Breastfeeding is the best and most accessible means of preventing various diseases in children and adults. During the first six months of postnatal life, it fully satisfies all nutritive needs of the infant. After the sixth month, breast milk no longer satisfies all nutritive requirements for adequate infant growth and development, which means it is time to introduce complementary feeding.
Bearing the benefits of breastfeeding for both the mother and infant in mind, the European Society for Paediatric Gastroenterology, Hepatology and Nutrition (ESPGHAN) and the North American Society for Paediatric Gastroenterology, Hepatology and Nutrition (NASPGHAN) promote breastfeeding as the healthiest diet. The focus of the research agenda of the ESPGHAN Committee on Nutrition is the influence of breastfeeding on infants’ health, as well as their health later in life.
The next question that needs to be addressed is when should complementary feeding be introduced.
The first two years represent a “critical” window for the influence of nutrition on health. Due to the long-term influences of the diet of infants and small children, nutrition in this earliest period of life lies at the centre of interest and activities of both the World Health Organization (WHO) and UNICEF.
DEFINING COMPLEMENTARY FEEDING
WHO uses the term complementary feeding to refer to all solid or liquid foods other than breast milk.
ESPGHAN uses the term in reference to all solid or liquid foods other than breast milk or infant formula. This definition is certainly more comprehensible and acceptable for healthcare workers and parents.
Some authors use the term “weaning foods” to refer to food that will gradually replace breastfeeding. This definition is unacceptable, since it is important for both the mother and infant to continue breastfeeding even after complementary feeding has been introduced.
The period of complementary feeding is the period when infants are given other food or liquids in addition to breast milk.
Due to an increase in infant undernutrition in developing and underdeveloped countries on the one hand, and obesity and eating disorders in developed countries on the other, WHO and UNICEF place complementary feeding among priority topics in infant and child nutrition.
The timely introduction of complementary feeding is necessary for both nutritive and developmental reasons, and to enable a timely transition from breastfeeding to family foods. The ability of breast milk to meet the infant’s energy, macro- and micronutrient requirements becomes limited with the increasing age of the infant. This lack must be compensated by complementary feeding.
The untimely introduction of complementary feeding among infants and small children may cause malnutrition, which can ultimately lead to underdeveloped function and motor skills, and subsequent poor results in school. Similarly, it increases the risk of infections which can even cause death. Complementary feeding can be qualitatively or quantitively inadequate from a nutritionist point of view. The quality of complementary feeding depends on the parents’ knowledge of its importance, as well as the economic and ecological conditions in which the child lives.
BREASTFEEDING AND COMPLEMENTARY FEEDING
Recommendations regarding the optimal timing for introducing complementary feeding and the nature of the foods given vary between countries, largely due to limited scientific evidence on the short- and long-term effects on health of introducing complementary feeding.
At its 54th Assembly held in 2001, WHO recommended exclusive (full) breastfeeding during the first 6 months and partial breastfeeding (coupled with complementary feeding) thereafter, until the age of 2.
However, ESPGHAN recommends that complementary feeding be introduced no sooner than the 17th and no later than the 26th week. ESPGHAN also points out that the optimal time for introducing complementary feeding may differ depending on the country. Differences and disagreements in the practices of individual countries are a result of insufficient scientific evidence in developed countries, on which the above-mentioned recommendations are based. Disagreements relate to the dis/advantages of introducing complementary feeding in the period between 4 and 6 months of age, provided the child has previously been exclusively breastfed.
Existing research includes randomised studies conducted in developing countries and observation studies conducted in developed countries. In underdeveloped countries, exclusive breastfeeding compensates for the lack of clean drinking water and different types of solid foods. Due to the socio-economic conditions in industrially developed countries, the conclusions of randomised studies conducted in developing countries hardly apply to children in developed European countries.
On the other hand, the results of some observational studies indicate that there are no differences in growth between infants exclusively breastfeed for 3–4 months and those who have been exclusively breastfed for 6 months. However, there is a certain connection between the longer period of exclusive breastfeeding and the low frequency of infectious diseases of the digestive tract. Differences in the frequency of infections of the respiratory tract and atopic dermatitis have not been proven. In developing countries, it is therefore important to prolong breastfeeding even after complementary feeding has been introduced. In Europe, where the frequency of communicable diseases is low, the recommended length of partial breastfeeding (that which continues after complementary feeding has been introduced) has not been strictly defined. It is considered that breastfeeding should continue for as long as the mother and infant desire (the nutritive and psychosocial benefits of breastfeeding should be considered). WHO recommends that breastfeeding be continued for at least two years, while the American Academy of Pediatrics recommends that it be continued for at least one year.
The optimal timing of introducing complementary feeding may be an issue with infants born to malnourished mothers, or mothers following strict vegan or macrobiotic diets. The question is whether their breast milk satisfies all the infant’s requirements during the first 6 months. Some evidence suggests that breast milk from malnourished mothers or mothers following restrictive diets contains satisfactory levels of proteins, fat and carbohydrates, but that the amount of milk is questionable. The breast milk of mothers following strict vegan or macrobiotic diets may not contain sufficient levels of some vitamins (especially vitamins A and D), iodine and some fatty acids. Possible vitamin B12 deficiency creates the risk of severe megaloblastic anaemia and neurological disorders.
It is therefore recommended that breastfeeding women who follow a strict vegan diet take vitamin B12 supplements. The risk is even greater if complementary foods do not contain animal proteins. Some studies suggest that, due to deficiencies of calories, protein, vitamin B12, vitamin D, riboflavin and calcium, infants breastfed by mothers following strict vegan or macrobiotic diets experience an impairment of growth and psychomotor development.
TIMING OF INTRODUCTION OF COMPLEMENTARY FEEDING
Some studies report that certain South American countries introduce complementary feeding in the form of teas too early, which leads to a reduction of the breastfeeding period. The same study reveals problems with the later introduction of complementary feeding, e.g. at the age of 10 months.
While there is a relatively clear attitude related to the timing of introducing complementary feeding, the optimal timing for the introduction of individual types of food into the infant’s menu has yet to be scientifically defined. Practices regarding the introduction of individual complementary foods therefore vary widely between countries. For example, most countries recommend that cow’s milk should not be introduced before the age of 12 months, whereas Denmark, Sweden and Canada state it can be introduced from the age of 9 to 10 months. The suggested age for the introduction of fish or eggs (egg whites) also varies considerably depending on the country: some recommend the introduction of these food items from 4 to 6 months, while others recommend waiting until 9 or 12 months.
BIOLOGICAL AND DEVELOPMENTAL ASPECTS OF COMPLEMENTARY FEEDING – PHYSIOLOGICAL AND NEUROLOGICAL MATURATION
Available scientific data suggest that both the kidney and digestive system are sufficiently mature to metabolise nutrients from complementary foods by the age of 4 months. On the other hand, introducing solid foods and switching from a high-fat to a high-carbohydrate diet leads to an increase in the enzymatic maturation of the digestive tract. The maturation of the digestive tract is therefore connected to the infant’s diet.
As far as neurodevelopment and, consequently, the development of the motor skills necessary for eating solid foods are concerned, it is known that most infants are able to sit with support and scoop food off a spoon using their upper lip by around 6 months of age. By around 8 months, they develop sufficient tongue flexibility to enable them to chew and swallow more solid lumpier food in larger portions. From 9 to 12 months, most infants possess the motor skills needed to feed themselves and drink from a standard cup using both hands. It is important to bear in mind that if solid foods are not introduced by around the age of 10 months, this may increase the risk of feeding difficulties later in life.
Different causes of somatic growth were recently discovered among European breastfed infants. On most current growth charts, 3-month-old exclusively breastfed infants typically show a deceleration of growth when compared with the growth acceleration of formula-fed infants. Therefore, WHO recently published a new growth standard based only on the growth of healthy breastfed infants.
Compared to the speed of growth of breastfed infants, the acceleration of growth of formula-fed infants may suggest the possibility of introducing complementary foods earlier. Since WHO defines infant formula as a type of supplementary feeding, we cannot consider its introduction as the beginning of complementary feeding, but rather as its continuation. However, WHO is afraid that different recommendations regarding the timing of the introduction of complementary foods for exclusively breastfed and formula-fed infants may confuse healthcare workers and, consequently, parents. This is why their latest recommendations do not mention differences in the timing of introducing complementary feeding for exclusively breastfed and formula-fed infants.
When compared to breast milk, infant formula contains higher levels of certain micronutrients, primarily iron and zinc. This might lead us to conclude that, due to their increased micronutrient requirements, complementary feeding should be introduced earlier to exclusively breastfed infants. Some recommendations claim that, due to increased iron and zinc requirements, meat should be introduced earlier to breastfed infants.
Zinc deficiency may be expected in the case of dysmaturity, prematurity and infants born to mothers with poor nutrition during pregnancy, which results in insufficient intrauterine zinc storage in the liver. Some studies suggest that maternal zinc concentration and intake have little effect on zinc levels in breast milk. Gibson et al. state that in the period between 9 and 11 months, more than 90% of iron and zinc requirements are introduced via complementary foods (meat). Prolonged breastfeeding, coupled with the absence of complementary foods (meat), can result in lower iron levels in the infant organism. Phytates and iron bioavailability in grains also affect the iron and zinc status. Ascorbic acid improves iron bioavailability in grains.
MILK FEEDING DURING THE COMPLEMENTARY FEEDING PERIOD
Continued breastfeeding is recommended along with the introduction of complementary feeding. If it is no longer possible to breastfeed, infants should continue to be fed by formula. Most countries recommend waiting until 12 months before introducing cow’s milk. The reason for this delay is the link between the introduction of cow’s milk into the infant’s diet and iron deficiency. Microscopic intestinal bleeding provoked by the premature introduction of cow’s milk leads to anaemia. However, Canada, Sweden and Denmark claim that cow’s milk can be introduced from 9 to 10 months of age.
It has been suggested that the intake of cow’s milk can promote rapid growth, increase blood pressure and the risk of obesity. Regardless of its energy value and the current obesity pandemic, skimmed milk is not recommended for infants before the age of 3.
EFFECTS OF COMPLEMENTARY FEEDING
Due to a lack of scientific evidence, it is difficult to conclude how exactly complementary feeding (more specifically, individual types of foods) indirectly influences infant growth. Infant weight was found to predict the age at which complementary foods were introduced. Heavier infants typically begin to consume solid food earlier. However, the decision when to introduce complementary foods should be based on the infant’s age, not weight.
The percentage of fat in infant nutrition should satisfy the infant’s energy needs. Results of a study conducted in 19 countries in Central and South America observed poor growth among infants with less than 22% of fat content in their diet. In contrast, excessive intake of energy-dense foods can lead to increased risk (by 2 to 3 times) of obesity at school age. A 16%-protein intake (or higher) in complementary feeding in the period between 8 and 24 months of age are associated with weight problems later in life. This correlation was not found in cases when protein intake was below 15%.
Numerous studies have shown that breastfeeding is linked to better neurological development, but the large number of mediatory factors makes it difficult to specify this causal link. The critical period in which certain nutrients influence the maturation of the cortex remains unknown. Nowadays, scientific efforts are aimed at determining how nutrients affect the brain structure, functions and activities. Nutrition recommendations should be based on these findings. It would be useful to know when (considering the periods of neurogenesis and synaptogenesis) to administer nutrients that are (to a lesser or greater degree) relevant for normal neuron growth and brain development. The last 25 years have not yielded any significant findings in this respect. The positive effects of iron, iodine and zinc on brain development have been observed. Recently, the positive effects of docosahexaenoic acid (DHA), choline and vitamin B12 have been confirmed.
Some evidence suggests that DHA-rich nutrition (especially lots of egg yolk) from 6 to 12 months of age results in better vision acuity. This presents indirect evidence of the influence of DHA on infant cortex development. It was also discovered that high levels of LCPUFA (a component of oily fish) in complementary foods lead to an increase in DHA concentration in the organism, which, in turn, leads to increased infant cortex development. These studies indicate a possible link between complementary feeding and cognitive function development. Further research is required to establish whether these effects persist, whether they are limited to the visual cortex and whether they affect other cognitive functions as well.
Morgan’s study proves that introducing red and white meat as complementary foods between 4 and 6 months has a positive effect on psychomotor development. It was calculated that an average increase in meat intake of 2.3 g/day was associated with a 1-point increase in the Bayley Psychomotor Development Index. Krebs’ study shows that introducing meat as the first complementary food between 5 and 7 months leads to faster psychomotor development, compared to infants feeding on iron-supplemented grains or legumes. The reason for this lies in the fact that meat is a rich source of micronutrients such as iron and zinc, and arachidonic acid (the major LCPUFA), which have been proven to have positive effects on neurocognitive development.
Although there is no strong evidence to suggest that moderate iron deficiency and a low intake of LCPUFA have an adverse effect on neurodevelopment, ESPGHAN recommends including good sources of both iron (e.g. meat) and LCPUFA (e.g. oily fish) into complementary feeding.
Introducing complementary feeding and allergy development
The increase in atopic infant illnesses raises the question of whether or not highly allergenic foods (eggs, fish, nuts, sea food) should be introduced in infant nutrition and whether or not they can help prevent atopy. Observational evidence suggests that the early introduction (before the age of 4 months) of more than four foods is associated with an increased risk of atopic dermatitis, both in infancy and in a 10-year follow up. On the other hand, delaying the introduction of allergenic foods does not prevent or delay the development of allergies. It can be concluded that exclusive breastfeeding during the first 4 to 6 months could provide the best protection against allergies.
Eliminating allergens from maternal nutrition during pregnancy does not reduce the risk of infant allergies. Similarly, there is no convincing evidence to suggest that maternal nutrition during breastfeeding has long-term preventive effects on the development of atopic illnesses among infants.
Meta-analysis conducted in the Netherlands indicates that breastfeeding has a positive effect on temporary episodes of childhood atopic dermatitis, wheezing and asthma. The same meta-analysis observed that children who were breastfed for less than 3 months were at increased risk of Type I diabetes later in life.
In contrast, the American Academy for Allergy, Asthma and Immunology suggests that in at-risk infants, the introduction of milk and dairy products should be delayed until 12 months; eggs until 24 months; and peanuts, nuts, fish and sea food until 3 years. The benefits of these recommendations have been brought into question, since avoiding fish and consequently reducing the intake of LCPUFA could have negative consequences on the infant’s cognitive and neurological development. The study conducted by Poole et al. shows that exposure to grains after the age of 6 months increases the risk of wheat allergy.
Regarding the relationship between complementary feeding and its later influence on cardiovascular diseases, links have been identified between the early introduction of sodium on the one hand, and increased salt sensitivity and higher blood pressure in childhood on the other.
Increased LCPUFA intake – a result of introducing oily fish to complementary feeding – helps lower systolic arterial blood pressure.
Meta-analyses conducted by Norris, Klement and Akobeng address the links between chronic inflammatory intestine diseases and breastfeeding. Six observational studies have confirmed that breastfeeding provides permanent protection against celiac disease. The risk of celiac disease was significantly reduced in infants who were breastfed at the time when gluten was introduced. However, breastfeeding does not provide complete protection against celiac disease and may only delay its symptoms. Norris et al. proved that both the early introduction (before the third month) and the late introduction (after the seventh month) of gluten increases the risk of celiac disease and Type 1 diabetes mellitus among genetically predisposed individuals.
Sugar intake is the major dietary risk factor for the formation of dental caries. Sucrose is the most cariogenic sugar because it can form glucans which enable bacterial adhesion to teeth and limit the diffusion of acid in the plaque. Juice and other drinks containing sugar should be avoided and the infant should not sleep with a bottle. Furthermore, it is important to limit cariogenic food and maintain dental hygiene.
Although different types of food may contain spores of Clostridium botulinum, the consumption of honey is most commonly associated with infant botulism. Honey should therefore not be introduced to complementary feeding before 12 months of age, unless the spores have been inactivated by adequate high-pressure and high-temperature treatment, as used in industry.
It does not matter whether complementary feeding begins with fruit or vegetables, i.e. with apples, carrots, rice or potatoes. The only thing that matters is that complementary feeding not be introduced before the fourth month, and that new types of food are introduced gradually, one type at a time. The initial choice of food generally depends on the dietary habits of the family. It is important to note that children are born with innate preferences for sweet and salty tastes, and the rejection of sour and spicy tastes. It is therefore important to persistently offer complementary foods that are neither sweet nor salty; accepting such food will reduce the infant’s predisposition to obesity and hypertension. Some foods are more likely to trigger immunologically mediated reactions of hypersensitivity. These include milk, fish, egg whites, clams, gluten, soy, peanuts and pome fruits. Earlier recommendations claimed that, in families with allergic predispositions, these foods should be introduced into complementary feeding at a later stage. However, prospective studies suggest the opposite: that delaying the introduction of these foods, especially if the infant is no longer breastfed, increases the risk of allergies. The only prevention is exclusive breastfeeding for 4 to 6 months. Delaying the introduction of complementary feeding until the age of 6 months does not prevent allergies, but can actually contribute to their development. There is no scientific evidence to link the elimination of allergenic foods from the diets of pregnant women, breastfeeding women or infants (after the age of 6 months) with allergies, regardless of allergic disposition. The delayed introduction of grains that contain gluten, especially if the nutrient is no longer found in breast milk, does not prevent celiac disease or gluten allergy. Gluten should therefore be gradually and slowly introduced into the diet between 4 and 6 months of age, provided that the infant is still breastfed.
The limited scientific evidence currently available does not provide a satisfactory basis for establishing proper guidelines on introducing complementary feeding and its influence on the frequency of diseases later in life. This should be the focus of future studies.
A 2007 study conducted in the US concluded that the best way to introduce complementary feeding to the breastfed infant is to add various fruit and vegetables to the main meal, but also between meals. If we ensure a great variety of fruit and vegetables (in terms of their colour and flavour), the child is more likely to accept the food and the newly discovered flavours. The period between 5 and 10 months of age is considered to be optimal for accepting different flavours and textures of food.
Recommendations regarding exclusive breastfeeding during the first 6 months and partial breastfeeding during the period of complementary feeding are important for infant growth and development. Continuing breastfeeding contributes to further infant digestive tract modulation, which has long-lasting health benefits.
ESPGHAN recommends that complementary foods be introduced no sooner than the 17th and no later than the 26th week.
- Of primary importance are the infant’s age, physiological, immunological and neuromotor maturity, not the infant’s weight.
- The premature introduction of complementary feeding can lead to weight increase in infancy, as well as later in life.
- The order in which individual foods are introduced is less important.
- The intake of protein-rich food in the period between 8 and 24 months of age creates the risk of obesity and high blood pressure, so protein intake which constitutes around 15% of the total caloric intake is recommended.
- Fat intake should constitute more than 25% of the total caloric intake.
- The intake of LCPUFA (oily fish) and DHA (egg yolk) influences cognitive development.
- Meat should be introduced as a complementary food after 9 months of age.
- The intake of grains with different phytate levels has little influence on the status of Fe and Zn.
- Cow’s milk should not be introduced as a complementary food before 12 months of age.
- In the case of exclusive breastfeeding for the first 6 months, postponing the introduction of allergenic foods is not justified; what is more, their delayed introduction may increase the risk of atopic illnesses, especially if the infant is no longer breastfed at that time.
- Gluten should be introduced slowly and gradually, between 4 and 6 months; it is recommended that the infant still be breastfed at that time.
- Vegan and macrobiotic diets are not recommended during infancy.
- Complementary foods without added sugar or salt are recommended as they do not increase the predisposition to salty and sweet foods.
- Nutrition rich in fruits in early childhood can have a protective role against cancer in adulthood.
- Nutrition rich in vegetables, fruit and dairy products in infancy can have a positive influence on blood pressure during childhood and adolescence.
Based on the recommendations presented above, the Croatian Society for Childhood Gastroenterology, Hepatology and Nutrition prepared the following recommendations on healthy infant nutrition:
- Natural food (breast milk) should be provided until the age of 6 months; breastfeeding should continue after the introduction of complementary feeding, even after the child’s first year of life.
- If the child is not breastfed, infant formula is recommended.
- Cow’s milk as a basic dairy product is not recommended during the first 12 months; however, small amounts can be added to complementary feeding at an early stage.
- The time frame for introducing complementary feeding is between 17 and 26 weeks.
- Different types of food should be introduced gradually and one at a time.
- Postponing the introduction of complementary foods after the age of 6 months does not prevent allergies or chronic illnesses such as celiac disease and is therefore not justified. The same is true of introducing potentially allergenic foods (milk, fish, eggs, gluten) to healthy children with or without an atopic predisposition.
- There is no evidence to suggest that the elimination of allergens from the diets of pregnant and breastfeeding women prevents atopic illnesses in their children, and is therefore not recommended (with the possible exception of atopic dermatitis). This only applies to healthy infants, with or without atopic anamnesis.
- Soy-based infant formulae are not intended as nutrition for healthy infants, do not have a preventive effect on allergies, and are not recommended.
To these recommendations, we add the following:
- Complementary feeding should satisfy 90% of the breastfed infant’s iron requirements.
- With infants with increased allergy risks, complementary feeding should be conducted in one-week intervals; during that time, potential allergic reactions should be observed.
- Foods with low allergenic potential include carrots, potatoes, courgettes (zucchinis), bananas, etc.
- Fish and eggs should be introduced to children with allergic predispositions after the age of 12 months.
- Honey should be introduced as a complementary food after the age of 12 months.
- Children receiving a vegetarian diet should consume a minimum of 500 ml of breast milk or infant formula. Considering the potential deficiency of basic nutrients among vegan children, regular medical check-ups are recommended.
In developing countries, around 1/3 of children below the age of 5 are malnourished; the number of children suffering from a deficiency of one or more micronutrients is significantly larger. The latest data show that more than half of infants between 6 and 9 months of age are given both breast milk and complementary feeding; among breastfed infants aged 20–23 months, only 39% are given complementary feeding.
WHO estimates that in developing countries and countries with a low GNP, two out of five children experience poor growth and development due to inadequate complementary feeding.
Quantitively and qualitatively inappropriate complementary feeding in this period is responsible for inadequate growth and frequent infections, as well as increased mortality rates. UNICEF therefore believes it is necessary to improve infant nutrition during the first two years.
When continued after the sixth month, breastfeeding should satisfy more than half of the infant’s nutrition requirements; between 12 and 24 months of age, it satisfies only one third of nutrition needs, while the rest is satisfied through appropriate complementary feeding.
The low quality of complementary foods in developing countries represents a risk of malnutrition and accompanying illnesses. Complementary feeding is often introduced too early or too late. Low-quality complementary feeding may reduce milk production, which decreases the benefits of breastfeeding.
UNICEF therefore suggests the following:
- a global strategy for improving infant and childhood complementary feeding;
- the first step: improving the nutritional quality of complementary food, considering the possible differences between rural and urban areas; locally available food should be the priority for all children;
- the second step: providing assistance with regard to food, micronutrients and lipids to all endangered children (children who are not breastfed, children from very poor families, HIV-infected children, malnourished children or children living in extreme conditions);
- the third step: directed towards educating mothers, as well as towards the health and social environment in general
- the fourth important step: securing support for developing countries so that they may enforce the International Code of Marketing of Breast-Milk Substitutes at their respective national levels, and that complementary foods and infant nutrition in general may follow international expert recommendations. The continuing education of healthcare workers is an essential part of this.
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- ESPGHAN Committee on Nutrition: Carlo Agostoni, Tamas Decsi, Mary Fewtrell, Olivier Goulet, Sanja Kolacek, Berthold Koletzko, Kim Fleischer Michaelsen, Luis Moreno, John Puntis, Jacques Rigo, Raanan Shamir, Hania Szajewska, Dominique Turck, and Johannes van Goudoever. Complementary Feeding: A Commentary by the ESPGHAN Committee on Nutrition. J Pediatr Gastroenterol Nutr 2008; 46: 99-110.
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