Skip to main content
×
Home
    • Aa
    • Aa

Evolution of lactation: nutrition v. protection with special reference to five mammalian species

  • Holly L. McClellan (a1), Susan J. Miller (a2) and Peter E. Hartmann (a1)
Abstract

The evolutionary origin of the mammary gland has been difficult to establish because little knowledge can be gained on the origin of soft tissue organs from fossil evidence. One approach to resolve the origin of lactation has compared the anatomy of existing primitive mammals to skin glands, whilst another has examined the metabolic and molecular synergy between mammary gland development and the innate immune system. We have reviewed the physiology of lactation in five mammalian species with special reference to these theories. In all species, milk fulfils dual functions of providing protection and nutrition to the young and, furthermore, within species the quality and quantity of milk are highly conserved despite maternal malnutrition or illness. There are vast differences in birth weight, milk production, feeding frequency, macronutrient concentration, growth rate and length of lactation between rabbits, quokkas (Setonix brachyurus), pigs, cattle and humans. The components that protect the neonate against infection do so without causing inflammation. Many protective components are not unique to the mammary gland and are shared with the innate immune system. In contrast, many of the macronutrients in milk are unique to the mammary gland, have evolved from components of the innate immune system, and have either retained or developed multiple functions including the provision of nourishment and protection of the hatchling/neonate. Thus, there is a strong argument to suggest that the mammary gland evolved from the inflammatory response; however, the extensive protection that has developed in milk to actively avoid triggering inflammation seems to be a contradiction.

    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Evolution of lactation: nutrition v. protection with special reference to five mammalian species
      Available formats
      ×
      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your Dropbox account. Find out more about sending content to Dropbox.

      Evolution of lactation: nutrition v. protection with special reference to five mammalian species
      Available formats
      ×
      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your Google Drive account. Find out more about sending content to Google Drive.

      Evolution of lactation: nutrition v. protection with special reference to five mammalian species
      Available formats
      ×
Copyright
Corresponding author
*Corresponding author: H. L. McClellan, fax +61 8 6488 1148, email hlm@student.uwa.edu.au
References
Hide All
1Schiebinger L (1993) Why mammals are called mammals: gender politics in eighteenth-century natural history. Am Hist Rev 98, 382411.
2Pond C (1984) Physiological and ecological importance of energy storage in the evolution of lactation: evidence for a common pattern of anatomical organization of adipose tissue in mammals. In Symposia of the Zoological Society of London, Physiological Strategies in Lactation, vol. 51, pp. 129 [Peaker M, Vernon RG and Knight CH, editors]. London: Academic Press.
3Oftedal OT (2002) The mammary gland and its origin during synapsid evolution. J Mammary Gland Biol Neoplasia 7, 225252.
4Oftedal OT (2002) The origin of lactation as a water source for parchment-shelled eggs. J Mammary Gland Biol Neoplasia 7, 253266.
5Vorbach C, Capecchi MR & Penninger JM (2006) Evolution of the mammary gland from the innate immune system? Bioessays 28, 606616.
6Brawand D, Wahli W & Kaessmann H (2008) Loss of egg yolk genes in mammals and the origin of lactation and placentation. PLoS Biol 6, e63.
7Vorbach C, Scriven A & Capecchi MR (2002) The housekeeping gene xanthine oxidoreductase is necessary for milk fat droplet enveloping and secretion: gene sharing in the lactating mammary gland. Genes Dev 16, 32233235.
8Vorbach C, Harrison R & Capecchi MR (2003) Xanthine oxidoreductase is central to the evolution and function of the innate immune system. Trends Immunol 24, 512517.
9Cao Y, Bonizzi G, Seagroves TN, et al. . (2001) IKKα provides an essential link between RANK signaling and cyclin D1 expression during mammary gland development. Cell 107, 763775.
10Brisken C (2002) Hormonal control of alveolar development and its implications for breast carcinogenesis. J Mammary Gland Biol Neoplasia 7, 3948.
11Nishimori K, Young LJ, Guo Q, et al. . (1996) Oxytocin is required for nursing but is not essential for parturition or reproductive behavior. Proc Natl Acad Sci U S A 93, 1169911704.
12Friedrichsen S, Harper CV, Semprini S, et al. . (2006) Tumor necrosis factor-α activates the human prolactin gene promoter via nuclear factor-κB signaling. Endocrinology 147, 773781.
13Terzidou V, Lee Y, Lindstrom T, et al. . (2006) Regulation of the human oxytocin receptor by nuclear factor-κB and CCAAT/enhancer-binding protein-β. J Clin Endocrinol Metab 91, 23172326.
14Ramji DP & Foka P (2002) CCAAT/enhancer-binding proteins: structure, function and regulation. Biochem J 365, 561575.
15Seagroves TN, Krnacik S, Raught B, et al. . (1998) C/EBPβ, but not C/EBPα, is essential for ductal morphogenesis, lobuloalveolar proliferation, and functional differentiation in the mouse mammary gland. Genes Dev 12, 19171928.
16Chow CW, Clark MP, Rinaldo JE, et al. . (1995) Multiple initiators and C/EBP binding sites are involved in transcription from the TATA-less rat XDH/XO basal promoter. Nucleic Acids Res 23, 31323140.
17Nanbu-Wakao R, Fujitani Y, Masuho Y, et al. . (2000) Prolactin enhances CCAAT enhancer-binding protein-β (C/EBPβ) and peroxisome proliferator-activated receptor γ (PPARγ) messenger RNA expression and stimulates adipogenic conversion of NIH-3T3 cells. Mol Endocrinol 14, 307316.
18Kawai M, Namba N, Mushiake S, et al. . (2007) Growth hormone stimulates adipogenesis of 3T3-L1 cells through activation of the Stat5A/5B-PPARγ pathway. J Mol Endocrinol 38, 1934.
19Wan Y, Saghatelian A, Chong LW, et al. . (2007) Maternal PPARγ protects nursing neonates by suppressing the production of inflammatory milk. Genes Dev 21, 18951908.
20Vidal-Puig AJ, Considine RV, Jimenez-Linan M, et al. . (1997) Peroxisome proliferator-activated receptor gene expression in human tissues. Effects of obesity, weight loss, and regulation by insulin and glucocorticoids. J Clin Invest 99, 24162422.
21Hewitt DP, Mark PJ & Waddell BJ (2006) Placental expression of peroxisome proliferator-activated receptors in rat pregnancy and the effect of increased glucocorticoid exposure. Biol Reprod 74, 2328.
22Darwin C (1902) On the Origin of Species by Means of Natural Selection or the Preservation of Favoured Races in the Struggle for Life. London: Grant Richards.
23Oftedal OT & Iverson SA (1995) Comparative analysis of nonhuman milks. A. Phylogenetic variation in the gross composition of milks. In Handbook of Milk Composition, pp. 749789 [Jensen RG, editor]. San Diego, CA: Academic Press.
24Dickman C & Woodford Ganf R (2007) A Fragile Balance: The Extraordinary Story of Australian Marsupials. Melbourne: Craftsman House.
25Tyndale-Biscoe CH & Janssens PA (1988) Introduction. In The Developing Marsupial: Models for Biomedical Research, pp. 17 [Tyndale-Biscoe CH and Janssens PA, editors]. Berlin: Springer-Verlag.
26Miller S (2005) The Composition of the Milk of the Quokka (Setonix brachyurus) and its Consumption by the Joey. PhD Thesis, The University of Western Australia, Crawley, WA, Australia.
27Croft DB & Eisenberg JF (2006) Behaviour. In Marsupials, pp. 108136 [Armati PJ, Dickman CR and Hume ID, editors]. Cambridge: Cambridge University Press.
28Janssens PA & Rogers AMT (1989) Metabolic changes during pouch vacation and weaning in macropodoids. In Kangaroos, Wallabies and Rat-Kangaroos, pp. 367376 [Grigg G, Jarman P and Hume I, editors]. Chipping Norton, NSW: Surrey Beatty and Sons.
29Russell EM (1989) Maternal behaviour in the Macropodoidea. In Kangaroos, Wallabies and Rat-Kangaroos, pp. 549569 [Grigg G, Jarman P and Hume I, editors]. Chipping Norton, NSW: Surrey Beatty and Sons.
30Shield J (1968) Reproduction of the quokka, Setonix brachyurus, in captivity. J Zool (Lond) 155, 427444.
31Trott JF, Simpson KJ, Moyle RLC, et al. . (2003) Maternal regulation of milk composition, milk production, and pouch young development during lactation in the tammar wallaby (Macropus eugenii). Biol Reprod 68, 929936.
32Cowie AT (1969) Variations in the yield and composition of the milk during lactation in the rabbit and the galactopoietic effect of prolactin. J Endocrinol 44, 437450.
33Jelliffe DB & Jelliffe EF (1978) Adaptive suckling. J Trop Pediatr Environ Child Health 24, 99102.
34Tyndale-Biscoe CH (2001) Australasian marsupials – to cherish and to hold. Reprod Fertil Dev 13, 477485.
35Hartmann PE, McCauley I, Gooneratne AD, et al. (1984) Inadequacies of sow lactation: survival of the fittest. In Symposia of the Zoological Society of London, Physiological Strategies in Lactation, vol. 51, pp. 301326 [Peaker M, Vernon RG and Knight CH, editors]. London: Academic Press.
36Smith N (1994) Biochemical and physiological investigations of parturition and lactation in the pig. PhD Thesis, The University of Western Australia, Crawley, WA, Australia.
37Gooneratne A, Hartmann PE, McCauley I, et al. . (1979) Control of parturition in the sow using progesterone and prostaglandin. Aust J Biol Sci 32, 587595.
38McGann B (2008) Bike Race Info. Tour de France Winners, Podium, Times. http://bikeraceinfo.com/tdf/tdfindex.html (accessed March 2008).
39Norman HD, Thornton LLM & Wiggans GR (2008) State and national standardized lactation averages by breed for cows calving in 2006. AIPL Research Report. http://aipl.arsusda.gov/publish/dhi/current/lax.html (accessed March 2008).
40Shillito Walser E (1977) Maternal behaviour in mammals. In Symposia of the Zoological Society of London, Comparitive Aspects of Lactation, vol. 41, pp. 313331 [Peaker M, editor]. London: Academic Press.
41Coates DB, Mannetje L & Seifert GW (1987) Reproductive performance and calf growth to weaning of Hereford and Belmont Red cattle in subtropical, subcoastal Queensland. Aust J Exp Agric 27, 110.
42Grondahl AM, Skancke EM, Mejdell CM, et al. . (2007) Growth rate, health and welfare in a dairy herd with natural suckling until 6–8 weeks of age: a case report. Acta Vet Scand 49, 16.
43Fischler C (1981) Food preferences, nutritional wisdom, and sociocultural evolution. In Food, Nutrition and Evolution, pp. 5967 [Walcher D and Kretchmer N, editors]. New York: Masson Publishing.
44Stuart-Macadam P (1995) Breastfeeding in prehistory. In Breastfeeding: Biocultural Perspectives, pp. 7599 [Stuart-Macadam P and Dettwyler KA, editors]. New York: Aldine de Gruyter.
45Fomon SJ & Nelson SE (2002) Body composition of the male and female reference infants. Annu Rev Nutr 22, 117.
46World Health Organization (2006) WHO Child Growth Standards: methods and development. Length/height-for-age, weight-for-age, weight-for-length, weight-for-height and body mass index-for-age. http://www.who.int/childgrowth/standards/technical_report/en/index.html (accessed February 2008).
47Thomson D (1983) Children of the Wilderness. Melbourne: Currey O'Neil.
48Wickes IG (1953) A history of infant feeding. I. Primitive peoples; ancient works; Renaissance writers. Arch Dis Child 28, 151158.
49Geyer LA & Kare MR (1981) Taste and food selection in the weaning of nonprimate mammals. In Food, Nutrition and Evolution: Food as an Environmental Factor in the Genesis of Human Variability, pp. 6982 [Walcher D, editor]. New York: Masson Publishing.
50Case TJ (1978) On the evolution and adaptive significance of postnatal growth rates in the terrestrial vertebrates. Q Rev Biol 53, 243282.
51Konner M & Worthman C (1980) Nursing frequency, gonadal function, and birth spacing among !Kung hunter-gatherers. Science 207, 788791.
52Hartmann PE (2007) Mammary gland: past, present and future. In Hale and Hartmann's Textbook of Human Lactation, pp. 316 [Hartmann PE and Hale T, editors]. Amarillo, TX: Hale Publishing.
53Rendle-Short M & Rendle-Short J (1966) The Father of Child Care. Life of William Cadogan (1711–1797). Bristol: John Wright and Sons Ltd.
54Truby King M (1941) Mothercraft. Sydney: Whitcombe and Tombs Ltd.
55Lussky HO (1951) A study of breast feeding at the Evanston Hospital. Q Bull Northwest Univ Med Sch 25, 251256.
56Daly SE, Owens RA & Hartmann PE (1993) The short-term synthesis and infant-regulated removal of milk in lactating women. Exp Physiol 78, 209220.
57Wickes IG (1953) A history of infant feeding. II. Seventeenth and eighteenth centuries. Arch Dis Child 28, 232240.
58Wickes IG (1953) A history of infant feeding. III. Eighteenth and nineteenth century writers. Arch Dis Child 28, 332340.
59Wickes JG (1953) A history of infant feeding. IV. Nineteenth century continued. Arch Dis Child 28, 416422.
60Wickes IG (1953) A history of infant feeding. V. Nineteenth century concluded and twentieth century. Arch Dis Child 28, 495502.
61Kent JC, Mitoulas LR, Cregan MD, et al. . (2006) Volume and frequency of breastfeedings and fat content of breast milk throughout the day. Pediatrics 117, e387e395.
62Sharp JA, Cane KN, Lefevre C, et al. . (2006) Fur seal adaptations to lactation: insights into mammary gland function. Curr Top Dev Biol 72, 275308.
63Bonner W (1984) Lactation strategies in Pinnipeds: problems for a marine mammalian group. In Symposia of the Zoological Society of London, Physiological Strategies in Lactation, vol. 51, pp. 253272 [Peaker M, Vernon RG and Knight CH, editors]. London: Academic Press.
64Odde KG, Kiracofe GH & Schalles RR (1985) Suckling behavior in range beef calves. J Anim Sci 61, 307309.
65Hillerton JE, Knight CH, Turvey A, et al. . (1990) Milk yield and mammary function in dairy cows milked four times daily. J Dairy Res 57, 285294.
66Zarrow MX, Denenberg VH & Anderson CO (1965) Rabbit: frequency of suckling in the pup. Science 150, 18351836.
67Cross BA (1977) Comparative physiology of milk removal. In Symposia of the Zoological Society of London, Comparitive Aspects of Lactation, vol. 41, pp. 193210 [Peaker M, editor]. London: Academic Press.
68Blanks AM, Shmygol A & Thornton S (2007) Regulation of oxytocin receptors and oxytocin receptor signaling. Semin Reprod Med 25, 5259.
69Prime D, Geddes D & Hartmann PE (2007) Oxytocin: milk ejection and maternal-infant well-being. In Hale and Hartmann's Textbook of Human Lactation, pp. 141155 [Hartmann PE and Hale T, editors]. Amarillo, TX: Hale Publishing.
70Argiolas A & Gessa GL (1991) Central functions of oxytocin. Neurosci Biobehav Rev 15, 217231.
71Tindal JS & Knaggs GS (1969) An ascending pathway for release of prolactin in the brain of the rabbit. J Endocrinol 45, 111120.
72Blanks AM, Shmygol A & Thornton S (2007) Regulation of oxytocin receptors and oxytocin receptor signaling. Semin Reprod Med 25, 5259.
73Smith KK (2001) Early development of the neural plate, neural crest and facial region of marsupials. J Anat 199, 121131.
74German RZ & Crompton AW (2000) The ontogeny of feeding in mammals. In Feeding Form, Function and Evolution in Tetrapod Vertebrates, pp. 449457 [Schwenk K, editor]. San Diego, CA: Academic Press.
75Wolf LS & Glass R (1992) Feeding and Swallowing Disorders in Infancy. Tuscon, AZ: Therapy Skill Builders.
76Ardran GM, Kemp FH & Lind J (1958) A cineradiographic study of breast feeding. Br J Radiol 31, 156162.
77Ardran GM, Kemp FH & Lind J (1958) A cineradiographic study of bottle feeding. Br J Radiol 31, 1122.
78Ardran GM & Kemp FH (1959) A correlation between suckling pressures and the movements of the tongue. Acta Paediatr 48, 261272.
79Geddes DT, Kent JC, Mitoulas LR, et al. . (2008) Tongue movement and intra-oral vacuum in breastfeeding infants. Early Hum Dev 84, 471477.
80Thexton AJ, Crompton AW, Owerkowicz T, et al. . (2004) Correlation between intraoral pressures and tongue movements in the suckling pig. Arch Oral Biol 49, 567575.
81Rasmussen MD & Mayntz M (1998) Pressure in the teat cistern and the mouth of the calf during suckling. J Dairy Res 65, 685692.
82Ramsay DT, Kent JC, Hartmann RA, et al. . (2005) Anatomy of the lactating human breast redefined with ultrasound imaging. J Anat 206, 525534.
83Hartmann PE & Hughes PE (1996) Lactation. In World Animal Science, Pig Production, vol. C10, pp. 89112 [Taverner MR, editor]. Amsterdam: Elsevier.
84Cannon JR, Bakker HR, Bradshaw SD, et al. . (1976) Gravity as the sole navigational aid to the newborn quokka. Nature 259, 42.
85Widstrom AM, Ransjo-Arvidson AB, Christensson K, et al. . (1987) Gastric suction in healthy newborn infants. Effects on circulation and developing feeding behaviour. Acta Paediatr Scand 76, 566572.
86Pereira M (2006) Aleitamento Materno (Maternal Breast-feeding). Loures, Portugal: Lusociência.
87Diamond JM (1987) Evolutionary adaptations. Aristotle's theory of mammalian teat number is confirmed. Nature 325, 200.
88Saint L, Maggiore P & Hartmann PE (1986) Yield and nutrient content of milk in eight women breast-feeding twins and one woman breast-feeding triplets. Br J Nutr 56, 4958.
89Prosser CG, Saint L & Hartmann PE (1984) Mammary gland function during gradual weaning and early gestation in women. Aust J Exp Biol Med Sci 62, 215228.
90Dewey KG & Lonnerdal B (1986) Infant self-regulation of breast milk intake. Acta Paediatr Scand 75, 893898.
91Sosa R, Klaus M & Urrutia JJ (1976) Feed the nursing mother, thereby the infant. J Pediatr 88, 668670.
92Prentice A, Paul A, Prentice A, et al. (1986) Cross-cultural differences in lactational performance. In Human Lactation 2, Maternal and Environmental Factors, pp. 1344 [Hamosh M and Goldman AS, editors]. New York: Plenum Press.
93Lonnerdal B (2000) Breast milk: a truly functional food. Nutrition 16, 509511.
94Arthur PG, Kent JC & Hartmann PE (1991) Metabolites of lactose synthesis in milk from women during established lactation. J Pediatr Gastroenterol Nutr 13, 260266.
95McVeagh P & Miller JB (1997) Human milk oligosaccharides: only the breast. J Paediatr Child Health 33, 281286.
96Patton S & Jensen R (1976) Biomedical Aspects of Lactation. With Special Reference to Lipid Metabolism and Membrane Functions of the Mammary Gland. Oxford: Pergamon Press.
97Pang WW & Hartmann PE (2007) Initiation of human lactation: secretory differentiation and secretory activation. J Mammary Gland Biol Neoplasia 12, 211221.
98Tyndale-Biscoe CH & Janssens PA (1988) The Developing Marsupial: Models for Biomedical Research. Berlin: Springer-Verlag.
99Jensen RG (1995) Handbook of Milk Composition. San Diego, CA: Academic Press.
100Coppa G, Gabrielli O, Pierani P, et al. . (1993) Changes in carbohydrate composition in human milk over 4 months of lactation. Pediatrics 91, 637641.
101Neville M, Allen J & Watters C (1983) The mechanisms of milk secretion. In Lactation: Physiology, Nutrition and Breastfeeding, pp. 49102 [Neville M and Neifert M, editors]. New York: Plenum Press.
102Lonnerdal B, Woodhouse LR & Glazier C (1987) Compartmentalization and quantitation of protein in human milk. J Nutr 117, 13851395.
103Shekar PC, Goel S, Rani SD, et al. . (2006) κ-Casein-deficient mice fail to lactate. Proc Natl Acad Sci U S A 103, 80008005.
104Holt C & Horne D (1996) The hairy casein micelle: evolution of the concept and its implication for dairy technology. Neth Milk Dairy J 50, 85111.
105Gooden JM, Brandon MR, Hartmann PE, et al. . (1971) Factors affecting lipid output and flow of thoracic duct lymph in newborn calves. Aust J Biol Sci 24, 13091318.
106Jordan SM & Morgan EH (1968) The changes in the serum and milk whey proteins during lactation and suckling in the quokka (Setonix brachyurus). Comp Biochem Physiol 25, 271283.
107Simpson KJ, Ranganathan S, Fisher JA, et al. . (2000) The gene for a novel member of the whey acidic protein family encodes three four-disulfide core domains and is asynchronously expressed during lactation. J Biol Chem 275, 2307423081.
108Piotte CP, Marshall CJ, Hubbard MJ, et al. . (1997) Lysozyme and α-lactalbumin from the milk of a marsupial, the common brush-tailed possum (Trichosurus vulpecula). Biochim Biophys Acta 1336, 235242.
109Hayssen V & Blackburn D (1985) α-Lactalbumin and the origins of lactation. Evolution 39, 11471149.
110Kontopidis G, Holt C & Sawyer L (2004) Invited review: β-lactoglobulin: binding properties, structure, and function. J Dairy Sci 87, 785796.
111Collet C, Joseph R & Nicholas K (1991) A marsupial β-lactoglobulin gene: characterization and prolactin-dependent expression. J Mol Endocrinol 6, 916.
112Hernández-Ledesma B, Recio I & Amigo L (2007) β-Lactoglobulin as source of bioactive peptides. Amino Acids 35, 257265.
113Martin JC, Bougnoux P, Antoine JM, et al. . (1993) Triacylglycerol structure of human colostrum and mature milk. Lipids 28, 637643.
114Breckenridge WC, Marai L & Kuksis A (1969) Triglyceride structure of human milk fat. Can J Biochem 47, 761769.
115Innis SM, Quinlan P & Diersen-Schade D (1993) Saturated fatty acid chain length and positional distribution in infant formula: effects on growth and plasma lipids and ketones in piglets. Am J Clin Nutr 57, 382390.
116Ogg SL, Weldon AK, Dobbie L, et al. . (2004) Expression of butyrophilin (Btn1a1) in lactating mammary gland is essential for the regulated secretion of milk-lipid droplets. Proc Natl Acad Sci U S A 101, 1008410089.
117Cavaletto M, Giuffrida MG, Giunta C, et al. . (1999) Multiple forms of lactadherin (breast antigen BA46) and butyrophilin are secreted into human milk as major components of milk fat globule membrane. J Dairy Res 66, 295301.
118Michalski MC, Briard V, Michel F, et al. . (2005) Size distribution of fat globules in human colostrum, breast milk, and infant formula. J Dairy Sci 88, 19271940.
119Czank C, Mitoulas L & Hartmann PE (2007) Human milk composition – fat. In Hale and Hartmann's Textbook of Human Lactation, pp. 4967 [Hartmann PE and Hale T, editors]. Amarillo, TX: Hale Publishing.
120Iverson SJ & Oftedal OT (1995) Comparative analysis of nonhuman milks. B. Phylogenetic and ecological variation in the fatty acid composition of milks. In Handbook of Milk Composition, pp. 789827 [Jensen RG, editor]. San Diego, CA: Academic Press.
121Hrboticky N, MacKinnon MJ & Innis SM (1990) Effect of vegetable oil formula rich in linoleic acid on tissue fatty acid accretion in the brain, liver, plasma, and erythrocytes of infant piglets. Am J Clin Nutr 51, 173182.
122Moir RJ, Sharman G, Somers M, et al. . (1954) Ruminant-like digestion in a marsupial. Nature 173, 269270.
123Hartman L, Shorland FB & McDonald IRC (1955) The trans-unsaturated acid contents of fats of ruminants and non-ruminants. Biochem J 61, 603607.
124Demarne Y, Lhuillery C, Pihet J, et al. . (1978) Comparative study of triacylglycerol fatty acids in the milk fat from two leporidae species: rabbit (Oryctolagus cuniculus) and hare (Lepus europaeus). Comp Biochem Physiol B 61, 223226.
125Cowie AT, Forsyth IA & Hart IC (1980) Monographs on Endocrinology, Hormonal Control of Lactation, vol. 15. Berlin: Springer-Verlag.
126Bell RG, Stephens CJ & Turner KJ (1974) Marsupial immunoglobulins: an immunoglobulin molecule resembling eutherian IgA in serum and secretions of Setonix brachyurus (Quokka). J Immunol 113, 371378.
127Brambell FWR (1970) The Transmission of Passive Immunity from Mother to Young. Amsterdam: North-Holland Publishing Company.
128Yadav M, Eadie M & Stanley NF (1972) The thymus glands of a marsupial, Setonix brachyurus (quokka) and their role in immune responses. VI. Maternal transfer of immunoglobulins. Aust J Exp Biol Med Sci 50, 347356.
129Yadav M & Eadie M (1973) Passage of maternal immunoglobulins to the pouch young of a marsupial, Setonix brachyurus. Aust J Zool 21, 171181.
130Yadav M (1971) The transmissions of antibodies across the gut of pouch-young marsupials. Immunology 21, 839851.
131Goldman AS, Chheda S & Garofalo R (1998) Evolution of immunologic functions of the mammary gland and the postnatal development of immunity. Pediatr Res 43, 155162.
132Newburg DS & Neubauer SH (1995) Carbohydrates in milks: analysis, quantities, and significance. In Handbook of Milk Composition, pp. 273349 [Jensen RG, editor]. San Diego, CA: Academic Press.
133Leman AD (1992) Optimizing farrowing rate and litter size and minimizing nonproductive sow days. Vet Clin North Am Food Anim Pract 8, 609621.
134Hanson L (2004) Immunobiology of Human Milk: How Breastfeeding Protects Babies. Amarillo, TX: Pharmasoft Publishing.
135Hanson L (2007) The role of breastfeeding in the defense of the infant. In Hale and Hartmann's Textbook of Human Lactation, pp. 159192 [Hartmann PE and Hale T, editors]. Amarillo, TX: Hale Publishing.
136Campbell DI, Bunn JE, Weaver LT, et al. . (2006) Human milk vacuolating cytotoxin A immunoglobulin A antibodies modify Helicobacter pylori infection in Gambian children. Clin Infect Dis 43, 10401042.
137Freed LM, Berkow SE, Hamosh P, et al. . (1989) Lipases in human milk: effect of gestational age and length of lactation on enzyme activity. J Am Coll Nutr 8, 143150.
138Czank C, Mitoulas L & Hartmann PE (2007) Human milk composition – carbohydrate. In Hale and Hartmann's Textbook of Human Lactation, pp. 6973 [Hartmann PE and Hale T, editors]. Amarillo, TX: Hale Publishing.
139Peaker M (1991) Production of hormones by the mammary gland: short review. Endocr Regul 25, 1013.
140Selman PJ (1995) Effects of progestin administration in the dog. PhD Thesis, Utrecht University, The Netherlands.
141Pearlman WH (1991) Hormones and tissue growth factors in milk: evolutionary implications. Endocr Regul 25, 49.
142Yadav M, Stanley NF & Waring H (1972) The microbial flora of the gut of the pouch-young and the pouch of a marsupial, Setonix brachyurus. J Gen Microbiol 70, 437442.
143Messer M & Elliott C (1987) Changes in α-lactalbumin, total lactose, UDP-galactose hydrolase and other factors in tammar wallaby milk (Macropus eugenii) during lactation. Aust J Biol Sci 40, 3746.
144Dellow DW & Hume ID (1982) Studies on the nutrition of macropodine marsupials IV. Digestion in the stomach and the intestine of Macropus giganteus, Thylogale thetis and Macropus eugenii. Aust J Zool 30, 767777.
145Lonnerdal B & Atkinson SA (1995) Human milk proteins. In The Handbook of Milk Composition, pp. 369387 [Jensen RG, editor]. New York: Academic Press.
146Bell SJ, Grochoski GT & Clarke AJ (2006) Health implications of milk containing β-casein with the A2 genetic variant. Crit Rev Food Sci Nutr 46, 93100.
147Ferrazzano GF, Cantile T, Ingenito A, et al. . (2007) New strategies in dental caries prevention: experimental study on casein phosphopeptides. Eur J Paediatr Dent 8, 183187.
148Brew K & Hill RL (1975) Lactose biosynthesis. Rev Physiol Biochem Pharmacol 72, 105158.
149Pellegrini A, Thomas U, Bramaz N, et al. . (1999) Isolation and identification of three bactericidal domains in the bovine α-lactalbumin molecule. Biochim Biophys Acta 1426, 439448.
150Bullen JJ, Rogers HJ & Leigh L (1972) Iron-binding proteins in milk and resistance to Escherichia coli infection in infants. BMJ 1, 6975.
151Oddy WH, Holt PG, Sly PD, et al. . (1999) Association between breast feeding and asthma in 6 year old children: findings of a prospective birth cohort study. BMJ 319, 815819.
152Lopez-Alarcon M, Villalpando S & Fajardo A (1997) Breast-feeding lowers the frequency and duration of acute respiratory infection and diarrhea in infants under six months of age. J Nutr 127, 436443.
153Isaacs CE, Thormar H & Pessolano T (1986) Membrane-disruptive effect of human milk: inactivation of enveloped viruses. J Infect Dis 154, 966971.
154Reiner DS, Wang CS & Gillin FD (1986) Human milk kills Giardia lamblia by generating toxic lipolytic products. J Infect Dis 154, 825832.
155Mather IH & Jack LJ (1993) A review of the molecular and cellular biology of butyrophilin, the major protein of bovine milk fat globule membrane. J Dairy Sci 76, 38323850.
156Morrison SD (1952) Human Milk: Yield, Proximate Principles and Inorganic Constituents. Farnham Royal, Bucks: Commonwealth Agricultural Bureaux.
157Green B, Merchant J & Newgrain K (1997) Lactational energetics of a marsupial carnivore, the eastern quoll (Dasyurus viverrinus). Aust J Zool 45, 295306.
158Janssens PA & Ternouth JH (1987) The transition from milk to forage diets. In Nutrition of Herbivores, pp. 281305 [Hacker JB and Ternouth JH, editors]. Sydney: Academic Press Australia.
159Lonnerdal B (1986) Effects of maternal dietary intake on human milk composition. J Nutr 116, 499513.
160Zavaleta N, Lanata C, Butron B, et al. . (1995) Effect of acute maternal infection on quantity and composition of breast milk. Am J Clin Nutr 62, 559563.
161Lonnerdal B, Zavaleta N, Kusunoki L, et al. . (1996) Effect of postpartum maternal infection on proteins and trace elements in colostrum and early milk. Acta Paediatr 85, 537542.
162Ahnadi CE, Beswick N, Delbecchi L, et al. . (2002) Addition of fish oil to diets for dairy cows. II. Effects on milk fat and gene expression of mammary lipogenic enzymes. J Dairy Res 69, 521531.
163Peterson DG, Matitashvili EA & Bauman DE (2003) Diet-induced milk fat depression in dairy cows results in increased trans-10, cis-12 CLA in milk fat and coordinate suppression of mRNA abundance for mammary enzymes involved in milk fat synthesis. J Nutr 133, 30983102.
164Silber GH, Hachey DL, Schanler RJ, et al. . (1988) Manipulation of maternal diet to alter fatty acid composition of human milk intended for premature infants. Am J Clin Nutr 47, 810814.
165Insull W Jr & Ahrens EH Jr (1959) The fatty acids of human milk from mothers on diets taken ad libitum. Biochem J 72, 2733.
166Daly SE, Di Rosso A, Owens RA, et al. . (1993) Degree of breast emptying explains changes in the fat content, but not fatty acid composition, of human milk. Exp Physiol 78, 741755.
167Knight CH (1999) Metabolic stress unravelled. In Hannah Research Institute Yearbook, pp. 3237. Ayr, UK: Hannah Research Institute.
168Auldist DE & King RH (1995) Piglets' role in determining milk production in the sow. In Manipulating Pig Production V: Proceedings of the Fifth Biennial Conference of the Australasian Pig Science Association, pp. 114118 [Hennessy DP and Cranwell PD, editors]. Werribee: Australasian Pig Science Association.
169Knight CH & Peaker M (1982) Compensatory increases in milk yield after hemimastectomy in lactating goats. J Physiol (Lond) 329, 36P.
170Atwood CS & Bowen RL (2007) Metabolic clues regarding the enhanced performance of elite endurance athletes from orchiectomy-induced hormonal changes. Med Hypotheses 68, 735749.
171Rudolph MC, McManaman JL, Phang T, et al. . (2007) Metabolic regulation in the lactating mammary gland: a lipid synthesizing machine. Physiol Genomics 28, 323336.
172McClellan HL, Prime DK, Geddes DT, et al. (2008) Breastfeeding with persistent pain: frequency, duration and volume. In The Science of Human Lactation: Foundations of Clinical Practice, pp. 9293. Perth, WA: ISRHML, 2008 International Society for Research in Human Milk and Lactation 14th Biennial Conference, abstract 92. http://www.liebertonline.com/doi/pdfplus/10.1089/bfm.2008.8000.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Nutrition Research Reviews
  • ISSN: 0954-4224
  • EISSN: 1475-2700
  • URL: /core/journals/nutrition-research-reviews
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords:

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 35
Total number of PDF views: 334 *
Loading metrics...

Abstract views

Total abstract views: 355 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 20th October 2017. This data will be updated every 24 hours.