- The study examined the effect of pregnancy on bone mineral density (BMD) and bone turnover markers in 80 postpartum women in Saudi Arabia. - Biochemical tests found that 64 women (80%) had low BMD, with 16 (25%) having osteoporosis. Vitamin D levels were deficient in 35.37% of women. - BMI was the only predictor of BMD based on multiple regression analysis. No significant differences were found in bone markers between immediate postpartum and 12-month follow up for 27 women. - The study concluded osteoporosis/osteopenia is a significant health problem in this group of postpartum women and further studies are needed.

1. Bone health of postpartum women
IJGOR
Bone health of postpartum women: Unexpected high
prevalence of a health problem in Saudi postpartum
women
Haifaa A Mansouri1*
, Sawsan Ashor2
, Nashwa AlDardeir3
, Hassan Nasrat4
, Rajaa AlRaddadi5
,
Hashim Sindi6
and Samera AlBasri7
1*,2,3,4,5,6,7
Department of Obstetrics and Gynecology, King Abdulaziz University Hospital, P.O Box 80215, Jeddah
21589, Saudi Arabia
The aim was to see the effect of pregnancy on Bone Mineral Density (BMD) and bone turnover
markers (BTMs) in the immediate postpartum period and 12 months thereafter. Eighty women
delivered at KAUH (May 2009-Oct 2010) had BMD, bone profile, 25-OH vitamin D and (BTMs).
Inclusion criteria: Singleton pregnancy without medical or pregnancy complications. Exclusion
criteria: multiple pregnancies, history of diabetes thyroid or bone disease, and use of any
medication that affect calcium metabolism.
Biochemical tests were repeated for 27 women after one year. Statistical analysis was done using
SPSS 16. Eighty women had BMD before discharge. Sixty four women (80%) had low BMD; sixteen
of these (25%) had osteoporosis. Although bone profiles were normal, Vitamin D levels were
moderately or severely deficient in 35.37% of women. After adjustment for BMI and age there was
no correlation between BMD and other variables. Multiple linear regressions showed that BMI was
the predictor for BMD (P=0.0014). There was no significant difference between postpartum bone
BTMs and bone profiles, and those after twelve months.
Osteoporosis/ osteopenia is a significant health problem in this group of women. Further studies
are needed to look into predisposing factors.
Key words: Osteoporosis, osteopenia, postpartum, Bone Mineral Density (BMD), Bone Turnover Markers (BTM), 25
OH vitamin D
INTRODUCTION
Osteoporosis is a major health problem affecting a large
sector of population leading to devastating disabilities
including inability to walk and requiring long term care
and that can also be a burden on costs of health care
(Riggs and Melton, 1995; Consensus Conference From
the National Institutes of Health, 2001; Cooper et al.,
1993)
Sadat-Ali M et al., (2004) reported a prevalence of
osteoporosis (46.7%) in a group of Saudi
postmenopausal women. Similarly, Ghannam et al.,
(1999) estimated the prevalence of osteopenia and
osteoporosis in a group of Saudi female subjects>/=31
years old to be18-41% and 0-7%, respectively, and
related that to increased number of pregnancies and
longer duration of lactation.
Corresponding Author: Haifaa Mansouri, Associate Professor,
Department of Obstetrics and Gynecology, King Abdulaziz
University Hospital, P.O Box 80215, Jeddah 21589, Saudi
Arabia. E-mail: hajmansouri@gmail.com, Tel: +96626408382,
Fax: +96626991443
International Journal of Gynecology and Obstetrics Research
Vol. 2(2), pp. 018-023, August, 2015. © www.premierpublishers.org ISSN: 1407-8019 x
Research Article

2. Bone health of postpartum women
Mansouri et al. 018
Previous studies have provided conflicting findings on the
long-term effects of pregnancy and lactation on bone
mineral density (BMD, g/cm2). Two retrospective
(Sowers, et al., 1993; Parra-Cabrera, et al., 1996) and
one prospective. (Black, et al., 2000) studies, showed
that number of pregnancies and lactation had a
deleterious effect on BMD with an average loss of 4.8,
3.5% loss at femoral neck and spines.
On the other hand, other investigators, found no relation
between pregnancy, lactation and BMD. ( Sowers et al.,
1991; Tuppurainen et al.,1995; Laskey et al., 1997)
Berehi et al.,(1996) found no significant influence on
BMD of the number of children, when they studied 159
Omani women with a high average number of children of
5 (range: 0–14). To the contrary, a large retrospective
study of 2230 women aged <65 years showed that each
additional birth conferred a 1.4% increase in distal radial
bone density, (Fox et al., 1993). Even These variations in
reporting the effects of pregnancy and lactation on BMD
could be explained by the fact that investigators had
studied different sites for bone densities, (Olausson et al.,
2008). Some of these studies suggested that bone
density may decrease in skeletal regions rich in
trabecular bone, such as the spine and hip (More et al.,
2001; Pearson et al., 2004; Ulrich et al., 2003; Kaur et al.,
2003; Naylor et al., 2000; Prentice, 2003; Holmberg-
Marttila et al., 2000). with either no change or an increase
in regions rich in cortical bone, (Ulrich et al., 2003). In
addition, these studies have suggested that there is
considerable variation between women in the skeletal
response to pregnancy, for reasons that are unclear,
(Kaur et al., 2003; Naylor et al., 2000; Prentice et al.,
2003; Holmberg-Marttila et al., 2000; Prentice, 2003
suppl). LM Paton et al., (2003). in their unique study of
twin pairs (study 1, 2, 3), which thus eliminating genetic
factors and partially also environmental effects, observed
that there were no significant within-pair differences in
BMD between parous and nulliparous women (study 1,
included: 83 women>18 years).
This study was done to prospectively evaluate the effect
of pregnancy and lactation on bone health postpartum
and after twelve months.
MATERIAL AND METHODS
The study was approved by the ethical committee of King
Abdul-Aziz University Hospital. Women delivered
normally at King Abdul-Aziz University between May 16/
2009 to July 20/2010, were recruited, the inclusion
criteria used were: singleton full term pregnancy, no
medical or pregnancy complications, no history of bone
disease, and no history of use of medications for bone
disease (e.g. steroids) other than regular ante natal
supplements including iron and a daily dose of calcium
carbonate (600mg), women with multiple pregnancy,
bone disease, or on steroids were excluded.
After obtaining an informed consent, these women were
tested for bone profile, 25 OH vitamin D, bone turn-over
markers and BMD. The demographic data of these
women included: age, parity BMI, and ethnicity.
Behavioral history included smoking, exposure to sun,
and dietary calcium which was assessed by the
interviewer and considered adequate if daily intake was
equivalent to 1200 mg/day).
These women were advised to come back for follow up, 6
weeks postpartum and after one year. Despite the clear
and long discussion and encouragement to come for
follow up, only 27 women came because of difficulty
coming to hospital ( nobody to look after the children
,difficult or expensive transport, illiterate or low socio-
economic status). These were tested for bone profile and
BTM.
The methodology of the tests of the study was done as
follows:
The bone turnover markers were analyzed manually by
ELISA (Enzyme Linked Immuno Sorbent Assay) for both
Osteocalcin (serum biomarker of bone formation and CTx
(C-terminal telopeptide -serum biomarker of bone
turnover ). Vitamin D level ( 25 hydroxy vitamin D-
25OHD) was measured and analyzed using automated
based ECL (Electro-Chem-Liumencint) technique in
Modular system. Bone profile included: serum Calcium,
Phosphate, Total Proteins, Albumin and Alkaline
phosphatase, and it was analyzed using a method of
automated based on Spectrophotometer in Dimension
System.
Bone mineral density was measured by DXA (Lunar MD
with software 4.7e; GELunar Corporation, Madison, WI).
The interpretation of the reports was done using WHO
criteria for defining normal or abnormal scores. Although
the reference values of postpartum women is not known,
and because the relationship between BMD and fracture
risk is not well established in this population, Writing
Group for the ISCD Position Development Conference
Diagnosis of osteoporosis in men, premenopausal
women, and children, (2004). Z-scores ≤-2.0 , not T-
scores, will be used in this group as recommended by
WHO and The International Society for Clinical
Densitometry (ISCD), (Binkley et al., 2007).
The statistical analysis used was the paired t-test to
compare the means of bone profile and BTMs of
postpartum women to those after 12 months.
The effect of age, parity, weight, height, BMI, antenatal
visits, birth weight ,on BMD, BTM, Bone profile and 25
OH vitamin D will be studied using multiple regression
analysis using SPSS 16. The mean BMI of the study
group will be used as an independent variable.

3. Bone health of postpartum women
Int. J. Gynecol. Obstet. Res. 019
Table 1. Demographic characteristics of postpartum women (90)
Demographic characteristics Mean Standard deviation/SEM
Age 28.2 6.3/0.73
Gravida 3.7 2.7/0.29
Para:
0-1
2-4
>/5
41 (45.6%)
33 (36.7%)
15 (16.7%)
1: missing data
Weight kg 69.69 1.6/1.7
Height m 1.54 1.76/1.88
BMI 28.3 5.18/0.56
Antenatal visits 2.5 1.87/0.198
Birth weight gm 3000 0.52/0.27
Table 2. The mean of postpartum serum bone profile, serum turnover markers and BMD
Test Mean Standard Deviation
Serum Calcium 2.48 0.08
Serum Phosphate 1.105 0.172
Alkaline phosphate 172.69 5.9
25 OH vitamin D 35.35 1.98
Osteocalcin 11.01 7.24
CTx 2.93 3.16
BMD spine 0.88 0.099
Tscore spine 1.54 0.85
Zscore spine 1.46 0.83
BMD left femur 0.802 0.095
BMD right femur 0.78 0.155
NB:
Serum calcium: Normal range (2.12-2.52 mmol/l)
Serum phosphate (PO4): Normal range (0.8-1.58 mmol/l)
Alkaline phosphatase: Normal range ( 50-136 U/l )
25 hydroxy vitamin D: Normal range (75-200 nmol/l)
Serum osteocalcin: Normal range ( 4-15 ng/ml)
Serum CTx: Normal range (0.1-1.27 ng/ml)
RESULTS
Ninety women, who delivered spontaneously and have
no antenatal complications, were recruited for the study.
Ten of these women were discharged before BMD
studies were done.
The demographic data of these women were shown in
Table 1. More than 50% of the study group were
multigravidas (54.4%).Three women were black, two
were Asians, and only one was Mediterranean and the
rest were Saudi citizens ( not included in the table). The
mean BMI of the study group was 28.3%. Of the women
studied, 53 % had adequate dietary calcium intake but
only three (3.33%) continued regular calcium
supplements throughout pregnancy.
All postpartum values of the bone profile of these women
were within normal range. The mean of postpartum
serum 25 OH vitamin D was 35.35 nmol /l (Normal 75-
200 nmol/l). Only Three women (3.33%) had normal 25
OH vitamin D, while fifty (55.56%) had mild deficiency
(25-75 nmol/l), and twenty nine (32.22%) had moderate
(12.5-25 nmol/l) to severe (<12.5 nmol/l) deficiency. Eight
values were missing (8.89%).
The mean serum level of osteocalcin and CTx were
11.01 ng/ml (Normal 4-15 ng/ml) and mean serum CTx
level was 2.93 (Normal o.1- 1.27) respectively. Twenty
four women (26.67%) had osteocalcin levels higher than
normal, while most postpartum women (81.33%) had
higher values than normal of CTx bone resorption
marker.
The BMD, T and Z score of lumbar spine, and BMD of
the neck of the femur (left and right) of these women was
shown in Table 2. According to WHO criteria and Using
ISCD cut-off Z score of =/<-2.0, it was observed that
osteoporosis was present in 16 (17.78%) and osteopenia
in 48 (53.3%) women as interpreted by the radiographer.

4. Bone health of postpartum women
Mansouri et al. 020
Table 3. Correlation between BMD and other independent variables after adjusting for ageand BMI.
P valuerVariable
0.70.26Number of pregnancies
0.30.72Parity
0.1-0.88Lactation (month )
0.90.13CTX PP
0.4-0.56Osteocalcin pp
0.6-0.4425-OH Vitamin D3
Where r is the correlation coefficient
BMD: the dependent variable
CTx pp: CTx postpartum
Osteocalcin pp: osteocalcin postpartum
Table 4. Correlation between BMD and other variables after adjusting for age and BMI.
Control Variables
G P
Lactation
month BMD CTX-PP Osteo-pp vitD
age & BMI G Correlation 1.000 .686 -.255 .256 .439 .588 -.786
Sign (2-tailed) . .314 .745 .744 .561 .412 .214
P Correlation .686 1.000 -.868 .724 -.101 -.168 -.938
Sign (2-tailed) .314 . .132 .276 .899 .832 .062
Lactation
month
Correlation -.255 -.868 1.000 -.883 .298 .630 .676
Sign (2-tailed) .745 .132 . .117 .702 .370 .324
BMD Correlation .256 .724 -.883 1.000 .125 -.558 -.442
Sign (2-tailed) .744 .276 .117 . .875 .442 .558
CTXPP Correlation .439 -.101 .298 .125 1.000 .555 .161
Sig (2-tailed) .561 .899 .702 .875 . .445 .839
Osteopp Correlation .588 -.168 .630 -.558 .555 1.000 -.088
Sign (2-tailed) .412 .832 .370 .442 .445 . .912
vitD Correlation -.786 -.938 .676 -.442 .161 -.088 1.000
Sign (2-tailed) .214 .062 .324 .558 .839 .912 .
Osteo-pp: osteocalcin postpartum
CTx-pp: CTx postpartum
Table 5. Multiple linear regressions showed that BMI was a significant predictor for BMD. Variables in the model included parity, gravidity,
BMI, Age, & vitamin D.
Coefficientsa
Model
Unstandardized Coefficients
Standardized
Coefficients
t Sig.
95.0% Confidence Interval for B
B Std. Error Beta Lower Bound Upper Bound
1 (Constant) .627 .071 8.886 .000 .485 .768
BMI .009 .002 .451 3.610 .001 .004 .014
a. Dependent Variable: BMD
A correlation was done between the BMD and the
demographic data (including: number of pregnancies,
parity, number of months of lactation and serum 25OH-
vitamin D3) and after adjustment for BMI and age there
were no significant correlation between BMD and other
variables, Table 3 and 4. Multiple linear regression
showed that BMI was a significant predictor for BMD
(P=0.001). Variables in the model included parity,
gravidity , BMI, Age, and vitamin D, Table 5.
Twenty seven women came for follow up. The mean
serum level of osteocalcin and CTx was 12.98 ng/ml and
5.54 ng/ml, respectively.
Using paired t-test, there was no significant difference of
serum level of bone turnover markers (osteocalcin and
CTx) twelve months after delivery when compared to
those within the first few days postpartum (P value= 0.25,
and 0.065) respectively, Table 6 and 7 respectively. But it
is observed that the mean level at 12 months after

5. Bone health of postpartum women
Int. J. Gynecol. Obstet. Res. 021
Table 6. Paired t-test comparing postpartum levels of osteocalcin & CTx to their levels after one year
Paired Samples Statistics
Mean Std. Deviation St d. Error Mean
Pair 1 Osteocalcin (pp) 11.0109 7.24002 1.50965
Osteocalcin (12m) 12.9783 8.09034 1.68695
Paired Samples Test
Paired Differences
t df Sig. (2-tailed)Mean Std. Deviation
Std. Error
Mean
95% Confidence Interval of
the Difference
Lower Upper
Pair 1 Ost pp - Ost.12m -1.96741 7.98775 1.66556 -5.42157 1.48675 -1.181 22 .250
Osteocalcin postpartum (Ost pp)
Osteocalcin after 12 months (Ost.12m)
Table 7. Paired t-test comparing postpartum levels of CTx to their levels after one year
Mean Std. Deviation Std.Error Mean
Pair 1 CTXPP 2.9268 3.16390 .67455
CTx12m 5.5364 6.21040 1.32406
Paired Samples Test
Paired Differences
t df Sig. (2-tailed)Mean
Std.
Deviation
Std. Error
Mean
95% Confidence Interval of
the Difference
Lower Upper
Pair 1 CTXPP -
CTx12m
-2.60955 6.29752 1.34264 -5.40171 .18262 -1.944 21 .065
CTx postpartum (Ost pp)
CTx after 12 months (Ost.12m)
delivery was almost twice (1.9 times) more than
postpartum levels, but did not reach statistical
significance which may suggest increased bone
resorption, but the number was small.
DISCUSSION
It is noticed from this study that the prevalence of Low
Bone Density (osteopenia/ osteoporosis) is high in this
group of Saudi women (71.11%). This finding was
immediately postpartum which denotes that the loss
occurred prior to delivery: either during pregnancy or
before pregnancy. A BMD study before pregnancy would
have helped to differentiate between these two.
A high prevalence of osteoporosis in postmenopausal
women was reported (Sadat-Ali et al., 2004) to be 46.7%,
the rate in this study was even higher in these
postpartum women.
This finding (this color 24062014) may suggest indirectly
that a low BMD during the women’s reproductive years
could be a predictive factor for future osteoporosis/
osteopenia in postmenopausal women. A BMD of
Japanese women postpartum and a repeat after 5-10
years, demonstrated that 71% who had been osteopenic
or osteoporotic postpartum remained so after
menopause, (Wu XP et al., 2004). A low BMD of Saudi
women could be normal to this population age group, and
some investigators suggested to compare the BMD of
postmenopausal women to this young age group, before
diagnosing osteopenia/osteoporosis,(Ardawi et al., 2004).
Another explanation is that the age of peak bone mass
could be at older age than expected depending on racial
or ethnic background, ,(Ardawi et al., 2004; Johansen et
al., 1988). Severe vitamin D deficiency and low calcium
intake were, among other factors, that might explain why
adolescents did not achieve their genetic potential for
calcium deposition and bone health and metabolism.
With the presence of high estrogen levels during
pregnancy and the marked decrease in level during
lactation, it was commonly hypothesized that lactation
was the culprit of low BMD and or osteopenia/

6. Bone health of postpartum women
Mansouri et al. 022
osteoporosis. In this study the osteopenia/ osteoporosis
complex was present before lactation even started. What
caused that was it due to low BMD before pregnancy, or
during adolescent period, and or the effect of substrate
deficiencies essential for bone metabolism. These were
some of the areas thought need to be studied in the
future.
CONCLUSION
Low Bone Density, including Osteoporosis is a
significant health problem in this group of women. More
studies are needed to look into factors that increases the
risk in this young group of patients .Could that be related
to poor attainment of PBM or early pregnancy in
adolescent age or to high parity or the known factors in
this population including poor dietary calcium, lack of sun
exposure or lack of exercise. Further studies are needed
to look into these factors.
Conflict of Interest Statement
We declare that we have no conflict of interest.
ACKNOWLEDGEMENT
This project had been funded by deanship of Scientific
Research (DSR) / King Abdul-Aziz University, under
grant number (5/007/429). Therefore we acknowledge
with thanks DSR support for scientific research. Special
thanks are to Miss Manal Baklo to her help in obtaining
data.
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Accepted 20 August, 2014
Citation: Mansouri HA, Ashor S, AlDardeir N, Nasrat H,
AlRaddadi R, Sindi H, AlBasri S (2015). Bone health of
postpartum women: Unexpected high prevalence of a
health problem in Saudi postpartum women. International
Journal of Gynecology and Obstetrics Research, 2(2):
018-023.
Copyright: © 2015 Mansouri et al. This is an open-
access article distributed under the terms of the Creative
Commons Attribution License, which permits unrestricted
use, distribution, and reproduction in any medium,
provided the original author and source are cited.