Curr Paediatr 2004_ p83.pdf

7/25/2019 Curr Paediatr 2004_ p83.pdf

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www.elsevierhealth.com/journals/cuoe

CURRENT PAEDIATRICS

Weaning: a worry as old as time

D.P. Daviesa,b,*, B. OHarea,b

aUniversity of Wales College of Medicine, Wales, UKbUniversity Hospital of Wales, Heath Park, Cardiff CF14 4XN, UK

Summary Against a background of an historical appreciation that sets the scene forour current understanding, this article highlights present day practices in weaning,the process of gradually replacing breast or bottle milk with solid foods as the mainsource of nutrition for the young infant. Gastrointestinal, renal and nervous systempreparation provides the biological determinants for when weaning should begin.The major nutrients of the weaning diet that best provide for optimum growth,development and health are outlined. This understanding serves to help appreciatethe ideal programme of weaning and how its adequacies are best monitored,traditionally by the correct interpretation of serial weight measurement. Moderncontroversies are touched upon, especially the definition of weaning and theparticular problems of certain vulnerable infant groups. Finally, the worry andconcern still expressed by mothers, carers and health professionals alike aboutweaning, is highlighted. This largely reflects the lack of a strong evidence-base forthe weaning process: further research in this area is needed.&2003 Published by Elsevier Ltd.

Practice points

* Weaning, the process of gradually repla-cing breast milk or formula milk with solidfoods, continues to cause anxiety tomothers, nurses and doctors alike

* Biological determinants of weaning requirepreparation of the young infant especiallyin relation to maturity of the nervoussystem and its neuro-muscular coodina-tion; a functionally mature gastrointestinaltract that can digest and absorb nutrientsand have sufficient motility; renal functionthat must allow the young weanling tocope with an increased solute load

* Current UK recommendations are, for themajority of infants, whether breast milk orformula fed, to be introduced to solidfoods between 4 and 6 months. Thiscontrasts with recent World Health Orga-nisation (WHO) recommendations, heavilyinfluenced by the situation in resource-poor countries, which recommend exclu-sive breast-feeding for 6 months

* The scientific basis of weaning is therequirement for food energy, protein, fats,major minerals, iron, vitamins and othermicronutrients to satisfy normal growthdevelopment and optimise health

* The weaning period, which lasts between 6and 9 months, has at its broad expectationthe basis of a healthy adult type diet givenin 3 meals a day interspersed with smallsnacks, with milk still an important food

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KEYWORDSNutrition;

Infant;

Weaning;

Breast-feeding;

Developing countries;

Health

*Corresponding author. Tel.: 44-1443-238-190.E-mail address: [email protected] (D.P. Davies).

0957-5839/$ - see front matter&2003 Published by Elsevier Ltd.doi:10.1016/j.cupe.2003.11.006

Current Paediatrics (2004) 14, 8396


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* Special considerations need to be given toweaning in vulnerable infants, including:those at risk of atopic disease; pre-termand other low birth weight infants; those inminority cultures, especially where themother might be of vegetarian/vegan

tradition; and infants in economically poorcountries especially those where there is ahigh risk of HIV

* Adequacy of the weaning process is stillbest conventionally monitored by measure-ment and correct interpretation of weightgain

* Many mothers do have difficulty adheringto conventional advice and introduce solidsbefore 4 months of age. Evidence isemerging that this may often be relatedmore to social tradition rather than by

biological necessity. It remains to be seenwhether early weaning is associated witheither short or long term significant im-pairment of health.

Introduction

Many errors are daily committed in the method of

weaning children.

Treatise on the management of female complaints,Alexander Hamilton, 1792

She shall feed the child only on (mothers) milk, butwhen he has cut his front teeth it is well to accustom

him to more solid food, as women do of their own

accord, having learnt by this experience.

Galen of Pergamun, 170 A.D

The Jelliffes, those powerful advocates of breast-feeding throughout the 1970s and 1980s, remindedus many years ago of the notion of the human new-born as an extero-gestate fetus for the first 9months or so after birth. Over this period ofspecially rapid growth and development the younginfant is, in biological terms, completely depen-

dent on the mother for warmth, protection andfood, with the breast serving as an externalplacenta. Nature then dictates that mothers milk,in both its quantity and nutritional qualities,becomes gradually nutritionally insufficient forher babys growth and special nutritional needs,necessitating the extero-gestate fetus to become atransitional being, getting accustomed to newfoods of ever varying textures, tastes and nutrientdensities, until a full mini adult diet is reached.

It is the process of gradually replacing breastmilk, or in the modern world, formula milk, by solid

food as the main source of macro and micronu-trients and energy that is embraced by the termweaning, a word derived from the Anglo-SaxonwenianFto accustom. But some variation indefinition does exist. Thus a recent (2002) WorldHealth Organisation (WHO) definition uses the term

weaningto indicate a complete cessation of breast-feeding.1 Interestingly, this concept is embraced insome Romance cultures where, for example, inFrench weaning is referred to as servage and inSpanish, destetar, both words referring to separa-tion from the breast. More conventionally weaningis used to describe a period, not a single event,where there is a gradual replacement of milk(whether breast or formula), with its high fat, lowcarbohydrate content, by non-milk foods of low fatand high carbohydrate makeup. This latter defini-tion is preferred in this article, being more realisticin contemporary western societies.

The matter of weaning continues to cause moreanxiety to mothers, nurses and doctors than almostany other issue in paediatric nutrition. But, perhapsthis should not come as too much of a surprise sincein this aspect of infant nutrition comparativelylittle research has been undertaken, especially interms of the best age to wean, what constitutes themost appropriate weaning foods and also whateffects weaning has on long term health. Thisarticle offers a working synopsis of prevailingviews. Hopefully this will go some way to removesome of the widely held trepidation!

HistoryFa necessary prelude tocontemporary understanding

Throughout history, frequent reference is made tothe weaning of the baby from the breast. Frombiblical times written references to weaning haveoften appeared in scrolls, diaries, journals, papers,books, many written, perhaps surprisingly, by men!The likely reason for such preoccupation is thatweaning was (and in many economically poor

countries is even now) the most dangerous periodin early childhood, through its associations withparticular diseases often leading to high mortality.Thus in 18th century London up to 70% of infantsfailed to survive their second birthday, a majorcontribution to this appalling death toll being someof the more common weaning diseases, especiallygastrointestinal infections.

Weaning from the breast was also a period ofchange not only of diet but also of station. Asuckling was an infant with all that this implied,but once the breast was left for good, the baby was

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then generally regarded as a true child and as suchbecame a real member of the family. The upperclass child left the wet nurse and returned home tothe biological mother, while among the poorerclasses they were no longer fed at different timesbut ate out of the family pot.

Until the dawning of the modern industrial era inwestern countries early in the 19th century, adviceabout weaning was dominated by the writings ofthe Greek/Roman school of thought, led especiallyby Soranus of Ephesus (90117 AD) and Galen ofPergamun (130200 AD). For well over a thousandyears of literature on weaning, there is constantreference made to these medical authors and theirpupils. Indeed even the widely respected writingsof the Byzantine and Arab schools, so dominant inthe middle ages, seem simply to have adapted thisancient teaching to their more contemporary ways.The discovery of the printing press in medieval

Europe towards the end of the 15th century furthercascaded these ancient teachings. There is muchcommon sense in all of these writings, some areeven evidence-based, and their understanding isfundamental to the appreciation of current con-cerns about weaning in the modern world.

When to start?

Surprisingly, when the baby should be initiallytaken off the breast is not an aspect which receivesmuch consideration, since medical authorities

seem to have assumed that women would giveadditional foods either when the child appeared tobe ready for them, or according to custom amongfamily and friends. (How little things have chan-ged!) Sometimes it seems to have been theeruption of teeth that offered guidance, but theage at which foods other than breast milk wereactually first given was probably much earlier thanthe time recommended by physicians and midwives(again nothing new here!). Throughout historythere has also been an important thread that it isthe child rather than the mother who should decide

when weaning should take place.

What to give?

Initial foods commonly given to infants up to themodern era included paps and panadas. Paps werefoods made of flour and bread cooked in milk withadditives for flavouring or added nutrition; panadaswere stews of bread, broth, milk and eggs. Manyrecipes used to be made up from these foods;indeed, in many parts of the developing world papsand panadas are still widely used. However, there

does seem to be a difference between introducingfoods (the paps and the panadas) as a complemen-tary food to breast milk, and the weaning processitself which not uncommonly proceeded well intothe second year of life when children would be inpossession of several teeth and be capable of

sitting at the table and possessing some ability tofeed themselves. A theme condemned by manymedical writers was the custom of giving foods pre-chewed by the nurse or mother.

Down the ages it has also been a commonpractice to give the infant alcoholic drinks,especially gin, grape wines and brandy in thewealthy families and beer in the poor, a customthat achieved great popularity during the late 17thand 18th centuries (Fig. 1).

Although it is now unthinkable that a child asyoung as 612 months of age should be givenalcoholic drinks it has to be recognised that until

the development of clean water supplies, waterwas rarely drunk by the general population becauseof its widespread contamination. The most commondrink with a fairly high alcohol content for peoplein Britain was ale, beer, or small beer, althoughsmall beer was much weaker. It was therefore notsurprising that once a child was weaned and atesimilar food to the rest of the family, it was also

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Figure 1 yythroughout history it has also been notuncommon practice to give the infant alcoholic drinks.Taken from Hogarth, Gin Lane 1751. Note the infantbeing fed gin. (Taken from Fildes, V.)

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natural for them to have the same drink. Thefollowing quotation by the Edinburgh doctor,William Buchan (1769) in his book DomesticMedicine; or The Family Physician says it all: Allstrong liquors are harmful to children. Someparents teach their children to guzzle ale and

other strong liquors at every meal, but such apractice cannot fail to do mischief: milk water,butter milk or whey make the most proper drinkfor children. If they have anything stronger, it maybe fine small beer, or a little wine mixed withwater.

But some interesting pointers to the beginning ofthe weaning process do emerge. Soranus advisedthat babies should be breast-fed completely for 6months, although this was far from the actualpractice at that time. He also recognised that itwas bad to withhold solid foods until the child wastoo old since this would lead to digestive problems

and difficulties in adapting to new foods. The Koranadvised the beginning of weaning at 2 years, butthis is not in any way a strict ruling, allowing thechild to be weaned earlier if necessary. In the 16thcentury the ideal age for introducing mixed feedingseems to have been between 79 months, butapparently during the late 17th and 18th centuriesmuch earlier weaning from the breast was fa-voured, as early as 24 months. If there is a generaloverall message that comes down the ages it isthat the process of weaning was recommended overthe wide age range, from 624 months. Late

weaning seems to have been advised for weakor treasured children, but from the late 17thcentury, a long suckling period did attract thedisapproval of many medical writers. Other factorsalso considered when weaning a child earlyincluded the help of a nurse and the state of themothers milk.

How to wean?

Most medical writers agreed that gradual weaningis preferable to sudden weaning, a very cruel

practice sadly still all too prevalent in somedeveloping countries. Ways in which weaning fromthe breast was achieved included giving food priorto breast-feeding and encouraging suckling only atnight. But sometimes it was so very difficult towean the child from the breast belonging to themother or wet nurse that it was necessary to anointtheir breast with mustard, or by rubbing the top ofthe 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 Julietsweaning when 3 years oldy

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 dugy.

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, verytraumatic for the child and probably even more sofor the mother. Indeed, perhaps this was causallyrelated to the high prevalence of melancholia inthe mother that was written about so much duringthe 16th and 17th centuries. Any obvious distress tothe baby accompanying weaning was soothed byadministering laxatives, alcohol and even opiates.

In the western world in industrial times, theredoes appear to be a gradual decrease in the age ofweaning which probably relates to the growingavailability and the social acceptability of artificial

feeding, the fall in the number of wet nurses forthe middle classes and the movement of thepopulation from the countryside into towns. Thebeginning of industrialisation also began to seechildren weaned progressively in a way similar totoday, beginning with pureed or minced foodcontaining milk or broth, and progressing to foodseaten by the rest of the family, mashed and cut intosmall pieces as the child becomes older.

Importance of milk: the diseases of weaning

An important aspect was the recommendation forfoods containing milk being an important part ofthe weaning diet, with the increasing awareness ofspecific diseases resulting from deficient weaningpractices, especially scurvy, rickets (Fig. 2), blad-der stones, night blindness and a very lowresistance to infection. Indeed it appears that the18th century saw a definite decline in the nutri-tional value of foods when compared to the 16thcentury. Surprisingly the diet, especially that of thewealthy, did not include many milk or milkproducts. This diet of mainly cereal and meat,excluded vitamins A, D and C, also the amount of

calcium it contained was insufficient for a growingchild. Hence the laying down of the seeds of somespecific diseases of weaning. Poorer families,however, seemed paradoxically to have a differenttype of diet consisting mainly of bread, cheese, millsalt, meat and pulses, so the poorer child wasprobably much better fed in nutritional terms,providing that enough food was given. White meatsand dairy foods, including eggs were eaten by thepoor and many cottages in the countryside kept acow, so milk was far more likely to be drunk bythese families than by the wealthy. But for as long

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as milk was in the diet, irrespective of the type ofmilk, bone disease was less common.

The gastrointestinal disorders of weaning were

well described by the Scottish surgeon, John Aitkenin 1876 This is a violent purging frequentlyattended with vomiting, wasting, etc. Causes: 1)early 2) weaning improper food Cure: removal ofcauses. This is a good description of weanlingdiarrhoea so prevalent in areas of India, Africa andCentral America today, where stunted growth,leanness and wasting are still associated with earlyweaning.

The Present

When to begin?

The timing of introducing non-milk foods is condi-tional on some important physiological determi-

nants that are needed to prepare the young infantfor the nutritional transition that constitutes theweaning process:

* The nervous system needs to have acquired alevel of maturity of neuromuscular coordinationthat permits the safe taking of solid food from aspoon and its movement as a bolus though themouth into the upper gastrointestinal tract to beswallowed. Head control also has to be suffi-ciently mature to maintain a suitable posture forthe safe movement of this food.

* The gastrointestinal tract must be functionally

prepared to digest and absorb dietary nutrients.It must be sufficiently motile to transport thefood the length of the gut. The baby also has tobe protected by the process of gut closure fromthe ingress into its body of large foreign proteinmolecules that can lead to an abnormal immuneresponse and with it, physical illness. SecretoryIgA and other protective substances producedwithin the gut wall play a vital role in thisfunction and they also reduce significant bacter-ial colonisation of the gut, which is a risk factorfor serious infection. Once again, the umbrella

of protection conferred by human milk, espe-cially cells, IgA, numerous chemical substancesand enzymes play an important and insufficientlyappreciated role in preparation for weaning. Thegut also prepares itself for the diverse demandsof obtaining nutrients from a mixed diet, byenhancing growth of its epithelium. For exam-ple, the large amount of sphingomyelin in humanmilk, 35% of its total phospholipid, and manyother locally produced growth factors andhormones have a major role promoting epithelialgrowth. They act via their relevant receptors inthe small intestine to mediate this function and

are superimposed on genetic pre-programming;* The kidney must also be physiologically prepared

to allow the young weanling to cope with anincreasing solute load. It does this by improvingits concentration ability to preserve intact themilieu interieu. If this physiological determi-nant fails, the danger of hyperosmolar statesthat were so prevalent in the 1970s with thewidespread use of high solute formula milks andthe very early introduction of non-milk foods,both contributing to hypernatraemia with itsserious short and long term complications.

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Figure 2 Rickets was noted a prevalent disease in the18th century, a condition particularly associated withweaning. The skeleton of Bowed Joseph, an 18thcentury Edinburgh character whose skeleton is in theAnatomy Museum of Edinburgh University. (Taken fromFildes, V.)



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What does this state of multi-organ physiologicalpreparation tell us about the age to move from theexterogestate fetus to the transitional humanbeingthe weanling? This is often a difficult tight-rope to negotiate, especially for infants in poordeveloping countries. The too early introduction of

non-milk foods and (in HIV endemic parts of theworld) early cessation of breast-feeding will riskforeign protein-mediated food intolerances, includ-ing coeliac disease. It can also expose the young toinfection, particularly of the gastrointestinal tract,whilst also sewing the seeds of malnutrition andabnormal internal body milieu states, especiallyin the presence of diarrhoea and perhaps evenincreasing the risk of childhood asthma. Beginningweaning too late will risk undernutrition, as theneeds of the young increasingly outstrip thecapacity of the mothers milk (or indeed milkformula) to satisfy these requirements for growth

and development and for certain micro-nutrients,especially iron and zinc.

Delay in introducing solid foods of varyingtextures, tastes and consistencies will also inhibitthe development of neuro-muscular mechanismsneeded to mechanically prepare and deliver non-milk foods to the gastrointestinal tract, such aschewing and moving the bolus of food in the mouth.Missing out on this critical period may make forfeeding difficulties later. It is important to recog-nise that the eruption of teeth has no effect on theweaning process, although in history (as mentioned

above), it has often been considered a usefulmarker for the timing of weaning.

Current recommendations

For the majority of infants, solid foods for breast ormilk formula fed babies should be introducedbetween 4 and 6 months of age, following the1994 Department of Healths (DoH) recommenda-tion2. There is no magic test to determine whenweaning should begin. It is essential that the health

professionals who purvey advice are sensitive tothe mother or other carers perception that thebaby, through its physical size and changed beha-viour, might no longer be satisfied by milk alone,whatever the official recommendations may be.As a determinant for the starting of weaning, thisdictation by the baby and its pick-up by a sensitivemother is critical and all too often denied by thosewho set guidelines. In the western world this leadsto the reality that the majority of babies are beingintroduced to solid foods by about 4 months of age.Some (very few) seem to need solids before 3

months of age and as long as this is in response to ababys perceived needs, there should be noproblem even though this is a very early introduc-tion to solids. Throughout history, some babies aregiven solid foods as a complementary food, simplyas a taster and not as part of a planned weaning

process. However, in most instances the giving ofnon-milk foods does signal the beginning of theweaning process itself.

Against this background it might come as asurprise to read the 2002 WHO revised recommen-dation for weaning from the breast, which is thatmothers should exclusively breast feed for at least6 months and continue breast-feeding up to, oreven beyond, 2 years1. The background to this isthe situation that applies to breast-feeding in poorcountries, with special reference to the current HIVpandemic and the hazards of replacement feeding.These are two critical factors that influence the

timing of weaning that can sometimes be seen to bein opposition to each other. These issues are worthexploring in a more detail.

In 2002 there were 800,000 children newlyinfected with HIV, 90% of these by mother to childtransmission (MTCT) and 75% of this number were insub Saharan Africa. Where there are no interven-tions such as antenatal anti-retroviral therapy andCaesarean section, the risk of transmission duringpregnancy is 510%, and during labour 1020%.Added to this, the additional risks from breast-feeding must be considered. In the first 2 months

breast-feeding adds an extra 2

10% risk of trans-mission. Breast-feeding after 2 months but stoppingat 6 months adds another 15% chance of transmis-sion, which increases a further 510% if the baby isbreast-fed until 1824 months of age. A recentUNICEF factsheet on breast-feeding and HIV sum-marises these figures, warning that a baby breast-fed for 6 months has one-third the risk oftransmission during breast-feeding than that of ababy breast-fed for 2 years, although both groupsstill having the 1530% risk of transmission duringpregnancy and delivery. The risks of breast-feedingfor continuing MTCT are therefore considerable.

And what does HIV infection mean to a childliving in, for example, sub-Saharan Africa? The vastmajority (90% in some studies) of children infectedwith HIV at birth will die by the time they are 3years of age. The remainder will die in their firstdecade, generally when they are 6 or 7 years of agehaving suffered multiple episodes of gastroenter-itis, respiratory tract infections often includingtuberculosis and frequent episodes of oral candi-diasis. Even if the child is seronegative, if itsmother is infected with HIV the risk of mortality isgreatly increased.

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The reverse argument also has to be considered,namely the risks in this setting of not breast-feeding. Eleven million children under the age of 5die every year worldwide from malnutrition, andtwo-thirds of these can be attributed to poorfeeding practices in the first year of life. UNICEF

warns that a baby who is receiving replacementfeeding in the first 2 months of life has a six-foldincreased mortality due to diarrhoea and otherinfectious diseases. It is common in many resource-poor countries to complement breast milk withdrinks such as water and tea. Yet it has been shownthat despite the climate, exclusively breast-fedbabies are no more likely to become dehydratedand there is no nutritional benefit to these feeds.Fewer than 35% of babies are exclusively breast-fedfor the first 4 months of life worldwide.

In summary, how are these issues resolved inresource-poor developing countries (compared with

the developed industrial world) where additionaldeterminants for the timing of weaning include:lack of appropriate available breast milk substi-tutes; high risk of microbiological contamination offoods; few opportunities to administer antiretro-virals to HIV positive mothers; and an earlier returnto potential fertility with early cessation of lacta-tion amenorhoea that inevitably follows stoppingbreast-feeding. In these countries, delaying theintroduction of non-milk foods to 6 months isseen as a factor that may help reduce mortalityand immediate and later morbidity, recognising at

the same time the continuing risks of HIV transmis-sion. In rich countries where there are readilyaffordable non-milk foods, where general hygieneminimises contamination of food and where effec-tive contraception is readily available, there isreally no need to change the 1994 WHO recom-mendation. Indeed, in this and other industrialcountries the (unrealistic) advice of exclusivebreast-feeding for 6 months (without extendingstatutory maternity leave!) might even lead someto not bother with breast-feeding in the first place.A recent large study of weaning in normal termbabies in Britain showed that only 2% of breast-fed

infants did not receive any other foods for theirfirst 6 months.

What little scientific data there is availablesupports the view that exclusive breast-feedingfor 6 months is probably safe for most babies interms of nutritional adequacy, providing that themother is well nourished. But, for the less wellnourished mother, babies exclusively breast-fed forthe first 6 months may be at risk of poor weightgain. More robust evidence must be sought on thisrecommendation before it can be universallyimplemented. Indeed, it is also salutary to recall

that consideration has never been given to possibledifferences in the weaning requirements for breastor formula fed babies. Without this evidence it isprobably fair to say that reality and pragmatismdictate, at least in the developed world, thatweaning best takes place between 4 and 6 months

of age, although the recent WHO recommendationsmay, on balance, be seen as a necessary populationstrategy for developing countries and for certainindividual babies in the developed world.

The process of weaning

There are many influences on the process ofweaning to which culture, taboos, religious belief,ethnicity, tradition, medical opinion and dietaryfads all contribute in their individual ways. Also thevariation in rates at which young infants acquire

those special motor feeding skills that are aprerequisite for safe weaning must be considered.

This article focuses on weaning in Britain wherethe broad aim is to achieve, by about 12 months ofage the basis of a healthy adult type diet given in3 meals a day, interspersed with small snacks andwith milk still considered as an important food.Over the weaning period a wide range of foodswith different tastes and textures need to beoffered to enrich the palatal experiences of theyoung infant. The process of introducing new foodsmust be gradual and babies are likely to adapt best

if solid foods are offered initially from the spoon, orgiven as finger foods, and not as solids made intodrinks, or given dissolved in milk or other fluids in abottle. It is also sensible not to introduce too earlythose foods that are associated with nutritionalintolerances, atopic disease and allergies (seelater).

How these prerequisites are translated into theactual weaning diet make up the process ofweaning and this can be best understood byconsidering the particular vulnerabilities and re-quirements of the young human infant at thisdevelopmental stage. At the core of these require-

ments is the need for the infant to satisfy normalphysical growth and the accompanying develop-ment that proceeds so rapidly at this time. This isall made possible by providing protein buildingblocks in the diet, complemented by key micro- andmacro-nutrients. Specific dietary reference valuesprovide the range of individual nutrient require-ments to satisfy these needs. These are notreferred to further in this article but the interestedreader can consult relevant texts to learn more. Inwhat follows the emphasis is more on qualitativeaspects of the weaning diet.

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Food Energy

Fat is a major contributor to the energy content ofthe weaning diet although as a steadily diminishingpercentage falling from over 50% in breast milk at46 months to around 35% in the diet at about 18

months. Most of the weanlings fat comes in milkcomplemented by a variety of other weaning foods.Strongly contraindicated in the weaning diet arelow fat foods that can only slow down growth anddevelopment. Semi-skimmed milk, provided thediet is sufficiently varied, should await at least thethird year for its introduction. A recent surveyconducted through Mother and Baby magazinefound that, worryingly, many mothers were intro-ducing their babies to low fat, low calorie meals inorder to lessen the risks of their children becomingoverweight. It needs to be impressed on mothersthat 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 ab-sorbed starches in cooked cereal products and rice.Extrinsic sugars, as added sugars in fruit juices,honey and table sugars for example, are alsoneeded although they should be used sparingly toprevent young infants developing the habit oftoo sweet a tooth and its links with poor dentalhealth later.

Structural fats and neural development

The continuing rapidity of the growth of the brainand other neural tissues requires large amounts ofphospholipids that are rich in long chain polyunsa-turated fatty acids (LCPFAs), especially docosahex-anoic and arachidonic acids. It is likely also thatLCPFAs are needed for vascular endothelial growthand the cell membranes of other tissues. Theirsynthesis during weaning requires an adequateamount in the diet of the essential linolelic andalpha-linolenic fatty acids.

Non-absorbable carbohydrates

The weaning diet also has to accommodate thoseelements that contribute to normal gastrointestinalmotility, especially of the large bowel, to preventsluggish bowel movement that ultimately leads toconstipation, which is a scourge of contemporarywestern type societies. The main contributors tothis function are non-starch polysaccharides (NSP)and complex polymers (previously called dietaryfibre and derived mostly from plant cell walls). But

it must be remembered that these are low energydense foods and giving too much NSP duringweaning is to be discouraged, as they may displacemore energy rich foods, and cause diarrhoea. Manyfoods rich in NSP, such as cereal products andlegumes, also happen to be a rich source of

phytates that reduce bioavailability and hencethe absorption of micronutrients, especially ironand zinc. In the indigenous British culture there islittle danger of the weaning diet having an over-abundance of NSP, although the same perhapsmight not always be said of those cultures andindividuals who embrace vegetarian and (espe-cially) vegan practices. With constipation such acurrent concern the weaning period must be seenas a good opportunity to lay down good futuredietary practices, as well as to satisfy currentnutritional needs. Encouraging young infantsto take and enjoy plant foods and fruit can do

much to help.

Protein

The essential determinants of lean body mass andlinear growth are provided mostly in the protein ofmeat, fish, eggs and milk that contribute a properbalance of essential amino acids. In westerncountries protein deficiency is rare in otherwisehealthy children. But it is important to rememberthat non-animal products and many plant foods aremuch lower in protein and essential amino acids

than equivalent animal sources. This is why soyaprotein-based formulas and other foods (such astofu) are such valuable elements to the weaningdiets in vegetarian and vegan families.

Major minerals

The fact that the skeleton, not forgetting theteeth, contains most of the calcium, magnesiumand phosphate in the body shows how important itis to ensure an adequate intake of these minerals inthe weaning diet. These are best provided in milk,

milk products and foods derived from calciumfortified white flour. Phosphorous is also neededfor basic cellular metabolic processes includingenergy release, as well as being an integralcomponent of phospholipids in cell membranes.Sodium is the most important extracellular mineraland this is well provided for in nearly all weaningfoods. Indeed, if anything there is now a concernthat many proprietary foods are overly rich insodium. The young kidney has only a limited abilityto excrete a sodium load and although risks ofhypernatraemia have virtually disappeared with

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weaning practices that now contribute much less ofa solute load than a couple of decades ago, thelinks that are now emerging between early sodiumintake and the tracking of high blood pressure intoadulthood makes sodium intake a very importantissue. The palate must be conditioned not to need

more salt. It goes without saying, therefore, thatsalt should never be added to the weanlings diet.Other minerals, particularly potassium, zinc and

copper are essential for cell and tissue growth aswell as on a general basis for enzyme synthesis. Inthe average western weaning diet these should beall well provided for.

Iron

Nutritional iron deficiency continues to be the mostcommonly diagnosed nutritional disorder of early

childhood worldwide, and Britain is no exception.With iron a vital component of haemoglobin,myoglobin and many enzyme systems, psychomotorapathy, poor weight gain and increased vulnerabil-ity to infections are all important and worryinglycommon clinical consequences. The seeds are oftensown in bad weaning practices especially in certainhigh-risk communities, notably Asian families thathave recently arrived in this country and othersocially disadvantaged inner city families. Redmeat and other meat products from which iron isreadily available, are an important part of theweaning diet and their intake must be encouraged

along with other iron fortified foods. The non-haemiron that is present in vegetables and other plantshas a much reduced bioavailability. Fibre, espe-cially from cereals, legumes and other vegetables,can also inhibit iron absorption through their highphytate content. The vulnerability of those onvegetarian and especially vegan diets is obvious.(See also later). Another major risk factor for irondeficiency is the giving of cows milk too early.Cows milk is low in iron, causing intestinal bloodloss and also filling up the infant, thereforediscouraging other foods. It is for this reason that

breast milk or a fortified infant formula and notcows milk should be an essential part of theweaning diet until the second year of life. Ironabsorption is enhanced by vitamin C in the diet,hence the value in vulnerable groups of thisparticular supplement and also the inclusion offruits and lightly cooked or raw vegetables.

Vitamins

Most vitamins have specific functions. Vitamin A isobtained from animal products and fish oils as pre-

formed retinol and as carotenes in vegetables andfruit. It is essential for growth and neural develop-ment, immune function and as an anti-oxidant. TheB group vitamins found in a wide range of all foodsare integral to cell processes and tissue regenera-tion. Vitamin C, found especially in vegetables and

fruits (prolonged cooking can destroy vitamins), areimportant as anti-oxidants and also assist theabsorption of iron from vegetable and other non-haem iron sources. Vitamin D is vital for calciumabsorption and the deposition of calcium in bone. Itis naturally present in very few foods, with theobvious exception of fatty fish, although research isnow showing that more Vitamin D might occurnaturally in eggs and meat than was previouslythought. Fortunately it is readily synthesised in theskin by the action of ultra-violet B radiation on thesteroid precursor 7-dehydrocholesterol, the pro-cess being completed in the liver and kidney to the

active vitamin D metabolite. Vitamin E is made upof tocopherols, the most active being alpha-tocopherol, found in fortified foods and especiallyin fatty fish. It is needed to preserve the structuralintegrity of phospholipid cell membranes and alsoto help protect vascular endothelium and neuralcells from free radical damage.

This basic understanding of the major nutrientsof the weaning diet can now be translated into thefollowing general weaning programme that shouldapply to most young infants in this country.

46 months

At this early stage the important learning skill forthe baby is to become accustomed to taking foodfrom a spoon. Patience is essential throughout theweaning process. An initial first food could include;a cereal; baby rice mixed with the babys usualmilk; mashed potatoes; yoghurt; and custard. It isimportant to recognise that food intake at this veryearly stage serves largely as a taster given byspoon 2 to 3 times a day. Milk continues to beessential for all nutrient needs. Other suitableearly foods once the baby accepts these bland

foods and is able to take food from the spooninclude pureed meats, pulses, fruit and a widevariety of cereals.

69 months

This phase now sees solid foods as an increasinglymore important provider of energy and generalnutrition, with milk gradually becoming less im-portant. Vegetables, lean meat, cheese, yoghurtsand bread are then gradually added in a mashed orpureed form. These provide more varied tastes andtextures. Babies themselves may now be able to

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put foods into their own mouths, experimentingwith finger foods, for example toast.

912 months

This stage is now beginning to reflect a moremature diet with 2 or 3 meals interspersed with

healthy snacks. The texture of food is now lesspureed. At this stage eggs and fish can be added,although nut products are best delayed until thesecond year.

In summary, providing the young infant with amixture of available foods, maintaining an intake offortified formula or breast milk (if the mother is ofadequate nutritional state) along with moderateexposure to summer sunlight should provide anadequately balanced weaning diet in this country.The change from breast or infant formula to cowsmilk should ideally be delayed until after the firstbirthday, cows milk being a major risk factor foriron deficiency. Water and fruit juices are impor-tant. Adding salt or sugar is also strongly discour-aged because of respective links with laterhypertension and the general development of toosweet a tooth, which sows the seeds for laterobesity and dental caries. The too early use of acup from the bottle is also to be discouraged sincethe coordination needed to feed from a cup is oftendifficult. There is the general recommendation thatafter 12 months bottle feeds should be discour-aged, with cup feeding being preferred. But if thecup skill is overemphasised, fluid intake will be

insufficient. Babies themselves will determinethrough their own individual skills, the timing whenfluids can satisfactorily be taken from the cup.Maintaining a high fluid intake is also necessary tokeep a good urinary flow, therefore lessening therisks of urinary-tract infection.

An example of weaning in a young child living inBritain is shown inTable 1.

Practical Aspects

Weaning foods can be home prepared, commercialor mixtures of the two types of baby foods. Thischoice largely depends on the shopping and cookingcapabilities of the mother and father, and otherfamily choices. Financial considerations and con-fidence also play a part early on when only smallamounts of food are used with the potential forhuge wastage. Data on the nutritional compositionof many home prepared foods show great varia-bility with, if anything, a tendency to be rather lowin protein, fat and iron and even of lower energydensity. Hence the potential value early on of

feeding commercial foods, either alone or as asupplement. It would seem, however, that afterabout 18 eighteen months the use of commerciallyavailable baby foods in this country has declinedconsiderably. When the family pot is used it isimportant once again to emphasise that salt and

sugar should not be added.Irrespective of the type of food fed to the baby,great care must always be taken regarding foodhygiene, including cooking and storage, to preventfood borne microbial illness. Increasing use ofmicrowave cooking also means the risk of burningthe young infants mouth. These practical detailsmust always be emphasised as essential compo-nents of the weaning process along with theperhaps more interesting, nutritional aspects. Notto be forgotten is the need for patience. Duringweaning, infant behaviour is often frustrating withfood refusal, spitting and smearing food on cloths

and utensils, etc. Parents and other carers have tobe assured that this is all part of the normalexploratory weaning process.

Vulnerable groups

In some infants special consideration may need tobe given to the general process of weaning that hasjust been described because of their particularvulnerability. (Excluded from this section areinfants with diseases already diagnosed and whomay require special nutrition for illnesses such as

coeliac disease or 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 atrisk of asthma, hayfever, atopic dermatitis andother allergies, a delay beyond the usual recom-mendations of introducing weaning foods is advi-sable especially in view of the physiological fall inthe levels of secretory IgA in the gut over the first 6months of life. (This of course is naturally compen-

sated for by the high quantity of IgA in breast milkduring this period). There is, however, no goodclinical or epidemiological evidence to supportdelaying the introduction of potential food aller-gens commonly linked with these disorders, notablymilk protein, eggs and nuts, or even to prolongbreast feeding beyond 4 to 6 months to lessen therisks of future illness by sensitisation. It is sensiblefor a breast-feeding mother to avoid eating thesecommon food antigens in the early months afterbirth since this could lessen the risk of illness inher baby.

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Pre-term and other low birth weight infants

Although some of these babies may go home fromthe neonatal unit with poor weight gain and feedingproblems, including sucking and swallowing diffi-

culties, the general rules of weaning still apply. Itmay be thought that for infants who have sufferedintra-uterine growth retardation, introducing solidfoods before 4 months might be demanded by thebabies themselves. The reality seems to be theopposite. In a recent national study of 2000 babies,small for date babies, whether breast or formulafed were less likely to have been started on solidsbefore 12 weeks. It may be that their size led togreater parental concern and, therefore, a greaterlikelihood to stick with the guidelines. Maybe eventheir babies perceived small size downplayed the

need for solids, just as higher weights at around 6weeks often leads to very early weaning. For pre-term babies, some studies have even linkedimproved growth rates and improved iron status ifsolids, especially those of higher energy density and

protein content, are introduced to the diet atabout 3 months of age. More research is needed toimprove the evidence and to provide guidelines forthese two special categories of low birth weightinfants. This must also include the long terminfluences on growth and health.

Infants in minority cultures

There is no doubt that culture, tradition andreligious beliefs have a profound effect on dietary

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Table 1 One example of a typical pattern of weaning in a young child living in Britain.

dFrom about 4 monthsEarly morning: breast or bottle feed 6 amBreakfast: baby cereal mixed with milk from feed. Breast or bottle feed 10 amDinner: finely sieved broth. Breast or bottle feed 2 pmTea: breast or bottle feed 6 pm

Late evening: breast or bottle feed 10 pm

dFrom about 7 monthsWhen cows milk is commenced, the opportunity should be taken to introduce a vitaminsupplement, such as the A, D and C drops available at Child Health ClinicsEarly morning: breast or bottle feed 6 amBreakfast: baby cereal mixed with milk from feed. Scrambled, poached or boiled egg. Breastor bottle feed

10 am

Dinner: minced meat and vegetables or mashed white fish and vegetables. Fruit puree, custardor milk pudding. Cup of milk

2 pm

Tea: savoury ready-prepared food or sandwiches with savoury filling, for example soft cheese.(Fine-textured wholemeal bread can be used at this stage.) Breast or bottle feed

6 pm

Late evening: breast or bottle feed 10 pm

dFrom about 9 monthsEarly morning: milk or fruit juice. On AwakeningBreakfast: breakfast cereal with milk. Scrambled, poached or boiled egg. Fingers of toast withbutter. Cup of milk

9 am

Dinner: junior savoury ready-prepared food or well chopped meat and vegetables. Peeledapple, banana or milk pudding. Cup of milk if required

1 pm

Tea: cheese or fish dish or sandwiches with savoury filling. Cup of milk 5 pmLate evening: breast or bottle feed 8 pm

dFrom about 12 monthsBreakfast: breakfast cereal with milk. Crisply grilled bacon or egg. Toast with butter. Bottle/cup of milk/breast feed

8 am

Mid-morning: drink of fruit juice 10.30 am

Dinner: chopped meat, chicken or steamed fish. Chopped vegetables and mashed potatoes.Milk pudding, blancmange or yoghurt

1 pm

Tea: scrambled, poached or boiled egg. Bread and butter. Orange, apple, banana or soft fruitin season

5 pm

Evening: bottle/cup of milk/breast feed 8 pm



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practices. Ethnic minority communities in thiscountry are likely to vary in their weaningbehaviours. However, we need to be reminded thatthere is no single ethnic minority culture and, aswith other instances of weaning, variations needto be tolerated, indeed often encouraged, provid-

ing of course that the basic nutritional require-ments are met. The following points need to beconsidered.

Iron, vitamin D and other micronutrient deficien-cies have been identified as major problems insome Asian populations where whole cows (door-step) milk is introduced at a very early age andcontinued in large volumes. Not only does this riskprimary nutrient deficiencies, especially anaemiaand biochemical rickets, but by filling the stomachthe infant is less eager to take solid foods. Mothers,especially those from Muslim backgrounds, aremore likely to introduce solid foods later, thus

compounding iron and vitamin D deficiencies. Theyalso have a tendency to use more convenience babyfoods, which are high in carbohydrates. It isimportant to recognise that these patterns are alsoto be found across other minority ethnic groups aswell as in the ethnic majority in inner cities andother equivalent areas. As with all instances ofprolonged bottle feeding, babies miss out oncritical periods of the taste and texture variationsof solid weaning foods, which can lead to therejection of mixed tastes later on.

Awareness of these potential problems should

help in the primary care management and preven-tion of these weaning difficulties. But it is alsoessential to involve the wider network of familyand friends to help the often vulnerable mother,confused by unfamiliarity with food, a low incomeand isolation.

Vegetarian/Vegan traditions

Hindu parents are more than likely to give avegetarian diet, but increasingly more of thepopulation from all cultures in this country are

adopting vegetarian practices. Less restrictivelacto vegetarian or lacto ovo-vegetarian diets canprovide perfectly adequate nutrition during wean-ing, although some parents may need to beeducated in how best to provide for their babysneeds. It is especially important that these diets,which can be bulky and often low in energy, mightmake it difficult for the baby to take in enoughenergy for growth and developmental needs. Manylegumes are also high in phytates which, throughtheir inhibitory activities, diminish the bioavail-ability of certain dietary minerals, especially iron.

This is another reason why the weaning diet ofvegetarian families should be rich in vitamin C.

Those on vegan diets are in theory morevulnerable, although in day to day practice thereseem to be few problems. It is, important that thefood proteins given contain a good balance of

essential amino acids. Also, since vegetables andfruit tend to be more bulky than cereals, toomuch can reduce the amount of energy in thediet. Similar problems to vegetarians apply tohigh levels of phytate in the diet. A strictlyadhered to vegan diet cannot provide sufficientvitamin B12 and advice how best to make up forthis potential vitamin deficiency should besought. Limited though these diets might seem tobe, vegan diets can promote normal infantgrowth, providing that sensible guidelines areoffered. This especially applies to appropriatebreast milk substitutes; supplements, the type

and amount of dietary fat and also the nature ofsolid foods.

Attention also has to be given to vegan motherssince the composition of their breast milk may varyconsiderably in its fat content. Infants may needvitamin supplements if the maternal diet is in anyway inadequate and the same applies to infantsduring weaning. Tofu, dried beans and meatanalogues should be introduced as part of theweaning process. Another concern is the longtermoutcome in terms of the calcification of bone. Soybased formulas should continue to be given well

into the childhood years to prevent these variouspotential deficiencies. The involvement of apaediatric dietician is essential when confrontedwith these specials often difficult and sensitiveproblems.

Monitoring the weaning process

Whether weaning is proceeding normally is bestjudged overall by serial and accurate recordings ofweight gain on up to date charts. It is very

important to be able to correctly interpret profilesof weight gain, which is not always an easy mattersince there continues to be insufficient recognitionof the fact that between about 6 and 12 monthsconsiderable variation still exists in the profile ofweight gain in individual infants. Movement down(and up) centile channels are still often the norm,so it is difficult to give a precise definition of failureto thrive that is a possible pointer to inadequateweaning. A declining rate of weight gain is the basisfor this diagnosis and any baby who crosses acentile line in a downward direction could be

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potentiallyconsidered as one who is not being fedsufficiently well, but this is only part of theargument. Weight must be viewed in a holisticway in the context of a careful history taken of foodintake, general health and also ethnicity, wheresubtle variations in profiles of weight gain may not

be allowed for on a weight chart that relates moreto a total population. Thus, for example, downwardcentile crossing in Chinese babies on charts derivedfrom the ethnic majority in this country is a wellrecognised phenomenon that does sometimes leadto an incorrect diagnosis of sub-optimal weightgain. The same applies also to head growth and (ifmeasured) to growth in length. If inadequateweight gain is diagnosed there needs to be anexamination of the nutritional adequacy of theweaning diet, but not only its content. Non-organicfailure to thrive associated with behaviouralproblems through sub-optimum maternal/child

interaction, must always be considered, especiallywhere there might be a history in the mother ofeating difficulties, for example anorexia nervosa.The very real difficulties babies with cerebral palsyand other neuro-developmental problems havewith mechanical aspects of weaning, especiallythose concerned with swallowing, chewing andtransporting the food through the mouth, fre-quently lead to poor weight gain.

Another worry that frequently emerges duringthe monitoring of weaning is abnormal fatness.Understanding the background to this is also

necessary to interpret the seemingly acceleratedweight gain. At 6 months babies are naturallychubby with fat contributing 25% of body weight: itis almost as though nature is having to provide afood reserve, anticipating the special vulnerabilityof later weaning! As with failure to thrive, it is notthe absolute pattern of weight gain that isimportant, but the context in which this takesplace, which includes family size and the nature offoods that are given.

A qualitative measure of the adequacy of theweaning diet is the stool pattern. Western coun-tries are seeing an explosion in problems of

constipation that so often have their origins inpoor weaning practices, where the intake of NSPsare minimal. As mentioned above, it is veryimportant for the weaning diet to contain sufficientvegetables and fruit, along with cereals to sow theseeds for satisfactory bowel motility.

Finally the iron status of the infant is a veryspecific measure of the adequacy of the weaningdiet. Iron deficiency and anaemia is an importantand a particular problem in young children, wherethe special difficulty in establishing a good patternof solids in the diets and without over-reliance on

cows milk renders many infants vulnerable to thiscomplication.

Conclusion

After the secure transition to immediate extra-uterine life and the establishment of milk feeding,weaning is the next major hurdle the young infanthas to clear in its journey through infancy and earlychildhood. Weaning still causes a lot of worry toparents and also to their professional advisors (whoall too often give inconsistent advice that servesonly to confuse) as it has done throughout history.As we have shown in this article, many problemscan emerge as a consequence of poor weaningpractices, some immediate as well as some in thelonger term. Yet in 1994 the Department of Health

produced an extremely well referenced booklet onweaning which, though perhaps lacking a soundevidence-base in certain areas, nonetheless pro-vides for sound and safe practices that do notexpose the young weanling to risk.2 Unfortunately,knowledge of the nations guidelines on weaning onthe part of health professionals is limited, suggest-ing lack of awareness of the guidelines. It isimportant for health professionals to offer consis-tent and accurate guidelines, speaking with onevoice in a language easily understood. The situationis sometimes made more challenging by the multi-

cultural nature and makeup of our society.The problems facing the weanling in the devel-oping world are enormous and of a totally differentcalibre and nature to those in rich countries.Culture, taboos, food choices, practices of foodpreparation, abject poverty often dominated by ill-informed elders and peer-groups often lead to poorquality of food intake with its well known con-sequences. To these are added the problems causedby AIDS in the developing world. We have barelytouched on these issues in this article but hopefullywe have given sufficient pointers to stimulate thereader to read more about them elsewhere.

All parents (to be) should have received educa-tion about nutrition in their infants and this ideallyshould have begun during the school years. Antena-tal classes provide later opportunities. In theseclasses, considerable time is spent on breast-feeding but all too often too little time is spenton the transitional human beingFthe weanling.Paediatricians need to be more involved with thisaspect than they are. The various child healthrecord booklets now widely used should alsoinclude key points to help the mother wean herbaby. It has also to be appreciated that, and

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especially for young parents, reliance on theirhome networks within their own communities alsoprovide critical support. Parents of children whohave special medical needs, and where there arestrong cultural and religious beliefs that mightintroduce risk into the weaning process, need to be

dealt with sympathetically and with understandingif their infants are to thrive at this time. Expertdietetic advice must also be available to helpwhere difficulties might arise.

There is evidence to suggest that many mothersdo find it difficult to comply with national guide-lines on when to introduce solid foods and areintroducing their babies to solids at 3 months orearlier. Maybe this is simply a reflection of theweakness in the evidence-base that underpinsthese guidelines. But there is another possibleexplanation. Formula feeding is a strong predictorof early weaning, along with young maternal age,

cigarette smokings social class and the babysweight during the first couple of months. Is weaningdriven by biological needs in the baby, or is itsocially driven by peer group pressure to conform?When this takes place early, does it reflect lessgood health behaviour, maybe leading to increasedfatness and a higher incidence of chest disorders?History points more to the latter. It is easy is for theyoung infant to form habits to caretaker prac-tices. Very early weaning is not usually drivenby the biological imperative but more by thesocial one.

Weaning times and weaning diets in many waysconstitute uncontrolled experimental interven-

tions. Difficult though outcome studies will be toassess these interventions in terms of physicalgrowth and health, in both short and long terms,only if this research (often necessarily opportunis-tic), is undertaken will we be more able to bestprovide for the needs of the weanling. Out of

course, this necessity pales alongside the disastrousconsequences of inapropriate weaning for so manychildren in the developing world, where majormortalities and significant morbidity, have theirorigins in this most hazardous of times.

References

1. World Health Organisation (WHO). Infant and young childnutrition. 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

2. Department of Health. Weaning and the weaning diet. Reporton health and social subjects, no. 46. HMSO, London, 1994.

Further reading

1. Fewtrell MS, Lucas A, Morgan JB. Factors associated withweaning in full term and pre-term infants. Arch Dis ChildFetal Neonatal Ed2003; 88:F296F301.

2.Fildes V. Breasts, bottles and babies: a history of infantfeeding. Edinburgh: Edinburgh University Press; 1986.

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