Abstract
Primary lactose intolerance may arise only as an extremely rare congenital abnormality in babies, since lactose is crucial to normal health and development of human babies.

Secondary lactose intolerance in babies results from damage to the brush border of the gastrointestinal tract and/or an inadequate fat intake during feeds

“Lactose overload” may more correctly describe this secondary lactose intolerance. The resulting cascade of clinical features is oftencalled “colic” by health professionals as well as the general community.

Identification of causative factors followed by appropriate management provides fast resolution of symptoms without interruptions to breastfeeding.

Unfortunately, while practitioners continue to regard lactose overload in breastfed babies as a primary  condition, mothers are commonly advised to wean their babies onto lactose-free or lactose-hydrolysed formulae. Ongoing use of  lactose-free formulae may pose an unacceptable risk to babies’ long term mental and cognitive development.

Accumulating research  evidence shows a clear correlation between early weaning onto artificial baby milks and short-and long-term morbidity.

Introduction
Significant research describing the mechanisms of lactose overload in breastfed babies was published nearly ten years ago but has  not become widely known amongst practitioners who work with breastfed babies and their mothers (1). Woolridge and Fisher  described a type of lactose overload which is due entirely to low fat feeds. This may arise if babies are not permitted to nurse long  enough during feeds, such as when feeds are clock-regulated, or if mothers need to shorten feeds because they are painful. Babies  may also be inefficient feeders who are unable to milk the breast well enough to extract the fattier milk that comprises the end of  feeds (hind milk). Low fat feeds cause fast gastric clearance, thence overloading the small intestine’s capacity to metabolise lactose 1,6).

Clinicians have long known that infective agents, infant prematurity and some gastrointestinal conditions cause varying degrees  of lactase insufficiency in babies,but have been less aware that allergens derived from the maternal diet or supplementary formula feeds  may also compromise a breastfed baby’s lactase sufficiency (2,3,4,5). This occurs when the allergic response targets and damages the brush border of the baby’s gastrointestinal tract (7).

Recognition of the likely causes of lactose overload in breastfed babies provides  the means by which resolution of symptoms and maintenance of breastfeeding are both achieved.
Lactose is a disaccharide molecule composed of single glucose and galactose units joined by a chemical bond. In its disaccharide form, lactose cannot be digested by humans.
Lactose digestion begins in the small intestine where the brush border secretes the enzyme, lactase, necessary for splitting  the chemical bond between the two simple sugar units. Because lactase is secreted only at a relatively slow rate (regardless of the levels of lactose that may be present ), fast gastric clearance does not allow for the equivalently slow hydrolisation of lactose that is programmed by human physiology.(3)

All human babies are necessarily lactose tolerant with extremely rare congenital exception. Varying degrees of acquired lactose intolerance as a result of genetically determined lactase insufficiency occur from the age of 5 years in about 70% of the world’s  population (5).
Therefore lactose intolerance in breastfed babies arises only secondarily under any conditions which:
(1) cause overly fast gastric clearance or
(2) damage the brush border of the small intestine. (5,6)

Clinical features of lactose intolerance
When the levels of lactose in the lumen of the small intestine exceed the capacity of the available lactase:

• the gastrointestinal (GIT) microbial flora ferment excess lactose, particularly in the colon, producing gases (carbon dioxide, hydrogen and methane) and acid· lactose fermentation products in the colon increase the osmolarity of the lumen’s contents, therefore increasing the volume of water that must be retained in the lumen.
• any unsplit lactose still remaining in the colon also mandates retention of water by the colon
• GIT transit time is shortened
• depending on severity, mucus may be evident in stools due to irritation of the GI mucosa (6). Hence the presenting symptoms of lactose overload in breastfed babies are:
• excessive flatus (a “windy” baby)
• frequent explosive watery stools which may be yellow or green, depending on severity
• “colic” (defined in this case as crying due to overproduction of intestinal gases)
• unsettled baby
• perianal acid burns may occur
• stools may be mucousy (8)

Clinical features of lactose overload
The normal clinical picture is that intestinal gases are inevitably generated as part of the gastrointestinal passage of food, but not in such volumes as to cause significant distress to the baby. (5,9)

Until 6 weeks of age, fully breastfed babies may also be expected to pass frequent yellow bowel motions throughout every 24 hour period, but many of these stools areof only small amounts (up to a few teaspoonfuls). Our recommendation is that at least one bowel motion in every 24 hours is of fairly substantial volume, about half to a cupful. (A “good handful” is a fairly graphic description that parents quickly relate to!) The stools are unformed and often have a noticeable watery component. Although yellow is the normal colour of these stools, an infrequent greenish yellow stool is acceptable (perhaps 1 - 2 over a week). After the first week, urine should be colourless, but a pale yellow is acceptable.

Beyond 6 weeks of age, the anal reflex that previously stimulated peristaltic activity at every feed, diminishes greatly. Thereafter, stools remain yellow (until other foods are introduced) but stool consistency becomes more like that of whipped cream. A noticeable watery component is unusual in these stools. The frequency of bowel motions subsides, commonly to one every day or so. Some fully breastfed babies stool once every 3 - 10 days or so, the colour thereof being more generally a light brown due to longer oxidation with slower GIT passage. Stool volumes are copious, around a cupful, even more with infrequent stooling. The urine is usually colourless.
When the baby’s output conforms with these criteria, good weight gains are guaranteed, and the baby will usually be well settled between feeds, crying very little as long as his needs are promptly met. (If urine colour seems too yellow to match a perfectly adequate urinary and faecal output, it may be related to strong yellow colours in the mother’s diet such as from vitamin B supplements.)

“What goes in has to come out”
An explanation that “what goes into the baby has to come out (the other end)” is one of the most helpful that practitioners can give to parents. World-wide, research has repeatedly found that one of the main reasons given by mothers for early weaning from the breast is perceived low supply (10). In fact, within the first 3 months postpartum, lactating women are commonly oversupplied due to endocrine mechanisms that embellish the more usual autocrine control (supply equals demand) that operates beyond these early months (11). Given that so much parental anxiety is unnecessarily expended over “knowing if the baby is getting enough (milk)” and whether or not the mother has enough milk, practitioners can be a powerful force in relieving these parental concerns and simultaneously improving long-term breastfeeding rates. If parents have a clear picture of what the baby’s normal output should be, they are capable of using their baby’s output as an assessment tool. When the baby’s output matches the previously described criteria, parents have their own day-to-day reassurance that the baby is most certainly “getting enough” and that this automatically means that the mother’s milk supply is quite adequate. On the other hand, when the baby’s output is not sufficient or is abnormal, parents have an “early warning sign” to seek professional help well before problems become dire.

Using the output as an assessment tool
When to ignore a green stool:
Parents need to be reassured that a single green stool in a fully breastfed baby is not usually significant. When accompanied by pain, it may reflect something unusual or excessive in the maternal intake, including medications. It is also desirable that parents understand that the darker the hues of green of freshly passed stools, the faster the passage of food through the baby’s GIT. As the underlying problem is dealt with, green stools steadily become yellow. Occasionally a bowel motion may have been passed some time before the nappy is changed. The longer the time since the motion was fresh, the greener it is likely to be from oxidation processes. Therefore these green stools are not a reliable indicator of the colour of fresh stools. Testing the stool for reducing sugars is not done at our clinic because the clinical presentation of lactose overload is seen as a clear enough indication of the presence of reducing sugars. In any case, a certain level of reducing sugars will normally be present in the stools of fully breastfed symptom-free babies, particularly those who are less than 6 weeks of age. (5)

Assessment of at least one breastfeed is an important means of establishing the effectiveness of the baby’s suck. Simple positioning and attachment issues are often identified and mothers are helped to overcome these. This may be all that is required to resolve lactose overload, since these issues can in themselves be the cause of significant reduction in the baby’s fat intake.

(“Attachment” refers to the amount of breast tissue taken into the baby’s mouth during breastfeeds. “Positioning” refers to the way that the baby’s body is positioned for a breastfeed.)
Since the baby’s fat intake steadily increases towards the end of feeds, it can be seen that any problem that reduces the baby’s ability to reach the end of the feed will reduce his fat intake (1). The lower the fat levels of the feed, the faster will be the gastric clearance time. This results in various degrees of lactose overload.
The most common problems that may reduce the baby’s fat intake are:

• shortened breastfeeds due to maternal breast/nipple pain/damage,
• poor attachment resulting in long feeds and minimal milk intakes
• poor positioning resulting in baby having difficulty maintaining adequate breast tissue in his mouth throughout the feed
• timed feed schedules eg “10 minutes each side, 4 hourly”
• infant oral thrush
• suck problems including suck confusion due to the baby’s oral experiences with such objects as nipple shields, teats and pacifiers
• infant infections

An inadequate fat intake in the maternal diet appears to make a direct contribution to the intensity of lactose overload symptoms, resulting in lower fat and higher lactose levels in their breast milk. (12,13,14)
á protein + á fat + á complex carbohydrate + â simple sugars (maternal diet)
â [lactose] + á fat (breast milk)

Another aspect of maternal diet is that particular foods, commonly cow milk products, may cause allergic responses in the baby (15,16,17). When this allergic response targets the mucosa of the baby’s gastrointestinal tract, the ensuing damage to the brush border may in itself be the cause of lactose overload, lactase production being directly compromised (18). In some of our cases, the maternal intake of the offending food has been minimal, but the baby’s sensitivity has been extreme. We have also noted that this form of lactose overload often begins to manifest some weeks after birth, steadily becoming worse as long as the allergen remains in the mother’s diet. It is not unusual for these babies to have blood in their stools. (These stools may be bright orange, may have obvious red or pink components or be black and tarry.) Once the allergen is removed from the maternal diet, symptoms begin to subside within days, but complete healing of GIT damage may require up to 6 weeks, with symptoms persisting at a lower level of intensity for many of these weeks. Others have reported
similar cases (19,20,21,22).

Successful management of lactose overload depends on identification and correction of the underlying cause. The involvement of lactation consultants may be crucial to this process.

• If the baby’s fat intake is the core of the problem, Woolridge and Fisher’s research is summarised as:                                       “Finish the first side first.” (1)

In order to “finish the first side first”, some babies may need to be put back to the first breast again (1 - 3 times) before being offered the second breast. In occasional cases, symptoms may subside only when one breast is used per feed. (This means that the baby is put back to the same breast until he is sated. If he wants a “top-up” within an hour following his feed, he is returned to the same breast.)

When a baby is not feeding effectively, feeds may become never-ending marathons, with the baby never/rarely taking himself off the breast. These “all day suckers” never reach the end of the feed - they do not detach themselves from the breast because they know they have not finished. These babies may simply need to be more optimally positioned and attached for breastfeeds - others need interventions such as supplementing after shorter times at the breast, preferably with the mother’s own milk so that her supply is easily maintained.

We have shown that bottles and teats can be used to supplement these babies and to steadily improve their competence at the breast only if the teats are long round teats. In Australia, the only ones available in a flow rate suitable for very young babies are Cannon newborn teats (round, not “orthodontic”) - our preference is for latex rather than silicone teats because of infant oral sensory feedback considerations.
Our experience is that when babies become accustomed to feeding with the end of the teat stimulating the junction of the hard and soft palates, over 90% of babies can be expected to resolve their breastfeeding difficulties within 1 - 6 weeks (23).

When the maternal diet contributes to lactose overload, mothers need to be guided with specific examples of the changes that may be necessary, and why.
For example, when the maternal diet has too little fat and too many simple sugars:
 

When cow milk products in the maternal diet need to be excluded:
 

Note: Soy protein is as potentially allergenic as cow milk protein, so only small amounts (less than a cup per day) should be substituted (24,25,26). Goat milk appears to be considerably less likely to incite allergic responses, but is not generally acceptable to most adults because of its strong taste.

In our experience, it is extremely unusual for food allergy to necessitate removal of more than one type of food from the maternal diet. (We refer these mothers to a dietician with particular expertise in managing these special situations.) It is desirable that mothers have as little dietary restriction as possible, not merely because of the inconvenience involved, but mainly because unnecessary food restrictions carry a risk of generating further food allergies(27). This may happen if basic commonsense dietary rules are not obeyed:

1. Have lots of variety in your diet
2. Eat everything in moderation

Why should weaning from the breast be avoided?
Practitioners frequently advise weaning for breastfed babies with symptoms of lactose intolerance because human milk has much higher lactose levels than other milks. This approach focuses erroneously on lactose as the cause of problems while discounting the importance of lactose in particular and human milk in general for human babies.

Lactose is a specific nutrient for infancy, supplying about 40% of the baby’s energy needs, facilitating calcium and iron absorption, promoting a normal healthy GIT microflora which discourages and retards the growth of GIT pathogens, and perhaps most importantly of all, providing the galactose which is incorporated directly as galactolipids into the tissues of the central nervous system (28).

Considering the nutritional importance of lactose for human babies and the considerable time span during which lactose-free (soy) infant formulae have been marketed, it is remarkable that there appears to be no research exploring whatever short- and long-term consequences may predictably result from exclusion of lactose from babies’ nutritional intakes(28).
In 1997, one manufacturer of a soy infant formula produced an advertisement for health care providers stating that their product “helps resolve both lactose intolerance and cow’s milk allergy in one step” and that it is “suitable from birth to six months of age”. The advertisement does not provide any other information and includes a photograph of a happy thriving baby. This kind of advertising, while superficially matching WHO guidelines for the marketing of infant formulae, nonetheless does not satisfy the spirit of the guidelines - the reader is not informed of other possible morbidities that may arise from the product’s use, nor of the unproven safety status of lactose-free formulae for human babies.
 

It has not helped practitioners that formula manufacturers have avoided mention of these and many other critical issues related to artificial feeding, promoting instead a distorted, idealised view of their products in the minds of many health care providers(29,30,34). In fact, the use of any kind of infant formula should be recognised as having a status similar to most drugs - an automatic cause of side
effects in the short-, medium- and long-term (35). In the western country with the poorest of all breastfeeding rates (breastfeeding initiation rates no higher than 26%), the American Academy of Pediatrics has now firmly acknowledged the importance of human milk for human babies with new breastfeeding guidelines that recommend babies be breastfed for at least the first year of life (36).

Artificially fed children have been shown to have a greater risk of:(30,39,40)
 

With increasing concern over health spending, the economic value of breastfed babies to our world community needs to be emphasised. In Australia alone, it is easy to show that if our national target for the year 2000 were achieved - 80% of babies still breastfed at 6 months of age (instead of the current 22%), billions of dollars would be saved from our health care bills(37,38). Unfortunately, in place of this understanding of the cost of artificial feeding of infants, Australian perceptions are that illnesses such as middle ear infections are a “normal”, inevitable part of childhood.

In conclusion:
Lactose intolerance in breastfed babies is not so much a problem with lactose itself as a problem with conditions impacting on lactose metabolism in the GIT. Unfortunately, terminology that focuses on lactose naturally tends to distract practitioners from the core issues which are actually responsible for the presenting symptoms. It has not helped clinicians that multinational baby food manufacturers have not closely adhered to WHO guidelines on the marketing of their products, even with their agreement to do so in Australia in 1992. This has resulted in a certain amount of advertising being offered to health care providers in the guise of professional information which is superficially true but which also fosters incorrect impressions and beliefs in the health professional community. This situation has contributed to professional advice to wean breastfed babies with lactose intolerance symptoms. In reality there is no need for babies to be weaned off the breast because of lactose overload in the GIT. Maintenance of breastfeeding primarily benefits mothers and their babies, but has far wider health and economic repercussions for all of us.
 

References

 1. Woolridge MW, Fisher C 1988 Colic, “overfeeding” and symptoms of lactose malabsorption in the breast-fed baby: a possible artifact  of feed management. Lancet 2:382

 2. Akre J(ed) 1990 Infant Feeding: the physiological basis supplement to vol67 of the WHO Bulletin WHO, Geneva. 28

 3. NHMRC 1996 Infant feeding guidelines for health workers Australian Government Publishing Service, Canberra, Australia.31-33

4. Lawrence RA 1994 Breastfeeding: A guide for the medical profession Mosby  St Louis, USA. 271

 5. Brodribb W(ed) 1997 Breastfeeding Management in Australia  Nursing Mothers’ Association of Australia, Melbourne, Australia
     303-306

 6. Paige DM, Bayless TM  1981 Lactose Digestion: clinical and nutritional implications Johns Hopkins University Press, Baltimore,
     USA 51-57

 7. Burgess J, Newbold D 1993  Food Intolerance in Breastfed Babies. Nursing Mothers’ Association of Australia, Topics in
     Breastfeeding paper, Lactation Resource Centre, Melbourne, Australia

 8. Gryboski J, Walker WA 1983 Gastrointestinal Problems in the Infant WB Saunders Company, Philadelphia, USA 593-596

 9. Wyngaarden JB, Smith LH(ed) 1985 Cecil Textbook of Medicine WB Saunders Company, Philadelphia, USA 649

 10. NHMRC 1996 Infant feeding guidelines for health workers Australian Government Publishing Service, Canberra, Australia.23

 11. Lawrence RA 1994 Breastfeeding: A guide for the medical profession Mosby  St Louis, USA  66-76

 12. Abakada AO, Hartmann PE 1988 Maternal Dietary Intake and Human Milk Composition Breastfeeding Review (NMAA) 1:13 
       43-45

 13. Hatherly PA 1994 The Manipulation of Maternal Diet and Its Effect on the Infant with Particular Reference to Gastrointestinal
       Disturbance....A Series of Case Studies JAust CollegeNutrEnvironMed 13:2  1-4

 14. Riordan J, Auerbach KG 1993 Breastfeeding and Human Lactation Jones and Bartlett Publishers, Boston, USA 112

 15. Brodribb W(ed) 1997 Breastfeeding Management in Australia  Nursing Mothers’ Association of Australia, Melbourne, Australia
       319-323

 16. Akre J(ed) 1990 Infant Feeding: the physiological basis supplement to vol67 of the WHO Bulletin WHO, Geneva. 26

 17. Cunningham AS 1990 Breastfeeding, bottlefeeding & illness: an annotated bibliography LRC (Lactation Resource Centre) Series No
       2, NMAA (Nursing Mothers’ Association of Australia), Melbourne, Australia 19-22

 18. Minchin M 1992 Food for Thought Alma Publications, Melbourne, Australia 15-17

 19. Lawrence RA 1994 Breastfeeding: A guide for the medical profession Mosby  St Louis, USA  434-435

 20. Lake AM, Whitington PF, Hamilton SR 1982  Dietary protein-induced colitis in breast-fed infants JPediatr 101:906

 21. Schmerling DH 1983 Dietary protein-induced colitis in breast-fed infants JPediatr 103:500

 22. Israel D, Levine J, Pettel M et al 1989 Protein induced allergic colitis (PAC) in infants PediatrRes 25:116A

 23. Noble R, Bovey A 1997  Therapeutic teat use for babies who breastfeed poorly Breastfeeding Review (NMAA) 5:2 37-42

 24. Hamburger R 1990  Food Intolerance. Issues in Infant Nutrition.Carnation Nutritional Products, Glendale,CA

 25. Kerner J 1995  Formula allergy and intolerance GastroClinNthAm 24(1):1-253

 26. Gryboski J, Walker WA 1983 Gastrointestinal Problems in the Infant WB Saunders Company, Philadelphia, USA 89

 27. Minchin M 1992 Food for Thought Alma Publications, Melbourne, Australia 66

 28. Akre J(ed) 1990 Infant Feeding: the physiological basis supplement to vol67 of the WHO Bulletin WHO, Geneva. 27-28

 29. Minchin M 1987  Infant formula: a mass, uncontrolled trial in perinatal care Birth 14:1 25-34

 30. Cunningham AS 1990 Breastfeeding, bottlefeeding & illness: an annotated bibliography LRC (Lactation Resource Centre) Series No
       2, NMAA (Nursing Mothers’ Association of Australia), Melbourne, Australia 1-38

 31. Weintraub R, Hams G, Meerkin M, Rosenberg AR 1986  High aluminium content of infant milk formulas ArchDisChild
       61:914-916

 32. Bishop N, McGraw M, Ward N 1989  Aluminium in infant formulas Lancet 1:490

 33. Clayton V 1995  Soy milk formula may harm infants ALCA News 6:2 29 (from a letter to NZMedJ, 24-5-1995, by Prof. Cliff
       Irvine)

 34. Auerbach KG 1992  One result of marketing: breastfeeding is the exception in infant feeding JTropPediatr 38:210-213

 35. Newman J 1997  When breastfeeding is not contraindicated Breastfeeding Abstracts 16:4 27-28

 36. American Academy of Pediatrics 1997  Breastfeeding and the use of human milk Pediatr 100:1035-1039

 37. Riordan JM 1997  The cost of not breastfeeding: a commentary JHumLact 13:2 93-97

 38. Drane D 1997  Breastfeeding and formula feeding: a preliminary economic analysis Breastfeeding Review (NMAA) 5:1 7-15

 39. Walker M 1992  ILCA (International Lactation Consultant Association) Summary of the hazards of  infant formula

 40. Minchin M 1993 Breastfeeding: Advantages for Developed Nations (Booklet)Alma Publications, Melbourne, Australia
 
 

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