Optimal feeding patters during infancy and childhood are determinants of health later in life. The beneficial effects of breast-feeding for healthy infants were previously established. Multiple organizations that deal with infant nutrition have recommended exclusive breast-feeding for the first 6 months of life (1–4). Extensive human epidemiological data have indicated that postnatal nutrition influences infant growth, development, and cognition (3–5). Furthermore, breast-feeding as opposed to infant formula feeding may affect adult health as well (1,6–16) via prevention of obesity or a decreased adult susceptibility to diet-related chronic diseases such as cardiovascular disease, insulin resistance, and type 2 diabetes, as well as cancer. Choice of formula may also affect infant health because formulas may differ in macronutrients and micronutrients such as long-chain polyunsaturated fatty acids, nucleotides, and oligosaccharides (17).
Infant formulas are sold directly to parents, often without a pediatrician's input, and infants may undergo multiple formula changes without any nutritional or medical guidance. The precipitating factors governing these changes may be of paramount importance to parents, but of minor consequence for pediatricians. Because any nutritional intervention during the early months of life may affect future health, we attempted to identify the frequency and factors that led to switching the source of infant nutrition in the first 6 months of life in term infants.
PATIENTS AND METHODS
The study sample consisted of 200 parents of infants ages 6 to 18 months who were brought for routine well-child care to 4 of the 47 maternal and child health care centers in the Haifa subdistrict of Israel between November 2002 and May 2003. The centers chosen were representative of the entire population of the Haifa area. The interviews were administered in a quiet and comfortable environment by a single interviewer and lasted approximately 30 minutes. Compliance with requests to interview was 100%. The infants' age range was limited to a maximum of 18 months to reduce recall bias. Chart records of the infants' weight as measured by the public health nurses in the centers were used. We had weight measurements for most of the group (birth weight for 200 infants, weight at 6 months for 185 infants, and weight at the time of the study for 129 infants. z scores, which were calculated using the NCHS 2000 growth tables, are a special application of the transformation rules. The z score for an item indicates how much and in what direction that item deviates from its distribution's mean, expressed in units of its distribution's standard deviation.
The questionnaire included 34 questions and was divided into 4 parts: demographic characteristics of the family (eg, urban vs rural community, ethnicity, religion, parents' age, parents' birth place, parents' year of immigration if applicable, parents' education, habits), infant health history (eg, age, sex, details on pregnancy and delivery, general health), feeding history for the first 6 months (eg, breast-feeding, duration, reason for stopping if applicable, supplements to breast-feeding, reason for supplementation and who suggested the addition if applicable, and formula use, specifically first formula, reason for choosing this formula, whether advertising affects formula choice, formula changes, change to what type and at what age, reasons for switching formulas, milk thickening and reasons for its use if applicable), and weight z scores. The study was approved by the ethical committee of the Israeli Ministry of Health.
Data analysis was performed using the SPSS statistical package (SPSS, Chicago, IL). The association between categorical variables was examined using the χ2 test. Number of formula changes was considered an ordinal variable because it is not normally distributed, and therefore nonparametric tests were used: Mann-Whitney test to compare number of changes between 2 subgroups (of dichotomous variables) and Spearman correlation coefficient to evaluate the relationship with education and with z score weight at birth, at 6 months, and at the time of administration of the questionnaire. Multiple linear regression analysis was performed to estimate adjusted effect.
Two hundred infants participated in the study: 117 boys and 83 girls ranging in age from 6 to 18 months (Table 1). Thirty-one infants (15.5%) were exclusively breast-fed for 6 months. The remaining 169 infants (84.5%) were fed infant formula exclusively (n = 39) or as a supplement to breast-feeding (n = 130). Changes in breast-feeding and formula supplementation in the first 6 months are presented in Fig. 1. Being the infant of orthodox Jewish parents was the only demographic parameter that was positively associated with breast-feeding.
Frequency of Formula Changes
Forty-seven percent of the infants experienced changes in their formula during the first 6 months: 35% experienced 1 change and 12% experienced ≥2 changes. Most changes (67%) were to another cow's milk–based formula. Twenty-two percent switched to a soy-based formula, 7% to an antireflux formula, and 4% to an elemental diet. The first change occurred at an average of 3 ± 1.7 months (range, 2 weeks to 6 months) and the second change occurred at an average of 3.5 ± 1.7 months. The main reasons for switching formula were regurgitation or vomiting (24%), followed by restlessness in 18% and no particular cause in 15% (Fig. 2). Pediatricians were involved in only 4% of formula changes.
The mother's education level had a significant inverse effect on formula changes. The more educated the mother, the less she reported changing her infant's formula (Spearman ρ, P = 0.002). We found no association between the number of changes and other demographic parameters such as sex, religion, nationality, parental age, and birth order (Mann-Whitney test). Forty-four percent of the parents thought the formula change led to an improvement of the symptoms reported.
Choice of Formula
Ninety percent of parents chose a cow's milk–based formula for their infant's first formula. Nine percent started with a soy-based formula and 1% started with an antireflux formula. Previous experience was the most common reason reported for choosing a specific formula (31%). Twenty-one percent continued with the formula supplied in the hospital where the infant was born, 18% proceeded according to the recommendations of a friend or a family member, and 12% chose to continue with the brand of a sample formula that they had received in the hospital. Only 3% of parents chose their infant's formula due to an advertisement in the commercial media. The reasons for choosing soy-based formula were previous experience in 50%, a friend or family member's recommendation in 20%, no particular cause in 20%, a nurse's recommendation in 5%, and a dietitian's recommendation in 5%. It is interesting to note that 50% of those who started with a soy milk–based formula switched to a cow's milk–based formula at some time.
Almost 60% of the breast-fed infants also received supplementation with an infant formula. A planned weaning (34%), a feeling of insufficient breast milk (28%), and restlessness (26%) were the main reasons cited for the addition of formula. Other reasons were the mother's return to work (11%) and a slow rate of growth of the infant (1%). Supplementation with a formula was usually a parental decision (72%) but was also done in response to a doctor's advice (13%), a nurse's advice (13%), or the recommendation of a friend or family member (3%).
Use of Formula Thickeners
Among the cohort of 200 babies, 65 (32.5%) received a cereal-enriched formula. The thickening was obtained with a soluble corn flour in 42%, a ready-made corn flour–thickened formula in 32%, rice cereal in 20%, and cooked corn flour in 6%. In most babies the thickening was begun after the age of 3 months. The reasons for formula thickening are shown in Fig. 3.
The decision to thicken the infant's formula was that of the parents in 43% of cases and was also in response to the public health nurse's recommendation (21.5%), the pediatrician's recommendation (20%), a family member's recommendation (3%), and a nanny's recommendation (3%). The thickening was considered effective in 43 infants (66%) and ineffective in 12.3%. Among those who reported that the thickening was to improve the infant's night sleep, thickening was reported effective in 83% of cases (n = 24).
Weight measurements were available for most of the infants enrolled: birth weight was available for 200 infants, weight at 6 months for 185 infants, and weight at the time of the study for 129 infants (Table 2). Lower z scores at birth were significantly associated with a higher number of formula changes (Spearman ρ = −0.156; P = 0.043). Nevertheless, the z score at 6 months or Δz1 (z score at 6 months minus z score at birth) had no effect on formula changes. In addition, we found that Δz2 (z score at the time of the questionnaire minus z score at birth) was associated with significantly more formula changes (analysis of variance, P = 0.004; Fig. 4), indicating that the children who had more formula changes thrived better. When we controlled for z score at birth, we found by using multiple regression analysis that birth weight and number of formula changes were positively associated with weight z scores. z Score at 6 months was significantly higher (t test, P = 0.048) for babies who received supplementation to breast milk compared with those who were exclusively fed with breast milk. We found no relation between milk thickening and growth (t test).
The first months of life constitute a critical period for the infant. Nutritional interventions may have consequences later in adulthood (7,11–13,15,16). Although exclusive breast-feeding is best for the infant, only 15% of mothers in our study exclusively breast-fed for the first 6 months. The majority (65%) started breast-feeding and then supplemented with a formula. The American Academy of Pediatrics and Israeli Pediatric Society recommend a cow's milk–based formula for non–breast-fed infants, and the majority of Israeli mothers (90%) start their infants on a cow's milk–based formula. However, nearly 50% of parents will switch formulas, usually without consultation with a health professional, and often for a perceived health problem. The most common indications for formula change were regurgitation, vomiting, and fussiness, indicating that parents believed that these symptoms reflect intolerance to formula. The choices made by the parents (eg, switching to another cow's milk–based formula) indicate their ignorance regarding components of formula, as well as their unwillingness to seek advice from a health professional.
Switching formula may reflect parental concerns regarding infant health and a belief that many problems in infancy may stem from food. This has been shown in the study by Forsyth et al (18). Our findings that infants who are born smaller have more formula changes, leading to a greater weight gain, may reflect more insecure behavior of the part of parents and more active involvement in feeding. Increased weight gain is not necessarily a sign of health. Formula feeding as opposed to breast-feeding may increase weight gain without improving infant health, and may be associated with higher frequency of obesity in later in life (6,8,10). This may be worsened further with increased energy density caused by unnecessary thickening.
Future health implications have also been linked to the use of soy-based formulas (19). Nine percent of parents initiated feeding with soy-based formulas and 22% of parents eventually switched to soy-based formulas without justifiable indications (20–22), almost all without involving health care professionals. The fact that 50% switch back to cow's milk–based formula demonstrates that most of the changes to soy milk–based formulas are indeed unjustified and that the public is unaware of the major risk of soy (20–22). The European Society of Pediatric Gastroenterology, Hepatology, and Nutrition Committee on Nutrition suggests that soy protein–based formulas should be used only in specified limited circumstances (eg, severe persistent lactose intolerance, galactosemia, and religious or ethical reasons) because they may have nutritional disadvantages such as high concentrations of phytate, aluminum, phytoestrogens, trypsin inhibitors, lectins, and goitrogenic substances. It is recommended that soy protein formulas should not be used during the first 6 months of life in infants with food allergy for the prevention of allergy and for the prevention or management of infantile colic, regurgitation, or prolonged crying (22).
Our study showed that almost 60% of the breast-fed infants received supplementation with an infant formula. There is evidence that supplementation of breast-fed infants with infant formulas increases the likelihood of stopping breast-feeding (4) and reduces the overall duration of breast-feeding (23). In addition, the addition of formula to breast-feeding reduces the advantages of exclusive breast-feeding (14). There is no doubt that the prevalence of supplementation is excessive and every effort should be made to limit the addition of formula to breast-fed infants unless there is a medical problem that mandates it.
We found only 2 previous studies in the literature that have dealt with switching infant formulas. Forsyth et al (18) followed 189 breast-fed and 184 formula-fed infants from birth. From telephone interviews conducted at the age of 4 months, they found that 11% of the breast-fed infants and 25% of cow's milk formula–fed infants were given cow's milk–free formulas (mainly soy based). Twenty-three percent of mothers believed that such a change solved the problem and an additional 29% believed the change alleviated the problem. The main reasons for change were excessive crying, colic, vomiting, diarrhea, spitting up, constipation, and feeding difficulties.
Polack et al (24), in a similar study of 175 parents conducted in 1995, found that 9% of infants started on a non–cow's milk–based formula. Another 36% of those who were started on cow's milk–based formula were then switched to a non–cow's milk–based formula (mainly soy based, especially in the outpatient clinic group). Colic and regurgitation were the main reasons for switching formulas. Improvement or complete resolution of symptoms was reported in 80%. In contrast to our study, the decision to change formula was made in 44% of the cases by the pediatrician, possibly reflecting changes due to suspected milk allergy.
We have concerns regarding the infrequent involvement of health care professionals and especially pediatricians on infant nutrition in a population with easy access to pediatricians and health care nurses. We believe nutrition is a relatively neglected issue in Israel and elsewhere that has significant consequences on infant future growth, morbidity, and development. Major efforts should be undertaken by health authorities to improve this situation. Educational interventions should be directed to the public and parents as well as health care professionals. Indications for using special formulas should be mandated on packaging. Health care professionals involved in well child care should definitely be more actively involved in giving nutritional advice to parents of young infants and evaluating these infants for causes that truly mandate formula change. Any change should be done with caution and for well-defined reasons. Pediatricians, nurses, and dietitians can play an important role in alleviating parental anxiety.
In conclusion, the most common reason for switching formula was concern regarding common infantile symptoms or behavior patterns perceived by parents to be related to formula intolerance. The choices of alternative formulas were usually made by the parents without consulting a health professional, and were most often to another cow's milk–based formula. Health care workers should be more actively involved in decisions regarding infant nutrition.
The authors thank all of the nurses of the maternal and child health care centers for their help and cooperation in the study.
1. Gartner LM, Morton J, Lawrence RA, et al
. Breastfeeding and the use of human milk. Pediatrics 2005; 115:496–506.
3. Koletzko B, Baker S, Cleghorn G, et al
. Global standard for the composition of infant formula: recommendations of an ESPGHAN coordinated international expert group. J Pediatr Gastroenterol Nutr 2005; 41:584–599.
4. Work Group on Breastfeeding. Breastfeeding and the use of human milk. Pediatrics
5. Agostoni C, Domellof M. Infant formulae: from ESPGAN recommendations towards ESPGHAN-coordinated global standards. J Pediatr Gastroenterol Nutr 2005; 41:580–583.
6. Agras WS, Hammer LD, McNicholas F, et al
. Risk factors for childhood overweight: a prospective study from birth to 9.5 years. J Pediatr 2004; 145:20–25.
7. Barker DJ. Fetal origins of coronary heart disease. BMJ 1995; 311:171–174.
8. Dietz WH. Overweight in childhood and adolescence. N Engl J Med 2004; 350:855–857.
9. Gluckman PD, Hanson MA. Living with the past: evolution, development, and patterns of disease. Science 2004; 305:1733–1736.
10. Hedley AA, Ogden CL, Johnson CL, et al
. Prevalence of overweight and obesity among US children, adolescents, and adults, 1999–2002. JAMA 2004; 291:2847–2850.
11. Levin BE. Metabolic imprinting on genetically predisposed neural circuits perpetuates obesity. Nutrition 2000; 16:909–915.
12. Lucas A. Programming by early nutrition in man. CIBA Found Symp 1991; 156:38–50.
13. Patel MS, Srinivasan M. Metabolic programming: causes and consequences. J Biol Chem 2002; 277:1629–1632.
14. Schack-Nielsen L, Michaelsen KF. Breast feeding and future health. Curr Opin Clin Nutr Metab Care 2006; 9:289–296.
15. Singhal A, Lucas A. Early origins of cardiovascular disease: is there a unifying hypothesis? Lancet 2004; 363:1642–1645.
16. Waterland RA, Garza C. Potential mechanisms of metabolic imprinting that lead to chronic disease. Am J Clin Nutr 1999; 69:179–197.
17. Eshach AO, Berant M, Shamir R. New supplements to infant formulas. Pediatr Endocrinol Rev 2004; 2:216–224.
18. Forsyth BW, McCarthy PL, Leventhal JM. Problems of early infancy, formula changes, and mothers' beliefs about their infants. J Pediatr 1985; 106:1012–1017.
19. Mendez MA, Anthony MS, Arab L. Soy-based formulae and infant growth and development: a review. J Nutr 2002; 132:2127–2130.
20. American Academy of Pediatrics Committee on Nutrition. Soy protein-based formulas: recommendations for use in infant feeding. Pediatrics
21. American Academy of Pediatrics Committee on Nutrition. Hypoallergenic infant formulas. Pediatrics
22. Agostoni C, Axelsson I, Goulet O, et al
. Soy protein infant formulae and follow-on formulae: a commentary by the ESPGHAN Committee on Nutrition. J Pediatr Gastroenterol Nutr 2006; 42:352–361.
23. Hornell A, Hofvander Y, Kylberg E. Solids and formula: association with pattern and duration of breastfeeding. Pediatrics 2001; 107:E38.
24. Polack FP, Khan N, Maisels MJ. Changing partners: the dance of infant formula changes. Clin Pediatr (Phila) 1999; 38:703–708.
© 2007 Lippincott Williams & Wilkins, Inc.