This document summarizes the unique nutritional composition and immunological properties of human breastmilk that make it ideally suited to meet the developmental needs of newborn infants, both term and preterm. It discusses the stages of lactation and changing composition of colostrum, transition milk, and mature milk. Key components described include proteins, fatty acids like DHA critical for brain development, vitamins, minerals and their high bioavailability due to breastmilk's composition. The document also outlines the cellular and soluble immune factors in breastmilk, including antibodies, white blood cells and other defenses that protect infant health.

1. REV. HOSP. CLÍN. FAC. MED. S. PAULO 58(1):49-60, 2003
BREASTFEEDING: MAKING THE DIFFERENCE IN
THE DEVELOPMENT, HEALTH AND NUTRITION OF
TERM AND PRETERM NEWBORNS
Maria Beatriz Reinert do Nascimento and Hugo Issler
NASCIMENTO MBR do et al. - Breastfeeding: making the difference in the development, health and nutrition of term and
preterm newborns. Rev. Hosp. Clín. Fac. Med. S. Paulo 58(1):49-60, 2003.
Breastfeeding is the natural and safe way of feeding small infants, providing nutritional, immunological, psychological
and economic recognized and unquestionable advantages. These qualities are especially important in premature infants,
because of their vulnerability. Despite highly desirable, there is, in general, little success in breastfeeding preterm infants,
especially in special care neonatal units. There are evidences that a high supportive hospital environment, with an
interdisciplinary team, makes possible to these infants to be breastfed. In this article, the authors present an up-to-date
review about the components of human milk and its unique characteristics, as well as describes aspects that make the breast
milk particularly suitable for feeding the premature newborn.
DESCRIPTORS: Infant feeding. Breastfeeding. Human milk. Newborn. Premature infant.
INTRODUCTION tional and immunological needs of the The transitional phase lasts from
child1,3,8. the seventh to the tenth day, up to two
Maternal breastfeeding is the most Lactation progresses through three weeks post partum, during which the
natural and safe way to feed a small well-identified periods, i.e., the stages composition of colostrum changes,
child. Breastfeeding provides a unique of colostrum, transition milk and ma- with a decrease in the concentration of
combination of proteins, lipids, carbo- ture milk4. Colostrum is a yellowish immunoglobulins and proteins and an
hydrates, minerals, vitamins, enzymes fluid of high density and small volume increase in lactose and fat levels and
and living cells, as well as known and that fills the alveolar cells during the in energy content, until reaching the
unquestionable nutritional, immuno- last trimester of gestation1. Its high con- characteristics of mature milk10.
logical, psychological and economic tent of proteins and minerals, in addi- Mature human milk is a homog-
benefits1-6. tion to low concentrations of fat and enous mixture consisting of three frac-
The nutritional composition of lactose, reflects the needs of the new- tions: emulsion (fat droplets), suspen-
breast milk, which possesses the exact born during the first week of life8. Co- sion (casein micelles) and solution (wa-
proportion of nutrients for good devel- lostrum provides 67 kcal/dl, is rich in ter soluble components)4,11. Different
opment of the human brain, differs immunoglobulins, lactoferrin and energy contents have been described to
from the milk of other mammals, such leukocytes, and facilitates the growth mature milk in the literature, ranging
as rabbit milk which contains large of Lactobacillus bifidus in the from 65.7 kcal/dl12, 71 kcal/dl13 to 75
amounts of protein for rapid growth of gastrointestinal tract and the elimina- kcal/dl10. Variations in the nutritional
the species, or from whale milk which tion of meconium9,10. components of human milk exist, which
is rich in fat in order to guarantee sur- depend on the stage of lactation, the
vival in cold water7. Human milk is a From the Department of Pediatrics, Hospital time of day, period of feeding, mater-
das Clínicas, Faculty of Medicine, University
complex species-specific biological of São Paulo. nal nutrition and age, and gestational
fluid, adapted throughout human ex- Received for publication on age of the infant, as well as individual
April 23, 2002.
istence to perfectly satisfy the nutri- aspects of each lactating mother5,8,10.
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2. Breastfeeding: making the difference REV. HOSP. CLÍN. FAC. MED. S. PAULO 58(1):49-60, 2003
Nascimento MBR et al.
NUTRITIONAL COMPOSITION human milk is perfectly adequate, with concentration being higher in
OF HUMAN MILK a reduced amount of phenylalanine breastfeeding infants than in those fed
and tyrosine. The newborn shows a re- artificial milk5. There is evidence show-
With respect to the biochemical duced capacity of metabolizing these ing the beneficial effect of a higher
composition of human milk, maternal aromatic elements which, at high cholesterol concentration during this
milk contains 88% of water and its os- plasma levels, can cause lethargy13. phase of life based on its better
molarity is similar to that of plasma2. Taurine, important for the develop- bioavailability to the developing brain
Therefore, exclusive breastfeeding on ment of the retina and for the stability and for maintaining low and appropri-
demand, without water supplementa- of cell membranes, is found in human ate blood levels of cholesterol during
tion, keeps the nursing infant perfectly but not in cow’s milk14. The ratio of adult life1,10,14.
hydrated1,11. the sulfur-containing amino acids me- Digestion of triglycerides in the
The total protein content of human thionine/cystine in human milk is neonate is facilitated by a combination
milk is the lowest among all mammals close to one, a ratio seven times lower of enzymes, such as lingual lipase
due to the relatively slow growth of than that found in cow’s milk10. The which initiates hydrolysis in the diges-
the child14. The real amount is about enzyme cystathionase, which is re- tive tract, gastric lipase, pancreatic li-
0.8 to 0.9 g/dl, including a high frac- sponsible for the transformation of me- pase and, especially, bile-stimulated
tion of non-protein nitrogen corre- thionine to cystine, is absent in the lipase provided by the human milk fat
sponding to 20 to 25%1,3. However, brain and liver of premature newborns, droplets themselves and activated by
many of the properties beneficial to and thus cystine becomes essential for bile salts in the duodenum3,11.
the nursing infant can be attributed to these children1. Human milk also con- Human milk represents the best
the protein compartment, such as tains carnitine, a protein of high source of essential fatty acids. A great
defense factors, digestive enzymes, bioavailability, which is vital during difference between human and artifi-
hormones and growth factors4. immediate post-natal life for the deg- cial milk concerns the concentration
Milk proteins include casein and radation of long-chain fatty acids, of long-chain polyunsaturated fatty
lactalbumins, or serum proteins10, and since newborns show a reduced capac- acids, which are essential for the nor-
are not completely available for nutri- ity to synthesize carnitine 8,14,15. The mal development of nursing infants,
tional use by the nursing infant, since decrease in protein content during the with emphasis on docosahexaenoic
those with a defense function against course of lactation leads to the fact acid which is important for the devel-
infections appear intact in the feces and that human milk, without the use of opment of the brain and retina, and
are not absorbed4. Casein forms stable additional components, is not com- arachidonic acid as a precursor of
conglomerates with calcium and phos- pletely adequate for the feeding of pre- prostaglandins and leukotrienes17. The
phorus, thus favoring the transport of mature newborns16. reserves of these fat elements are lim-
these minerals11,13. The main serum Fat is the most variable component ited at birth, especially in premature
proteins include a-lactalbumin, impor- of maternal milk, corresponding to 3- newborns, and rapidly decrease when
tant for the synthesis of lactose, and 4 g/dl13, and represents the main en- lacking in the diet18. Several clinical
protective factors such as lactoferrin, ergy source for the newborn, provid- studies have demonstrated that enrich-
lysozyme and immunoglobulins. ß- ing 35 to 50% of its daily needs1. Al- ment of industrialized infant milk with
Lactoglobulin, which is highly aller- most all lipids in human milk are long-chain polyunsaturated fatty acids,
genic, is predominantly found in present in the form of droplets, which simulating the composition of human
cow’s milk, and is only detected in permit stabilization of the emulsion milk, improves visual and cognitive
small amounts in human milk where it and increases the bioavailability of li- functions in term and preterm
probably originates from cow’s milk posoluble components1. Lipid compo- newborns19. However, further studies
ingested by the breastfeeding nents include triglycerides, phospho- are needed to determine the long-term
mother4,14. The serum protein/casein lipids and cholesterol, as well as free beneficial effects of this supplementa-
ratio in human milk reported in differ- fatty acids, and are derived from cir- tion and its side effects17,19.
ent studies ranges from 80/20 to 60/ culating fat originating from the diet The main carbohydrate of human
40, a fact that results in the formation and from maternal body reserves, or are milk is lactose, whose concentration is
of a smoother gastric curd, reducing synthesized from glucose in the breast about 7 g/dl and which is metabolized
the time of gastric emptying and facili- itself 5. into galactose, the primary source of
tating digestion1,8,10. Human milk shows a high concen- the white matter of the growing
The amino acid composition of tration of cholesterol, with its plasma brain1,8. Lactose facilitates the absorp-
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3. REV. HOSP. CLÍN. FAC. MED. S. PAULO 58(1):49-60, 2003 Breastfeeding: making the difference
Nascimento MBR et al.
tion of calcium3,14 and supports the tion from human milk is five times The predominant immunocompetent
presence of a fecal flora protective higher than absorption from cow’s cells in human milk are macrophages
against bacteria and of feces of ad- milk and is facilitated by the presence (40-50%) and polymorphonuclear
equate consistency 20. Other sugars, of lactose and vitamin C, as well as by neutrophils (40-50%), which have
such as glycolipids, glycoproteins and low levels of protein and phosphorus phagocytic capacity and exert bacte-
oligosaccharides, exist which play an in maternal milk3,8. ricidal and fungicidal actions25. In ad-
important role in the defense against All water soluble vitamins are dition, macrophages synthesize the C3
infections3,4. found in breast milk, and the concen- and C4 complement components, lys-
The concentration of minerals in tration of vitamin C is eight to ten ozyme and lactoferrin, and are a vehi-
maternal milk is about one-third lower times higher than in the mother’s cle for the transport and storage of
than in cow’s milk13. This fact, together plasma. Vitamin B 12 levels are fre- immunoglobulins10. Lymphocytes rep-
with the reduced protein content, leads quently low in the milk of mothers resent 5 to 10% of white cells of milk,
to a lower solute load which is ad- consuming vegetarian diets, a fact that and are mainly formed by T
equate for the newborn’s immature kid- might lead to deficiency of this com- lymphocytes which exert a cytotoxic
ney8. The total mineral content of hu- pound in the nursing infant5. Of the li- action on microorganisms and stimu-
man milk is generally constant and in- posoluble vitamins, vitamin A and E late the immunological system of the
cludes minerals such as sodium, potas- contents are adequate in human milk. nursing infant, while B lymphocytes
sium, chloride, calcium, magnesium However, vitamin K supplementation are responsible for the production of
and phosphorus, and the trace ele- is required for all newborns since its specific antibodies against numerous
ments iron, fluor, zinc, copper, manga- endogenous production by enteric bac- pathogens8.
nese, selenium, and iodide5. teria only starts some days after birth. When a pathogen in the respiratory
Several studies have demonstrated The low vitamin D concentration in or digestive tract of the maternal or-
a high bioavailability of minerals and human milk requires the use of exog- ganism is captured by a macrophage,
their relationship with other nutrients enous vitamin supplements in the case the antigenic information is passed on
present in human milk, which facili- of nursing infants who are not regularly to T lymphocytes and then to B
tates their absorption, metabolism and exposed to the sun3,18. lymphocytes, which, upon transforma-
excretion3. Although present in small tion into plasma cells, release specific
amounts in human milk, calcium is antibodies directly into the breast. The
well absorbed and its concentration is IMMUNOLOGICAL enterobronchomammary system as-
sufficient in term newborns, with a cal- COMPOSITION OF HUMAN sures that any pathogen threatening
cium/phosphorus ratio of 2:18. How- MILK the mother stimulates the production
ever, the calcium and phosphorus con- of specific antibodies which are found
centrations are too low to satisfy the One of the most valuable aspects in maternal milk1.
requirements of bone mineralization in of human milk is the presence of The specific soluble factors are
preterm infants20. defense elements which, together with represented by immunoglobulins (Ig).
The sodium content of human milk the perfect composition and purity of The main immunoglobulin is secre-
declines during the course of lactation. this milk14, guarantee a protective ef- tory IgA, which corresponds to 10% of
This reduced concentration, together fect in terms of child morbidity and milk protein and prevents the adhe-
with the high potassium content, mortality6,21-24. sion of microorganisms to the intesti-
seems to be beneficial to the nursing The protective components of hu- nal surface, in addition to acting
infant; however, it does not satisfy the man milk conferring active and pas- against diverse infectious agents such
needs of premature newborns who re- sive protection on the newborn and as rotavirus, respiratory syncytial vi-
quire large amounts of this mineral16. nursing infant can be divided into spe- rus, Escherichia coli, Vibrio cholerae,
The high bioavailability of zinc in hu- cific and nonspecific cellular and hu- Shigella, Salmonella, Clostridium
man milk compensates for its low con- moral factors10. Cellular defense ele- difficile, Giardia lamblia and
centration, with zinc deficiency being ments include live leukocytes, which Campylobacter. Secretory IgA in-
rare, thus preventing enteropathic ac- are present in high numbers at the be- cludes dimeric IgA bound to poly-
rodermatitis in breastfeeding infants1,8. ginning of lactation9 and are known to meric immunoglobulin receptors (J
Iron deficiency is a rare disorder in exert activity in the gastrointestinal chain) and conjugated to a glycopro-
breastfeeding infants since, even in the tract of the nursing infant, inducing a tein produced in epithelial cells, which
case of a low iron content, its absorp- local and systemic immune response. represents the secretory component25.
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4. Breastfeeding: making the difference REV. HOSP. CLÍN. FAC. MED. S. PAULO 58(1):49-60, 2003
Nascimento MBR et al.
The milk of mothers of low detergent action of free fatty acids and proteases, interleukins, prostaglandins,
birthweight newborns contains larger monoglycerides released by the hy- acetylhydrolase of platelet activating
amounts of IgA than the milk of moth- drolysis of triglycerides mediates the factor, secretory IgA, and antioxidants
ers of term infants, conferring greater lysis of bacteria, viruses and such as vitamins and peroxidases. Hor-
protection during a period when the protozoans27. mones and growth factors also play an
child is more susceptible to infec- Oligosaccharides promote the de- important role by promoting gastro-
tion26. velopment of the bifid flora which, intestinal maturation and by contribut-
With respect to the other antibod- through a decrease in pH, impairs the ing to the development of the neonate’s
ies of the different immunoglobulin multiplication of enterobacteria such own defenses31.
classes, IgD participates in the immune as Shigella, Salmonella and E. coli,
response in the mammary gland. IgE, and inhibits the adhesion of bacteria
together with antigens in the intesti- such as Pneumococcus to mucosal sur- THE MAIN ADVANTAGES OF
nal lumen, releases chemical mediators faces, thus playing an important role BREASTFEEDING
that increase vascular permeability, fa- in the prevention of infectious diseases
cilitating the liberation of IgG to per- in newborns4. Based on the anti-infectious, anti-
form its opsonizing activity on bacte- Evidence indicates the existence of inflammatory and immunomodulatory
ria and viruses. IgG also mediates the numerous other protective factors in properties of human milk described
activation of the complement system, addition to those described earlier, for earlier, breastfeeding offers protection
while IgM is important for the initial example, gangliosides, resistance fac- against diverse pathologies8,32, with a
protection of neonates exposed to ma- tor, interferon, fibronectin, glycosami- consequent reduction in the incidence
ternal infections25. noglycans, and stimulated bile li- of hospital admissions21.
Many nonspecific protective factors pase10,27,28. In addition to its anti-infec- Maternal milk confers protection
are found in human milk. Lactoferrin is tious function, new studies have dem- against gastrointestinal and respiratory
a protein that acts as a bacteriostatic onstrated that human milk can modu- infections23,24. Children who have not
agent by depriving microorganisms of late the immune response in the nurs- been breastfed show a 17-fold higher
iron, in addition to exerting bacteri- ing infant through immunomodulatory probability of being hospitalized due
cidal, antiviral, anti-inflammatory and and anti-inflammatory substances that to pneumonia than those who exclu-
immunomodulatory activities25,27. Lys- alter the host’s reaction to injury30. sively received human milk. This pos-
ozyme is a protein component found in The immunomodulatory factors sibility is even higher in nursing in-
large amounts in human milk, which present in maternal milk include prol- fants aged less than three months33.
mediates bacterial lysis and can exert actin, lactoferrin, nucleotides and In developing countries, the main
an immunomodulatory effect by releas- cytokines which, in addition to their causes of death in the pediatric age
ing elements from the bacterial cell other biological and antimicrobial func- range are protein-calorie malnutrition
wall25,27. tions, are able to actively regulate the and infectious diseases, especially
The components of the complement synthesis and maturation of the immune gastroenterocolitis. Malnutrition is
system are found in colostrum and ma- system of the neonate. This activity particularly observed in places where
ture milk, but in smaller amounts than stimulates lymphocyte proliferation and the weaning diet has a low nutritional
those observed in maternal serum or in the production of immunoglobulins, value. In these countries, the effect of
the nursing infant, and protect against and increases cell activity. A direct anti- natural feeding on infant mortality is
respiratory and enteric infections. Vita- inflammatory action of maternal milk significant34-36. The risk of death due
min B12-binding protein prevents the has not yet been demonstrated in vivo, to diarrhea and acute respiratory infec-
incorporation of this vitamin by E. coli but epidemiological studies have sug- tions increases 14.2- and 3.6-fold in
and bacterioids, thus inhibiting their gested that the breastfeeding infant is weaned infants, respectively 22 .
growth10. protected against infection, without the Breastfed infants show a greater pro-
Some fat elements of human milk observation of evident lesion of the in- tection against death due to infection
also show antimicrobial functions. testinal or respiratory mucosa due to an and, at a lower age, a higher mortality
Among the components of the cell inflammatory response. This is the re- risk when not breastfed. The probabil-
membrane of fat droplets, glyco- sult of a well-established anti-inflam- ity of death due to infectious diseases
proteins such as mucins prevent the matory system in human milk and has during the first two months of life is
binding of bacteria and viruses to the been discovered only recently. The anti- six times higher in non-breastfed in-
intestinal mucosa27,28. In addition, the inflammatory factors include anti- fants6.
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5. REV. HOSP. CLÍN. FAC. MED. S. PAULO 58(1):49-60, 2003 Breastfeeding: making the difference
Nascimento MBR et al.
Breastfeeding has been also asso- A recent meta-analysis has sug- with a greater benefit being observed
ciated with a reduction in the inci- gested that breastfeeding is associated for low birthweight infants and with a
dence of acute otitis media37, urinary with a 50% lower risk of sudden infant longer duration of breastfeeding56.
tract infection 38 , and meningitis death syndrome, although the etiology Maternal breastfeeding has a
caused by Haemophilus influenzae39. of this event is still not well estab- higher social impact in poor countries
Allergic diseases are also less com- lished and the studies analyzed pre- where the use of human milk as a nu-
mon and less severe in breastfed in- sented limitations50. tritional source is crucial due to its
fants8. Artificial feeding has been as- The long-term effects of breast- economic value57. Breastfeeding leads
sociated with a higher incidence of feeding include a reduced risk of obes- to significant savings for the family
asthma, diarrhea, vomiting and pro- ity, since breastfeeding is associated since no money is spent on the acqui-
longed colds 40. Around the third or with a lower rate of obese children (2.8 sition of maternal milk substitutes or
fourth month of life, 62% of infants versus 4.5% of children who have medication, and for society as a whole.
fed artificial milk present chronic na- never been breastfed). Thus, breast- Not breastfeeding increases the costs
sal obstruction and diarrhea versus feeding represents a preventive meas- for the health system. For each one
13% of breastfed infants 41. A long- ure for reducing the incidence of car- thousand non-breastfed infants, there
term follow-up study has demonstrated diovascular diseases and other disor- is an additional number of 2033
that the prevalence of atopic manifes- ders resulting from overweight51. pediatric visits, 212 days of hospitali-
tations, including eczema and food Breastfeeding provides better con- zation, and 606 medical prescriptions
and respiratory allergies, is higher in ditions for the development of the for the treatment of diarrhea, respira-
the group of non-breastfed patients or mother-child bond. The psychological tory diseases and acute otitis, media
patients breastfed for a short period of effects of breastfeeding on the mother compared to children exclusively
time42. and the child have been widely recog- breastfed for at least three months.
The action of human milk on the nized, since preparing the newborn for This additional demand generates an
immune system of the nursing infant breastfeeding establishes a proximity extra cost of US$331 to US$475 for
might explain the finding that allergic between them that is the optimal dis- each child during the first year of life58.
disorders8,42 and insulin-dependent dia- tance for the infant to visualize its The act of breastfeeding corre-
betes43 are less prevalent in breastfed mother’s face52. This affective connec- sponds to a significant part of the re-
children, and that weaning has been de- tion leads to reciprocal feeding from productive life of a woman, generating
scribed as a risk factor for Crohn’s dis- the psychological point of view53. The new sensations and improving her self-
ease 44 , childhood lymphoma 45 , and early contact between the mother and esteem59. In addition, the beneficial ef-
even for breast cancer during adult- her child since birth and during lying fects of breastfeeding on maternal
hood46. This effect should also be con- in together can increase the incidence health are numerous. In the breast-
sidered to explain the better response and duration of breastfeeding and re- feeding puerpera, adequate involution
of antibody production after vaccine duce the occurrence of abuse, negli- of the uterus accompanied by a reduc-
doses against poliomyelitis, tetanus gence and abandonment during child- tion in post-partum bleeding protects
and diphtheria in breastfeeding infants hood54. the maternal iron reserves, thus lead-
compared to those receiving artificial At the time the newborn is ing to lower rates of anemia2,11.
milk47. breastfed, alterations occur in its cer- Maternal nutrition has a low effect
Breastfeeding also has a beneficial ebral activity, which are characterized on the production and composition of
effect on the development of the oral by a significant increase in the ampli- human milk, since the lactating mother
cavity of the child, leading to ad- tude of its electroencephalogram in the is able to mobilize nutrients from her
equate tooth alignment and rare cases posterior cortical areas of both hemi- own organism even in the presence of
of malocclusion, thus reducing the spheres which are related to mecha- malnutrition. Under these conditions,
need to use an orthodontic apparatus nisms involved in hunger, satiety, regu- the concentration of the human milk
and the risk of sleep apnea during lation of affective satisfaction and components is conserved, except for
adulthood48. Breastfed infants show a sleep cycle modulation55. the lipid fraction2,60.
lower incidence of caries2, while in- Breastfeeding has been correlated Lactation is believed to cause rapid
fants receiving bottles containing milk with the child’s cognitive prognosis. weight loss in the lactating mother, es-
or juice rich in carbohydrates at night Breastfed infants show significantly pecially during the first month post
show a higher risk of developing bot- better scores in developmental tests partum, and persists, to a lesser extent,
tle caries49. than those receiving artificial milk, until the time of weaning61. There are
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6. Breastfeeding: making the difference REV. HOSP. CLÍN. FAC. MED. S. PAULO 58(1):49-60, 2003
Nascimento MBR et al.
also reports showing a lower risk of os- infants, valorization of the breast as a the rules of the “Ten Steps to Success-
teoporosis in breastfeeding women62. sex symbol, lack of enthusiasm on the ful Breastfeeding”78.
Breastfeeding has been suggested part of health professionals, and lack This set of measures started with
to exert a protective function against of knowledge about the advantages of the preparation of health professionals
breast cancer. The longer the duration breastfeeding on the part of the moth- who, from the prenatal period on, were
of breastfeeding, the lower the risk of ers70. As a result of urbanization, the provided with correct information
developing this type of tumor during extended family has been replaced by about the qualities of natural feeding
the premenopausal period63. A nega- the nuclear family, with girls having and guidance to solve problems of lac-
tive correlation between breastfeeding fewer opportunities to learn informally tation79,80. The latter aspect is as impor-
and ovarian cancer has also been re- the art of breastfeeding71. tant as the former since most pregnant
ported64. The contraceptive effect of In Brazil, this phenomenon was women, although recognizing the su-
lactation, with a consequent increase correlated with economic transforma- periority of breastfeeding, lack knowl-
in the interval between gestations, is tions that occurred at the beginning of edge about the art of breastfeeding81.
important to reduce maternal morbid- the 20th century, accompanied by ur- The implementation of the strategy
ity and mortality in developing coun- ban-industrial growth which favored “Baby-Friendly Hospital” has been re-
tries65,66. the occurrence of the nuclear family lated to a significant increase in the
The practicality of feeding maternal and a consumer society, leading to the duration of breastfeeding of term
milk is unquestionable, since no mix- use of bottles and importation of in- newborns82; however, information re-
ing, heating or sterilizing is required dustrialized milk11. National produc- garding its impact on the feeding of
and the milk is always available at the tion of artificial milk, which was am- premature infants is still insufficient.
adequate temperature, in an unbreak- plified at the beginning of the forties,
able container and especially pro- and exaggerated advertising of mater-
jected7. Therefore, breastfeeding is the nal milk supplements have stimulated USE OF HUMAN MILK IN
ideal method for feeding newborns and early weaning11,72. PREMATURE INFANTS
nursing infants and should be exclu- Awareness of this problem and its
sively used until six months of age67. consequences, especially infant mor- The recommendation of breast-
After this age, complementation food tality due to malnutrition and gastro- feeding for the premature newborn has
should be offered, but breastfeeding enterocolitis34, led to the creation of been defended on the basis of the im-
can be beneficially maintained until the National Program for the Encour- munological properties of human milk,
two years or more67,68. agement of Breastfeeding (PNIAM) in its role in gastrointestinal maturation,
1981 by the Ministry of Health, which formation of the mother-child bond,
represented an ample educational pro- and improvement in neurobehavioral
BREASTFEEDING AND EARLY gram with the objective to rescue natu- performance, shown by breastfed chil-
WEANING ral feeding72,73. dren83,84. Feeding of premature infants
The decade of the eighties was char- with human milk has been suggested
Despite the qualities of maternal acterized by the valorization of to have short-, medium- and long-term
breastfeeding, a decline in the world- breastfeeding, with the development benefits85. Premature infants show a
wide rates of breastfeeding was ob- of a worldwide movement on behalf of better suction-deglutition coordina-
served at the end of the 19th century, the rescue of breastfeeding 74-77. In tion during breastfeeding. The transcu-
at the time of the Industrial Revolution 1989, the World Health Organization taneous partial oxygen pressure levels,
and was intensified after World War II. and UNICEF promoted a meeting in oxygen saturation and body tempera-
This decrease started in the urban Florence, Italy, attended by representa- ture have been shown to be higher
centers of developed countries and has tives of various countries, including than those observed during bottle feed-
gradually spread to developing coun- Brazil, who signed the “Innocenti Dec- ing86-89, confirming that breastfeeding
tries69. laration”78 which determined actions is a more physiological process.
The reasons for this decline have to be implemented by health services Human milk exerts a protective ef-
been attributed to processes of urbani- to facilitate breastfeeding. On this oc- fect on premature infants against necro-
zation and industrialization, including casion, the “Baby-Friendly Hospital tizing enterocolitis. Lucas and Cole90
working mothers, occupation of Initiative” was created to stimulate observed a six to ten times higher in-
women in modern society, the advent maternity hospitals to promote, protect cidence of this disorder in premature
of milk products exclusive for nursing and support natural feeding, based on newborns who exclusively received
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7. REV. HOSP. CLÍN. FAC. MED. S. PAULO 58(1):49-60, 2003 Breastfeeding: making the difference
Nascimento MBR et al.
artificial milk compared to those fed tween 7.5 and 8 years of age, in strategy, which results in a better
human milk. Likewise, the incidence preterm children fed human milk. This weight gain of premature newborns, is
of any infection, including sepsis and study was carried out with scientific to offer hindmilk that contains up to
meningitis, has been found to be sig- rigor, with adjustment for factors such three times more fat than foremilk111.
nificantly lower among very low as social class and educational level of The milk produced by mothers of pre-
birthweight newborns fed human milk the mother, days of mechanical venti- mature newborns during the first four
than among those receiving exclu- lation, and gender. Since most prema- weeks post partum contains a higher
sively artificial milk91,92. ture newborns received milk by gav- concentration of nitrogen, proteins
During the hospital stay of the age, there is evidence that the best psy- with immunological functions, total
mother and the premature infant, the chomotor development was due to the lipids, medium chain fatty acids, vita-
mother produces antibodies against milk itself and not to the quality of mins A, D and E, calcium, sodium, and
nosocomial microorganisms that occur mother care, supporting the statement energy than the milk of mothers of
at the neonatal unit, a fact important that human milk is the optimal diet for term infants. Therefore, milk obtained
for the prevention of infection in the the developing brain102. from the milk bank pool might be nu-
neonate during the hospital stay 93. Epidemiological evidence suggests tritionally inadequate for premature
These data were confirmed by the ob- that feeding human milk is related to infants12,112.
servation of a significant reduction in a lower incidence of rehospitalization Industrialized additives derived
the incidence of severe infections in of premature infants, even after the in- from cow’s milk are available and rec-
patients submitted to the Kangaroo troduction of food supplements. There- ommended by some sources in order
Mother Care, in which the newborn is fore, even partial breastfeeding should to satisfy the nutritional needs of the
maintained in a vertical position, in be encouraged in this population8,85,93. child16,113. A wide variety of human
prone decubitus, against the mother, The biological benefits of mater- milk additives exists, most of them pre-
leading to early and growing contact nal milk render it an excellent food for pared on the basis of protein, carbohy-
between them94, compared to patients premature newborns, even when con- drates, calcium, phosphorus, magne-
treated by the traditional method95,96. sidering that eventual losses of nutri- sium and sodium, which can also con-
Maternal milk has been found to ents due to collection, processing and tain zinc, copper and vitamins114. The
protect premature infants with a fam- storage and to the method used to of- addition of these nutrients of bovine
ily history of atopy against allergy, es- fer human milk to patients of neonatal origin to human milk has guaranteed
pecially in terms of the incidence of units83,103-107 might be responsible for appropriate growth rates for very low
eczema. After 18 months of age, chil- the lower growth rate observed for birthweight newborns113,115, without af-
dren who received artificial milk these newborns compared to those re- fecting gastric emptying or food tol-
showed a higher risk of developing ceiving artificial milk 108. Although erance116.
this type of reaction than those receiv- neonatal growth performance is better Neonatologists need not only to be
ing human milk from a milk bank97. in preterm infants fed premature formu- convinced of the multiple advantages
Omega 3 fatty acids are essential las, this is not true for measurements of breastfeeding and of the possibility
for a normal development of the retina, of weight, height, head circumference to feed human milk to premature
especially in very low birthweight and cutaneous fold around nine newborns, but should also integrate
newborns98. These fatty acids, together months and eight years of age, which the management of lactation into the
with antioxidant substances such as were found to be similar irrespective planning of therapeutic actions for
vitamin E, ß-carotene and taurine, of whether the diet received was pref- these patients117. In view of the enor-
might explain the protective effect of erentially maternal milk or exclusively mous advances in neonatology since
human milk on the development of artificial milk109. the end of the sixties, especially the
premature retinopathy, since the inci- The diet of choice for premature development of new support tech-
dence and severity of this disease are newborns is the milk of their own niques for critically ill newborns, a
significantly lower in premature in- mothers. In the case the child is unable population of premature very low
fants exclusively fed with maternal to directly suck at the breast, it should birthweight newborns has arisen,
milk or who ingested at least 80% of receive manually expressed milk. which, until recently, did not survive
their milk in the form of human milk99. When necessary, this milk should be and which, due to treir immaturity and
Lucas et al.100,101 observed advan- supplemented with nutrients that are clinical complications, is subject to
tages in terms of cognitive perform- found in human milk itself (reformu- childhood malnutrition and rehospi-
ance, assessed at 18 months and be- lated human milk)110. Another feeding talization118. Studies making breast-
55

8. Breastfeeding: making the difference REV. HOSP. CLÍN. FAC. MED. S. PAULO 58(1):49-60, 2003
Nascimento MBR et al.
feeding viable for this risk population fied help and family support125. breastfeeding to the mother. This, in
have unquestionable social importance Breastfeeding premature infants turn, requires training in health educa-
since these children, due to their im- represents a challenge. The premature tion and a true revolution in the hab-
munological impairment 119, would newborn shows physiological and its of clinical management and, con-
particularly benefit from breastfeeding, neurological immaturity, muscle hypo- sequently, subsidies for the function-
especially in Brazil, a developing tony and hyperreactivity to environ- ing of the program.
country with high infant mortality rates mental stimuli, and remains alert for It is also compensatory to help
and endemic malnutrition in various short periods of time only 126. How- mothers of premature infants, who fre-
regions120. ever, despite its inadequate suction- quently experience feelings of guilt
Although desirable, a low success deglutition-respiration control 127, a and anger, by showing that
rate of breastfeeding has been observed premature newborn is able to feed at breastfeeding, in addition to being im-
among mothers of premature neo- the breast as long as appropriate help portant for the health and development
nates121, since many hospital barriers to is provided128. of the newborn, is a practical and posi-
breastfeeding still exist122, especially in The success of the work of promo- tive way for the mother to cope with
high risk neonatology services123, and tion, protection and support for the early birth of their child.
weaning from the breast frequently oc- breastfeeding in premature infants de- Even better would be to permit that
curs even before discharge of the pre- pends on an interdisciplinary team hospitalized premature newborns be
mature newborn from the high risk nurs- consisting of neonatologists, nursing neither deprived of the presence of
ery124. professionals, nutritionists, occupa- their mothers nor of breastfeeding. As
During the stay at the neonatal tional therapists, physiotherapists, so- Colette Clark said:
unit, many mothers perceive that nurs- cial assistants and phonoaudiologists,
ing their child is the only thing that who should be prepared to integrate “The newborn has only three es-
they can effectively do to collaborate the clinical hospital management of sential needs: the human warmth of
in the recovery of the premature new- lactation within the routine function- the mother’s arms, the certainty of the
born; however, only few mothers are ing of high risk nurseries. This team mother’s presence, and the milk of her
able to initiate and maintain an ad- should be motivated and capable to breasts. Breastfeeding satisfies all
equate milk production without quali- provide consistent information about three.”
RESUMO
NASCIMENTO MBR do e col. - Alei- cológicas e econômicas reconhecidas e o aleitamento nestas crianças. Neste ar-
tamento materno: fazendo a dife- inquestionáveis. Estas qualidades ad- tigo, os autores apresentam uma revisão
rença no desenvolvimento, saúde e quirem relevo especial em se tratando atualizada sobre os componentes do
nutrição dos recém-nascidos de ter- de recém-nascidos pré-termo, por sua leite humano e suas características úni-
mo e pré-termo. Rev. Hosp. Clín. maior vulnerabilidade. Apesar de alta- cas, bem como descrevem aspectos que
Fac. Med. S. Paulo 58(1):49-60, mente desejável, observa-se, de modo tornam o leite materno particularmente
2003. geral, baixa incidência de êxito na adequado para a alimentação do recém-
amamentação de prematuros, especial- nascido prematuro.
O aleitamento materno é o modo mente em unidade neonatais de risco.
natural e seguro de alimentação para a Há evidências de que uma postura hos- DESCRITORES: Alimentação
criança pequena, proporcionando van- pitalar favorável, com apoio de uma infantil. Aleitamento materno. Leite
tagens nutricionais, imunológicas, psi- equipe multiprofissional, torne possível humano. Recém-nascido. Prematuro.
56

9. REV. HOSP. CLÍN. FAC. MED. S. PAULO 58(1):49-60, 2003 Breastfeeding: making the difference
Nascimento MBR et al.
REFERENCES
1. AKRÊ J - Alimentação Infantil: bases fisiológicas. IBFAN/ 17. HAMOSH M, SALEM N Jr. - Long-chain polyunsaturated fatty
Instituto de Saúde de São Paulo, 1994. (Trad. Anna acids. Biol Neonate 1998; 74:106-120.
Volochko).
18. VAN BEEK RHT, CARNIELLI VP, SAUER PJJ - Nutrition in
2. VALDÉS V, SÁNCHES AP, LABBOK M - Manejo clínico da the neonate. Curr Opin Pediatr 1995; 7:146-151.
lactação: assistência à nutriz e ao lactente. Rio de Janeiro,
Revinter, 1996. (Trad. Marcus Renato de Carvalho). 19. UAUY R, HOFFMAN DR - Essential fat requirements of preterm
infants. Am J Clin Nutr 2000; 71 Suppl:245-250.
3. PICCIANO MF - Human milk: nutritional aspects of a dynamic
food. Biol Neonate. 1998; 74:84-93. 20. SCHANLER RJ, HURST NM, LAU C - The use of human milk
and breastfeeding in premature infants. Clin Perinatol 1999;
4. KUNZ C, RODRIGUEZ-PALMERO M, KOLETZKO B et al. - 26:379-398.
Nutritional and biochemical properties of human milk, part
I: general aspects, proteins and carbohydrates. Clin Perinatol 21. FALLOT ME, BOYD JL, OSKI F - Breast-feeding reduces
1999; 26:307-333. incidence of hospital admissions for infection in infants.
Pediatrics 1980; 65:1121-1124.
5. RODRIGUEZ-PALMERO M, KOLETZKO B, KUNZ C et al. -
Nutritional and biochemical properties of human milk, part 22. VICTORA CG, VAUGHAN JP, LOMBARDI C et al. - Evidence
II: lipids, micronutrients and bioactive factors. Clin Perinatol for protection by breast-feeding against infant deaths from
1999; 26:335-359. infectious diseases in Brazil. Lancet 1987; 2:319-322.
6. WORLD health organization (WHO) - Collaborative Study Team 23. WRIGHT A, HOLBERG CJ, MARTINEZ FD et al. - Breastfeeding
on the role of Breastfeeding on the prevention of infant and lower respiratory tract ilness in the first year of life. BMJ
mortality. Effect of breastfeeding on infant and child mortality 1989; 299:946-949.
due to infectious disease in less developed countries: a pooled
ananlysis. Lancet 2000; 355:451-455. 24. HOWIE PW, FORSYTH JS, OGSTON AS et al. - Protective
effect of breastfeeding against infection. BMJ 1990; 300:11-
7. MULLER M - O matador de bebês. Recife, Companhia Editora 16.
de Pernambuco, 1995.
25. XANTHOU M - Immune protection of human milk. Biol
8. RIORDAN J - The biologic specificity of breastmilk. In: Neonate 1998; 74: 121-133.
RIORDAN J, AUERBACH KG - Breastfeeding and human
lactation. 2.ed. Boston, Jones and Bartlett Publishers, 1998. 26. GRUMACH AS, CARMONA RC, LAZAROTTI D et al. -
p. 121-161. Immunological factors in milk from brazilian mothers
delivering small-for-date term neonates. Acta Paediatr 1993;
9. RUOCCO RMSA - Colostro humano: contribuição ao estudo da 82: 284-290.
sua composição leucocitária. São Paulo, 1992. Tese
(Doutorado) - Faculdade de Medicina, Universidade de São 27. HAMOSH M - Protective function of proteins and lipids in
Paulo. human milk. Biol Neonate 1998; 74:163-176.
10. LAWRENCE RA - Breastfeeding: a guide for the medical 28. PETERSON JÁ, PATTON S, HAMOSH M - Glycoproteins of
profession. 4th ed. St. Louis, Mosby, 1994. the human milk fat globule in the protection of the breast-
fed infant against infections. Biol Neonate 1998; 74:143-
11. ALMEIDA JAG - Amamentação: um híbrido natureza-cultura. 162.
Rio de Janeiro, Editora Fiocruz, 1999.
29. GAROFALO RP, GOLDMAN AP - Cytokines, chemokines, and
12. GROSS SJ, DAVID RJ, BAUMANN L et al. - Nutritional colony-stimulating factors in human milk: the 1997 update.
composition of milk produced by mothers delivering preterm. Biol Neonate 1998; 74:134-142.
J Pediatr 1980; 96:641-644.
30. GRAZIOSO CF, WERNER AL, ALLING DW et al. -
13. CALIL VMLT - Composição nutricional do colostro de mães de Antiinflamatory effects of human milk on chemically induced
recém-nascidos adequados e pequenos para a idade colitis in rats. Pediatr Res 1997; 42:639-643.
gestacional. São Paulo, 1990. Dissertação (Mestrado) -
Faculdade de Medicina, Universidade de São Paulo. 31. GAROFALO RP, GOLDMAN AP - Expression of functional
immunomodulatory and anti-inflammatory factors in human
14. LAWRENCE PB - Breast milk: best source of nutrition for term milk. Clin Perinatol 1999; 26:361-377.
and preterm infants. Ped Clin North Am 1994; 41:925-941.
32. SIROTA L, STRAUSSBERG R, NOTTI I et al. - Effect of human
15. SCAGLIA F, LONGO N - Primary and secondary alterations of colostrum on interleukin-2 production and natural killer cell
neonatal carnitine metabolism. Semin Perinatol 1999; activity. Arch Dis Child 1995; 73: 99-102.
23:152-161.
33. CÉSAR JÁ, VICTORA CG, BARROS FC et al. - Impact of breast
16. CANADIAN paediatric society (CPS) - Nutrition Comittee. feeding on admission for pneumonia during postneonatal
Nutrition needs and feeding of premature infants. Can Med period in Brazil: nested case-control study. BMJ 1999;
Assoc J 1995;152:1765-1785. 318:1316-1320.
57

10. Breastfeeding: making the difference REV. HOSP. CLÍN. FAC. MED. S. PAULO 58(1):49-60, 2003
Nascimento MBR et al.
34. SIGULEM DM, TUDISCO ES - Aleitamento natural em 51. VON KRIES R, KOLETZKO B, SAUERWALD T et al. -
diferentes classes de renda no município de São Paulo. Arch Breastfeeding and obesity: cross sectional study. BMJ 1999;
Latinoam Nutr 1980; 30:400-416. 139:147-150.
35. COUSENS S, NACRO B, CURTIS V et al. - Prolonged 52. KLAUS MH, KLAUS PH - The amazing newborn.
breastfeeding: no association with increased risk of clinical Massachussetts, Addison-Wesley Pub, 1992.
malnutritionin young children in Burkina Faso. WHO
Bulletin 1993; 71:713-722. 53. VINHA VHP - Amamentação materna: incentivo e cuidados.
São Paulo, Sarvier, 1983.
36. ISLAM MA, RAHMAN MM, MAHALANABIS D - Maternal
and socioeconomic factors and the risk of severe malnutrition 54. KLAUS MH, KENNEL JH - The doula: an essential ingredient
in a child: a case-control study. Eur J Clin Nutr 1994; 48: of childbirth rediscovered. Acta Paediatr 1997; 86:1034-
416-424. 1036.
37. DUNCAN B, EY J, HOLBERG CJ et al. - Exclusive breastfeeding 55. LEHTONEN J, KÖNÖNEN M, PURHONEN M et al. - The
for at least 4 months protects against otitis media. Pediatrics effect of nursing on the brain activity of the newborn. J
1993; 91:867-871. Pediat 1998; 132:646-651.
38. PISACANE A, GRAZIANO L, MAZZARELLA G et al. - Breast 56. ANDERSON JW, JOHNSTONE BM, REMLEY DT -
feeding and urinary tract infection. J Pediatr 1992; 120:87- Breastfeeding and cognitive development: a meta-analysis.
90. Am J Clin Nutr 1999; 70:525-535.
39. SILFVERDAL AS & OLCÉN P - Protective effect of 57. VILLALPANDO S, HAMOSH M - Early and late effects of
breastfeeding: an ecologic study of Haemophilus influenzae breast-feeding: does breast-feeding really matter? Biol
meningitis and breastfeeding in a Swedish population. Int J Neonate 1998; 74:177-191.
Epidemiol 1999; 28:152-156.
58. BALL TM, WRIGHT AL - Health care costs of formula-feeding
40. MERRET TC, BURR ML, BUTLAND BK Infant feeding and in the first year of life. Pediatrics 1999; 103:870-676.
allergy: twelve-month prospective study of 500 babies born
in allergic families. Ann Allergy 1988; 61:13-20. 59. SCHMIED V, BARCLAY L - Connection and pleasure, disruption
and distress: women’s experience of breastfeeding. J Hum
41. HARRIS MC, KOLSKI GB, CAMPBELL DE - Ontogeny of the Lact 1999; 15:325-334.
antibody response to cow milk proteins. Ann Allergy 1989;
63:439-442. 60. RIORDAN J, AUERBACH KG. - Maternal health. In: RIORDAN
J, AUERBACH KG - Breastfeeding and human lactation.
42. SAARINEN UM, KAJOSAARI M - Breast-feeding as prophylaxis Boston, Jones and Bartlett Pub, 1993. p. 349-377.
against atopic disease: prospective follow-up study until 17
years old. Lancet 1995; 346: 1065-1069. 61. ABUSABHA R, GREENE G - Body weight, body composition,
and energy intake changes in breastfeeding mothers. J Hum
43. MAYER EJ, HAMMAN RF, GAY EC et al. - Reduced risk of Lact 1998; 114:119-124,.
IDDM among breast-fed children. Diabetes 1988; 37:1625-
1632. 62. KRITZ-SILVERSTEIN D, BARRET-CONNOR E,
HOLLENBACH KA -Pregnancy and lactation as determinants
44. DAVIS MK, SAVITZ DA, GRAUBARD BI - Infant feeding and of bone mineral density in postmenopausal women. Am J
childhood cancer. Lancet 1988; 2:365-368. Epidemiol 1992; 136:1052-1059.
45. KOLETZKO S, SHERMAN P, COREY M et al. - Role of infant 63. BYERS T, GRAHAM S, RZEPKA T et al. - Lactation and breast
feeding practices in development of Crohn’s disease in cancer: evidence for a negative association in premenopausal
childhood. BMJ 1989; 298:1617-1618. women. Am J Epidemiol 1985; 121:664-674.
46. FREUDENHEIN JL, MARSHAL JR, GRAHAN S et al. - 64. SCHNEIDER AP - Risk factor for ovarian cancer [Letter]. N
Exposure to breastmilk in infancy and the risk of breast Engl J Med 1987; 317:508-509.
cancer. Epidemiology 1994; 5:324-331.
65. SAADEH R, BENBOUZID D - Lactancia materna e
47. HAHN-ZORIC M, FULCONIS F, MINOLI I et al. - Antibody espaciamento de los nacimientos: importancia de la obtención
response to parenteral and oral vaccines are impaired by de información para las políticas de salud pública. Bol of
conventional and low protein formulas as compared to breast- Sanit Panam 1991; 111:122-130.
feeding. Acta Paediatr Scand 1990; 79:1137-1142.
66. KENNEDY KI, KOTELCHUCK M - Policy considerations for
48. PALMER B - The influence of breastfeeding on the development the introduction and promotion of the Lactacional
of the oral cavity: a commentary. J Hum Lact 1998; 114:93- Amenorrhea Method: advantages and disadvantages of LAM.
98. J Hum Lact 1998; 14:191-203,.
49. LOESCHE WJ - Nutrition and dental decay in infants. Am J 67. WORLD Health Organization (WHO). - The optimal duration
Clin Nutr 1985; 41: 423-435. of exclusive breastfeeding. Note for the press n.º 7, April 2,
2001. Available at: http://www.who.int/inf-pr-2001/en/
50. MCVEA KLSP, TURNER PD, PEPPLER DK - The role of note2001-07.html.
breastfeeding in sudden infant death syndrome. J Hum Lact
2000; 16: 13-20.
58

11. REV. HOSP. CLÍN. FAC. MED. S. PAULO 58(1):49-60, 2003 Breastfeeding: making the difference
Nascimento MBR et al.
68. WORLD Health Organization (WHO). - Indicators for assessing 86. MEIER P, ANDERSON GC - Responses of small preterm infants
breast-feeding practices. Geneva, 1991. to bottle and breastfeeding. MCN Am Matern Child Nurs
1987; 12:97-105.
69. COATES MM - Tides in breastfeeding practices. In: RIORDAN
J, AUERBACH KG - Breastfeeding and human lactation. 87. MEIER P - Bottle and breastfeeding : effects on transcutaneous
Boston, Jones and Bartlett Pub, 1993. p. 3-26. oxygen pressure and temperature in preterm infants. Nurs
Res 1988; 37:36-41.
70. JELLIFFE DB - Evolución de la alimentación infantil. In: OMS
- La nutrición infantil en las zonas tropicales e 88. BIER JB, FERGUSON A, ANDERSON L et al. - Breast-feeding of
subtropicales. Ginebra, Organización Mundial de la Salud, very low birth weight infants. J Pediatr 1993; 123:773-778.
1970; 29:13-32. Série de monografias.
89. CHEN C, WANG T, CHANG H et al. - The effect of breast and
71. JELLIFFE DB & JELLIFFE EFP - Human milk in the modern bottle-feeding on oxygen saturation and body temperature
world. 2nd ed. New York, Oxford University Press, 1979. in preterm infants. J Hum Lact 2000; 16:21-27.
72. MINISTÉRIO DA SAÚDE (MS). - Instituto Nacional de 90. LUCAS A, COLE TJ - Breastmilk and neonatal necrotising
Alimentação e Nutrição. Programa nacional de aleitamento enterocolitis. Lancet 1990; 336:1519-1523.
materno. Brasília, 1991.
91. EL-MOHANDES AAE, PICARD M, SIMMENS SJ - Human
73. MATTAI J. - The brazilian national breast-feeding program. milk utilization in the ICN decreases the incidence of bacterial
Assign Child 1983; 6:225-247. sepsis [abstract]. Pediatr Res 1995; 37:306A.
74. FEINSTEIN JM, BERKELHAMER JE, GRUSKA ME et al. - 92. HYLANDER MA, STROBINO DM, DHANIREDDY R - Human
Factors related to early termination of breastfeeding in an milk feedings and infection among very low birth weight
urban population. Pediatrics 1986; 78:210-215. infants [abstract]. Pediatrics 1998; 102:630.
75. BARROS FC, VICTORA CG, VAUGHAN JP - Breastfeeding 93. GOLDMAN AS, CHHEDA S, KEENEY SE et al. - Immunologic
and socioeconomic status in southern Brazil. Acta Paediatr protection of the premature newborn by human milk. Semin
Scand 1986; 75:558-562. Perinatol 1994; 18:495-501.
76. ISSLER H, LEONE C, QUINTAL VS. - Duração do aleitamento 94. MINISTÉRIO da Saúde (MS) - Secretaria de políticas de saúde.
materno em uma área urbana de São Paulo, Brasil. Bol Of Área técnica da saúde da criança. Normas de atenção
Sanit Panam 1989; 106:513-522. humanizada ao recém-nascido de baixo peso: Método
Canguru. Brasília, 1999.
77. WEILE B, RUBIN DH, KRASILNIKOFF PA et al. - Infant feeding
patterns during the first year of life in Denmark: factors 95. SLOAN NL, CAMACHO LWL, ROJAS EP et al. - Kangaroo
associated with the discontinuation of breastfeeding. J Clin mother method: randomised controlled trial of an alternative
Epidemiol 1990; 43:1305-1311. method of care for stabilised low-birthweight infants. Lancet
1994; 344:782-785.
78. WORLD Health Organization (WHO)/UNICEF - Protecting,
promoting and supporting breastfeeding: the special role of 96. CHARPAK N, RUIZ-PELÁEZ JG, CALUME ZF et al. -
maternity services. A joint WHO/UNICEF statement. Geneva, Kangaroo mother versus traditional care for newborn infants
1989. <2000 grams: a randomized, controlled trial. Pediatrics 1997;
100:682-688.
79. LAMOUNIER JA - Promoção e incentivo ao aleitamento
materno: Iniciativa Hospital Amigo da Criança. J pediatr 97. LUCAS A, BROOKE OG, MORLEY R et al. - Early diet of
(Rio J) 1996; 72:363-368. preterm infants and development of allergic or atopic disease:
randomised prospective study. BMJ 1990; 300:837-840.
80. NEIFERT MR - The optimization of breast-feeding in the
perinatal period. Clin Perinatol 1998; 25:303-326. 98. UAUY RD, BIRCH DG, BIRCH EE et al. - Effect of dietary
Omega-3 fatty acids on retinal function of very low birth
81. ISSLER H, SÁ MBSR, SENNA DM. - Knowledge of newborn weight neonates. Pediatr Res 1990; 28:485-492.
healthcare among pregnant women: basis for promotional
and educational programs on breastfeeding. São Paulo Med 99. HYLANDER MA, STROBINO DM, DHANIREDDY R - Human
J/ Rev Paul Med 2001; 119:7-9. milk feedings and retinopathy of prematurity among very
low birth weight infants [abstract]. Pediatr Res 1996;
82. WRIGHT A, RICE S, WELLS S - Changing hospital practices to 37:214A .
increase the duration of breastfeeding. Pediatrics 1996;
97:669-675. 100. LUCAS A, MORLEY R, COLE TJ et al. - Early diet in preterm
babies and developmental status at 18 months. Lancet 1990;
83. SCHANLER RJ, HURST NM - Human milk for the hospitalized 335:1477-1481.
preterm infant. Semin Perinatol 1994;18:476-484.
101. LUCAS A, MORLEY R, COLE TJ et al. - Breastmilk and
84. SCHANLER RJ - Suitability of human milk for the low subsequent intelligence quotient in children born preterm.
birthweight infant. Clin Perinatol 1995; 22:207-222. Lancet 1992; 339:261-264.
85. MEIER P, BROWN L - State of the Science: Breastfeeding for 102. UAUY R, PEIRANO P. - Breat is best: human milk is the optimal
mothers and low birth weight infants. Nurs Clin North Am food for brain development. Am J Clin Nutr 1999; 70:433-
1996; 31:351-365. 434.
59

12. Breastfeeding: making the difference REV. HOSP. CLÍN. FAC. MED. S. PAULO 58(1):49-60, 2003
Nascimento MBR et al.
103. WILLIAMSON S, FINUCANE E, ELLIS H et al. - Effect of 116. MCCLURE RJ, NEWELL SJ - Effect of fortifying brest milk on
heat treatment of human milk on absorption of nitrogen, fat, gastric emptying. Arch Dis Child 1996; 74:60-62.
sodium, calcium and phosphorus by preterm infants. Arch
Dis Child 1978; 53:555-563. 117. AMERICAN academy of pediatrics (AAP) - Work group on
breastfeeding. Breastfeeding and the use of human milk.
104. BATES CJ, LIU DS, FULLER NJ et al. - Susceptibility of Pediatrics 1997; 100:1035-1039.
riboflavin and vitamin A in breast milk to photodegradation
and its implications for the use of banked breast milk in 118. BERNFIELD M - Foreword. In: CLOHERTY J, STARK AR ed.
infant feeding. Acta Paediatr Scand 1985; 74:40-44. - Manual of Neonatal Care. Boston, Little Brown, 1991.
105. STEIN H, COHEN D, HERMAN AAB et al. - Pooled pasteurized 119. FALCONER AE, CARR, EDWARDS SW - Impaired neutrophil
breast milk and untreated own mother’s milk in the feeding phagocytosis in preterm neonates: lack of correlation with
of very low birthweight babies: a randomized controlled expression of immunoglobulin or complement receptors.
trial. J Pediatr Gastroenterol Nutr 1986; 5:242-247. Biol. Neonate 1995; 68:264-269 .
106. PARDOU A, SERRUYS E, MASCART-LEMONE F et al. - Human 120. MINISTÉRIO DA SAÚDE (MS). Secretaria de assistência à
milk banking: influence of storage processes and of bacterial saúde. Coordenação materno-infantil. Manual de assistência
contamination on some milk constituents. Biol Neonate 1994; ao recém-nascido. Brasília, 1994.
65:302-309.
121. WOHLBERG LK, GEARY BF. - Team approach to breastfeeding
107. JOCSON MA, MASON EO, SCHANLER R.J - The effects of the ELBW infant: a case report. J Hum Lact 1994; 10:181-
nutrient fortification and varying storage conditions on host 183.
defense properties of human milk. Pediatrics 1997; 100:240-
243. 122. POWERS NG, NAYLOR AJ, WESTER RA - Hospital policies:
crucial to breastfeeding success. Semin Perinatol 1994;
108. NICHOLL RM GAMSU HR - Changes in growth and 18:517-524.
metabolism in very low birthweight infants fed with fortified
breast milk. Acta Paediatr 1999; 88:1056-1061. 123. PANTAZI M, JAEGER MC, LAWSON M - Staff support for
mothers to provide breast milk in pediatric hospitals and
109. MORLEY R, LUCAS A - Randomized diet in the neonatal period neonatal units. J Hum Lact; 14:291-296.
and growth performance until 7,5-8y of age in preterm
children. Am J Clin Nutr 2000; 71:822-828. 124. RICHARDS MT, LANG MD, MCINTOSH C et al. - Breastfeeding
the VLBW infant: sucessful outcome and maternal
110. VINAGRE RD - Análise crítica do uso do leite humano procedente expectation. Pediatr Res 1986; 20:383A.
de banco de leite na alimentação do recém-nascido prematuro.
São Paulo, 1999. Dissertação (Mestrado) - Faculdade de 125. MCCOY R, KADOWAKI C, WILKS S et al. - Nursing
Medicina, Universidade de São Paulo. management of breastfeedinf for preterm infants. J Perinat
Neonatal Nurs 1988; 2:42-55.
111. VALENTINE CJ, HURST NM, SCHANLER R.J - Hindmilk
improves weight gain in low-birth-weight infants fed human 126. NYQVIST KH, EWALD U, SJÖDÉN P - Supporting a preterm
milk. J Ped Gastroenterol Nutr 1994; 18:474-477. infant’s behaviour during breastfeeding: a case report. J
Hum Lact 1996; 12:221-228.
112. ATKINSON SA - Human milk feeding of the micropremie.
Clin Perinatol 2000; 27:235-247. 127. JAIN L, SIVIERI E, ABBASI S et al. - Energetics and mechanics
of nutritive sucking in the preterm and term neonate. J
113. GUERRINI P - Human milk fortifiers. Acta Paediatr 1994; Pediatr 1987; 111:894-898.
402:37-39. Supplement.
128. DROSTEN F - Case management of a premature infant
114. SCHANLER RJ - Fortified human milk: the nature’s way to feed transitioning to the breast. J Hum Lact 2001; 17:47-50.
premature infants. J Hum Lact 1998; 14:5-11.
115. SCHANLER RJ, SHULMAN RJ, LAU C - Growth of premature
infants fed fortified human milk. Pediatr Res 1997; 41:240A.
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