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International Journal of Gynecology and Obstetrics Research

Vol. 2(2), pp. 018-023, August, 2015. www.premierpublishers.org ISSN: 1407-8019

IJGOR

Research Article

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
21589, Saudi Arabia

80215, Jeddah

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

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: 014). 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; HolmbergMarttila 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 socioeconomic 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 D25OHD) 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 Tscores, 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.

Bone health of postpartum women

Int. J. Gynecol. Obstet. Res.

019

Table 1. Demographic characteristics of postpartum women (90)

Demographic characteristics
Age
Gravida
Para:
0-1
2-4
>/5
Weight kg
Height m
BMI
Antenatal visits
Birth weight gm

Mean
28.2
3.7

Standard deviation/SEM
6.3/0.73
2.7/0.29

41 (45.6%)
33 (36.7%)
15 (16.7%)
1: missing data
69.69
1.54
28.3
2.5
3000

1.6/1.7
1.76/1.88
5.18/0.56
1.87/0.198
0.52/0.27

Table 2. The mean of postpartum serum bone profile, serum turnover markers and BMD

Test
Serum Calcium
Serum Phosphate
Alkaline phosphate
25 OH vitamin D
Osteocalcin
CTx
BMD spine
Tscore spine
Zscore spine
BMD left femur
BMD right femur

Mean
2.48
1.105
172.69
35.35
11.01
2.93
0.88
1.54
1.46
0.802
0.78

Standard Deviation
0.08
0.172
5.9
1.98
7.24
3.16
0.099
0.85
0.83
0.095
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.

Bone health of postpartum women

Mansouri et al. 020

Table 3. Correlation between BMD and other independent variables after adjusting for ageand BMI.
Variable
Number of pregnancies
Parity
Lactation (month )
CTX PP
Osteocalcin pp
25-OH Vitamin D3

r
0.26
0.72
-0.88
0.13
-0.56
-0.44

P value
0.7
0.3
0.1
0.9
0.4
0.6

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
age & BMI

Correlation
Sign (2-tailed)
Correlation
Sign (2-tailed)
Correlation
Sign (2-tailed)
Correlation
Sign (2-tailed)
Correlation
Sig (2-tailed)
Correlation
Sign (2-tailed)
Correlation
Sign (2-tailed)

P
Lactation
month
BMD
CTXPP
Osteopp
vitD

G
1.000
.
.686
.314
-.255
.745
.256
.744
.439
.561
.588
.412
-.786
.214

P
.686
.314
1.000
.
-.868
.132
.724
.276
-.101
.899
-.168
.832
-.938
.062

Lactation
month
-.255
.745
-.868
.132
1.000
.
-.883
.117
.298
.702
.630
.370
.676
.324

BMD
.256
.744
.724
.276
-.883
.117
1.000
.
.125
.875
-.558
.442
-.442
.558

CTX-PP
.439
.561
-.101
.899
.298
.702
.125
.875
1.000
.
.555
.445
.161
.839

Osteo-pp
.588
.412
-.168
.832
.630
.370
-.558
.442
.555
.445
1.000
.
-.088
.912

vitD
-.786
.214
-.938
.062
.676
.324
-.442
.558
.161
.839
-.088
.912
1.000
.

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

(Constant)
BMI

Unstandardized Coefficients
B
Std. Error
.627
.071
.009
.002

Standardized
Coefficients
Beta
.451

t
8.886
3.610

Sig.
.000
.001

95.0% Confidence Interval for B


Lower Bound
Upper Bound
.485
.768
.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 25OHvitamin 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

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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

Pair 1

Osteocalcin (pp)
Osteocalcin (12m)

Mean
11.0109
12.9783

Std. Deviation
7.24002
8.09034

St d. Error Mean
1.50965
1.68695

Paired Samples Test

Paired Differences
95% Confidence Interval of
Std.
Error the Difference
Mean
Std. Deviation Mean
Lower
Upper
t
Pair 1 Ost pp - Ost.12m -1.96741 7.98775
1.66556
-5.42157
1.48675
-1.181

df
22

Sig. (2-tailed)
.250

df

Sig. (2-tailed)

21

.065

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

Pair 1 CTXPP
CTx12m

Mean

Std.
Deviation

Std.
Mean

-2.60955

6.29752

1.34264

95% Confidence Interval of


Error the Difference
Lower
Upper
t
-5.40171

.18262

-1.944

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 womens 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/

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 openaccess 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.

Bone health of postpartum women

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