Calcium supplementation, bone mineral density and bone
mineral content. Predictors of bone mass changes in
adolescent mothers during the 6-month postpartum period
SUMMARY. We determined the effect of calcium
supplementation on bone mineral density (BMD) and
bone mineral content (BMC) and identified predictors
of bone mass changes in adolescent mothers 6 months
postpartum. A prospective, analytical, clinical study
was performed in adolescent mothers (.19 years old;
n=37) from La Plata, Argentina. At 15 days postpartum,
mothers were randomly assigned into one of two
groups and started with calcium supplementation; one
group received dairy products (932 mg Ca; n=19) and
the other calcium citrate tablets (1000 mg
calcium/day; n=18). Weight, height and dietary intake
were measured and BMD was determined by DEXA
at 15 days (baseline) and 6 months postpartum. BMC,
total body BMD and BMD were assessed in lumbar
spine, femoral neck, trochanter and total hip. Regression
models were used to identify the relationship of
total body BMD and BMC with independent variables
(calcium supplementation, months of lactation,
weight at 6 months, percent weight change, lean mass
at 6 months, percent lean mass change, total calcium
intake). Results showed that changes in BMD and
BMC at the different sites were similar in both groups,
and changes in percent body weight and total calcium
intake were the main predictive factors. In conclusion,
the effect of calcium was similar with either form of
supplementation, i.e., dairy products or tablets, and
changes in percent body weight and total calcium intake
were predictors of total body BMD and BMC
Key words: Calcium supplementation, bone mineral
density, bone mineral content, adolescent mothers,
body composition, calcium citrate, dairy product.
RESUMEN. Suplementacion con calcio, densidad mineral
osea y contenido mineral oseo. Predictores de cambios en la
masa osea en madres adolescentes a los 6 meses postparto.
El objetivo del estudio fue determinar el efecto de dos formas de
suplementare calcio sobre la densidad mineral osea (DMO) y el
contenido mineral oseo (CMO), e identificar predictores de cambios
en la masa osea en madres adolescentes a los 6 meses postparto.
Se realizo un estudio prospectivo, analitico y clinico en
madres adolescentes (.19 anos; n=37) de la ciudad de La Plata,
Argentina. A partir de los 15 dias postparto, las adolescentes fueron
distribuidas al azar en 2 grupos y comenzaron con la suplementacion
con calcio; un grupo recibio productos lacteos (932
mg Ca; n=19) y el otro citrato de calcio (1000 mg calcio/dia;
n=18). Se midio peso, altura y consumo de alimentos y se determino
la DMO por DEXA a los 15 dias (linea de base) y a los 6
meses postparto. Tambien se determino CMO, DMO corporal
total y DMO de columna lumbar, cuello femoral, trocanter y cadera
total. Se usaron modelos de regresion para identificar relaciones
entre DMO corporal total y CMO con variables
independientes (tipo de suplementacion, meses de lactancia, peso
a los 6 meses, porcentaje de cambio de peso, masa magra a los
6 meses, porcentaje de cambio de masa magra, consumo total de
calcio). Los resultados muestran que los cambios en DMO y
CMO en los distintos sitios fueron similares en ambos grupos, y
que los cambios en los porcentajes de peso corporal e ingesta
total de calcio fueron los principales factores predictivos. En conclusion,
el efecto del calcio fue similar tanto con productos lacteos
como con comprimidos. Los cambios porcentuales en peso
corporal e ingesta total de calcio resultaron factores predictivos
de los cambios de la DMO corporal total y el CMO.
Palabras clave: Suplementacion con calcio, densidad mineral
osea, contenido mineral oseo, madres adolescentes, composicion
corporal, citrato de calcio, productos lacteos.
Bone mass loss and recovery after weaning and resumption
of menses have been reported in both lactating
adult (1-6) and adolescent (7,8) mothers. In an
earlier report of adolescent mothers, we found a significant
bone mineral density (BMD) loss at the hip
(5%) and in total body BMD (2%), with subsequent
bone mass recovery during the 12-month follow-up
(8). Such recovery occurred during the early postpartum
period and was not related to eventual BMD losses
during pregnancy, being slightly lower in younger
mothers and in those who had not resumed menses.
Agustina Malpeli, Maria Apezteguia, Jose L. Mansur, Alicia Armanini, Melisa Macias Couret,
Rosa Villalobos, Marta Kuzminczuk and Horacio F. Gonzalez
IDIP . Instituto de Desarrollo e Investigaciones Pediatricas gProf. D. Fernando E. Viterih,
Hospital de Ninos de La Plata, (MS/CIC-PBA), La Plata,Argentina
ARCHIVOS LATINOAMERICANOS DE NUTRICION
Organo Oficial de la Sociedad Latinoamericana de Nutricion
Vol. 62 No 1, 2012
CALCIUM SUPPLEMENTATION, BONE MINERAL DENSITY AND BONE MINERAL CONTENT 31
Calcium supplementation during lactation has been
studied in lactating adult (9,10) and adolescent (11)
mothers. In adult women, calcium salts did not have a
marked effect; Prentice et al. (9) suggest that breastfeeding
women with low calcium intake may not benefit
from calcium supplementation, and that the physiological
mechanisms developed during lactation provide
the necessary calcium for milk production. In the case
of Kalwarf et al. (10), the authors found that supplementation
with 1 g calcium per day does not prevent
bone mass loss during lactation, observing a light improvement
in bone mass gain after weaning. On the
other hand, Chan et al. (11) have suggested that an
adequate calcium intake (dairy products and calcium
rich food) may prevent bone loss during lactation in
adolescent mothers, and Abrams (12), in an editorial
reviewing the effects of calcium supplementation, concludes
that adult breastfeeding women would not benefit
from a higher calcium intake, but emphasizes the
importance of the nutrient in the reproductive cycle.
The mentioned author further reports that adolescent
breastfeeding mothers are a very important risk group
that could benefit from such supplement. In this regard,
the percentage of births to women under 20 years
of age in Argentina amounts to 15.6% (13), and the
National Nutrition and Health Survey (14) indicates
that calcium intake in women under the age of 19 is
very low (482 mg/day) in our population. In fact, two
previous studies performed by our group show that
calcium intake in lactating adolescent mothers was
<600 mg/day (895 mg/day during puerperium, falling
to 547 mg/day 12 months postpartum) (8,15). Other
results suggest that low-calcium diets over a prolonged
time may impact negatively on one of the critical periods
of bone accretion (16).
In view of the above mentioned evidence, the present
study aimed to determine the effect of two forms
of calcium supplementation on BMD and bone mineral
content (BMC), and to identify predictive factors
of bone mass change in adolescent mothers 6 months
MATERIALS AND METHODS
An analytical, prospective clinical design was used
to assess 37 Caucasian adolescent mothers recruited
within 15 days after delivery at the Maternity from the
Hospital General de Agudos "Jose de San Martin", La
Plata, Argentina. The city of La Plata is located at 34‹
Follow-ups were performed at the Outpatient Ward
of IDIP . Instituto de Desarrollo e Investigaciones Pediatricas
gProf. Dr Fernando Viterih, ChildrenLs Hospital
gSor Maria Ludovicah, La Plata, Argentina.
Women who were healthy, . 19 years, primiparous,
with term, singleton pregnancy (newborn birth weight
. 2500 g) and under natural or intrauterine dispositive
(IUD) contraceptive methods were included in the
study. Exclusion criteria were mothers who did not
breastfeed exclusively for at least 3 months, the presence
of chronic and/or acute diseases, history of rickets
and osteomalacia, infectious disease the moment
of the study, use of any drug, and unwillingness to participate
in the study.
A social worker surveyed adolescent mothers within
15 days after delivery, and invited those who complied
with the inclusion criteria to participate in the
study. Written informed consent was obtained from
each adolescent and a responsible adult. A general clinical
examination was done before starting the trial;
studies and follow-ups were performed at 15 days (baseline)
and 6 months postpartum, respectively. A questionnaire
about breastfeeding, resumption of menses
and contraceptive methods was also performed by the
nutritionist and the clinician.
Adolescents were assigned into one of two groups
following a systematic random technique. Group 1
(n=19) was given a biscuit fortified with skimmed
milk powder (SanCorR, SanCor CUL, Argentina) and
the following ingredients: eggs, wheat flour, sugar and
vanilla essence. Port salut cheese (SanCorR) (1/2
kg/week) was also given to complete the supplement.
This food provided 2073.28 kJ or 496 kcal, 61.2 g carbohydrates,
34.7 g proteins, 11.4 g fat, 932 mg calcium
and 0.32 ƒÊg vitamin D. The nutritionist asked adolescents
to replace some habitual food in their breakfast
or snack to avoid a higher calorie intake. They were
also asked not to take mineral or vitamin supplements
unless they were provided by the healthcare team. Mothers
from this group were surveyed weekly when they
collected their food and were all given a calendar to
record the monthly intake of fortified biscuits and cheese,
marking on each day with a cross whether the biscuit
or cheese was consumed; the supplement not
ingested was subtracted from the daily average intake.
Group 2 (n=18) received 3 capsules of calcium citrate
(CalcimaxR and Calcimax ForteR, Laboratorios
32 MALPELI et al.
Gador, Buenos Aires, Argentina) providing 1000 mg
calcium/day. The assigned supplement was given
when participants entered the study (15 days postpartum;
baseline) up to 6 months postpartum. Data about
calcium supplement intake were collected from telephone
follow-ups and pill count. Participants received
monthly a bottle of pills with the total number of pills
they had to take; on the day of follow-up, pills were
counted and the remaining ones, if any, were discounted
from the daily average intake.
Body weight was electronically measured with a
Tanita 1582 digital balance (100 g accuracy) and
height was measured with a SECA 222 stadi
(mm graduation, 1 cm accuracy) at 15 days and 6
months postpartum. Maximum weight during pregnancy
was taken from case histories.
The infantLs feeding pattern was determined by asking
mothers whether they were exclusively breastfeeding,
bottle feeding, or both. The food-frequency
semi-quantitative method was used to estimate the dietary
intake of mothers at baseline (15 days postpartum;
it reflects the dietary intake during the last months of
pregnancy) and 6 months after the study. The survey
included calcium dietary intake plus calcium from
each dietary supplements (17). All food groups were
included in the survey (dairy products, meat, eggs,
fruits, vegetables, cereals, beans, flour and derivatives,
drinks, candies, fat, oil, and bread). According to the
food ingested, the amount of nutrient consumption per
day was calculated, estimating daily intake of energy
(kJ/day, kcal/day), proteins (g/day), calcium (mg/day),
phosphorus (mg/day), and vitamin D (ƒÊg/day) with the
USDA Food composition data base (18). The questionnaire
was designed by a registered nutritionist
based on food models to clearly identify serving sizes.
Bone mineral densitometry was assessed by dualenergy-
X-ray absorptiometry (DEXA) with a LUNAR
DPX-L instrument with pediatric software version 4.6f
(GE Lunar Corporation, Madison, WI, USA). The in
vivo reproducibility, expressed as percent BMD coeficient
of variation, was as follows: lumbar spine (L2-
L4), 1.3%; femoral neck (FN), 1.5%; trochanter (TR),
1.4%; total hip (TH), 0.9%; total body BMD, 0.8%.
Measurements were performed by a single expert observer.
We determined BMC and total body BMD.
BMD was measured in all sites and body composition
was also estimated by DEXA (19,20). Results were
expressed as absolute values (g/cm2), as percent BMD
changes in all sites studied, and as percent BMC changes
from baseline up to 6 months (final BMD/baseline
BMD x 100 [percent BMD] and final BMC/baseline
BMC x 100 [percent BMC]). In order to detect a mean
3% difference in BMC variation (ƒÀ = 0.2; ƒ¿ = 0.05),
at least 18 patients per group were needed.
Vitamin D supplement was not recommended because
geographical location (latitude 34o) and environmental
conditions did not advice about its prescription
The study began at the end of winter-start of spring
and follow-ups were made in summer-start of autumn.
The study protocol was approved by the Institutional
Research Protocols Review Board of IDIP.
The statistical analysis was performed with SPSS
version 13 (SPSS Inc, Chicago, IL, USA). Comparisons
of means between groups were made with Student
Ls t-test for independent samples. Regression
models were built to study the relationship of percent
BMD and BMC changes (dependent variables) with
supplementation group 1 or 2 (dichotomic variable)
and months of lactation, weight at 6 months (kg),
weight at 6 months (kg)/weight at baseline (kg) x 100,
lean mass at 6 months (kg), lean mass at 6 month
(kg)/lean mass at baseline (kg) x 100, and total calcium
intake (independents variables). The choice of
variables was made with backward elimination procedures
to obtain the simplest models.
From a total of 37 adolescent mothers, 19 belonged
to group 1 (diet supplemented with dairy products) and
18 to group 2 (supplemented with calcium tablets).
The characteristics of the study sample are depicted
in Table 1. The parameters studied did not differ significantly
between groups at the beginning of the study.
All mothers were exclusively breastfeeding up to
3 months. At 6 months, 15 adolescents in each group
continued breastfeeding, while the rest fed their babies
with a mixture of bottle feeding and breast milk.
Weight, body mass index (BMI) and percent body
fat data (mean and SD) at baseline and 6 months postpartum
are presented in Table 2. The analysis of data
revealed no significant differences between groups.
Table 3 shows results of the dietary intake survey,
namely, energy (kJ/day, Kcal/day), protein (g/day),
calcium (mg/day), phosphorus (mg/day) and vitamin
D (ƒÊg/day) intake in both groups at baseline and 6
CALCIUM SUPPLEMENTATION, BONE MINERAL DENSITY AND BONE MINERAL CONTENT 33
Total body BMD, BMD changes at the different
sites (TH, FN and TR) and BMC did not differ between
Regression models for percent changes in total
body BMD and percent changes in BMC showed that
only percent body weight changes and total calcium
intake were significant, and would account for the
38% total body BMD and the 40% BMC variance
To our knowledge, this study is the first to compare
two calcium supplements and their effect on BMD at
different sites and on BMC in adolescent mothers exclusively
breastfeeding for at
least 3 months and followed-up
during the first 6 months postpartum.
Our data suggest that
changes in BMD and BMC 6
months postpartum were similar
in both intervention groups, and
that percent body weight changes
and total calcium intake
were significant predictors of
bone mass change.
Very few reports in the literature
have investigated the impact
of calcium supplements in the
diet or calcium salts on BMD in
lactating adolescent mothers.
Chan et al. (11) studied the efficacy
of a high calcium diet composed
of dairy products on BMD
loss in lactating adolescent mo-
Characteristics of adolescent mothers at the beginning of the study
Age at the beginning (y)
Group 1 Group 2
16.32 } 1.38 16.78 } 1.35
Height (m) 1.555 } 0.036 1.558 } 0.051
Age at menarche (y) 11.67 } 1.19 11.94 } 0.87
Weight gain during pregnancy (kg) 12.45 } 6.65 16.15 } 7.72
Newborn birth weight (kg) 3.098 } 0.420 3.353 } 0.404
Group 1, dairy products Group 2, calcium citrate
Anthropometric parameters at baseline and 6 months postpartum
Baseline 6 months
Group 1 Group 2 Group 1 Group 2
Weight (kg) 58.3 } 9.9 63.8 } 13.2 57.4 } 12.5 61.7 } 13.3
BMI (kg/m2) 24.06 } 3.61 26.22 } 4.88 23.48 } 4.70 25.03 } 5.89
Fat mass (%) 36.9 } 6.7 39.8 } 8.0 35.0 } 10.3 36.3 } 10.9
BMI, body mass index. Group 1, dairy products Group 2, calcium citrate
Results of the dietary survey at baseline and 6 months postpartum
Baseline 6 months
Group 1 Group 2 Group 1 Group 2
Energy (kJ/day) 14628 } 5356 15399 } 5311 12644 } 3318 10210 } 3979*
Energy (Kcal/day) 3500 } 1281 3684 } 1270 3025 } 810 2293 } 748**
Proteins (g/day) 116 } 37 121 } 42 117 } 29 80 } 28***
Calcium (mg/day) 1004 } 496 1223 } 890 1598 } 585. 1477 } 321.
Phosphorus (mg/day) 1186.59 } 555 1394 } 628.5 871.47 } 497.4 774.56 } 436.1
Vitamin D (ƒÊg/day) 2.05 } 1.84 2.84 } 2.39 2.3 } 2.08 2.13 } 2.09
*p = 0.04, **p = 0.013, ***p = 0.001 for differences between groups at 6 months. Group 1, dairy products Group 2, calcium citrate
.Data are means of the sum of the daily average calcium supplement intake and the daily dietary calcium intake.
months postpartum. Energy as well as protein intake
were higher in Group 1 (p = 0.013 and =0.001, respectively).
However, both groups complied with recommendations
Treatment adherence of adolescent mothers was
good (60%); calcium intake (average of the 180 days
of intervention) of either form of supplement (dairy
products or tablets) was 864 and 839 mg/day in Group
1 and 2, respectively.
Bone densitometry results (absolute value g/cm2)
and percent changes from baseline to follow-up are depicted
in Table 4. BMD in L2-L4 did not decrease 6
months postpartum in either group.
34 MALPELI et al.
thers during 4 months. The authors determined BMC
by photon absorptiometry of the distal radius, suggesting
that bone loss during lactation may be prevented
with adequate dietary calcium intakes (>1600 mg
Ca/day). However, the current calcium recommendation
is lower (1100 mg/day) (24). In our study, supplementation
lasted longer (6 month), BMD
measurements were performed with another method
(densitometry) and in other sites (lumbar spine, total
hip, total body), the calcium intake was lower, and two
forms of calcium supplementation were compared.
The average dietary intake of calcium at baseline
in the current study was slightly higher than that reported
in our previous report without supplementation
(approximately 1000-1200 mg Ca/day vs 895 mg
Ca/day) (8). At 6 months postpartum, there was a marked
decrease in calcium intake in both the previous
and the present report. Apparently, during pregnancy
mothers consume more energy, calcium and other nutrients,
but do not receive adequate counseling during
lactation, when dietary habits are similar to those of
the general adolescent population.
The current results show that BMD and BMC of
adolescents receiving a calcium supplement in their
diet or tablets were similar after the 6-month intervention.
Total body BMD and BMC had not significant
changes in either study group, and results were similar
at different hip sites (FN, TR, TH). Whereas some authors
(10,11,25) have studied calcium supplementation
in adult and adolescent mothers without evaluating
BMD at all hip sites, others (10,25) have measured it
in forearm and L2-L4, reporting that calcium supplementation
does not prevent bone loss during lactation
in L2-L4. In our study, BMD in L2-L4 remained unchanged
as compared to that observed at baseline. Similar
results were also reported in young adult
undernourished women from India without supplementation,
who did not present significant BMD losses
in L2-L4 6 months postpartum (26).
Chan et al. (11) found correlation between percent
BMD at different skeletal sites at baseline and 6 months postpartum
Baseline 6 months
Group 1 Group 2 Group 1 Group 2
L2-L4 (g/cm2) 1.060 } 0.085 1.077 } 0.121 1.069 } 0.091 1.105 } 0.137
percent variation* 101.01 } 6.7 102.7 } 6.5
FN (g/cm2) 1.013 } 0.085 1.046 } 0.148 0.960 } 0.112 1.011 } 0.173
percent variation 94.6 } 5.56 96.4 } 6.86
Tr (g/cm2) 0.765 } 0.0882 0.790 } 0.143 0.732 } 0.091 0.782 } 0.155
percent variation 95.99 } 8.89 98.94 } 7.66
TH (g/cm2) 0.996 } 0.0902 1.021 } 0.146 0.953 } 0.107 0.998 } 0.167
percent variation 95.63 } 5.91 97.62 } 6.42
Total body BMD (g/cm2) 1.099 } 0.0560 1.128 } 0.087 1.083 } 0.0634 1.12 } 0.0965
percent variation 98.55 } 2.68 99.40 } 2.17
BMC (g) 2165 } 220 2305 } 381 2116 } 249 2315 } 437
percent variation 97.4 } 4.89 100.19 } 6.83
*Percent variation from baseline to follow-up (final BMD value expressed as percentage of the initial value) L2-L4, lumbar spine FN,
femoral neck Tr, Trochanter TH, total hip total-body BMD, total body bone mineral density BMC, bone mineral content
Group 1, dairy products Group 2, calcium citrate
Regression models of percent total body BMD and Percent BMC
Dependent variable R2 Significant independent variable Coefficient p
Percent total body BMD 0.38 Percent body weight change 0.0125 0.0014
Total calcium intake 0.0142 0.0470
Percent BMC 0.40 Percent body weight change 0.2554 0.0088
Total calcium intake 0.0056 0.0035
Total body BMD, total body bone mineral density BMC, bone mineral content
CALCIUM SUPPLEMENTATION, BONE MINERAL DENSITY AND BONE MINERAL CONTENT 35
BMC changes and calcium intake in lactating adolescent
mothers. Our results show that not only percent
BMC but also percent total body BMD changes had a
linear dependence on calcium intake during the 6-
Concerning changes in anthropometric variables
during the 6-month follow-up (weight, BMI and fat
mass), they were similar to those published in our previous
Kulkarni et al. (26) have reported that maternal
weight and lean mass in young adult undernourished
women from India explained major variations in BMD
changes at various skeletal sites. Our findings show
that weight rather than lean mass had a significant association
with percent total body BMD and percent
BMC. Other studies also report such association in
adult pregnant women (27,28) and breastfeeding adolescents
(8). Evidently, body weight and its lean and
fat body mass components are three factors that play
a role on bone health.
BMD and BMC variations not only depend on hereditary,
racial and hormonal factors, but also on the
intake of calcium and other nutrients, the practice of
physical activity and the reproductive history (29). During
the first two decades of life, during pregnancy and
lactation, and particularly during adolescence, calcium
intake requirements are high. However, our population
can hardly meet calcium recommendations during
such a critical period. Further, compliance with the
calcium- or tablet-supplemented diet was the result of
a sustained and persistent intervention by the participating
Other variables such as duration of exclusive maternal
breastfeeding and resumption of menses were
not evaluated in this study because most adolescents
continued breastfeeding until the end of the intervention
and none had resumed menses; thus, their effect
on BMD changes could not be assessed.
Results of the regression analysis showed that belonging
to either supplementation group was not significant.
Therefore, covering the recommended dietary
intake (1100 mg) is mostly important, regardless of the
source of calcium supply. Probably, an adequate and
sustained calcium intake could be reached through a
mixed intervention and nutritional advice, without exceeding
the recommended upper limits (24).
One of the weaknesses of our study is the absence
of a control group. However, the lack of intervention
would have been ethically controversial, due to our previous
study in adolescent mothers without intervention
who evinced bone mineral loss (8). Nevertheless, we
believe that a controlled trial would be necessary.
Although both study groups were advised to go on
their habitual diet and the only advice was to replace
bread or biscuits by the calcium fortified biscuit provided
by our team, participants from group 1 spontaneously
consumed more energy than those from group 2.
In previous studies in adult and adolescent mothers,
either calcium salts or a higher calcium intake through
dairy products have been used for calcium supplementation
(9-11). However, one of our main objectives
was to compare the results obtained with both forms
of supplementation, expecting better results with dairy
product since it has been reported that not only calcium
and vitamin D but also proteins favor bone health
(30). Nevertheless, our data showed similar results
with either form of supplementation.
Our data suggest that there were no significant
changes in BMD and BMC 6 months postpartum in
none of the intervention groups, but percent body
weight changes and total calcium intake were significant
predictors of bone mass change.
This study was supported by a grant from Salud Investiga
(National Ministry of Health of Argentina).
Thanks are due to SanCor CUL and Laboratorios
Gador for the provision of calcium supplements. The
authors are grateful to the women who volunteered to
take part in the study. Thanks are also due to Adriana
Di Maggio for manuscript editing.
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