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Nutritional risk factors for postmenopausal
osteoporosis
Olfa Berriche, Amrouche Chiraz, Rym Ben Othman
*
, Hamdi Souheila, Ines Lahmer,
Chaabani Wafa, Imen Sebai, Haifa Sfar, Feten Mahjoub, Henda Jamoussi
Department A, National Institute of Nutrition, Tunis, Tunisia
Received 12 February 2016; revised 26 March 2016; accepted 31 March 2016
KEYWORDS
Osteoporosis;
Menopause;
Risk factors;
Nutrition
Abstract Background: Osteoporosis is a bone disease that combines both a decrease in bone den-
sity and its internal architecture changes. Nutrition is one of the major determinants of osteoporo-
sis.
Aim: The purpose of our study was to identify nutritional risk factors of osteoporosis of two
groups of osteoporotic women and witnesses.
Methods: We conducted a comparative cross-sectional study including 60 postmenopausal women
and screening for osteoporosis by a bone densitometry, recruited the outpatient service of Rheuma-
tology of the Institute KASSAB.
Results: We have identified excessive supply of saturated fatty acids (SFA) in the osteoporotic
compared with controls (13.27% vs 10.23%, p= 0.002) and an inadequate intake of monounsat-
urated fatty acids (MUFA) (12.6% vs 16.16%, p= 0.012).
A low calcium intake is another factor of risk of osteoporosis (574.27 ± 336.9 mg/day vs 782.45
± 340.54 mg/day; p= 0.021). This is explained by the low consumption of milk and milk products
objectified in the osteoporotic group (p= 0.001). We also found a negative relationship between
inadequate intakes of potassium and osteoporosis (2241.55 ± 1049.85 mg/day vs 2988.17
± 1146.52 mg/day; p= 0.011). This may be due to the low consumption in fruit and vegetables,
sources of potassium, found in the osteoporotic group (p= 0.003).
We found a significant increase in the consumption of the VVPO group in the osteoporotic toward
women witness (2.23 ± 0.99 number of times/day vs 1.67 ± 0.76 number of times/day; p= 0.019).
A high consumption of coffee appears also as a risk factor since the osteoporotic group consume
almost twice than controls (p= 0.002).
Conclusion: Nutritional risk factors of osteoporosis are all the most important that they are edita-
ble and can take their place in a prevention of public health policy.
Ó2016 Alexandria University Faculty of Medicine. Production and hosting by Elsevier B.V. This is an
open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
*Corresponding author. Tel.: +216 52262806.
E-mail address: benothmanr@gmail.com (R.B. Othman).
Peer review under responsibility of Alexandria University Faculty of Medicine.
Alexandria Journal of Medicine (2016) xxx, xxx–xxx
HOSTED BY
Alexandria University Faculty of Medicine
Alexandria Journal of Medicine
http://www.elsevier.com/locate/ajme
http://dx.doi.org/10.1016/j.ajme.2016.03.007
2090-5068 Ó2016 Alexandria University Faculty of Medicine. Production and hosting by Elsevier B.V.
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Please cite this article in press as: Berriche O et al. Nutritional risk factors for postmenopausal osteoporosis, Alex J Med (2016), http://dx.doi.org/10.1016/j.
ajme.2016.03.007
1. Introduction
Osteoporosis is a broadcast disease of the skeleton character-
ized by low bone mass and abnormal microarchitecture,
responsible for an increase in bone fragility.
1
Osteoporosis
greatly affects the health of postmenopausal women and is rec-
ognized as a major public health problem worldwide.
2
The evaluation of bone mineral density (BMD) surface
X-ray absorptiometry dual energy is currently used to retain
the diagnosis of osteoporosis and low BMD is the main risk
factor for the occurrence of fracture complications.
3
The determinism of osteoporosis is multifactorial, domi-
nated by genetic factors controlling bone metabolism. Among
the exogenous factors, nutrient intakes play an important role
appeared to be a target for cheaply therapeutic measures.
Besides the calcium and vitamin D, widely known as key com-
ponents of the metabolic bone, other nutrients may intervene
in a non negligible way the changes in bone mass. Thus
micronutrients and vitamins other than vitamin D, are sub-
stances essential to the success of numerous stages of bone
metabolism.
4
The objectives of our study were to determine nutritional
risk factors for osteoporosis by comparing two groups of
women with osteoporosis and controls.
2. Methods
This is a comparative cross sectional study involving 60 post-
menopausal women, recruited from outpatient in a rheumatol-
ogy service in Tunis, over a period of three months from
December 2014 to March, 2015.
Women over the age 50 and postmenopausal for at least
5 years were included in this study. Women with hormonal dis-
eases (hyperthyroidism, hyperparathyroidism) or inflamma-
tory rheumatic diseases (rheumatoid arthritis, ankylosing
spondylitis) or heparin or in some antiepileptic or in oral anti-
coagulants were excluded from the study.
Our population has been screened for osteoporosis by
BMD and was distributed into two groups according to the
results of this review.
The ‘‘control”group consisted of 30 women with a T-score
at the lumbar spine or hip to the upper 1 and group ‘‘case”
consists of 30 women with osteoporosis with a T-score at the
lumbar spine or hip or less equal to 2.5.
All women underwent anthropometric measurements
(weight in kilograms (Kg), height in meters (m), the calculation
of BMI body mass index).
A food survey was conducted using the recall method 24 h
and food consumption frequency specifying the changes in eat-
ing habits over the past ten years, the overall caloric intake, the
shares of major nutrients (carbohydrates, fat, saturated fatty
acids (SFA), monounsaturated fatty acids (MUFA), polyun-
saturated fatty acids (PUFAs), protein, animal protein (PA)
and vegetable protein (PV)), mineral intake, vitamins and
fiber.
We used a questionnaire, referred to the National Health
and Nutrition Program (PNNS), which consists of 20 items
that match the majority of foods that may be consumed, gath-
ered in groups 6 groups: milk and dairy products, meat, poul-
try, fish, eggs (MPFE), Fruits and vegetables, legumes and
starchy foods, drinks: coffee, tea and soft drinks, oil seeds
and olive oil.
5
.
In order to convert the intake of food nutrients we per-
formed a manual calculation using the food composition table
CIQAUL 2013.
3. Statistic study
We undertook a descriptive statistical analysis of both groups,
and a multivariate analysis using SPSS v 17.0 software.
In all comparisons, the level of significance was set at 0.05.
4. Results
The average age of the population is 56 years, and it is compa-
rable in both groups. However, the age of menopause is earlier
in the osteoporotic group compared with the control group
(p= 0.011) (Table 1).
Food survey found that the majority of the population
(71.7%) did not change their eating habits over the past ten
years, allowing to reflect the nutritional profile of our sample.
Thus, we found no significant difference between the two
groups (Table 2).
The average calorie intake was similar in both groups; it is
2131.43 ± 782.34 kcal/day in osteoporotic group and 2097.61
± 706.49 kcal/day in control and follows the recommenda-
tions of the AFSSA 2010.
6
As regards protein intake, it is
excessive in both groups and PA/PV ratio is greater than 1
(Table 3).
PUFA intakes reduced in osteoporotic group benefit contri-
butions in AGS are high. However, the intake of MUFA, was
significantly lower in osteoporotic group compared with con-
trols (12% vs 16.16%, P= 0.012) (Table 3).
The dietary fiber intake was comparable in both groups and
is below the recommendations of the AFSSA 2010.
The average calcium intake in osteoporotic group is signif-
icantly lower than that of controls (574.27 ± 336.90 mg/day vs
782.45 ± 340.54 mg/day; p= 0.021). Similarly, the average
intake of potassium was significantly lower in osteoporotic
women compared to controls (2241.55 ± 1049.85 mg/day vs
2988.17 ± 1146.522 mg/day; p= 0.011) (Table 4).
The average daily intake of copper, magnesium and phos-
phorus is lower in osteoporotic group than in controls, but
with no significant difference.
We found a dietary insufficiency of vitamin D in two
groups. However, these contributions are more important in
comparison with osteoporotic witnesses, but without signifi-
cant difference (Table 4).
The frequency of consumption of milk and dairy products
was significantly lower in osteoporotic group than in controls
(p= 0.001). However, daily consumption of meat is more
Table 1 General characteristics of the population.
Characteristics Cases Controls p
Age (years) 56.2 ± 3.74 56 ± 3.97 0.8
BMI (Kg/m
2
) 27.3 ± 5.27 28.21 ± 5.21 P= 0.503
Age at menopause
(years)
43.26 ± 3.91 45.66 ± 3.07 0.011
2 O. Berriche et al.
Please cite this article in press as: Berriche O et al. Nutritional risk factors for postmenopausal osteoporosis, Alex J Med (2016), http://dx.doi.org/10.1016/j.
ajme.2016.03.007
common in women with osteoporosis than in controls. Thus,
the total consumption frequency of MPFE group is signifi-
cantly higher in women with osteoporosis (p= 0.019). As
for the consumption of fruits and vegetables, it is significantly
lower in osteoporotic group compared to controls (0.002). Caf-
feine consumption frequency is doubled in osteoporotic group
(1.23 ± 0.87/0.61 ± 0.56 vs j/d; p= 0.002) (Table 5).
5. Discussion
The intake of saturated fatty acids (SFA) was significantly
higher in osteoporotic group compared to controls (13.27%
vs 10.23%, P= 0.02). This value is above the recommenda-
tions of the AFSSA, which advocates limiting total intake of
SFA to 12% of total fat intake.
The intake of monounsaturated fatty acids (MUFA) is
otherwise significantly lowered in osteoporotic women
(12.60% vs 16.16%, p= 0.012). From a qualitative stand-
point, clinical and preclinical studies have demonstrated that
the effect of the lipid on the bone varies depending on the
degree of saturation and the length of fatty acid chains.
Indeed, several studies have shown that a diet rich in saturated
fatty acids resulted in a decrease in calcium absorption and
decreased bone mineralization.
8
The literature has largely
related fat intake and the inflammatory status, a key player
involved in bone resorption. Presumably, Lipids have a duality
of action, sometimes with the pro and sometimes anti-
Table 4 Average daily intakes of micronutrients.
Controls (n= 30) Cases (n= 30) P
m±ET m±ET
Calcium (mg/J) 782.45 ± 340.54 574.27 ± 336.90 0.021
Copper (mg/J) 1.49 ± 1.51 1.13 ± 0.51 0.22
Iron (mg/J) 9.11 ± 3.09 9.03 ± 4.36 0.939
Magnesium (mg/J) 245.53 ± 74.80 232.01 ± 112.72 0.586
Manganese (mg/J) 2.62 ± 1.09 2.79 ± 1.58 0.637
Phosphorus (mg/J) 1426.14 ± 564.69 1212.09 ± 619.53 0.167
Potassium (mg/J) 2988.17 ± 1146.52 2241.55 ± 1049.85 0.011
Sodium (mg/J) 2099.36 ± 943.61 1967.06 ± 985.11 0.597
Zinc (mg/J) 8.19 ± 3.28 7.94 ± 3.90 0.783
Vitamin A (ER/J) 1230.21 ± 880.1 1044.51 ± 852.99 0.410
Vitamin B6 (mg/J) 1.71 ± 0.79 1.48 ± 1 0.338
Vitamin C (mg/J) 141.79 ± 96.55 115.82 ± 78.13 0.257
Vitamin K (lg/J) 15.35 ± 18.72 10.29 ± 15.29 0.257
Vitamin D (lg/J) 2.68 ± 4.55 2.35 ± 3.57 0.754
Table 3 Daily intake of energy and micronutrient.
Controls (n= 30) Cases (n= 30) P
m±ET m±ET
Caloric intakes (kcal/J) 2097.62 ± 706.5 2131.44 ± 782.34 0.861
Carbohydrates (g/J) 259.683 ± 88.992 253.01 ± 94.64 0.779
Lipids (g/J) 82.46 ± 38.86 88.65 ± 42.60 0.559
SFA
a
(g/J) 28.12 ± 14.23 39.21 ± 22.25 0.002
(%) 10.23 13.27
MUFA
b
(g/J) 44.44 ± 42.15 37.24 ± 23.25 0.012
(%) 16.16 12.6
PUFA
c
(g/J) 9.89 ± 12.56 12.19 ± 10.23 0.389
(%) 3.61 4.13
Proteins (g/J) 79.18 ± 32.29 80.37 ± 40.74 0.901
Fiber (g/J) 21.88 ± 7.23 21.72 ± 9.80 0.942
a
SFA: saturated fatty acids.
b
MUFA: monounsaturated fatty acids.
c
PUFA: polyunsaturated fatty acids.
Table 2 Change in eating habits before screening for
osteoporosis.
Change in eating habits Total
No Yes
Group Controls Effective 21 9 30
% 70% 30% 100%
Cases Effective 22 8 30
% 73.3% 26.7% 100%
Total Effective 43 17 60
% 71.7% 28.3% 100%
Risk factors for osteoporosis 3
Please cite this article in press as: Berriche O et al. Nutritional risk factors for postmenopausal osteoporosis, Alex J Med (2016), http://dx.doi.org/10.1016/j.
ajme.2016.03.007
inflammatory effects depending on their structures and their
metabolisms.
Studies reporting a correlation between the protein intake
and bone metabolism showed that an excess of a protein defi-
ciency caused an imbalance in the calcium balance. An
increase in protein intake increases the acid load to be removed
by the kidney and urinary calcium loss. We can estimate that a
doubling of the protein intake increases calcium excretion by
50%.
7
Indeed, the calcium/protein is the most important deter-
minant of bone acquisition during the third decade in women.
There is an inverse correlation between a high protein intake
and bone loss in women aged over 55 years.
8
It should be noted however that proteins must be sufficient
because a deficit is deleterious on bone metabolism, while any
excess not offset by increased intake of alkalizing foods is
unfavorable.
In most epidemiological studies, the increased risk of osteo-
porotic fractures is found in animal protein, and inversely cor-
related with the consumption of vegetable protein.
9
The results of a recent study showed among 457 women
aged 45–49 years that increased intake of dietary fiber
improves bone mineral density. However, other studies have
suggested that a diet rich in fiber (more than 40 g/day) may
impair the absorption of calcium.
7–10
Meanwhile, epidemiolog-
ical arguments are rather reassuring about the role of fiber in
the diet: three studies comparing women with vegetarian diets
and women with an omnivorous diet showed that women in
the first group showed no decrease in BMD.
11–13
Several studies have examined the relationship between
consumption of calcium and bone health. In 1990, a meta-
analysis of all published works on the relationship of calcium
intakes–bone mass found a positive relationship between the
two variables.
14
However, some research suggests that the
amount of calcium consumed is only moderately correlated
with bone health of the child or the adult
15
because calcium
is a threshold nutrient: beyond a swing value between 800
and 1200 mg/day, any additional increase in calcium consump-
tion does not seem to have any effect on bone tissue.
16
According to Lutz
17
Potassium can act on the bone through
its buffering capacity, that is to say its ability to compensate
for variations in pH, thus avoiding to request the bone calcium
in the event of excess of acidity. In fact, a synthesis of the
various recent studies suggests that an adequate intake of
potassium promotes renal calcium retention while a potassium
diet raises its urinary excretion.
Another study showed among 457 women aged 45–49 years
that the potassium intake reduction is associated with an
increased risk of osteoporotic fractures.
7
Vitamin D facilitates active uptake of calcium in the diges-
tive tract. This effect is more pronounced in case of low dietary
calcium intakes.
18
According to Dawson-Hughs et al.,
19
vita-
min D intake reduces the loss of winter bones and lowers the
high levels of PTH. Indeed, in a study carried out over three
years among 3270 women with an average age of 60, the extra
intake of calcium (1200 mg/day) and vitamin D (20 mg/day)
led to both a decrease of bone loss and fracture incidence at
the end of the first year.
20
Over the last thirty years, more than 250 ecological types of
observational studies, case-control and prospective have estab-
lished a relationship between the consumption of fruit and/or
vegetables and osteoporosis. In over 80% of them, a protective
effect of one or more fruit or vegetable groups was found.
21
A
growing number of studies in women describe a protection
effect against osteoporosis of fruit and vegetables at any age,
recently confirmed by the DASH intervention study that
showed a significant decrease in markers of bone turnover
related to an inadequate intake of fruits and vegetables.
22–23
Similarly, the Apple intervention study was a reduction of cal-
cium leakage in the kidneys when ingested daily serving of
fruits and vegetables pass from 3.6 to 9.5.
24
Fruit and vegetable consumption would by an alkalizing
effect and through various polyphenols to phyto-estrogenic
properties protect against osteoporosis. In addition, some
green leafy vegetables are significant sources of calcium. It is
clear that the available scientific data show a positive associa-
tion between the consumption of fruits and vegetables and a
reduced risk of the disease.
21
Although the bone protective role of calcium has been
widely demonstrated in several studies for decades, none of
the studies that have lingered to prove a link between the
consumption of dairy products and BMD could not conclude
a protective effect of this group food on bone health and the
preservation of bone mineral density in adulthood post-
menopausal women.
The lack of positive relationships between dairy consump-
tion and BMD could be explained by the involvement of some
factors that stimulate or inhibit the absorption of dairy
Table 5 Usual daily frequency of consumption of different
food groups.
Foods (number of
times/day)
Cases
(m± ET)
Controls
(m± ET)
P
Milk and milk products
Milk 0.87 ± 0.49 1.45 ± 0.85 0.002
Fermented milk 0.08 ± 0.07 0.17 ± 0.35 0.229
Yogurt 0.22 ± 0.25 0.43 ± 0.31 0.006
Cheese 0.23 ± 0.14 0.45 ± 0.32 0.001
Total 1.42 ± 0.72 2.51 ± 1.04 0.001
MPFE
a
Eggs 0.41 ± 0.27 0.35 ± 0.20 0.285
Meat and poultry 1.32 ± 0.77 0.83 ± 0.61 0.009
Fishes 0.16 ± 0.11 0.17 ± 0.11 0.803
Liver 0.08 ± 0.10 0.09 ± 0.08 0.751
Giblets 0.05 ± 0.06 0.05 ± 0.06 0.945
Total 2.23 ± 0.99 1.67 ± 0.76 0.019
Fruits and vegetables
Vegetables 0.85 ± 0.61 1.28 ± 0.68 0.012
Fruits 0.81 ± 0.73 1.51 ± 1.01 0.003
Total 1.66 ± 1.15 2.79 ± 1.47 0.002
Starchy foods and legumes
Bread 1.85 ± 0.78 1.53 ± 0.63 0.082
Cereals, pastas 1.03 ± 0.59 0.812 ± 0.48 0.132
Legumes 0.33 ± 0.13 0.28 ± 0.14 0.189
Total 3.22 ± 0.98 2.63 ± 0.78 0.014
Beverages
Soft drinks 0.23 ± 0.15 0.06 ± 0.07 0.001
Cafe
´1.23 ± 0.87 0.61 ± 0.56 0.002
Tea 0.65 ± 0.64 0.77 ± 0.67 0.487
Total 2.12 ± 0.86 1.45 ± 0.86 0.004
Olive oil 0.65 ± 0.80 0.87 ± 0.85 0.293
a
MPFE: meat, poultry, fish, eggs.
4 O. Berriche et al.
Please cite this article in press as: Berriche O et al. Nutritional risk factors for postmenopausal osteoporosis, Alex J Med (2016), http://dx.doi.org/10.1016/j.
ajme.2016.03.007
calcium and/or excretion; either a high protein intake, salt,
fiber, sugar or caffeine, or a reduced intake of vitamin D, K,
magnesium or phosphorus.
A study conducted by the University of California in 2001
found that women who got most of their protein from animal
sources had three times more bone loss and almost 4 times
more hip fractures than those obtained with the majority of
their protein from vegetable sources.
25
Among the five epidemiological studies that examined the
link between red meat consumption and bone mineral density,
ten of them have demonstrated the existence of a relationship
between a high protein intake and decreased bone mineral den-
sity.
26
Most epidemiological studies have highlighted the
potential risks from high consumption of meat on the develop-
ment of osteoporosis. However, other studies suggest that ade-
quate protein intake preserves greater bone mass.
27
Caffeine is an active substance with important physiologi-
cal effects. Consumed in adequate amounts, it is a nervous sys-
tem stimulant that reduces the perception of fatigue. We find
caffeine in coffee but also in tea, soft drinks and cocoa. Barger
et al have shown an increase in urinary calcium excretion dur-
ing caffeine ingestion.
28
Moreover, it was observed a positive
association between caffeine consumption and risk of fracture
at the hip. On the other hand, it has been demonstrated in
postmenopausal women consuming about 200 mg/day of caf-
feine and whose dairy consumption was irregular, a significant
decrease in BMD is noticed.
29–30
However, other epidemiolog-
ical studies found a positive association between tea consump-
tion and bone mineral density. This effect is explained by the
polyphenols, phytoestrogens, and fluoride in tea.
31
6. Conclusion
Nutrition is a major determinant of osteoporosis. Thus, aware-
ness of the protective role played by the power saw the emer-
gence of the concept of preventive nutrition that, given its
involvement in the acquisition of bone and its subsequent
preservation, it is obvious that the recommendations adapted
nutrition and nutrition education program targeting the gen-
eral population and particularly the population at risk would
pave the way for true prevention. Indeed, any prevention strat-
egy based on food will seek to overcome any deficiencies and
advise protective nutrients. It is therefore essential to promote
a diverse diet, following the major food balances, and this
throughout the life.
Prevention must be early because it promotes the acquisi-
tion of peak bone mass during the growing period and deter-
mines the speed of bone loss during aging.
Conflict of interest
Nothing to disclose.
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