Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Effects of maternal undernutrition during late gestation and/or lactation on colostrum synthesis and immunological parameters in the offspring

S. Chadio A E , A. Katsafadou A , B. Kotsampasi B , G. Michailidis C , K. C. Mountzouris D , D. Kalogiannis A and V. Christodoulou B

A Department of Anatomy and Physiology of Domestic Animals, Faculty of Animal Science and Aquaculture, Agricultural University of Athens, 75, Iera Odos, Athens 11855, Greece.

B Animal Research Institute, General Directory of Agricultural Research, Hellenic Agricultural Organisation-DEMETER, Paralimni Giannitsa 58100, Greece.

C Department of Animal Production, School of Agriculture, Aristotle University of Thessaloniki, Thessaloniki 54124, Greece.

D Department of Nutritional Physiology and Feeding, Faculty of Animal Science and Aquaculture, Agricultural University of Athens, 75, Iera Odos, Athens 11855, Greece.

E Corresponding author. Email: shad@aua.gr

Reproduction, Fertility and Development 28(3) 384-393 http://dx.doi.org/10.1071/RD14147
Submitted: 5 May 2014  Accepted: 13 June 2014   Published: 1 August 2014

Abstract

The emerging immune system is vulnerable to insult not only during fetal life, but also through colostrum transfer of maternal factors with immunomodulatory functions. The aim of the present study was to examine the effects of maternal undernutrition during late gestation and/or lactation on colostrum and milk synthesis, as well as on immunological parameters in offspring. Pregnant ewes were fed to 100% of nutrient requirements throughout pregnancy and lactation (Control) or to 50% during lactation (R1) or during the last 20 days of pregnancy and lactation (R2). Colostrum samples were collected 3 and 18 h after parturition and thymus glands were obtained from 5-month-old offspring. Lamb birthweight did not differ between groups, whereas growth rate was significantly lower in males in the R1 group and in females in both undernourished groups. There was a significant reduction in lactose percentage in the 18-h colostrum of the R2 group. The IgG concentration, as a percentage of protein, was significantly increased in 3-h colostrum samples of the R2 group. Quantitative polymerase chain reaction analysis revealed a significant increase in the expression of Toll-like receptor (TLR) 2, TLR4 and TLR9 in the thymus gland of female lambs in both undernourished groups. In conclusion, early life nutritional imbalances may impact on immune system function in later life due to programming effects.

Additional keywords: IgG, interleukin-10, Toll-like receptors.


References

Addah, W., Karikari, P. K., and Baah, J. (2012). Under nutrition in the ewe: foeto-placental adaptation, and modulation of lamb birth weight: a review. Liv. Res. Rur. Develop. 24, 161. open url image1

Association of Official Analytical Chemists (AOAC). (1990). ‘Official Methods of Analysis.’ (AOAC: Arlington, VA.)

Barker, D. J., Osmond, C., and Law, C. M. (1989). The intrauterine and early postnatal origins of cardiovascular disease and chronic bronchitis. J. Epidemiol. Community Health 43, 237–240.
The intrauterine and early postnatal origins of cardiovascular disease and chronic bronchitis.CrossRef | 1:STN:280:DyaK3c7htFGqsQ%3D%3D&md5=6d5abbfb1ce3a52aaf93ddcff792ce63CAS | 2607302PubMed | open url image1

Bartol, F. F., Wiley, A. A., Miller, D. J., Silva, A. J., Roberts, K. E., Davolt, M. L. P., Chen, J. C., Frankshun, A. L., Camp, M. E., Rahman, K. M., Vallet, J. L., and Bagnell, C. A. (2013). Lactation Biology Symposium: lactocrine signaling and developmental programming. J. Anim. Sci. 91, 696–705.
Lactation Biology Symposium: lactocrine signaling and developmental programming.CrossRef | 1:CAS:528:DC%2BC3sXlvVKnu78%3D&md5=0e622eae7fdc45589dd3c33ab1682f66CAS | 23100582PubMed | open url image1

Baumrucker, C. R., Burkett, A. M., Magliaro-Macrina, A. L., and Dechow, C. D. (2010). Colostrogenesis: mass transfer of immunoglobulin G1 into colostrums. J. Dairy Sci. 93, 3031–3038.
Colostrogenesis: mass transfer of immunoglobulin G1 into colostrums.CrossRef | 1:CAS:528:DC%2BC3cXhtVOhtrjI&md5=3a9d78779ce7980db8cb221421c73bd7CAS | 20630219PubMed | open url image1

Behringer, R. R., Eakin, G. S., and Renfree, M. B. (2006). Mammalian diversity: gametes, embryos and reproduction. Reprod. Fertil. Dev. 18, 99–107.
Mammalian diversity: gametes, embryos and reproduction.CrossRef | 16478607PubMed | open url image1

Bell, A. W., and Bauman, D. E. (1997). Adaptations of glucose metabolism during pregnancy and lactation. J. Mammary Gland Biol. Neoplasia 2, 265–278.
Adaptations of glucose metabolism during pregnancy and lactation.CrossRef | 1:STN:280:DC%2BD3czosF2htg%3D%3D&md5=fccf42c310d87dd4baca628798704f2bCAS | 10882310PubMed | open url image1

Bocquier, F., and Caja, G. (2000). Effects of nutrition on the composition of sheep’s milk. In: ‘Sheep and Goat Nutrition: Intake, Digestion, Quality of Products and Rangelands’. (Eds I. Ledin and P. Morand-Fehr.) pp. 59–74. (CIHEAM: Zaragoza.)

Brandtzaeg, P. (2003). Mucosal immunity: integration between mother and the breast-fed infant. Vaccine 21, 3382–3388.
Mucosal immunity: integration between mother and the breast-fed infant.CrossRef | 1:CAS:528:DC%2BD3sXlt1eisLg%3D&md5=38b27f63b696ed5d032cfa9e79fa5619CAS | 12850345PubMed | open url image1

British Standards Insitution (BSI) (1955). ‘British Standards Institution Gerber Method for the Determination of Fat in Milk Products. BS 696.’ (BSI: London.)

Burton, J. H., Hosein, A. A., McMillan, L., Grieve, D. G., and Wilkie, B. N. (1984). Immunoglobulin absorption in calves as influenced by dietary protein intakes of their dams. Can. J. Anim. Sci. 64, 185–186.
Immunoglobulin absorption in calves as influenced by dietary protein intakes of their dams.CrossRef | open url image1

Butterworth, M., McClellan, B., and Allansmith, M. (1967). Influence of sex in immunoglobulin levels. Nature 214, 1224–1225.
Influence of sex in immunoglobulin levels.CrossRef | 1:STN:280:DyaF1c%2FovFKiuw%3D%3D&md5=de1ac4a28aa9f28aeb8a05e7c428ba4cCAS | 4169229PubMed | open url image1

Cao, G., Alessio, H. M., and Cutler, R. G. (1993). Oxygen-radical absorbance capacity assay for antioxidants. Free Radic. Biol. Med. 14, 303–311.
Oxygen-radical absorbance capacity assay for antioxidants.CrossRef | 1:CAS:528:DyaK3sXksVClsrk%3D&md5=c90d25dd537691e9a18997839556c1e2CAS | 8458588PubMed | open url image1

Castellote, C., Casillas, R., Ramírez-Santana, C., Pérez-Cano, F. J., Castell, M., Moretones, M. G., López-Sabater, M. C., and Franch, A. (2011). Premature delivery influences the immunological composition of colostrum and transitional and mature human milk. J. Nutr. 141, 1181–1187.
Premature delivery influences the immunological composition of colostrum and transitional and mature human milk.CrossRef | 1:CAS:528:DC%2BC3MXmvFehtb0%3D&md5=8cde536aa75feb89dda58d31e194087bCAS | 21508211PubMed | open url image1

Chadio, S., and Kotsampasi, B. (2014). The role of early life nutrition in programming of reproductive function. J. Dev. Orig. Health Dis. 5, 2–15.
The role of early life nutrition in programming of reproductive function.CrossRef | 1:STN:280:DC%2BC2cjkvFOisA%3D%3D&md5=45c502adb60be2b1cfb651f70126a5faCAS | 24847686PubMed | open url image1

Chang, J.-S., Russell, G. C., Jann, O., Glass, E. J., Werling, D., and Haig, D. M. (2009). Molecular cloning and characterization of Toll-like receptors 1–10 in sheep. Vet. Immunol. Immunopathol. 127, 94–105.
Molecular cloning and characterization of Toll-like receptors 1–10 in sheep.CrossRef | 1:CAS:528:DC%2BD1cXhsFChtbfL&md5=de4d39573780bbdb1b53dc1451c48935CAS | 19004506PubMed | open url image1

European Parliament and of the Council of the European Union (2010). Directive 2010/63/EU of the European Parliament and of the Council of 22 September 2010 on the protection of animals used for scientific purposes. Available at: http://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32010L0063&from=EN [Verified January 2014].

Field, C. J. (2005). The immunological components of human milk and their effect on immune development in infants. J. Nutr. 135, 1–4.
| 1:CAS:528:DC%2BD2MXltlyluw%3D%3D&md5=9711c976c1434b4f2f59431634143547CAS | 15623823PubMed | open url image1

Fleming, T. P., Velazquez, M. A., Eckert, J. J., Lucas, E. S., and Watkins, A. J. (2012). Nutrition of females during the peri-conceptional period and effects on foetal programming and health of offspring. Anim. Reprod. Sci. 130, 193–197.
Nutrition of females during the peri-conceptional period and effects on foetal programming and health of offspring.CrossRef | 1:STN:280:DC%2BC38zht1ekuw%3D%3D&md5=dc39ee93700d8231386a1b0f330871a5CAS | 22341375PubMed | open url image1

Gao, F., Hou, X. Z., Liu, Y. C., Wu, S. Q., and Ao, C. J. (2008). Effect of maternal under nutrition during late pregnancy on lamb birth weight. Asian-Austr. J. Anim. Sci. 21, 371–375. open url image1

Garofalo, R., Cheda, S., Mei, F., Palkowetz, K. H., Rudloff, H. E., Schmalstieg, F. C., Rassin, D. K., and Goldman, A. S. (1995). Interleukin-10 in human milk. Pediatr. Res. 37, 444–449.
Interleukin-10 in human milk.CrossRef | 1:CAS:528:DyaK2MXlt1els70%3D&md5=ab792204fc4d5bc9c2031b698fdd4aa3CAS | 7596683PubMed | open url image1

Grundbacher, F. J. (1972). Human X chromosome carries quantitative genes for immunoglobulin M. Science 176, 311–312.
Human X chromosome carries quantitative genes for immunoglobulin M.CrossRef | 1:STN:280:DyaE387mtlejuw%3D%3D&md5=5d1e63d32a469ae7e068fd581cb8effeCAS | 5019789PubMed | open url image1

Hammer, C. J., Thorson, J. F., Meyer, A. M., Redmer, D. A., Luther, J. S., Neville, T. L., Reed, J. J., Reynolds, L. P., Caton, J. S., and Vonnahme, K. A. (2011). Effects of maternal selenium supply and plane of nutrition during gestation on passive transfer of immunity and health in neonatal lambs. J. Anim. Sci. 89, 3690–3698.
Effects of maternal selenium supply and plane of nutrition during gestation on passive transfer of immunity and health in neonatal lambs.CrossRef | 1:CAS:528:DC%2BC3MXhsVSqsrvP&md5=82d9afd36d46c6d24663ea2f86348cbcCAS | 21724938PubMed | open url image1

Hough, R. L., McCarthy, F. D., Kent, H. D., Eversole, D. E., and Wahlberg, M. L. (1990). Influence of nutritional restriction during late gestation on production measures and passive immunity in beef cattle. J. Anim. Sci. 68, 2622–2627.
| 1:STN:280:DyaK3M%2FgvVOhsA%3D%3D&md5=7d9f3800e02872f71f15d6b4b24aa651CAS | 2211390PubMed | open url image1

International Dairy Federation (IDF) (1993). ‘International Dairy Federation Determination of the Nitrogen Content of Milk, Kjeldahl Method, International Standard FID-IDF 20b, Part 1.’ (IDF: Brussels.)

Kotsampasi, B., Chadio, S., Papadomichelakis, G., Deligeorgis, S., Kalogiannis, D., Menegatos, I., and Zervas, G. (2009a). Effects of maternal undenutrition on the hypothalamic–pituitary–gonadal axis function in female sheep offspring. Reprod. Domest. Anim. 44, 677–684.
Effects of maternal undenutrition on the hypothalamic–pituitary–gonadal axis function in female sheep offspring.CrossRef | 1:CAS:528:DC%2BD1MXhtVaiurbM&md5=4bd693a364b8c106f424fde3b306e347CAS | 19642222PubMed | open url image1

Kotsampasi, B., Balaskas, C., Papadomichelakis, G., and Chadio, S. E. (2009b). Reduced Sertoli cell number and altered pituitary responsiveness in male lambs undernourished in uterο. Anim. Reprod. Sci. 114, 135–147.
Reduced Sertoli cell number and altered pituitary responsiveness in male lambs undernourished in uterο.CrossRef | 1:CAS:528:DC%2BD1MXms1yqu7c%3D&md5=a9e205a7a9ba3ac789031b2eb6fe78b9CAS | 18814977PubMed | open url image1

Kuypers, E., Collins, J. J. P., Jellema, R. K., Wolfs, T. G. A. M., Kemp, M. W., Nitsos, I., Pillow, J. J., Polglase, G. R., Newnham, J. P., Germeraad, W. T. V., Kallapur, S. G., Jobe, A. H., and Kramer, B. W. (2012). Ovine fetal thymus response to lipopolysaccharide-induced chorioamnionitis and antenatal corticosteroids. PLoS ONE 7, e38257.
Ovine fetal thymus response to lipopolysaccharide-induced chorioamnionitis and antenatal corticosteroids.CrossRef | 1:CAS:528:DC%2BC38XotlCrs7c%3D&md5=b4ad293714d46b1a81aa4bb769a207efCAS | 22693607PubMed | open url image1

Lichtman, M. A., Vaughan, J. H., and Hames, C. G. (1967). The distribution of serum immunoglobulins, anti-gamma-G globulins (‘rheumatoid factors’) and antinuclear antibodies in White and Negro subjects in Evans County, Georgia. Arthritis Rheum. 10, 204–215.
The distribution of serum immunoglobulins, anti-gamma-G globulins (‘rheumatoid factors’) and antinuclear antibodies in White and Negro subjects in Evans County, Georgia.CrossRef | 1:CAS:528:DyaF1cXitVGntg%3D%3D&md5=227ebde2c04d8628a3319280d088e408CAS | 4165682PubMed | open url image1

Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2 (2Delta Delta C(T)) method. Methods 25, 402–408.
Analysis of relative gene expression data using real-time quantitative PCR and the 2 (2Delta Delta C(T)) method.CrossRef | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=224f15b9dfd00d92fda868e1cb065922CAS | 11846609PubMed | open url image1

Marriott, I., and Huet-Hudson, Y. M. (2006). Sexual dimorphism in innate immune responses to infectious organisms. Immunol. Res. 34, 177–192.
Sexual dimorphism in innate immune responses to infectious organisms.CrossRef | 1:CAS:528:DC%2BD28Xot1Gqtb8%3D&md5=684b93ff69ea125d73c71e4877444052CAS | 16891670PubMed | open url image1

McDade, T. W. (2005). Life history, maintenance, and the early origins of immune function. Am. J. Hum. Biol. 17, 81–94.
Life history, maintenance, and the early origins of immune function.CrossRef | 15612049PubMed | open url image1

McDade, T. W., Kuzawa, C. W., Beck, M. A., and Adair, L. S. (2004). Prenatal and early postnatal environments are significant predictors of total IgE concentration in Filipino adolescents. Clin. Exp. Allergy 34, 44–50.
Prenatal and early postnatal environments are significant predictors of total IgE concentration in Filipino adolescents.CrossRef | 1:STN:280:DC%2BD2c%2Fms1Kmsw%3D%3D&md5=683cfbb942d0c37234ebce164b8da65bCAS | 14720261PubMed | open url image1

McMillen, I. C., and Robinson, J. S. (2005). Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol. Rev. 85, 571–633.
Developmental origins of the metabolic syndrome: prediction, plasticity, and programming.CrossRef | 1:CAS:528:DC%2BD2MXjt12lsLw%3D&md5=e60f1e5087cede1852b656d288b1cc2dCAS | 15788706PubMed | open url image1

Mellor, D. J. (1987). Nutritional effects on the fetus and mammary gland during pregnancy. Proc. Nutr. Soc. 46, 249–257.
Nutritional effects on the fetus and mammary gland during pregnancy.CrossRef | 1:STN:280:DyaL2szhslOisg%3D%3D&md5=e866ec0fc417eb1d257330f8c8973300CAS | 3306690PubMed | open url image1

Mellor, D. J., and Murray, L. (1985). Effects of maternal nutrition on udder development during late pregnancy and on colostrum production in Scottish blackface with twin lambs. Res. Vet. Sci. 39, 230–234.
| 1:STN:280:DyaL28%2FmvFChsg%3D%3D&md5=719483ab346e29ca1b2c492eed7b4996CAS | 4070789PubMed | open url image1

Meyer, A. M., Reed, J. J., Neville, T. L., Thorson, J. F., Maddock-Carlin, K. R., Taylor, J. B., Reynolds, L. P., Redmer, D. A., Luther, J. S., Hammer, C. J., Vonnahme, K. A., and Caton, J. S. (2011). Nutritional plane and selenium supply during gestation affect yield and nutrient composition of colostrum and milk in primiparous ewes. J. Anim. Sci. 89, 1627–1639.
Nutritional plane and selenium supply during gestation affect yield and nutrient composition of colostrum and milk in primiparous ewes.CrossRef | 1:CAS:528:DC%2BC3MXls1OhsrY%3D&md5=ce2a3d6227848fba6abb3ddb295738a2CAS | 21521822PubMed | open url image1

Navarro-Ruiz, M., Hernandez-Aguilar, T., Rodrıguez-Castellano, P., Lopez-Jaen, A. B., Valls-Belles, V., and Codoñer-Franch, P. (2013). Antioxidant capacity of colostrum milk is influenced by maternal diet. Proc. Nutr. Soc. 72, E37.
Antioxidant capacity of colostrum milk is influenced by maternal diet.CrossRef | open url image1

National Research Council (NRC) (1985). ‘Nutrient Requirements of Sheep. Sixth Revised Edition.’ (The National Academies Press: Washington, DC.)

Palmer, A. C. (2011). Nutritionally mediated programming of the developing immune system. Adv. Nutr. 2, 377–395.
Nutritionally mediated programming of the developing immune system.CrossRef | 1:CAS:528:DC%2BC3MXhtlOnsbbM&md5=45c675aded038bbfb6d48f62fbd1de67CAS | 22332080PubMed | open url image1

Quiles, J. L., Ochoa, J. J., Ramirez-Tortosa, M. C., Linde, J., Bompadre, S., Battino, M., Narbona, E., Maldonado, J., and Mataix, J. (2006). Coenzyme Q concentration and total antioxidant capacity of human milk at different stages of lactation in mothers of preterm and full-term infants. Free Radic. Res. 40, 199–206.
Coenzyme Q concentration and total antioxidant capacity of human milk at different stages of lactation in mothers of preterm and full-term infants.CrossRef | 1:CAS:528:DC%2BD2MXhtlGht7vI&md5=20a02b88275b252725eb0e6b548bd98bCAS | 16390829PubMed | open url image1

Rettew, J. A., Huet-Hudson, Y. M., and Marriott, I. (2008). Testosterone reduces macrophage expression in the mouse of Toll-like receptor 4, a trigger for inflammation and innate immunity. Biol. Reprod. 78, 432–437.
Testosterone reduces macrophage expression in the mouse of Toll-like receptor 4, a trigger for inflammation and innate immunity.CrossRef | 1:CAS:528:DC%2BD1cXisFSltbg%3D&md5=749271ae2b5acccb031d51476e7d6307CAS | 18003947PubMed | open url image1

Rousset, F., Garcia, E., and Banchereau, J. (1991). Cytokine-induced proliferation and immunoglobulin production of human B lymphocytes triggered through their CD40 antigen. J. Exp. Med. 173, 705–710.
Cytokine-induced proliferation and immunoglobulin production of human B lymphocytes triggered through their CD40 antigen.CrossRef | 1:CAS:528:DyaK3MXhsVWisro%3D&md5=d3fc8599abd76525efb5f61c2aff2931CAS | 1705282PubMed | open url image1

Shafer-Weaver, K. A., Corl, C. M., and Sordillo, L. M. (1999). Shifts in bovine CD4+ subpopulations increase T-helper-2 compared with T-helper-1 effector cells during the postpartum period. J. Dairy Sci. 82, 1696–1706.
Shifts in bovine CD4+ subpopulations increase T-helper-2 compared with T-helper-1 effector cells during the postpartum period.CrossRef | 1:CAS:528:DyaK1MXlsVyktbk%3D&md5=2492fbda3ac14c97eb2c7ad7ebf27a07CAS | 10480095PubMed | open url image1

Simos, Y., Metsios, A., Verginadis, I., D’Alessandro, A. G., Loiudice, P., Jirillo, E., Charalampidis, P., Kouimanis, V., Boulaka, A., Martemucci, G., and Karkabounas, S. (2011). Antioxidant and anti-platelet properties of milk from goat, donkey and cow: an in vitro, ex vivo and in vivo study. Int. Dairy J. 21, 901–906.
Antioxidant and anti-platelet properties of milk from goat, donkey and cow: an in vitro, ex vivo and in vivo study.CrossRef | 1:CAS:528:DC%2BC3MXhtVeit7rE&md5=66612840354a095242cb96433a950f33CAS | open url image1

SPSS Inc. (2006). ‘SPSS for Windows, Release 13.0.1.’ (SPSS Inc.: Chicago.)

Swanson, T. J., Hammer, C. J., Luther, J. S., Carlson, D. B., Taylor, J. B., Redmer, D. A., Neville, T. L., Reed, J. J., Reynolds, L. P., Caton, J. S., and Vonnahme, K. A. (2008). Effect of gestational plane of nutrition and selenium supplementation on mammary development and colostrum quality in pregnant ewe lambs. J. Anim. Sci. 86, 2415–2423.
Effect of gestational plane of nutrition and selenium supplementation on mammary development and colostrum quality in pregnant ewe lambs.CrossRef | 1:CAS:528:DC%2BD1cXhtFansbvN&md5=12866b5dcf17b0e8c29f0afcf068b095CAS | 18441080PubMed | open url image1

Takeuchi, O., and Akira, S. (2010). Pattern recognition receptors and inflammation. Cell 140, 805–820.
Pattern recognition receptors and inflammation.CrossRef | 1:CAS:528:DC%2BC3cXlsVSgu74%3D&md5=49b460f3a1b820890e8f1f7be19e458fCAS | 20303872PubMed | open url image1

Tirumurugaan, K. G., Dhanasekaran, S., Dhinakar Raj, G., Raja, A., Kumanan, K., and Ramaswamy, V. (2010). Differential expression of toll-like receptor mRNA in selected tissues of goat (Capra hircus). Vet. Immunol. Immunopathol. 133, 296–301.
Differential expression of toll-like receptor mRNA in selected tissues of goat (Capra hircus).CrossRef | 1:CAS:528:DC%2BD1MXhs1Wns7vM&md5=2a0a59f8f672b49b63b5156c8a1aa8feCAS | 19748133PubMed | open url image1

Tygesen, M. P., Nielsen, M. O., Norgaard, O., Ranvig, H., Harisson, A. P., and Tauson, A. H. (2008). Late gestational nutrient restriction: effects on ewes’ metabolic and homeorhetic adaptation, consequences for lamb birth weight and lactation performance. Arch. Anim. Nutr. 62, 44–59.
Late gestational nutrient restriction: effects on ewes’ metabolic and homeorhetic adaptation, consequences for lamb birth weight and lactation performance.CrossRef | 1:CAS:528:DC%2BD1cXht1Snug%3D%3D&md5=e35a7897291b8f3ad0f66ab193b67e1eCAS | 18341079PubMed | open url image1

Van Soest, P. J., Robertson, J. B., and Lewis, B. A. (1991). Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. J. Dairy Sci. 74, 3583–3597.
Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition.CrossRef | 1:STN:280:DyaK38%2FnvVCltA%3D%3D&md5=fcff29f51386ede2dc603370981d6116CAS | 1660498PubMed | open url image1

Wadhwa, P. D., Buss, C., Entringer, S., and Swanson, J. M. (2009). Developmental origins of health and disease: brief history of the approach and current focus on epigenetic mechanisms. Semin. Reprod. Med. 27, 358–368.
Developmental origins of health and disease: brief history of the approach and current focus on epigenetic mechanisms.CrossRef | 1:CAS:528:DC%2BD1MXhtFOis7zN&md5=a61a6d8cb8f17463a9a8ae17ebcde697CAS | 19711246PubMed | open url image1

Yilmaz, H. L., Saygili-Yilmaz, E. S., and Gunesacar, R. (2007). Interleukin-10 and -12 in human milk at 3 stages of lactation: a longitudinal study. Adv. Ther. 24, 603–610.
Interleukin-10 and -12 in human milk at 3 stages of lactation: a longitudinal study.CrossRef | 1:CAS:528:DC%2BD2sXhtVWnt7%2FK&md5=9e21b18fe4c626907c442d9c3c21ed8bCAS | 17660171PubMed | open url image1

Zanardo, V., Golin, R., Amato, M., Trevisanuto, D., Favaro, F., Faggian, D., and Plebani, M. (2007). Cytokines in human colostrum and neonatal jaundice. Pediatr. Res. 62, 191–194.
Cytokines in human colostrum and neonatal jaundice.CrossRef | 1:CAS:528:DC%2BD2sXnslKqtL0%3D&md5=159efafb20ff2e4d9265eb840fc1fc0eCAS | 17597660PubMed | open url image1

Zulueta, A., Maurizi, A., Frigola, A., Esteve, M. J., Coli, R., and Burini, G. (2009). Antioxidant capacity of cow milk, why and deproteinized milk. Int. Dairy J. 19, 380–385.
Antioxidant capacity of cow milk, why and deproteinized milk.CrossRef | 1:CAS:528:DC%2BD1MXkslKmtrY%3D&md5=1c8ae97a334483c9580e141687b5ddc0CAS | open url image1



Export Citation