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Weaning

CLINICAL PRACTICE                                      ADOLYGIAD CLINIGOL

1D.P.Davies, 2B.O'Hare
1University of Wales College of Medicine, Heath Park, Cardiff CF14 4XN
2University Hospital of Wales, Heath Park, Cardiff


"She shall feed the child only on (mothers) milk, but when he has cut his front teeth it is well to accstom him to more solid food, as women do of their own accord, having learnt by this experience."

Galen of Pergamum (A.D~170)

Summary
This review examines present day practices in weaning against a historical background. Gastrointestinal, renal and nervous system preparation provides the biological determinants when weaning should begin. The major nutrients of the weaning diet are outlined that best provide for optimum growth, development and health. This understanding helps appreciate the ideal programme of weaning and how its inadequacies are best monitored. Modern controversies are touched upon, especially the definition of weaning and the particular problems of certain vulnerable infant groups. Finally highlighted is the worry and concern still expressed by mothers, carers and health professionals alike about weaning due in large part to a lack of a strong evidence base for the weaning process.

Introduction
Those powerful advocates of breast feeding throughout the 1970's and 1980's, the Jelliffes, reminded us of the notion of the human new-born as an "extero-gestate" foetus for about the first nine months or so after birth. Over this period of rapid growth and development the young infant is completely dependent on the mother for warmth, protection and food, the breast serving as an external placenta. Nature then dictates that mother's milk, in both its quantity and nutritional qualities, becomes gradually nutritionally insufficient for her baby's growth and nutritional needs, necessitating the exterogestate foetus to become a "transitional" being, becoming accustomed to new foods of ever varying textures, tastes and nutrient densities, until a full 'mini' adult diet is reached.
   The process of gradually replacing breast milk, or, in the modern world, formula milk, by solid food as the main source of macro and micronutrients and energy is embraced by the term weaning, a word derived from the Anglo-Saxon "wenian" - to accustom. But some variation in definition does exist. A recent (2002) World Health Organisation (WHO) definition uses the term weaning to indicate a complete cessation of breast-feeding. This concept interestingly is embraced in some Romance cultures. In French for example weaning is referred to as "servage" and in Spanish, "destetar", both words referring to separation from the breast. In Welsh the term is diddyfnu which literally translated means "without sucking". More conventionally weaning is now used to describe not a single event but a period, where there is a gradual replacement of milk, (whether breast or bottle) with its high fat, low carbohydrate content by non-milk foods of low fat and high carbohydrate makeup. This latter definition is preferred in this article, being more realistic in contemporary western societies.
   Weaning continues to cause more anxiety to everyone (mothers, nurse and doctor alike) than almost any other in paediatric nutrition. But perhaps this should not come as too much of a surprise since in this aspect of infant nutrition comparatively little research has been undertaken, especially in terms of the best age to wean, what constitutes the most appropriate weaning foods and also what effects weaning has on long term health. This article offers a working synopsis of current views. Maybe it will go some way to remove some of the widely held trepidation!


"......throughout history it has also been not uncommon practice to give the infant alcoholic drinks." Taken from Hogarth, Gin Lane 1751. Note the infant being fed gin.

Historical prelude
Throughout history, frequent reference is made to the weaning of the baby from the breast. From biblical times written references to weaning have often appeared in scrolls, diaries, journals, papers, books, many indeed written, perhaps surprisingly, by men! The likely reason for such preoccupation is that weaning was (and in many economically poor countries even now, is) the most dangerous period in early childhood through its associations with particular diseases that lead often to high mortality. In 18th century London for example up to seventy per cent of infants failed to survive their second birthday, a major contribution to this appalling toll of death being some of common weaning diseases, especially gastrointestinal infections.
   Weaning from the breast was also a period of change not only of diet but also of station. A "suckling" was an infant with all that this implied, but once the breast was left for good, the baby was then generally regarded as a true child and became a real member of the family. The upper class child left the wet nurse and returned home to the biological mother, while among the poorer classes the young infants were no longer fed at different times but ate out of the family pot.
   Until the dawn of the modern industrial era in western countries early in the 19th century, advice about weaning was dominated by the writings of the Greek/Roman school of thought led, especially by Soranus of Ephesus (90-117 AD) and Galen of Pergamum (130-200 AD). For well over a thousand years of literature on weaning, there is constant reference made to these medical authors and their pupils. Indeed even the widely respected writings of the Byzantine and Arab schools, so dominant in the Middle Ages, seem simply to have adapted this ancient teaching to their more contemporary ways. The discovery of the printing press in medieval Europe towards the end of the 15th century further cascaded these ancient teachings. But, there is much common sense in all these writings, some even evidence based, and their understanding is fundamental to the appreciation of current concerns about weaning in the modern world.
  When to start? When the baby should be taken initially off the breast is surprisingly not an aspect which receives much consideration since medical authorities seem to have assumed that women would give additional foods either when the child appeared ready for them, or according to custom among family and friends. (How little things have changed!) Sometimes it seems to have been the eruption of teeth that offered guidance. But the age at which foods other than breast milk were actually first given was probably much earlier than the time recommended by physicians and midwives. (Again nothing new here!) Throughout history there has also been an important thread that it is the baby rather than the mother who should decide when weaning should take place.
  What to give? Initial foods commonly given to infants up the modern era included paps and panadas. Paps were foods made of flour and bread cooked in milk with additives for flavouring or added nutrition; panadas were stews of bread, broth, milk and eggs. Many recipes used to be made up from these foods. Indeed, in many parts of the contemporary developing world paps and panadas are still widely used. But there does seem to be a difference between introducing foods, the paps and the panadas, as a complementary food to breast milk a very common tradition, and the weaning process itself which not uncommonly continued well into the second year of life when children would be in possession of several teeth and able to sit at the table with some ability to feed themselves. A theme condemned by many medical writers was the custom of giving foods pre-chewed by the nurse or mother.
   Down the ages it has also been a not uncommon practice to give the infant alcoholic drinks, especially gin, grape wines and brandy in the wealthy and beer in the poor, a custom that achieved great popularity during the late 17th and 18th centuries. Although it is now unthinkable that a child as young as 6-12 months should be given alcoholic drinks it has to be recognised that until the development of clean water supplies, water was rarely drunk by the general population because of its widespread contamination. The common drink for most people in Britain was ale, beer or small beer with a fairly high alcohol content, although small beer was much weaker. It was, therefore, not surprising that once a child was weaned and ate similar food to the rest of the family, it was natural also to have the same drink. The following quotation by the Edinburgh doctor,William Buchan (1769) in his book "Domestic medicine; or The Family Physician", says it all. All strong liquors are harmful to children. Some parents teach their children to guzzle ale and other strong liquors at every meal, but such a practice cannot fail to do mischief:- milk water, butter, milk or weigh make the most proper drink for children. If they have anything stronger, it may be fine small beer, or a little wine mixed with water."
   But some interesting pointers to the beginning of the weaning process do emerge. Soranus advised that babies should be breast-fed completely for six months, although this was far from actual practice at that time. He also recognised that it was bad to withhold solid foods until the child was too old since this would lead to digestive problems and difficulties in adapting to new foods. The Koran inspired Islamic culture advised the beginning of weaning at two years, but this is not in any way a strict ruling allowing the child to be weaned earlier if necessary. In the 16th century the ideal age for introducing mixed feeding seems to have been seven to nine months, but apparently during the late 17th and 18th centuries much earlier weaning from the breast was favoured, as early as two to four months. But if there is a general overall message that comes down the ages it is that the process of weaning was recommended over the wide age range, 6-24 months. Late weaning seems to have been advised especially for weak or treasured children, but from the late 17th century, a long suckling period did attract the disapproval of many medical writers. Other factors also considered when weaning a child early included the help of a nurse and the state of the mother's milk.
   How to wean? Most medical writers agreed that gradual weaning was preferable to sudden weaning, a very cruel practice sadly still all too prevalent in some developing countries. Ways in which weaning from the breast was achieved included giving food prior to breast feeding and encouraging suckling only at night. But sometimes so very difficult was it to wean the child from the breast, belonging to mother or wet nurse, that it was necessary to anoint the nurses' breast with mustard, or rubbing the top of the nipple with aloe and other bitter substances. Recall the words of the nurse in Romeo and Juliet (c. 1594); who tells of the traumatic day of Juliet's weaning when three years old ...

"And she was weaned, I shall never forget it,
Of all the days of the year, upon that day;
For I had then laid wormwood to my dug....
When it did taste the wormwood on the nipple
Of my dug and felt it bitter, pretty fool.
To see it tetchy, and fall out with the dug."

   These methods were, perhaps not surprisingly, very traumatic for the child and probably even more so for the mother. Indeed, perhaps this was causally related to a high prevalence of melancholia in the mother that was written about so much in the 16th and 17th centuries. Any obvious distress to the baby accompanying weaning was soothed by administering laxatives, alcohol and even opiates to the baby.
   In industrial times there does appear in the western world a gradual decrease in the age of weaning which probably relates to the growing availability and the social acceptability by artificial feeding, the fall in the number of wet nurses for the middle classes and the movement of population from countryside into towns. The beginning of industrialisation also began to see children weaned progressively in a way similar to today, beginning with pureed or minced food containing milk or broth, progressing to foods eaten by the rest of the family mashed and cut into small pieces as the child becomes older.

Importance of milk: diseases of weaning
An important aspect was the recommendation for milk containing foods being an important part of the weaning diet with the increasing awareness of specific diseases resulting from deficient weaning practices, especially scurvy, rickets, bladder stones, night blindness and a very low resistance to infection. Indeed it appears that the 18th century saw a definite decline in the nutritional value of foods compared to the 16th century. Surprisingly the diet especially of the wealthy did not include much milk or milk products. The diet, mainly cereal and meat excluded vitamins A, D and C: also the amount of calcium was insufficient for the growing child. Hence the laying down of the seeds of some specific diseases of weaning. Poorer families, however, seemed, often, paradoxically to have a different type of diet consisting mainly of bread, cheese, mill salt, meat and pulses, so the poorer child could well have fed much better in nutritional terms, provided enough food was given, than the richer child. White meats, dairy foods, including eggs were eaten by the poor and many cottages in the countryside kept a cow so milk was far more likely to be drunk by these families than by the wealthy. But for as long as milk was in the diet, irrespective of the type of milk, bone disease was less common.
   The gastro intestinal disorders of weaning were well described by the Scottish surgeon, John Aitken in 1876 "This is a violent purging frequently attended with vomiting, wasting, etc.. It causes one early weaning to improper food, cure removal of causes." This is a good description of weanling diarrhoea so prevalent in areas of India, Africa and Central America today where stunted growth, leanness and wasting are still associated with early weaning.

The Present

When to begin?
The timing of introducing non-milk foods is conditional on some important physiological determinants that are needed to prepare the young infant for the nutritional transition that constitutes the weaning process.
• The gastro-intestinal tract must be functionally prepared to digest and absorb dietary nutrients and to be sufficiently motile to transport the food the length of the gut. The baby has also to be protected by the process of gut closure from the ingress into its body of large foreign protein molecules that can lead to an abnormal immune response and with it, physical illness. Secretory IgA and other protective substances produced within the gut wall play a vital role in this function as they also do to reduce significant bacterial colonisation of the gut, a risk factor for serious infection. Once again, the umbrella of protection conferred by human milk, especially cells, IgA and numerous chemical substances and enzymes play an important and insufficiently appreciated role in preparation for weaning. The gut also prepares itself for its very diverse demands of obtaining nutrients from a mixed diet by enhancing growth of its epithelium. For example, the large amount of sphingomyelin in human milk, 35% of its total phospholipid, and many other locally produced growth factors and hormones have a major role promoting epithelial growth acting via their relevant receptors in the small intestine to mediate this function and superimposed on genetic pre-programming.
• The nervous system needs to have acquired a level of maturity of neuromuscular coordination that permits the safe taking of solid food from a spoon and its movement as a bolus though the mouth into the upper gastro-intestinal tract and then swallowed. Head control has also to be sufficiently mature to maintain a suitable posture for the safe movement of this food.
• The kidney must also be physiologically prepared to allow the young weanling cope with an increasing solute load. This it does by improving its concentration ability to preserve intact the "milieu interieu". A warning of what can go wrong if this physiological determinant fails is the danger of hyperosmolar states that were so prevalent in the 1970's with the widespread use of high solute formula milks and the very early introduction of non-milk foods, both contributing to hypernatraemia with its serious short and long term complications.

   What does this state of multi-organ physiological preparation tell us about the age to move from the "exterogestate foetus" to the transitional human being, the weanling? There is often a difficult tightrope to negotiate especially in infants in poor developing countries. Too early introduction of non-milk foods and in HIV endemic parts of the world early cessation of breast feeding will risk foreign protein mediated food intolerances including coeliac disease, expose the young to infection, especially of the gastro intestinal tract sewing also the seeds of malnutrition and abnormal "internal body milieu" states, especially in the presence of diarrhoea and even perhaps an increased risk of childhood wheeze and asthma. Too late the beginning of weaning will risk undernutrition as the needs of the young increasingly outstrip the capacity of the mother's milk (or indeed milk formula) to satisfy these requirements for growth and development and certain micro-nutrients especially iron and zinc. Delay in introducing solid foods of varying textures, tastes and consistencies will also inhibit the development of neuro-muscular mechanisms needed to mechanically prepare and deliver non-milk foods to the gastro intestinal tract, such as chewing and moving the bolus of food in the mouth. Missing out on this critical period may make for later feeding difficulties. It is important to recognise, however, that the eruption of teeth has no effect on the weaning process, although in history as mentioned above, it has often been considered a useful marker for the timing of weaning.

Current recommendations
Since 1994 the Department of Health's (DoH) recommendation, reflecting those then of WHO, remain, namely that for the majority of infants, solid foods whether for breast or milk formula fed babies, should be introduced between four and six months.
   There is no magic test to determine when weaning should begin. It is essential, however, that the health professionals who purvey advice are sensitive to the role of the perception by the mother or other carer that the baby through its physical size and changed behaviour might no longer be satisfied by milk alone, whatever might be the "official" recommendations. As a determinant for the starting of weaning, this dictation by the baby and its pickup by a sensitive mother is critical and all too often denied by those who set guidelines. In the western world this all leads to the reality of the majority of babies being introduced to solid foods by about four months. Some (very few) seem to need solids before three months and as long as this is in response to a baby's perceived needs, there should be no problem even to this very early introduction. And as throughout history, some babies are given solid foods as a "complementary food", simply as a taster and not part of a planned weaning process.
   Against this background it might come as some surprise to read the 2001 WHO revised recommendation for weaning from the breast that mothers should exclusively breast feed for at least six months and to continue breast feeding up to, or even beyond, two years. The background to this is the situation that applies to breast feeding in poor countries, with special reference the current HIV pandemic and hazards of replacement feeding, two critical factors that influence the timing of weaning that can be seen to sometimes be mutually in opposition to each other. The issues are worth exploring in a little more detail.
   Weaning and HIV in the developing world In 2002 there were 800,000 children newly infected with HIV, 90% by mother to child transmission (MTCT) and three quarters of these in sub Saharan Africa. Where there are no interventions such as antenatal anti retroviral therapy and caesarian section the risk of transmission during pregnancy is 5-10% and during labour 10-20%. To this must be considered additional risks from breastfeeding. In the first two months breast feeding adds an extra 2-10% risk of transmission. Breastfeeding after two months but stopping at six months adds another 1-5% chance of transmission which increases a further 5-10% if the baby is fed until 18-24 months. A recent UNICEF factsheet on Breastfeeding and HIV sumarises these figures, warning that a baby fed for six months has 1/3 the risk of transmission during breastfeeding of a baby breast fed for two years, both groups still having the 15-30% risk of transmission during pregnancy and delivery. The risks of breast feeding for continuing MTCT are therefore considerable.
   And what does HIV infection mean to a child living in, for example, sub-Saharan Africa? The vast majority (90% in some studies) of children infected with HIV at birth will die by the time they are three years of age. The remainder will die in the first decade generally when they are six or seven years of age. The remainder will die in the first decade at about six or seven years having suffered multiple episodes of gastroenteritis, respiratory tract infections often including Tuberculosis and frequent episodes of oral candidiasis. Even if the child is seronegative, if its mother is infected with HIV the risk of mortality is greatly increased.
   But the reverse argument has also to be considered, namely the risks in this setting of not breastfeeding. There are 11 million deaths < 5 years per year worldwide from malnutrition, and 2/3 of these can be attributed to poor feeding practices in the first year of life. UNICEF warns that a baby who is receiving replacement feeding in the first two months of life has a six-fold increased mortality due to diarrhoeal and other infectious diseases. It is common in many resource poor countries to complement breastmilk with drinks such as water and tea, yet it has been shown that despite the climate exclusively breast fed babies are no more likely to become dehydrated and there is no nutritional benefit to these feeds: fewer than 35% of babies are exclusively breastfed for the first four months of life worldwide.
   In summary therefore how are these issues resolved in resource poor developing countries (compared with the developed industrial world) where additional determinants for the timing of weaning include lack of appropriate available breast milk substitutes, high risk of microbiological contamination of foods, few opportunities to administer antiretrovirals to the HIV positive mothers and an earlier return to potential fertility with early release of lactation amenorhoea that inevitably follows stopping breast feeding. In these countries, delaying the introduction of non-milk foods to six months is seen as a factor that might help reduce mortality and immediate and later morbidity recognising at the same time the continuing risks of HIV transmission. But in rich countries where there are readily affordable non-milk foods, where general hygiene minimises contamination of food and where effective contraception is readily available, there is really no need to change the 1994 recommendation. Indeed, in this and other industrial countries the (unrealistic) advice of exclusive breast feeding for six months (without extending statutory maternity leave!) might even lead some to never bother breast feeding in the first place. A recent large study of weaning in normal term babies in Britain showed the median age of first giving solids was 31/2 months, 21% were given solids before 3 months and only 6% after 4 months. Only 2% of breast fed infants did not receive any other foods for six months. Most babies were established on solids before 4 months with no problem. Independent prediction of early weaning were rapid early weight gain in the first 6 weeks and lower social class. The most important reason given for weaning was the perception by the mother that the baby was hungry.
   What scientific data is available (and there is not much) supports the view that exclusive breast feeding for six months is probably safe for most babies in terms of nutritional adequacy providing that the mother is well nourished. But for the less well nourished mother, babies may be at risk of growth faltering and poor weight gain with exclusive breast feeding up to six months. More robust evidence must be sought on this recommendation before it can be universally implemented. Indeed, it is also salutary to recall that consideration has never been given to possible differences in the weaning requirements for breast or formula fed babies. Without this evidence it is probably fair to say that reality and pragmatism dictate that, at least in the developed world, weaning best takes place between four and six months, although the recent WHO recommendations may, on balance, be seen as a necessary population strategy for developing countries and for individual babies in the developed world.

The process of weaning
There are many influences on the march of weaning to which culture, taboos, religious belief, ethnicity, tradition, medical opinion and dietary fads all contribute in their individual ways. Not forgotten also must be the variation in rates at which young infants acquire those special motor feeding skills that are a prerequisite for safe weaning.
   Our article focuses on weaning in Britain where the broad aim is to achieve by about twelve months or so the basis of a "healthy" adult type diet given in three meals a day, interspersed with small snacks and with milk still an important food. Over the weaning period a wide range of foods of different tastes and textures need to be offered to enrich the palatal experiences of the young infant. The process of introducing new foods must be gradual and babies are likely to adapt best if solid foods are offered initially from the spoon, or given as finger foods, and not as solids made into drinks, or given dissolved in milk or other fluids in a bottle. It is sensible also not to introduce too early those foods that are associated with nutritional intolerances, atopic disease and allergies (see also later).
   How these prerequisites are translated into the actual weaning diet make up the process of weaning and this can be best understood by considering the particular vulnerabilities and requirements of the young human infant at this developmental stage. At the core of these requirements is the need for the infant to satisfy normal physical growth and its accompanying development that proceed so rapidly at this time. This is all made possible by providing protein building blocks in the diet complemented by key micro-and macro-nutrients and with sufficient energy to put all of these into place. Specific Dietary Reference Values provide the range of individual nutrient requirements to satisfy these needs but these are not referred to further in this article the interested reader can consult relevant texts to learn more. In what follows the emphasis is more on qualitative aspects of the weaning diet.
Food Energy Fat is a major contributor to the energy content of the weaning diet although as a steadily diminishing percentage falling from over 50% in breast milk at 4-6 months to around 35% in the diet at about 18 months. Most of the weanling's fat comes in milk complemented by a variety of other weaning foods. Strongly contraindicated in the weaning diet are low fat foods that can only slow down growth and development. Semi-skimmed milk, provided the diet is sufficiently varied, should await at least the third year for its introduction. A recent survey conducted through "Mother and Baby" magazine found worryingly that many of mothers were introducing their babies to low fat, low calorie meals in order to lessen the risks of overweight. It needs to be impressed on mothers that a healthy weaning diet is not the same as a healthy adult diet.
   Other energy rich foods are those that contain the intrinsic cellular soluble sugars fructose, glucose and sucrose, along with efficiently absorbed starches in cooked cereal products and rice. Extrinsic sugars as added sugars in fruit juices, honey, table sugars for example, are also needed although they should be used sparingly to prevent young infants developing the habit of too sweet a tooth with its special links with later poor dental health.
Structural fats and neural development The continuing rapidity of the growth of the brain and other neural tissues requires large amounts of phospholipids that are rich in long chain polyunsaturated fatty acids (LCPFAs), especially docosahexanoic and arachidonic acids. It is likely also that LCPFAs are needed for vascular endothelial growth and the cell membranes of other issues. Their synthesis during weaning requires an adequate amount in the diet of the essential fatty acids linolelic and alpha-linolenic acids.
Non-absorbable carbohydrates The weaning diet has also to accommodate those elements that contribute to normal gastro-intestinal motility, especially of the large bowel, to prevent sluggish bowel movement that ultimately leads to constipation, such a scourge of contemporary western type societies. The main contributors to this function are non-starch polysaccharides(NSP), complex polymers, previously called "dietary fibre" and derived mostly from plant cell walls. But it must be remembered that these are low energy dense foods and giving too much NSP during weaning is to be discouraged, displacing as they may more energy rich foods, let alone causing diarrhoea. Many foods rich in NSP, such as cereal products and legumes, also happen to be a rich source of phytates that reduce bioavailability and hence the absorption of micronutrients, especially iron and zinc. In the "indigenous" British culture there is little danger of the weaning diet having an overabundance of NSP, although the same perhaps might not always be said of those cultures and individuals who embrace vegetarian and (especially) vegan practices. With constipation such a current concern the weaning period must be seen as a good opportunity to lay down good future dietary practices, as well as to satisfy current nutritional needs. Encouraging young infants to take and enjoy plant foods and fruit can do much to help.
Protein The essential determinants of lean body mass and linear growth are provided mostly in the protein of meat, fish, eggs and milk that contribute a proper balance of essential amino acids. In western countries there is rarely protein deficiency in otherwise healthy children. But it is important to remember that non animal products and many plant foods are much lower in protein and essential amino acids than equivalent animal sources. This is why soya protein based formulas and other foods (such as tofu) are such valuable elements to the weaning diets in vegetarian and vegan families.
Major minerals The fact that the skeleton, not forgetting the teeth, contains most of the calcium, magnesium and phosphate in the body shows how important it is to ensure an adequate intake of these minerals in the weaning diet. These are best provided in milk, milk products and foods derived from calcium fortified white flour. Phosphorous, of course, is also needed for basic cellular metabolic processes including energy release as well as an integral component of phospholipids in cell membranes. Sodium is the most important extracellular mineral and this is well provided for in nearly all weaning foods. Indeed, if anything there is now a concern that many proprietary foods are over rich in sodium. The young kidney has only a limited ability to excrete a sodium load and although risks of hypernataemia have virtually disappeared with weaning practices that now contribute much less of a solute load than a couple of decades ago, the links that are now emerging between early sodium intake and the tracking of high blood pressure into adulthood makes sodium intake a very important issue. The palate must be conditioned not to need more salt.
   It goes without saying, therefore, that salt should never be added to the weanling's diet. Other minerals particularly potassium, zinc and copper are essential for cell and tissue growth as well as a general basis for enzyme synthesis. In the average western weaning diet, these should be all well provided for.

Iron Nutritional iron deficiency continues the most commonly diagnosed nutritional disorder of early childhood worldwide and Britain is no exception. With iron a vital component of haemoglobin, myoglobin and many enzyme systems, psychomotor apathy, poor weight gain and increased vulnerability to infections are all important and worryingly common clinical consequences. The seeds are often sown in bad weaning practices especially in certain high risk communities, notably Asians recently arrived in this country and other socially disadvantaged inner city families. Red meat and other meat products from which iron is readily available, are an important part of the weaning diet and their intake must be encouraged along with other iron fortified foods. The non-haem iron that is present in vegetables and other plants contributes a much reduced bioavailability. Fibre, especially from cereals, legumes and other vegetables, can also inhibit iron absorption through their high phytate content. The vulnerability of vegetarian and especially vegan diets is obvious. (See also later.) Another major risk factor for iron deficiency is the too early giving of cow's milk, low in iron, causing intestinal blood loss and also filling up the infant, therefore discouraging other foods. It is for this reason that breast milk or a fortified infant formula and not cows milk should be an essential part of the weaning diet until the second year of life. Iron absorption is enhanced by vitamin C in the diet, hence the value in vulnerable groups of this particular supplement and also the inclusion of fruits and lightly cooked or raw vegetables.
Vitamins Most vitamins have specific functions. Vitamin A obtained from animal products and fish oils in the diet as pre-formed retinol and carotenes in vegetables and fruit is essential for growth and neural development, immune function and as anti-oxidants. The B group vitamins found in a wide range of all foods are integral to cell processes and tissue regeneration. Vitamin C found especially in vegetables and fruits (not forgetting how prolonged cooking can destroy vitamins) are important as antioxidants and also assist the absorption of iron from vegetable and other non-haem iron sources. Vitamin D is vital for calcium absorption and the deposition of calcium in bone. It is present naturally in very few foods, with the obvious exception of fatty fish, although, research is now showing that more Vitamin D might occur naturally in eggs and meat than was previously thought. But fortunately it is readily synthesised in the skin by the action of ultra-violet B radiation on the steroid precursor 7 dehydrocholesterol, the process being completed in the liver and kidney to the active vitamin D metabolite. Vitamin E is made up of tocopherols, the most active being alpha-tocopherol, found in fortified foods and especially in fatty fish and is needed to preserve the structural integrity of phospholipid cell membranes and also to help protect vascular endothelium and neural cells from free radical damage.

   This basic understanding of the major nutrients of the weaning diet can now be translated into the following general weaning programme that should apply to most young infants in this country.
   4-6 months: At this early stage the important learning skill for the baby is to become accustomed to taking food from a spoon. An initial first food could include a cereal, baby rice mixed with the baby's usual milk, mashed potatoes, yoghurt and custard. Patience is essential throughout the weaning process. But it is important to recognise that food intake at this very early stage serves largely as a "taster" given by spoon 2/3 times a day. Milk continues essential for all nutrient needs. Other suitable early foods once the baby accepts these early bland foods and is able to take food from the spoon include pureed meats, pulses, fruit and a wide variety of cereals.
   6-9 months: This phase now sees solid foods as an increasingly more major provider of energy and general nutrition with milk gradually becoming less important. Vegetables, lean meat, cheese, yoghurts, bread are then added gradually in a mashed or pureed form. These provide more varied tastes with varied textures. Babies themselves may now be able to put foods into their own mouths, experimenting with finger feeds (toast).
   9-12 months: This stage is now beginning to reflect a more mature diet in two or three meals interspersed with healthy snacks. The texture of food is now less pureed. At this stage egg and fish can be added, although nut products are best delayed until the second year.
   In summary, providing the young infant with a mixture of available foods, maintaining an intake of fortified formula or breast milk (mother being of adequate nutritional state) along with moderate exposure to summer sunlight should provide an adequately balanced weaning diet in this country. The change from breast or infant formula to dairy (cow's) milk should ideally be delayed until after the first birthday, cow's milk being a major risk factor for iron deficiency. Water and fruit juices are important. Added salt and sugar are also strongly ill-advised because of respective links with later hypertension and the general development of too sweet a tooth and with it sowing the seeds for later weight problems and dental caries. The too early use of the cup from the bottle is also to be discouraged since the coordination needed to feed from a cup is often difficult. There is the general recommendation that after twelve months bottle feeds should be discouraged, cup feeding being preferred. But if the cup skill is overemphasised fluid intake will be insufficient. Babies themselves will determine through their own individual skills the timing when fluids can satisfactorily be taken from the cup. Maintaining a high fluid intake is also needed to keep a good urinary flow to lessen the risks of urinary-tract infection.

An example of weaning in a young child living in Britain is shown below.

Practical Aspects
Weaning foods can be home prepared, commercial or mixtures of the two types of baby foods. This choice depends largely on the shopping and cooking capabilities of the mother and father and other family choices. Financial considerations and confidence also play a part early on when only small amounts of food are used with the potential for huge wastage. Data on the nutritional composition of many home prepared foods show great variability with, if anything, a tendency to be rather low in protein, fat and iron and even of lower energy density. Hence the potential value early on of feeding commercial foods, either in whole or as a supplement. It would seem, however, that after about eighteen months the use of commercially available baby foods in this country has declined considerably. When the family pot is used it is important once again to emphasise not to add salt and sugar.
   Irrespective of the type of food fed to the baby, great care must always be taken regarding food hygiene, including cooking and storage, to prevent food borne microbial illness. Increasing use of microwave cooking also means the risk of burning the young infant's mouth. These practical details must always be emphasised as essential components of the weaning process along with the perhaps, more interesting nutritional aspects. Not to be forgotten also is the need for patience. During weaning, infant behaviour is often frustrating with food refusal, spitting, depositing and smearing food on cloths and utensils, etc. Parents and other carers have to be assured that this is all part of the normal exploratory weaning process.

Vulnerable groups
In some infants special consideration may need to be given to the general process of weaning that has just been described because of their particular vulnerability. (Excluded from this section are infants with diseases already diagnosed and who may require special nutrition such as coeliac disease, milk intolerance). Infants with, or at risk from, atopic disease, recurrent wheezing and other allergies: It is tempting to believe that for infants with, or at risk from wheeze, bronchial asthma, hayfever, atopic dermatitis and other allergies, delay beyond the usual recommendations of introducing weaning foods is advisable in view especially of the physiological fall in the levels of secretory IgA in the gut over the first six months of life. (This of course is naturally compensated for by the high quantity of IgA in breast milk over this time). There is, however, no good clinical or epidemiological evidence to support delaying the introduction of potential food allergens commonly linked with these disorders, notably milk protein, eggs and nuts, or even to prolong breast feeding beyond four to six months to lessen the risks of future illness by sensitisation. It is, however, sensible for a breast feeding mother to avoid eating these common food antigens in the early months after birth since this could lessen the risk of illness in her baby.

Pre-term and other low birth weight infants
Although some of these babies may go home from the neonatal unit with poor weight gain and feeding problems, including sucking and swallowing difficulties, the general rules of weaning still apply. It may be, thought, however, that for infants who have suffered intra-uterine growth retardation, introducing solid foods before four months might be demanded by the babies themselves. The reality seems to be the opposite. In a recent national study of 2000 babies, small for dates babies, whether breast or formula fed were less likely to have been started on solids before twelve weeks. Maybe their size led to greater parental concern and, therefore, a greater likelihood to stick with the guidelines. Maybe even their babies' perceived small size downplayed the need for solids just as higher weights at around six weeks leads often to very early weaning. For pre-term babies, some studies have even linked improved growth rates and improved iron status if solids, especially of higher energy density and protein content, are introduced to the diet of babies born prematurely at about three months.
   More research is needed to improve the evidence for guidelines for these two special categories of low birth weight infants. This must also include the long term influences on growth and health.

Infants in minority cultures
There is no doubting that culture, tradition and religious beliefs have a profound effect on dietary practices. Ethnic minority communities in this country are likely therefore to vary in their weaning behaviours. However, we need to be reminded that there is no single "ethnic minority" culture and, as with other instances of weaning, variations need to be tolerated, indeed often encouraged, providing, of course, that the basic nutritional requirements are met. The following points need to be considered.
   Iron, vitamin D and other micronutrient deficiencies have been identified as major problems in some Asian and black the darker skin colour of the ethnic groups a major contributing factor especially to Vit D deficiency especially where there is low exposure to sunlight populations where whole cow's (doorstep) milk is introduced at a very early age and continued in large volumes. Prolonged breast feeding - little or no Vit D - also contributes. Not only does this risk primary nutrient deficiencies especially anaemia and biochemical rickets but by filling the stomach the infant is less eager to take solid foods. Mothers, especially from Muslim backgrounds, are also more likely than the white mothers to introduce solid foods later, so compounding iron and vitamin D deficiencies. They also have a tendency to use more convenience baby foods, high in carbohydrate. It is, however, important to recognise that these patterns are also to be found across other minority ethnic groups as well as the ethnic majority in inner cities and other equivalent areas. As with all instances of prolonged bottle feeding babies miss out on critical periods to vary tastes and texture of solid weaning foods that can lead to rejection of mixed tastes later on.
   Awareness of these potential problems should help in the primary care management and prevention of these weaning difficulties. But it is also essential to involve the wider network of family, friends to help the often vulnerable mother, confused by unfamiliarity with food, a low income and isolation.

Vegetarian/Vegan traditions Hindu parents are more than likely to give a vegetarian diet, but increasingly more of the population from all cultures in this country are adopting vegetarian practices. Less restrictive lacto vegetarian or lacto over-vegetarian diets can provide perfectly adequate nutrition during weaning, although some parents may need to be educated how best to provide for their baby's needs. Especially important is it that these diets, which can be bulky and often low in energy, might make it difficult for the baby to take in enough energy for their growth and developmental needs. Many legumes are also high in phytates which through their inhibitory activities diminish the bioavailability of certain dietary minerals, especially iron, another reason why the weaning diet of vegetarian families should be rich in vitamin C.
   Those on vegan diets - where no products related to animals are consumed - are, in theory at least, more vulnerable although in day to day practice there seem to be few problems. It is important that the food proteins given contain a good balance of essential amino acids. Also, since vegetables and fruit tend to be more bulky than cereals, too much can reduce the amount of energy in the diet. Similar problems to vegetarians apply to high levels of phytate in the diet. A strictly adhered to vegan diet cannot also provide sufficient vitamin B12 and advice how best to make up for this potential vitamin deficiency should be sought. Limited though these diets might seem to be, vegan diets can promote normal infant growth, providing that sensible guidelines are offered. This applies especially to appropriate breast milk substitutes, supplements, the type and amount of dietary fat and also the nature of solid foods. Attention at the same time has also to be given to vegan mothers since the composition of their breast milk may vary considerably in its fat content. Infants may well need vitamin supplements if the maternal diet is in any way inadequate and the same applies to infants during weaning. Tofu, dried beans and meat analogues should be introduced as part of the weaning process. Another concern is the long-term outcome in terms of the calcification of bone. Soy based formulas should continue to be given well into the childhood years to prevent these various potential deficiencies. The involvement of a paediatric dietician is essential when confronted with these special and often difficult and sensitive problems.

Is weaning proceeding normally?
Whether weaning is proceeding normally is best judged overall by serial and accurate recordings of weight gain and plotting individual weights on up to date weight charts. But it is very important to be able to correctly interpret profiles of weight gain, not always an easy matter since there continues to be insufficient recognition of the fact that between about six and twelve months considerable variation still exists in the profile of weight gain in individual infants. Movement down (and up) centile channels are still often the norm, so it is, therefore, difficult to give a precise definition of failure to thrive that is a possible pointer to inadequate weaning. A declining rate of weight gain is the basis for this diagnosis and any baby who crosses a centile line in a downward direction could be considered potentially as one who is not being fed sufficiently well, but this is only part of the argument. Weight must be viewed in a holistic way in the context of a careful history taken of food intake, general health and also ethnicity where subtle variations in profiles of weight gain may not be allowed for on a particular weight chart that relates more to a total population. Thus, for example, downward centile crossing in Chinese babies on charts derived from the ethnic majority in this country is a well recognised phenomenon that does sometimes lead to an incorrect diagnosis of suboptimal weight gain. The same applies also to head growth and, if measured, to growth in length. If inadequate weight gain is diagnosed there needs to be an examination of the nutritional adequacy of the weaning diet. But not only its content. Non-organic failure to thrive associated with behavioural problems through sub-optimum maternal/child interaction, must always be considered, especially where there might be a history in the mother of eating difficulties, for example anorexia nervosa. The very real difficulties babies with cerebral palsy and other neurodevelopmental problems have with mechanical aspects of weaning, especially those concerned with swallowing and chewing transporting the food through the mouth, frequently lead to poor weight gain.
   Another worry that not infrequently emerges during the monitoring of weaning is the mirror image of failure to thrive, abnormal fatness. Understanding the background to this is also necessary to interpret seeming accelerated weight gain. At six months babies are naturally chubby with fat contributing 25% of body weight: it is almost as though Nature is having to provide a food reserve, anticipating the special vulnerability of later weaning! As with failure to thrive, it is not the absolute pattern of weight gain that is important, but the context in which this takes place that includes family size and the nature of foods that are given.
   A qualitative measure of the adequacy of the weaning diet is the stool pattern. Western countries are seeing an explosion in problems of constipation that so often have their origins in poor weaning practices where the intake of NSP's are minimal. As mentioned above, it is very important for the weaning diet to contain sufficient vegetables and fruit, along with cereals to sow the seeds for satisfactory bowel motility.
   And finally, iron status of the infant is a very specific measure of the adequacy of the weaning diet. Iron deficiency and anaemia is such an important and a particular problem in young children, where the special difficulty in establishing a good pattern of solids in the diet and without over-reliance on cows milk renders many infants vulnerable to this complication.

Conclusion
After the secure immediate transition to immediate extra-uterine life and the establishment of milk feeding, weaning is the next major hurdle the young infant has to clear in its journey through infancy and early childhood. Weaning still causes a lot of worry to parents and also to their professional advisors, (as it has done throughout history), who all too often give inconsistent advice that serves only to confuse. As we have shown in this article, many problems can emerge as a consequence of poor weaning practices, both immediate as well as those in the longer term. Yet in 1994 the Department of Health produced an extremely well referenced booklet on weaning which though perhaps lacking a sound evidence base in certain areas, nonetheless provides for sound and safe practices that does not expose the young weanling to risk. Unfortunately, knowledge of the nation's guidelines on weaning on the part of health professionals is limited, suggesting lack of awareness of the guidelines. It is very important for health professionals to offer consistent and accurate guidelines, speaking with one voice in a language easily understood. The situation is sometimes made more difficult by the multicultural nature and makeup of our society, although at the same time this should offer a fascinating challenge.
   The problems facing the weanling in the developing world are enormous and of a totally different calibre and nature to those in rich countries. Culture, taboos, food choices, practices to prepare foods, abject poverty often dominated by ill-informed elders and peer-groups lead often to a poor quality of food intake with its well known consequences. To these can now be added problems caused by AIDS in the developing world. We have barely touched on these issues in this article but hopefully we have given sufficient pointers to stimulate the reader to read more about these in other texts.
   All parents (to be) should have received education about nutrition in their infants and this ideally should have begun during the school years. Antenatal classes provide later opportunities. In these classes, considerable time is spent on breastfeeding but all too often too little time on the "transitional" human being, the weanling. Paediatricians need to be more involved with this aspect than they are. The various child health record booklets now widely used should also include key points to help the mother wean her baby. But it has also to be appreciated that, and especially for young parents, reliance on their own home networks within their own communities also provide critical support. Parents of children who have special medical needs, and where there are strong cultural and religious beliefs, that might introduce risk into the weaning process, need to be dealt with sympathetically and with understanding if their infants are to thrive at this time. Expert dietetic advice must also be available to help where difficulties might arise.
   There is evidence to suggest that many mothers do find it difficult to comply with national guidelines to introduce solid foods, even when these are recommended and are introducing their babies to solids at three months or earlier. Maybe this is simply a reflection of the weakness of the evidence base that underpins these guidelines. But there is another possible explanation. Formula feeding is a strong predictor of early weaning, along with young maternal age, cigarette smoking and social class and the baby's weight in the first couple of months. Is weaning driven by biological needs in the baby, or is it socially driven by peer group pressure to conform, and when this takes place early, reflect less good health behaviour leading maybe to increased fatness and a higher incidence of chest disorders. History points more to the latter. So easy is it for the young infant to form habits to "caretaker" practices. Very early weaning is probably not usually driven by the biological imperative but more by a social one.
   Weaning times and weaning diets constitute in many ways, uncontrolled experimental interventions. Difficult though outcome studies will be to assess these interventions in terms of physical growth and health in both short and long terms, only if this research, often necessarily opportunistic, is undertaken will we be more able to best provide for the needs of the weanling. But, of course, this necessity pales alongside the disastrous consequences of weaning in so many children in the developing world where major mortalities and significant morbidity have their origins in this most hazardous of times.

Further Reading
1. Fewtrell, M.S., Lucas, A., J.B., Morgan; Factors associated with weaning in full term and pre-term infants. Arch. Dis. Child Fetal Neonatal Ed. 2003.88. F296-F301
2. DoH. Department of Health (Dott). Weaning and the weaning diet. Report on health and social subjects no 46. London: HMSO, 1994
3. WHO. Infant and young child nutrition. Global strategy on infant and young child feeding. WHO 55th World Health Assembly, 16 April 2002. A55/15. http//www.who.int/gb/EBWHA/PDF/WHA55/ea5515.pdf
4. Fildes, V., Breasts, bottles and babies: A History of Infant Feeding. Edinburgh University Pres. 1986
5. Why are babies weaned early? Data from a prospective population based study. C. M. Wriqht, K. N. Parkinson, R. J. Drewat. Arch. Dis. Child. 2004;80:815-816
6. Is nutritional ricketts returning? Allgrave, J. Arch. Dis. Child. 2004; 89: 699-701

 


 

Page Reference: 
Welsh Paed J 2005;22:51-63