which can have important
effects on intestinal calcium absorption as well as ur inary
calcium excretion [28]. Also, dietary lipids can influence
GH and osteoblast formation [21].
In their study, Rubinacci A. et al., show the presence
of positive relationships between bone mineral content
(BMC) and lipid intakes in the population of women in
early menopause, but they have no association between
glucids intakes and BMC [29]. In animal study, it has
been demonstrated in a group of rats with a diet rich on
fructo-oligosaccharides decreased content bone on c al c iu m
and phosphorus and resistance bone, compared to a con-
trol group [30]. But these results are contradictory with
data of other studies.
Regarding the dietary intake of micronutrients, our re-
sults show that low intake of magnesium is related with a
low bone mineral density. Rude et al. tested the effects of
deficient diets on bone tissue in rats [31]. The results
showed the histology decreased trabecular bone volume,
increased osteoclast activity without activation of osteo-
blasts and biologically hypercalcemia, a decrease in
serum parathyroid hormone (PTH) and 1, 25 (OH) vita-
min D. Thus, the Mg depletion would lead to bone
resorption uncoupled could exert inhibitory effect on
PTH. In the data of the literature, small epidemiologic
studies suggest that an excessive magnesium intake was
associated with higher BMD in elderly men and women
[32,33]. In clinical trials of magnesium supplementation,
there is a little evidence that magnesium is essential to
prevent osteoporosis in the general population [34,35].
Also, one recent study from the WHI suggested that
higher intakes of magnesium were associated with a risk
of wrist fracture [36].
Vitamin C is an essential cofactor for collagen forma-
tion and synthesis of hydroxyproline and hydroxylysine.
A several studies show a positive association between
vitamin C and bone mass. Low intakes of vitamin C are
associated with loss of BMD [37,38]. Celia J. Prynne et
al., explored the association between bone mineral status
and fruit and vegetable intakes in adolescent boys and
girls (aged 16 - 18 y), young women (aged 23 - 37 y),
and older men and women (aged 60 - 83 y). In boys, sig-
nificant positive asso ciations were found between d ietary
vitamin C and BMC and BMD. No significant univ ariate
association was found in the girls, and a significan t nega-
tive association with BMD was found in the older
women [39]. One study found that higher intake on vita-
min C was associated with fewer fractures; however,
there are no randomized clinical trials, [40]. In our study,
we found a significant association between low intake of
vitamin C and increased bone mineral density, which is
contradictory with the literature data.
In our data, we showed a negative association between
intake of vitamin E and BMD. In a Japanese study
including 441 women aged 20 to 35 years, they found
that increased vitamin E intake was associated with
greater total spine BMD [41]. Farrell V. A. et al. showed
that dietary vitamin E intake did not have any similar
BMD association [42].
Folate, vitamin B2 (riboflavin), and vitamin B12 may
affect bone directly or through an effect on plasma ho-
mocysteine levels [43]. In the current study, decreased
intake of folate was associated with high BMD. In a
study of Rejnmark L. et al., they found that high dietary
intake of folate exerts positive effects on BMD [31].
Also, Rivas A. et al. showed that the BMD was signify-
cantly associated with the intake of folate [44].
There was no association between BMD and the other
micronutrients.
Our study is limited by its cross-sectional design,
sample size and non-controlled design, but identification
of relationship between nutrition and bone status it so
important and especially in children with rheumatoid
arthritis like juvenile idiopathic arthritis. Thus, more re-
search on the role of diet on bone health is required. In
addition, more emphasis should be placed on under-
standing the role of diet and nutrition on bone health
during childhood and adolescence.
5. Conclusion
This study showed that in children with JIA, adequate
dietary intake of proteins and magnesium can have a
beneficial effect on the bone mass; low dietary intake of
vitamin C, vitamin E and folate ex erts positive effects on
BMD; but further studies are needed to confirm this as-
sociation.
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