DOI: 10.1111/j.1740-8709.2010.00246.

Original Article
Breast vs. bottle: differences in the growth of
Croatian infants mcn_246 389..396

Zlatko Mandić*, Antonija Perl Pirički†, Daniela Kenjerić†, Branka Haničar‡ and
Igor Tanasić§
*Faculty of Medicine, Josipa Huttlera 4, HR-31000 Osijek, Croatia, †Department of Food and Nutrition Research, Faculty of Food Technology, Franje
Kuhača 20, HR-31000 Osijek, Croatia, ‡Vladimira Nazora 4, HR-31000 Osijek, Croatia, and §SS Kranjčevića 13, HR-31326 Darda, Croatia

Abstract

The aim of the paper was to compare the growth of rural Croatian infants with 2000 Centers for Disease Control
and Prevention (CDC) growth standards and to evaluate the potential preventive influence of breastfeeding on
the development of obesity in infancy.Two hundred three infant–mother pairs from Baranja, an Eastern region of
Croatia, were enrolled into this study. Retrospective evaluation of infants’ medical charts was used to obtain
anthropometric data recorded at the birth, 1, 3, 6, 9 and 12 months of age. Infant feeding mode was self-reported
by mothers. Breastfed infants gained the least weight of all observed groups. Up to 6 months of age, formula fed
infants had the highest weight gain and after 6 months of age, mixed milk fed infants had the highest weight gain.
At 12 months of age, 6.4% of all study infants and 7.6% of mixed milk fed infants were at risk of overweight, while
the same risk for the group of breastfed infants was 4%. Most of the study infants achieved higher values of body
mass and length than the child growth standards. Exclusively breastfed infants, in comparison with other study
groups (formula fed infants, mixed milk fed infants and cow’s milk fed infants), had lower weight-for-length
z-scores during the first year, which suggests that breastfeeding may have a preventive impact on obesity
development.

Keywords: infants, breastfeeding, formula feeding, growth, obesity.

Correspondence: Daniela Kenjerić, Department of Food and Nutrition Research, Faculty of Food Technology, Franje Kuhača 18,
HR-31107 Osijek, Croatia. E-mail: daniela.kenjeric@ptfos.hr

Introduction and obesity represent an important public health

problem with about 11% of schoolchildren being
Obesity is becoming one of the biggest public health overweight (Antonić-Degač et al. 2004).
problems of the 21st century (Rossner 2002). The The association between infant nutrition and
basis for the development of overweight and obesity obesity development has been widely debated.
lies within genetic factors (Chagnon et al. 2000), but it Obesity during the first 6 months of infancy has been
is also undoubtedly associated with environmental found to be associated with obesity at 7 years of age
factors (Strauss & Knight 1999). The incidence of (Stettler et al. 2002), while obesity in pre-schoolers
obesity in Europe has tripled during the last two has been associated with obesity in adolescence
decades (World Health Organization 2007), and many (Johannsson et al. 2006).The prevailing opinion is that
studies have also indicated a large growth in the exclusive breastfeeding during the first 6 months,
prevalence of obesity among European children combined with the appropriate introduction of
(Rolland-Cachera et al. 2002). In Croatia, overweight complementary foods, has a protective effect on the

© 2010 Blackwell Publishing Ltd Maternal and Child Nutrition (2011), 7, pp. 389–396 389
390 Z. Mandić et al.

development of obesity (American Academy of Healthy, full-term (37–42 weeks), singleton infants
Pediatrics 2005; Harder et al. 2005).The rate of breast- weighing ⱖ2.5 kg at birth who scored more than 7 on
feeding in the Republic of Croatia, however, is low, Apgar evaluation (n = 203; 114 male and 89 female)
with only 36.6% of mothers exclusively breastfeeding from a rural part of Eastern Croatia and their
for longer than 3 months (Grgurić 1997). mothers were enrolled in the study.
Previous studies have indicated that infant formula All data were collected by retrospective assessment
feeding represents a risk factor for obesity during of infants’ medical charts. All anthropometric mea-
infancy (Grummer-Stawn & Mei 2004), childhood surements were performed by trained medical staff
and adolescence (Sholters et al. 2007), and adulthood according to the anthropometric standard procedures
(Baird et al. 2005). Consequences of overweight and (WHO Expert Committee 1995). Babies were
obesity in childhood include psychosocial difficulties weighed naked on an electronic Sartorius scale (Sar-
and health problems such as diabetes type 2, hyper- torius AG, Goettingen, Germany) accurate to ⫾5 g.
tension, hyperlipidemia and hyperinsulinemia (Lucas Crown-heel length was recorded as an average of three
& Feucht 2008). measures using infantometer. Growth data were
The relationship between infant feeding mode and recorded at regular intervals (birth, 1, 3, 6, 9, 12
infant growth and weight gain among the Croatian months) during visits to the health centre.
rural population has not previously been investigated. Information of infant feeding mode was based on a
The aim of this study was to investigate the influence of mother’s self-report. Infants were divided into four
infant feeding mode on the growth of infants in groups according to feeding mode: infants exclusively
Baranja.To achieve this objective, we evaluated differ- breastfed until 6 months of age (n = 50), formula fed
ences in weight, length, weight and length gain, and infants (n = 47), mixed milk fed infants (n = 79) and
z-scores among four groups of infants: breastfed, infants fed with cow’s milk (n = 27). Mothers were
mixed milk fed, formula fed and cow’s milk fed infants. interviewed by trained personnel to gather household
Additionally, study infants were compared with 2000 demographics (description of socio-economic status),
Centers for Disease Control and Prevention (CDC) which included details of education, housing condi-
growth standards (Kuczmarski et al. 2002). tions, occupation, parity, family size and number of
children.

Subjects and methods

This study was carried out in a Community Health
Outcome measures and explanatory variables
Centre in Beli Manastir and a paediatric service in
Darda, both in Baranya. The study was performed as The primary outcome measure of interest in this study
a part of a national project (as stated in the acknowl- was growth status from birth to 12 months computed
edgements) that is in all its parts in compliance with from age- and sex-specific z-scores of infants fed via
all international and local laws, regulations and direc- different feeding modes. Values of infant’s weight and
tions concerning protection of examinees. Addition- length were converted to weight-for-age, length-for-
ally, the study was approved by the Ethics Committee age and weight-for-length z-scores by using age- and
of the Faculty of Food Technology. sex-specific 2000 CDC reference values.

Key messages

• Compared with formula fed and mixed fed infants, exclusively breastfed infants in Croatia gained the least
weight over a 12 month period.
• Exclusively breastfed infants had the lowest weight-for-length z-scores during the first year.
• At 12 months of age, breastfed infants had the lowest risk of being overweight.
• Breastfeeding may have a preventive impact on obesity development.

© 2010 Blackwell Publishing Ltd Maternal and Child Nutrition (2011), 7, pp. 389–396
 Infant feeding and growth 391

The z-score represents the distance in standard Table 2 shows the mean ⫾ SD values of infant’s
deviations (SD) units from the normative reference anthropometric parameters (weight, length, head cir-
means for age and sex of the 2000 CDC standards cumference) at different intervals. At birth, the mean
(Kuczmarski et al. 2002). Two categorical variables weight and length for all infants were 3.41 ⫾ 0.43 kg
were used to determine infants’ risk for underweight and 50.27 ⫾ 2.04 cm, respectively. Considering weight
or overweight. A composite at-risk for underweight gain of infants, we observed that breastfed infants
variable was defined as weight-for-age, length-for-age gained less than other investigated groups, while
and weight-for-length z-scores lower than -2 SD, and a formula fed infants gained most weight up to 6
composite at-risk for overweight variable was defined months, and mixed milk fed infants gained most
as weight-for-age, length-for-age and weight-for- weight after 6 months.
length z-scores greater than 2 SD from median based The mean head circumferences were almost identi-
on 2000 CDC standards (Kuczmarski et al. 2002). cal up to 6 months for all feeding groups of infants, but
at 6 months, we found a significant difference between
breastfed and mixed milk fed infants (P < 0.01) and at
Statistical analysis
9 months between breastfed and formula fed infants
Statistical analysis was conducted with Statistica 7.1 and mixed milk fed infants (P < 0.05).
(StatSoft Inc., Tulsa, OK, USA). The acceptable level Figures 1–3 show the changes in average group
of statistical significance for all tests was P < 0.05. values of weight-for-age z-scores, length-for-age
z-scores and weight-for-length z-scores over the 12
months period.The weight-for-age, length-for-age and
Results
weight-for-length z-score trend lines showed only a
Demographic characteristics of infants and their few gender differences across the observed period
mothers by feeding mode of infants are reported in (data not shown).
Table 1. The rather low number (10/203, 5%) of The mean values of weight-for-age z-scores at birth
mothers with college education can be explained were – 0.30–0.13. As shown in Fig. 1, at birth and after
with the fact that the study population was a rural the first month, they were below the 2000 CDC
population. median for all investigated groups except for the

Table 1. General characteristic of studied rural infants and their mothers by feeding mode

Breastfeeding Formula feeding Mixed milk Cow’s milk All participants

(n = 50) (n = 47) feeding* (n = 79) feeding (n = 27) (n = 203)

Infant characteristics
Gender n (%)
Male 23 (46) 31 (66) 44 (56) 16 (59) 114 (56)
Female 27 (54) 16 (34) 35 (44) 11 (41) 89 (44)
Maternal characteristics
Mean number of children (n) 1.78 1.79 1.68 2.19 1.79
Number of delivery n (%)
1 26 (52) 21 (45) 37 (47) 10 (37) 94 (46)
2 and 3 21 (42) 24 (51) 38 (48) 15 (56) 98 (48)
>3 3 (6) 2 (4) 4 (5) 2 (7) 11 (5)
Education n (%)
Primary school 24 (48) 17 (36) 28 (35) 12 (44) 81 (40)
High school graduate 23 (46) 27 (57) 48 (61) 14 (52) 112 (55)
College graduate 3 (6) 3 (6) 3 (4) 1 (4) 10 (5)
Mother’s first birth <21 y 25 (50) 19 (40) 27 (34) 9 (33) 80 (39)
Mother employed 18 (36) 21 (45) 32 (41) 10 (37) 81 (40)

*Infants were fed with both breast milk and formula.

© 2010 Blackwell Publishing Ltd Maternal and Child Nutrition (2011), 7, pp. 389–396
 392
Z. Mandić et al.

Table 2. Average anthropometric parameters (mean ⫾ SD) of the study infants at different intervals

Breastfeeding Formula feeding Mixed milk feeding* Cow’s milk All participants
(n = 50) (n = 47) (n = 79) feeding (n = 27) (n = 203)

Birth
Weight (kg) 3.31 ⫾ 0.39 3.31 ⫾ 0.37 3.52 ⫾ 0.48 3.43 ⫾ 0.37 3.41 ⫾ 0.43
Length (cm) 49.64 ⫾ 2.04 49.91 ⫾ 1.84 50.78 ⫾ 2.08 50.59 ⫾ 1.89 50.27 ⫾ 2.04
Head circumference (cm) 34.50 ⫾ 1.51 34.68 ⫾ 1.28 34.91 ⫾ 1.32 34.70 ⫾ 1.29 34.73 ⫾ 1.36
1 month
Weight (kg) 4.20 ⫾ 0.55 4.24 ⫾ 0.48 4.34 ⫾ 0.52 4.26 ⫾ 0.52 4.27 ⫾ 0.52
Weight gain (kg) 0.89 ⫾ 0.28 0.93 ⫾ 0.38 0.82 ⫾ 0.29 0.83 ⫾ 0.31 0.87 ⫾ 0.31
Length (cm) 52.95 ⫾ 2.37 53.07 ⫾ 1.98 53.80 ⫾ 2.01 53.39 ⫾ 1.98 53.37 ⫾ 2.11
Head circumference (cm) 36.75 ⫾ 1.28 36.61 ⫾ 1.16 36.77 ⫾ 1.32 36.67 ⫾ 1.12 36.71 ⫾ 1.24
3 months
Weight (kg) 5.88 ⫾ 0.68 6.04 ⫾ 0.65 6.14 ⫾ 0.65 6.09 ⫾ 0.63 6.05 ⫾ 0.66
Weight gain (kg) 2.57 ⫾ 0.53 2.73 ⫾ 0.58 2.62 ⫾ 0.47 2.65 ⫾ 0.45 2.64 ⫾ 0.51
Length (cm) 59.60 ⫾ 2.30 60.07 ⫾ 2.42 60.65 ⫾ 2.48 60.65 ⫾ 2.32 60.26 ⫾ 2.43
Head circumference (cm) 39.97 ⫾ 1.28 39.95 ⫾ 1.23 40.08 ⫾ 1.31 40.09 ⫾ 1.19 40.02 ⫾ 1.26
6 months
Weight (kg) 7.68 ⫾ 0.74 7.94 ⫾ 0.83 8.24 ⫾ 0.74 8.09 ⫾ 1.01 8.01 ⫾ 0.83
Weight gain (kg) 4.37 ⫾ 0.69 4.63 ⫾ 0.76 4.71 ⫾ 0.73 4.66 ⫾ 0.89 4.60 ⫾ 0.76
Length (cm) 66.74 ⫾ 2.31 67.48 ⫾ 2.40 68.42 ⫾ 2.45 68.04 ⫾ 2.82 67.74 ⫾ 2.53
Head circumference (cm) 42.94 ⫾ 1.38 43.31 ⫾ 1.21 43.57 ⫾ 1.26 43.35 ⫾ 1.36 43.33 ⫾ 1.31
9 months
Weight (kg) 8.80 ⫾ 0.88 9.13 ⫾ 0.87 9.52 ⫾ 0.80 9.33 ⫾ 1.31 9.23 ⫾ 0.95
Weight gain (kg) 5.30 ⫾ 1.38 5.82 ⫾ 0.82 6.00 ⫾ 0.80 5.90 ⫾ 1.18 5.77 ⫾ 1.06
Length (cm) 70.51 ⫾ 2.52 71.48 ⫾ 2.24 72.57 ⫾ 2.39 72.81 ⫾ 2.70 71.84 ⫾ 2.57
Head circumference (cm) 44.79 ⫾ 1.37 45.38 ⫾ 1.31 45.33 ⫾ 1.35 45.24 ⫾ 1.40 45.20 ⫾ 1.36
12 months
Weight (kg) 9.95 ⫾ 0.87 10.42 ⫾ 1.13 10.86 ⫾ 0.92 10.57 ⫾ 1.35 10.50 ⫾ 1.08
Weight gain (kg) 6.64 ⫾ 0.79 7.11 ⫾ 1.08 7.34 ⫾ 0.93 7.14 ⫾ 1.26 7.09 ⫾ 1.01
Length (cm) 75.14 ⫾ 2.95 76.87 ⫾ 2.51 76.87 ⫾ 2.51 76.94 ⫾ 3.61 76.25 ⫾ 2.88

*Infants were fed with both breast milk and formula.

© 2010 Blackwell Publishing Ltd Maternal and Child Nutrition (2011), 7, pp. 389–396
 Infant feeding and growth 393

mixed milk had highest z-score values, which were

statistically higher at 3 months (P < 0.05), at 6, 9 and
12 months (P < 0.001) than the values of exclusively
breastfed infants which were the lowest of all groups.
Length-for-age z-scores followed a similar pattern
(Fig. 2), with baseline values at 0.0–0.42, until the first
month when they rapidly decreased below the 2000
CDC medians for all observed groups of infants, then
gradually increased until the sixth month. Breastfed
infants had the lowest values of weight-for-age and
Fig. 1. Weight-for-age z-scores (WAZ) of the study infants grouped length-for-age z-scores at all measured intervals.
according the feeding mode during the first year of life. As shown in Fig. 3, at birth, the mean weight-for-
length z-scores were below the 2000 CDC median
(-0.24 to 0.0) for all observed groups, and after 6
months of age values started to grow until 12 months
when they were the highest for all feeding modes.
A statistically significant difference (P < 0.001) was
found between infants who were breastfed and those
who were mixed milk fed at the age of 1 year (0.42
vs. 0.98).
We also tracked growth in terms of weight and
length of individual infants over the 12-month period.
Their weight-for-age, length-for-age and weight-for-
length z-scores showed that, in general, infants born
Fig. 2. Length-for-age z-scores (LAZ) of the study infants grouped
according the feeding mode during the first year of life. with lower z-scores had also lower values at the age
of 12 months. Additionally, a statistically significant
correlation was established between all observed
z-scores (weight-for-age, length-for-age and weight-
for-length) of infants between baseline values (at
birth) and values by 12 months, respectively (r = 0.33,
P < 0.001; r = 0.44, P < 0.001; r = 0.14, P < 0.05).

Discussion
This study evaluates the feeding mode and growth of
infants in Baranja, Eastern Croatia, and is the first
research of this type on the local infant population.
Fig. 3. Weight-for-length z-scores (WLZ) of the study infants
Results of the study showed positive impact of
grouped according the feeding mode during the first year of life.
breastfeeding on the growth of infants, as well as
potential preventive impact on the infant obesity
group of mixed milk fed infants. After that, a continu- prevention.
ous growth of the z-scores until 6 months was fol- Growth curves of all the groups of study partici-
lowed by fall in the ninth month, and again increased pants were similar until the third month, but after
up to the 12th month where mean values for all that, differences in growth among feeding groups
observed groups were above the median based on the started to appear. The greatest differences were
2000 CDC standards. The infants who were fed by obtained between the exclusively breastfed and

© 2010 Blackwell Publishing Ltd Maternal and Child Nutrition (2011), 7, pp. 389–396
394 Z. Mandić et al.

mixed milk fed infant groups in the sixth month and trast to previous findings of Butte and Kramer (Butte
beyond. A previously published study by Victora et al. et al. 2000; Kramer et al. 2004).
(1998) has shown that exclusively breastfed infants Despite paediatricians’ advice to avoid cow’s milk
grew more rapidly than the 2000 CDC references in during infancy (because of its inadequacy), our study
weight for the first 6 months and length in the period showed that some infants in this region were fed with
from 3 to 6 months but appeared to falter thereafter. cow’s milk since birth. This could be explained by the
The similar pattern of more rapid growth than the fact that the study was conducted in a rural popula-
2000 CDC references in the period from 3 to 6 tion that often breeds their own cattle. As expected,
months, followed by relative decline afterwards, was cow’s milk fed infants had statistically higher weight-
found in our study. for-age and length-for-age z-scores than breastfed
We also observed that breastfed infants gained less infants at 12 months. This is probably because infants
weight during the first 3 months than other investi- who were cow’s milk fed since birth will have con-
gated groups. Unfortunately, it is not possible to con- sumed higher amounts of proteins (about 4 g/100 mL)
clude, at least not from this particular study, that the than breastfed and formula fed infants. Most of the
observed differences are the result only of feeding infant formulas in the Republic of Croatia contain
mode as many other factors can influence the nutri- 1.4–1.8 g of proteins per 100 mL. This supports the
tion status of infants at the same time. In cases when suggestion that protein intake is a determining factor
lack of weight gain or a loss of weight gain happens in of growth and obesity development during the
a short time period, the child should be evaluated infancy (Rolland-Cachera et al. 1995; Agostoni et al.
more thoroughly, and all factors which can influence 2005). Some studies have shown that prolonged and
nutrition status (birth measures, genetic factors, exclusive breastfeeding is correlated with lower long-
illness and family social problems) should be included term risk of obesity (Hediger et al. 2000; Harder et al.
into that evaluation. Formula fed infants had the 2005; Sholters et al. 2007), while others report an
highest weight gain up to 6 months of age, and after 6 unclear relationship between breastfeeding duration
months, the highest weight gain was in mixed milk fed and obesity, but rather a major impact of family
infants, a finding similar to that shown in US infants factors (nutritional habits, low socio-economic status,
(Hediger et al. 2000). physical activity, mother’s obesity) on obesity devel-
In comparison with other mode of feeding groups, opment (Bergmann et al. 2003). Our study has shown
exclusively breastfed infants had statistically lower lower weight-for-length z-scores at the end of the first
weight-for-age z-scores in third, sixth and ninth year in breastfed infants compared with formula fed
month. These findings are in agreement with other and cow’s milk fed infants.
studies that have also showed that exclusively breast- It is important to consider that our study has some
fed infants show smaller weight gain than the infants limitations. A short period of observation should be
who are not breastfed (Agostoni et al. 1999; Butte considered as a limitation of our study, as at least 3
et al. 2000; Hediger et al. 2000; Kramer et al. 2004). In years period is recommended for children growth
comparison, studies that have investigated infant monitoring (Dewey 2003). Therefore, this study will
growth in undeveloped African countries (Mamabolo be continued through the further anthropometric
et al. 2004) and among lower socio-economic immi- parameters monitoring. Second, it is important to
grant groups (Neault et al. 2007) have showed that mention that the 2000 CDC Growth Charts used were
breastfed infants had higher weight gain than formula originally developed for the United States. It is pos-
fed ones. sible that some of the results would be slightly differ-
Our study also showed a statistically significant dif- ent if World Health Organization (WHO) Child
ference in head circumference at 6 months between Growth Standards were used. At the same time, it
exclusively breastfed and formula fed infants, and at 9 should be considered that the WHO standards dem-
months between exclusively breastfed and mixed onstrate that healthy children from around the world
milk fed and formula fed infants (P < 0.01), in con- who are raised in similar environments have very

© 2010 Blackwell Publishing Ltd Maternal and Child Nutrition (2011), 7, pp. 389–396
 Infant feeding and growth 395

similar growth patterns (WHO Multicentre Growth Antonić-Degač K., Kaić-Rak A., Mesaroš-Kanjski E.,
Reference Study Group & de Onis 2006). Third, Petrović Z. & Capak K. (2004) Nutritional status and
dietary habits of schoolchildren in Croatia. Paediatria
although the study sample is big enough to get an
Croatica 48, 9–15.
insight into the situation in Eastern Croatia, it should Baird J., Fisher D., Lucas P., Kleijnen J., Roberts H. & Low
be considered that this is a small study and the results C. (2005) Being big or growing fast: systematic review of
cannot be generalized or taken as a representative for size and growth in infancy and later obesity. British
any other group. Medical Journal 331, 929–935.
In summary, this study resulted in two main conclu- Bergmann K.E., Bergmann R.L., von Kries R., Böhm O.,
Richter R., Dudenhausen J.W. et al. (2003) Early deter-
sions. First, all study participants, regardless of feeding
minants of childhood overweight and adiposity in a birth
mode, achieved higher body weight and length as cohort study: role of breast-feeding. International
compared with the 2000 CDC growth chart median. Journal of Obesity 27, 162–172.
Second, exclusively breastfed infants had lower Butte N.F., Wong W.W., Hopkinson J.M., O’Brian Smith E.
weight-for-length z-scores during the first year than & Ellis K.J. (2000) Infant feeding mode affects early
growth and body composition. Pediatrics 106, 1355–1366.
infants from other observed feeding mode groups,
Chagnon I.C., Pérusse L., Weisnagel S.J., Rankinen T. &
suggesting that breastfeeding has a potential preven- Bouchard C. (2000) The human obesity gene map: the
tive impact on obesity prevention. 1999 update. Obesity Research 8, 89–117.
Dewey K.G. (2003) Is breastfeeding protective against
child obesity? Journal of Human Lactation 19, 9–18.
Acknowledgements Grgurić J. (1997) Istraživanje znanja i stavova roditelja o
prehrani i najčešćim zdravstvenim problemima djece u
Sincere thanks to all women who have participated in Republici Hrvatskoj. UNICEF Ured za Republiku
this study. Hrvatsku: Zagreb.
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project Nutrition and lifestyle in health protection Harder T., Bergmann R., Kallischnigg G. & Plagemann A.
(No. 113-0000000-0548) financed by the Ministry (2005) Duration of breastfeeding and risk of overweight:
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Conflicts of interest
from the third national health and nutrition examination
No conflicts of interest have been declared. survey, 1988–1994. American Journal of Clinical Nutri-
tion 72, 159–167.
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