Freeman, Valerie‡; Hof, Martin van't*; Haschke, Ferdinand†; Euro-Growth Study Group
International recommendations for feeding infants do not vary widely (1–5). Breast-feeding is universally accepted as the optimal milk-feeding method and is promoted actively (1,6). Infant formula, fortified with vitamins, minerals, and trace elements, is recommended for infants who are not breast fed or during the weaning period. Follow-up formula may be used between 5 and 36 months of age (7). Soy-based formulas, hydrolysates, and hypoallergenic formulas have been available since the late 1980s, but indications for their use have been controversial (8–12). Unmodified cow's milk is known to be unsuitable for infants until 12 months of age, because they receive little iron, linoleic acid, and vitamin E and have excessive intakes of sodium, potassium, and protein (3). Moreover, 6-month-old infants fed whole cow's milk showed increased gastrointestinal blood loss (13).
It is recommended that the introduction of complementary foods begin between the ages of 4 and 6 months for the majority of infants (14,15). Recommendations for the use of nutritional supplements—for example, vitamins—are less definite. Although in most European countries supplements are given to infants only on medical advice, practice varies from one country to another. To what extent these recommendations for infant feeding are met in European infants and young children is not known. Neither is it clear whether adherence to guidelines is uniform or varies widely between countries as a result of local customs or specific policies, which may not strictly follow international guidelines.
Little is known about current infant feeding trends in Europe. In 1986, Ballabriga and Schmidt (16) published a survey on prevalence of breast-feeding, use of infant formula, and cow's milk and the use of weaning foods. The survey was based on a questionnaire, that was sent to ESPGHAN members in 22 European countries. The results indicated substantial differences in the duration of breast-feeding between European countries. Commercial infant formula was used until 3 to 6 months of age and cow's milk was introduced between 5 and 9 months of age in most countries. Age of introduction of solids was between 2 and 4 months.
The Euro-Growth Study now allows a detailed analysis to be made of feeding habits in 12 European countries. It should be noted that the local study center may not necessarily reflect the national situation. In this longitudinal, observational, multicenter study of European infants, feeding habits were recorded at regular intervals during the first 3 years of life. Simultaneously, growth was measured, and disease patterns and socioeconomic and life-style variables, which may interact with growth and nutrition, were recorded. The objective of this article is to describe feeding habits of infants and young children and to consider how well feeding patterns of European infants adhere to international guidelines. Feeding practices, milk (type, volume, bottle or cup), solids (age of introduction, food type), supplements (iron, vitamins), and feeding frequency are discussed.
PATIENTS AND METHODS
The Euro-Growth Study was a longitudinal, observational multicenter study. Healthy infants (birth weight >2500 g, gestational ages 37–44 weeks) who had no signs of intrauterine growth pathology and who did not meet the remaining exclusion criteria (17) were enrolled before 30 days of age. Details of the methodology, background of the study population, and anthropometric measurements have been published (17,18).
The initial interview was completed before the infant reached the age of 30 days. Target ages for the interviews and measurement occasions were 1, 2, 3, 4, 5, 6, 9, 12, 18, 24, 30, and 36 months. On each occasion, semiquantitative dietary data (19), and illnesses (e.g., hypersensitivity reactions to food, allergies (20) and infections) of the infant were recorded. Atopic history of the family (mother, father, siblings) was recorded during the study period.
Breast-feeding was defined according to the World Health Organization (WHO) (21) as follows: full breast-feeding described taking solid food but no milk other than breast milk; partial breast-feeding described taking milk in addition to breast milk, with or without inclusion of solid foods. Exclusive breast-feeding (breast milk only—no other milk, no solid foods) could be derived from the data.
Feeding practices described in this article were recorded under the following headings:
• Breast milk: partial, full;
• Formula, infant: cow's milk–based (22), soy-based (8), partially hydrolyzed formula (`hypoallergenic') (9,10), extensively hydrolyzed formula (`hydrolysate') (9,10), other, iron-fortified;
• Formula, follow-up: cow's milk–based (7), soy-based (8);
• Cow's milk: full, low fat; milk volume (19) : usual consumption (in milliliters per day); breast milk volume was not assessed;
• Feeding method: bottle or cup.
Solid foods were recorded semiquantitatively (19) during the first 2 years. Categories were: never, sometimes (1–2 times per week), and every day. Food was categorized in the following groups: fruits, fruit juices; vegetables; beans, peas; infant milk-based cereals; bread, pasta, other cereals; rice, potatoes; milk products (yogurt, cheese); eggs; and meat, fish, and poultry.
No detailed dietary data were recorded in the third year. If children had a feeding problem and/or were consuming a special diet, it was specified as part of the record of general health information. Vitamin and iron supplements were recorded at each interview. Feeding frequency was recorded as the usual number of times the infant was fed per day.
Sample and Data Analysis
The cohort, which was drawn from 22 centers in 12 European countries, consisted of 2245 infants (1154 boys and 1091 girls) born from August 1990 through October 1993. At the ages of 12, 24, and 36 months, respectively, 2050 infants in 22 centers, 1667 infants in 20 centers, and 1071 infants in 16 centers continued to participate. A comparison between participants and nonparticipants revealed that the sample was representative for length and weight of mothers, urban residency, and gender and birth weight of infants, but not for maternal age and educational level. Participating mothers were 1 year older and had spent longer in formal education than nonparticipants (23).
A withdrawal analysis showed that withdrawal within 1 year was significantly selective for duration of breast-feeding (analysis of variance, P = 0.006) but not for introduction of solids (P = 0.50). Withdrawn infants had a mean duration of breast-feeding of 0.5 months less than the remainder. Infants withdrawn after 2 or 3 years did not show any significant differences in breast-feeding or introduction of solids compared with the others.
Duration of breast-feeding (age at cessation) and age of introduction of solids were derived from the longitudinal feeding data. The first problem in assessing these milestone ages was encountered when a measurement was missing. This was not a serious problem when a missing observation was surrounded by two equal observations. The twice-observed value was then assigned to the missing observation. For example, if a record for one occasion was missing, but the infant was fully breast fed on the occasion before and on the occasion after the missing record, it was assumed that the infant was fully breast fed at the time of the missing record. If the missing record was surrounded by two different values, the earlier or later value was used randomly. No attempt was made to estimate milestone ages in 55 infants who were withdrawn during the first 3 months (2.4%).
The second problem was encountered when an inconsistent longitudinal series was seen. This included situations of formula feeding followed by breast-feeding or very isolated early consumption of solids. In most cases only one unique solution was possible. In other multi-interpretable situations, random values were assigned to achieve consistency. For the estimation of the duration of breast-feeding, randomization was necessary in only 7.9% of the infants. The age of introduction of solids could not be estimated for 116 infants (5.2%) because of missing information. Certain analyses—for example, the duration of exclusive breast-feeding—were relevant only up to the age of 12 months.
Milk-feeding practices during the first year are shown in Table 1. At the age of 1 month, 52% of the infants were exclusively breast fed, 2% were fully breast fed (breast milk and solids), 26% were fed formula milk, and 21% were breast fed but were also receiving formula. At the ages of 2, 3, and 4 months, 35%, 25%, and 15% of infants, respectively, were breast fed exclusively. The duration of full and partial breast-feeding (1–12 months) in the total sample is shown in Table 2. Breast-feeding was less common than formula feeding after the age of 2 months. Differences in the distribution of breast-feeding duration between the study centers are shown in Appendix 1. At the ages 1, 2, 3, 4, 5, 6, 9, and 12 months, follow-up formula was fed to 0.9%, 2.0%, 2.4%, 8.2%, 28.9%, 45.0%, 66.1%, and 73.6% of formula-fed infants, respectively. At the ages of 18 and 24 months, few children received breast milk or infant formula.
Cow's milk was exclusively fed from the age of 2 months (Table 1). At the ages of 6 and 9 months, 9% and 18% of infants, respectively, were fed only cow's milk. Cow's milk was recorded as full fat, skimmed, or 1% to 2% fat (Table 3). Because neither skimmed nor reduced-fat milks are recommended for infants and small children (24), the two were combined for the purpose of the analysis and termed low-fat milk. Few infants consumed cow's milk during the first 2 months. The percentage of cow's milk–fed children who consumed low-fat milk increased gradually from 15% at the age of 3 months to 25% at the age of 12 months and 33% at the age of 36 months.
In total, 2011 (90%) children had even been formula fed (infant or follow-up formula). The majority of these (1780, 89%) were fed cow's milk–based formula. The remainder were fed a variety of specially modified formulas. Special formulas included partially hydrolyzed formula, extensively hydrolyzed formula, and infant or follow-up soy-based formula. Special formula was fed to 231 infants, but 79 were fed special formula on only one occasion, suggesting that the milk was not what the infant usually consumed, leaving 152 (8%) of formula-fed infants who regularly consumed a special milk. Table 4 shows the percentage of infants who consumed partially hydrolyzed formula, extensively hydrolyzed formula, soy-based formula, or any one of these (special). Depending on age, special formula was used by 3.9% to 7.3% of formula-fed infants during the first year of life. Use varied significantly between the centers. In certain centers (e.g., east and west Hungary; Athens, Greece; or Nancy, France) no infant received special formula on a regular basis, whereas in others (e.g., Vienna, Austria; Madrid, Spain; Dortmund, Germany; or Reims, France) these formulas were used for 12% to 34% of infants regularly.
Indications for the use of special milks include atopic disease of the infant and family history of allergy (12). The partially hydrolyzed formulas and extensively hydrolyzed formulas are used in an effort to prevent the development of atopy in non–breast-fed infants who are at risk of atopic disease. In addition, extensively hydrolyzed formulas are recommended for treatment of cow's milk allergy in bottle-fed infants (12). The family history of allergy (mother, father, and siblings) was recorded for 1735 children who were monitored until 24 months of age. Of the 123 consuming special milk, 33% had a family history of atopy. This is significantly greater (χ2 test, P = 0.0002) than the 16% in the 1612 consuming normal milk.
Atopic diseases of the infant reported during the first year were used to study the interaction between diseases and consumption of special formula. Disease information on 2111 infants was available. Of the 149 consuming special milk, 52% had reported an atopic disease compared with 29% of the 1962 consuming normal milk (χ2 test, P < 0.00001).
Combining both indications (perceived atopy of the infant and a family history of atopy) in the 1735 infants, it was observed that 68% of those consuming special milk had any indication, compared with 39% of those consuming normal milk (χ2, P < 0.00001).
The association between use of special milks and the presence of an indication for their use varied significantly between the centers. In most of of the centers, the milks appeared to be used mainly for children at risk of atopic disease or to treat atopy. In one French center, 22% of infants were fed a special milk, which indicates that these milks were also fed to infants when no specific indication for their use (12) could be derived from the data.
The volume of milk consumed was recorded for infants who were fed formula milks or cow's milk. Breast-fed and partially breast-fed infants were excluded from the analysis. The distribution of volumes consumed at each age is shown in Table 5. The mean ± SD volume of milk consumed ranged from 740 ± 160 ml/d at age 1 month to 840 ± 190 ml/d at age 3 months and decreased again to 490 ± 200 ml/d at the age of 12 months. Between the ages 2 and 4 months, 15% of non–breast-fed infants were reported to be drinking more than 1000 ml/d, whereas from the age of 9 months, 70% of infants drank less than 500 ml/d. These large milk volumes represent a quantity of approximately 250 ml/kg per day. Milk intake was recorded as the usual consumption per day and may have been somewhat overestimated. However, at the age of 3 months the upper limit of the 95% confidence interval of the mean volume of milk consumed was more than 850 ml/d in 15, and more than 900 ml/d in 9 of the 22 participating centers. This may reflect an increased demand for energy in advance of the introduction of complementary foods.
Whether the child was drinking from a bottle or a cup was recorded for 1151, 949, 653, and 594 children at the ages 18, 24, 30 and 36 months, respectively. Bottle use was common during the second and third years, decreasing gradually from 86% at 18 months to 62% at 36 months.
Introduction of Solids
For the purposes of the analysis, some of the recorded food groups were combined. The combinations were as follows: fruit or fruit juices (Fruit); vegetables, peas, and beans (Vegetable); cereals, rice, and potatoes (Cereal); bread, pasta (Bread); meat, poultry, and fish (Meat); eggs (Eggs); and milk products, yogurt, and cheese (Milk products). Table 6 describes the introduction of solid foods from 1 to 24 months. Solid foods were introduced from the age of 1 month; at the ages 3, 4, and 6 months, 50%, 67%, and 95% of infants, respectively, were receiving some solid food. Fruit (73%) and cereals (51%) were the first foods used for most infants (Table 7). The order in which the feeding of specific foods began varied among the centers, although fruits were used first and milk products last in the majority (Appendix 2).
Milk-feeding practice was considered in relation to the age of introduction of solids. Duration of breast-feeding was significantly (P < 0.0001) correlated (r = 0.41 [full] and r = 0.42 [part]) with age of introduction of solids. Eighty-three percent of those who stopped breast-feeding before the age of 1 month and 61% of those who were breast fed after 4 months had begun eating solids by the age of 4 months. When controlled for center, positive correlations (median r = 0.30) between breast-feeding and the age of introduction of solids remained highly significant.
Table 8 shows the percentage use of iron and vitamin supplements. Vitamin supplementation was much more common than iron supplementation; at the age of 5 months, 72% of infants were supplemented with vitamins and 6% with iron. Use of both increased during the first year and then decreased. Formula milks are fortified with vitamins and iron, but supplements may be recommended if infants are fed unmodified cow's milk. Therefore, the relationship between iron supplementation and cow's milk consumption was examined. Cow's milk consumption increased gradually during the first year, but use of supplemental iron remained relatively constant. Fifteen percent of infants who were fed cow's milk and 12% of those who were not fed cow's milk were given iron drops. When the association between having ever consumed cow's milk and having ever used iron drops in the first year of life was examined, there was no significant correlation in the total sample (χ2 test, P = 0.06) nor in the individual centers. However, when cow's milk consumption was categorized according to the month of introduction, a small but significant negative correlation with use of iron drops was evident (Pearson correlation r = −0.05, P = 0.036). The earlier the age at which cow's milk was introduced, the later iron drops were administered.
Feeding frequency (Table 9) was recorded as the number of feedings per day. In the total group, feeding frequency decreased significantly (P < 0.0001) from (mean ± SD) 6.7 ± 1.4 feedings per day at age 1 month to 4.6 ± 1.1 at age 6 months. At the age of 1 month, frequency of feeding for breast-fed, partially breast-fed, and formula-fed infants was 7.1 ± 1.5, 6.6 ± 1.3, and 6.1 ± 1.0, respectively. All differences were highly significant (P < 0.0001), even after correction for center. Feeding frequency also differed significantly among the centers (P < 0.001).
Whether earlier (1–5 months) feeding frequency was related to the frequency of feeding at the ages 6, 9, and 12 months was considered. Partially breast-fed infants were excluded from the analysis. Having controlled for the influence of center, feeding frequency at 1, 2, 3, 4, and 5 months was significantly (P < 0.05 to P < 0.001) related to frequency of feeding at 6 and 9 months and feeding frequency at 4 and 5 months significantly (P < 0.001) related to frequency at age 12 months (Table 10). Correlation coefficients were in the range of 0.14 to 0.51 (6 months), 0.14 to 0.20 (9 months), and 0.20 to 0.22 (12 months). There was no relationship between feeding frequency during the first 3 months and feeding frequency at age 12 months.
Whether the duration of full breast-feeding was related to the frequency of feeding was examined. Only infants who were fully breast fed at age 1 month (n = 1135) were included in the analysis. There was a positive correlation (r = 0.18;P = < 0.0001) between the frequency of breast-feeding at age 1 month and the duration of full breast-feeding in the total sample. Mothers who breast-fed more often were likely to continue breast-feeding longer. Although the correlations per center were no longer statistically significant, the tendency to a positive correlation was still evident (median, r = 0.08;P = 0.01–0.98).
Infants and young children grow more rapidly than adults. In the first year of life, infants triple their birth weight and double their surface area, an accomplishment that is not matched at any other time during the life cycle. Growth rate slows significantly only during the third year (25). During this critical period, patterns of food intake also change dramatically. The infant moves from a completely milk-based diet to consumption of a wide range of foods with potential for significant variation in how this change is achieved. Feeding recommendations are designed to give guidance on optimal nutrition and guarantee an adequate nutrient intake to sustain this rapid rate of growth and development.
The majority of infants in the Euro-Growth cohort were breast-feeding at the age of 1 month, with 74% fed some breast milk. However, only 25% and 15% of Euro-Growth infants were breast-feeding exclusively, according to WHO recommendations (21), at the ages 3 and 4 months. Breast-feeding patterns differed significantly between the centers, reflecting different levels of breast-feeding promotion. For example, in the longitudinal sample at age 1 month, 99% of infants in Athens and 97% in Umea were breast fed, whereas the corresponding statistic for Irish infants was 30%. It should be noted that breast-feeding practice in a study center is not necessarily representative of the country in which the center is located.
Frequency of feeding differed significantly between breast-fed and non–breast-fed infants at the age of 1 month. Frequent feeding is recommended as the physiological norm (1,2). Euro-Growth mothers who breast fed their infants more frequently at the age of 1 month continued to breast feed fully for a longer period than those who breast fed less frequently at this age. Prolonged breast-feeding as a result of increased feeding frequency is probably mediated through increased levels of prolactin, which enhances synthesis of milk protein and lactose (2). It has already been shown that breast-feeding frequency differed significantly among the centers (26) and has been hypothesized that advice given by professionals to breast-feeding mothers may influence them to breast feed less frequently. Frequent breast-feeding in the early weeks should be encouraged in an effort to increase the duration of breast-feeding in European infants.
From the age of 2 months, the majority of infants were formula fed. Infant formula was most commonly used, but follow-up formula, which is permitted for use only after the age of 4 months, was fed to a small percentage of infants during the first 3 months. Although their use is regulated under European Union legislation, in comparison with using infant formula, there is little scientific evidence to support the general use of follow-up formula (27,28), and more recent research indicates that levels of iron (29) in follow-up formula are unnecessarily high.
A partially hydrolyzed formula was used more commonly in the Euro-Growth cohort than either soy-based formula or extensively hydrolyzed formula. Use of soy-based formula was low, ranging from 0.4% to 1.6% of formula fed infants during the first year. In the United States, it was recently reported that 25% of formula used is soy-based formula (30). A soy-based formula provides an alternative to cow's milk based–formula if lactose-or galactose-free regimens are indicated or if the dietary regimen is vegan. They are not appropriate for use in the treatment of cow's milk protein allergy or intolerance. For infants who are not breast fed, `hypoallergenic' formulas may be recommended for prevention of allergic disease and cow's milk allergy in families with a history of atopy. An extensively hydrolyzed formula may also be used for treatment of cow's milk allergy (20). In the Euro-Growth cohort the use of these special milks was clearly related to the presence of atopic disease in either the infant or a first-degree relative. However, in one center in France, special milk was commonly used when no indication for its use could be determined from the data.
During the past 10 years, it appears that there has been a major improvement in the situation in Europe regarding the use of unmodified cow's milk for infants. In 1987, it was reported that 40% of infants at 6 months and 75% of infants at 9 months were consuming cow's milk (4). In the Euro-Growth study, only 18% at 6 months and 33% at 9 months were fed cow's milk; 18% of 9-month-old infants were fed only cow's milk. The role of cow's milk as a risk factor for iron-deficiency anemia in infancy is now well accepted (31). Low-fat cow's milk, which is commonly recommended for adults, provides an inadequate source of energy for infants (19), and it is therefore of concern that it is being fed to almost one quarter of cow's milk–fed infants from the age of 6 months.
The introduction of complementary food (solids) is not recommended before the age of 4 months, but more than half of the Euro-Growth infants were consuming some solid food by the age of 3 months. Most of these were eating only one or two foods, but 13% consumed three or more foods. This appears similar to what was shown in a previous European survey (15), in which it was reported by pediatricians that solid foods were introduced between 2 and 3 months. However, the results from the Euro-Growth study provide a much more accurate estimation of feeding practices in the participating countries. The earlier survey results were from on a variety of sources, including “guesstimates” of pediatricians. The Euro-Growth data were collected prospectively by interviewing parents or guardians at frequent, regular intervals during infancy. In the United Kingdom in 1995, 55% of infants were reported to be taking solid foods by the age of 3 months (32), a somewhat higher percentage than in the Euro-Growth cohort (46%).
Early introduction of solids has been associated with increased risk of wheezing, increased percentage of body fat, and increased body weight during childhood (24). However, in the Euro-Growth Study, a comparison of the impact on growth of introducing solids to breast-fed infants before or after the age of 4 months showed that earlier introduction of solids was associated with lower body mass index (BMI) between 1 and 12 months of age (33). By the age of 24 months, the differences were small and clinically nonsignificant. This contrasts with findings from the DARLING study, in which z-scores for weight, length, and weight for length did not differ (1–18 months) between breast-fed babies to whom solids were fed before or after the age of 6 months. Infants who consumed solids later (after the age of 6 months) gained less weight between 6 and 9 months than those to whom solids were fed before 6 months (34). It is well recognized that the early introduction of solid foods is common, but the long-term impact of this practice on health requires further clarification in both breast-and formula-fed infants. Studies that focus on additional outcome measures as well as growth may be of value.
There appears to be little consistency in the use of vitamin supplements in this sample of European children. This is not surprising because there is a scarcity of information on the vitamin status of infants, and recommendations for vitamin supplementation are not consistent throughout Europe. For example, in the United Kingdom, a supplement of vitamins A and D is recommended (35), whereas in Ireland no such recommendation exists (36).
The situation regarding iron supplementation has changed in recent years. Previously, when cow's milk, a poor source of iron, was commonly given to infants, iron supplementation was necessary to prevent the development of iron deficiency anemia. It is now recommended that breast milk or iron-fortified formula continue to be the main milk drink until the age of 12 months (3). From the age of 4 to 6 months, complementary foods, such as meat (37), should gradually become the main source of iron in the diet, and supplementation with iron should not be necessary. That there was no positive correlation (ever having cow's milk with ever receiving iron drops) and the small negative correlation (age of introduction of cow's milk with ever having iron drops) may reflect the fact that less well-informed mothers tend to use cow's milk without understanding the increased risk to the infant of an inadequate supply of iron. It was also shown in The Euro-Growth Iron Study (38) that the prevalence of anemia was four times higher in low (11.2%) versus high (2.7%) socioeconomic families.
The Euro-Growth Study reveals a relatively low level of breast-feeding initiation in many European centers (Dublin, Toulouse, Glasgow), whereas in others, the majority of infants are breast fed initially (Athens, Umea, west Hungary). Recent publications confirm the advantages of breast-feeding in the prevention of infection (39–41) and modulation of the immune response (42) and for its impact on growth (43,44). Further efforts are necessary to increase breast-feeding rates all over Europe to those seen in Umea and Athens. Programs should educate, encourage, and support mothers to initiate breast-feeding, to breast-feed exclusively during the early months, and to continue breast-feeding as complementary foods are introduced. The study also revealed early introduction of complementary foods and of cow's milk and inconsistency in relation to vitamin and mineral supplementation.
It is important to continue to provide nutrition education and support, targeted, in particular, toward less well-educated parents, to improve adherence to internationally accepted nutritional guidelines and, consequently, improve infant nutrition and health in Europe.
EURO-GROWTH STUDY GROUP
Austria (A): C. Male, A. Golser; C. Huemer, B. Pietschnig
Croatia (HR): I. Svel, G. Armano
France (F): J. Schmitz, J. L. Muns, J. Beley, B. Digeon, J. Panis; G. Degy
Germany (D): F. Manz, E. Jekov, M. Radke
Greece (G): T. Zachou; S. Egglezou, J. Sofatzis
Hungary (H): E. Barko, S. Darvay
Italy (I): M. Salerno
Ireland (IRL): H. Hoey, M. Gibney
Portugal (P): N. Teixeira Santos, A. Guerra, C. Rego, D. Silva
Spain (E): M. Hernandes, J. Molina, C. Ruiz; R. Tojo, E. Sanches, I. Rica; J. Argmeni, J. Rivera, C. Garcia-Caballero; M. Monleon, M. Manrique
Sweden (S): L. Persson, M. Lundstrom
United Kingdom (GB): J. Durnin, J. Reilly, S. Savage
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