Patin (Pangasius hypophthalmus) fish protein concentrate alters insulin-like growth factor (IGF)-1 and igf binding protein (IGFBP)-3 level of sprague dawley neonate rats-induced malnutrition
DOI:
https://doi.org/10.5219/1394Keywords:
FPC, Malnutrition, IGF-1, IGFBP-3Abstract
Malnutrition is caused by inadequate protein intake and affects growth factor. High protein from patin (Pangasius hypophthalmus) fish is a well-known protein source. This study aims to investigate the effect of patin fish protein concentrate (PFPC) in the IGF-1 and IGFBP-3 level of Sprague Dawley (SD) neonate rats-induced malnutrition. Thirty male SD neonate rats were divided randomly into five groups, namely normal control (K1), malnutrition control (K2), malnutrition with PFPC 13.26 mg.g-1 body weight (BW)/day (X1), malnutrition with PFPC 19.89 mg.g-1 BW/d (X2), and malnutrition with casein supplement 13.26 mg.g-1 BW/d (X3). K1 received a standard diet, while the others received a low 8% protein diet (L8PD) since those were born until 21 days. The standard diet was refed for all groups during the intervention (14 days). IGF-1 and IGFBP-3 levels were measured by ELISA. Normal data were analyzed by using One-way ANOVA which then was followed by post-hoc Bonferroni. Meanwhile, the others were analyzed by Kruskal Wallis and followed by Mann-Whitney U-test. Spearman test was used for correlation. PFPC contained 81.07% of protein, 4.08% of fat, 7.24% of moisture, 2.77% of ash, and 4.83% of carbohydrate. These contents had affected the growth factor. As a result, in the PFPC intervention, IGF-1, and IGFBP-3 levels (p <0.05) were decreased, while the controls were increased. The decreased values were shown in IGFBP-3 levels (p <0.05) while the increase was shown in both controls. On the other hand, the increase in body weight was shown in all groups, including control ones. A strong correlation was found between IGF-1 and IGFBP-3. PFPC has additional value on repairing malnutrition that is the best dose in effecting IGF-1 dan IGFBP3 levels is 13.26 mg.g-1 BW/d.
Downloads
Metrics
References
Aheto, J. M., Keegan, T. J., Taylor, B. M., Diggle, P. J. 2015. Childhood Malnutrition and Its Determinants among Under-Five Children in Ghana, Pediatric and Perinatal Epidemiology, Perinatal and Chilhood Outcome, vol. 29, no. 6, p. 552-561. https://doi.org/10.1111/ppe.12222 DOI: https://doi.org/10.1111/ppe.12222
Alishahi, A., Roshan, V. D., Hedayyati, M. 2013. Pretreatment Effects of Regular Aerobic Training on the IGF System and Hepatotoxicity Induced by Doxorubicin in Rats, Asian Pacific Journal of Cancer Prevention, vol. 14, no. 12, p. 7427-7431. https://doi.org/10.7314/APJCP.2013.14.12.7427 DOI: https://doi.org/10.7314/APJCP.2013.14.12.7427
Anthony, J. C., Yoshizawa, F., Anthony, T. G., Vary, T. C., Jefferson, L. S., Kimball, S. R. 2000. Leucine stimulates translation initiation in skeletal muscle of post-absortive rats via a rapamycin-sensitive pathwa, Journal of Nutrition, vol. 130, no. 10, p. 2413-2419. https://doi.org/10.1093/jn/130.10.2413 DOI: https://doi.org/10.1093/jn/130.10.2413
AOAC 2005. Official Methods of Analysis of AOAC International, AOAC Inc., 18th edn, Maryland, USA, AOAC International. .
AOAC International 2006. 45.3.06 AOAC Official Method 991.29 True Protein Digestibility of Foods and Food Ingredients Rat Bioassay First Action 1991, Washington DC, USA.
Bang, P., Brismar, K., Rosenfeld, R. G. 1994. Increased proteolysis of insulin-like growth factor-binding protein-3 (IGFBP-3) in noninsulin deendent diabetes mellitus serum, with elevation of a 29-kilodalton (kDa) glycosylated IGFBP-3 fragment contained in the approxymately 130-to 150-kDa ternary complex, The journal of clinical endocrinology and metabolism, vol. 78, no. 5, p. 1119-1127. https://doi.org/10.1210/jcem.78.5.7513716 DOI: https://doi.org/10.1210/jc.78.5.1119
Bartz, S., Mody, A., Hornik, C., Bain, J., Muehlbauer, M., Kiyimba, T., Kiboneka, E., Stevens, R., St Peter, J. V., Newgard, C. B., Freemark, M. 2014. Severe acute malnutritio in childhood: hormonal and metabolic status at presentation, response to treatment, and predictors of mortality, The Journal of Clinical Endocrinology and Metabolism, Endocrine Research, vol. 99, no. 6, p. 2128-2137. https://doi.org/10.1210/jc.2013-4018 DOI: https://doi.org/10.1210/jc.2013-4018
Bereket, A., Lang, C. H., Blethen, S. L., Fan, J., Frost, R. A., Wilson, T. A. 1995. Insulin-like growth factor binding protein-3 proteolysis in children with insulin-dependent diabetes mellitus: a possible role for insulin in the regulation of IGFBP-3 protease activity, The Journal of Clinical Endocrinology and Metabolism, vol. 80, no. 8, p. 2282-2288. https://doi.org/10.1210/jcem.80.8.7543110 DOI: https://doi.org/10.1210/jcem.80.8.7543110
Blossner, M., De Onis, M. 2005. Malnutrition : Quantifying the health impact at national and local levels, Environmental Burden of Disease, Geneva, World Health Organization Nutrition for Health Development Protection of the Human Environtment. Available at https://apps.who.int/iris/bitstream/handle/10665/43120/9241591870.pdf
Bonefeld, K., Moller, S. 2011. Insulin-like growth factor-I and the liver, Liver International, vol. 31, no. 7, p. 911-919. https://doi.org/10.1111/j.1478-3231.2010.02428.x DOI: https://doi.org/10.1111/j.1478-3231.2010.02428.x
Caregaro, L., Favaro, A., Santonastaso, P., Alberino, F., De Pascoli, L., Nardi, M., Favaro, S., Gatta, A. 2001. Insulin-like growth factor 1 (IGF-1), a nutritional marker in patients with eating disorders, Clinical Nutrition, vol. 20, no. 3, p. 251-257. https://doi.org/10.1054/clnu.2001.0397 DOI: https://doi.org/10.1054/clnu.2001.0397
Chen, J., Stavro, P. M., Thompson, L. 2009. Dietary Flaxseed Inhibits Human Breast Cancer Growth and Metastasis and Downregulates Expression of Insulin-Like Growth Factor and Epidermal Growth Factor Receptor, Nutrition and Cancer, vol. 43, no. 2, p. 187-192. https://doi.org/10.1207/S15327914NC432_9 DOI: https://doi.org/10.1207/S15327914NC432_9
Cherala, G., Shapiro, B. H., DAmello, A. P. 2006. Two Low Protein Diets Differentially Affect Food Consumption and Reproductive Performance in Pregnant and Lactating Rats and Long-Term Growth in Their Offspring, The Journal of Nutrition, Nutrient Requirements and Optimal Nutrition, vol. 136, no. 11, p. 2827-2833. https://doi.org/10.1093/jn/136.11.2827 DOI: https://doi.org/10.1093/jn/136.11.2827
Dardevet, D., Sornet, C., Bayle, G., Prugnaud, J., Pouyet, C., Grizard, J. 2002. Postprandial Stimulation of Muscle Protein Synthesis in Old Rats Can Be Restored by a Leucin-Supplemented Meal, Oxford Academic, vol. 132, no. 1, p. 95-100. https://doi.org/10.1093/jn/132.1.95 DOI: https://doi.org/10.1093/jn/132.1.95
Dauncey, M. J., Rudd, B. T., White, D. A., Shakespear, R. A. 1993. Regulation of insulin-like growth factor binding proteins in young growing animals by alteration of energy status, Growth Regulation, vol. 3, no. 3, p. 198-207. https://doi.org/7693100
Dauncey, M. J., Shakespear, R. A., Rudd, B. T., Ingram, D. L. 1990. Variations in somatomedin-C/insulin-like growth factor-I associated.with environmental temperature and nutrition, Hormonal dan Metabolic Research, vol. 22, no. 5, p. 261-264. https://doi.org/10.1055/s-2007-1004898 DOI: https://doi.org/10.1055/s-2007-1004898
Davenport, M. L., Isley, W. L., Pucilowska, J. B., Pemberton, L. B., Lyman, B., Underwood, L. E., Clemmons, D. R. 1992. Insulin-like growth factor-binding protein-3 proteolysis is induced after elective surgery, The Journal of Clinical Endocrinology and Metabolism, vol. 75, no. 2, p. 590-595. https://doi.org/10.1210/jcem.75.2.1379257 DOI: https://doi.org/10.1210/jcem.75.2.1379257
Deboer, M. D., Scharf, R. J., Leite, A. M., Ferrer RN, A., Havt, A., Pinkerton, R., Lima, A. A., Guerrant, R. L. 2017. Systemic inflammation, growth factors, and linear growth in the setting of infection and malnutrition, Nutrition, Applied nutritional investigation, vol. 33, p. 248-253. http://dx.doi.org/10.1016/j.nut.2016.06.013 DOI: https://doi.org/10.1016/j.nut.2016.06.013
Difedele, L. M., He, J., Bonkowski, E. L., Han, X., Held, M. A., Bohan, A., Menon, R. K., Denson, L. A. 2005. Tumor necrosis factor alfa-blokade restores growth hormone signaling in Murine Collitis, Gastroenterology, Basic-Alimentary Tract, vol. 128, no. 5, p. 1278-1291. https://doi.org/10.1053/j.gastro.2005.02.003 DOI: https://doi.org/10.1053/j.gastro.2005.02.003
Rafols, M. E. 2014. Adipose tissue: Cel heterogenity and functional diversity, Endocrinolia y Nutricion (English Edition), vol. 61, no. 2, p. 100-112. https://doi.org/10.1016/j.endoen.2014.02.001 DOI: https://doi.org/10.1016/j.endoen.2014.02.001
Fazeli, P. K., Klibanski, A. 2014. Determinants of GH resistance in malnutrition, Journal of Endocrinologgy, GH resistance in malnutrition, vol. 220, no. 3, p. 57-65. https://doi.org/10.1430/JOE-13-0477 DOI: https://doi.org/10.1530/JOE-13-0477
Ferry, R. J. Jr., Cerri, R. W., Cohen, P. 1999. Insulin-like growth factor binding proteins: new proteins, new functions, Homonal Research, vol. 51, p. 53-67. https://doi.org/10.1159/000023315 DOI: https://doi.org/10.1159/000023315
Gibson, R. S. 2005. Principles of Nutritional_Assessment, 2nd edn, New York, NY : Oxford Press, 425 p. ISBN-13 978-0-19-517169-3.
Guerrant, R. L., Oria, R. B., Moore, S. R., Oria, M. O., Lima, A. A. 2008. Malnutrition as an enteric infectious disease with long-term effects on child development, Nutrition Reviews, vol. 66, no. 9, p. 487-505. https://doi.org/10.1111/j.1753-4887.2008.00082.x DOI: https://doi.org/10.1111/j.1753-4887.2008.00082.x
Guntur, A. R., Rosen, C. 2013. IGF-1 regulation of key signaling pathways in bone, BoneKEy Reports, vol. 2, no. 437, p 1-6. https://doi.org/10.1038/bonekey.2013.171 DOI: https://doi.org/10.1038/bonekey.2013.171
Gupta, N., Lustig, R. H., Kohn, M. A., McCracken, M., Vittinghoff, E. 2011. Sex differences in statural growth impairment in Crohns disease: role of IGF-1, Inflammatory Bowel Diseases, vol. 17, no. 11, p. 2318-2325. https://doi.org/10.1002/ibd.21617 DOI: https://doi.org/10.1002/ibd.21617
Hawkes, C.P., Grimberg, A. 2015. Insulin-like growth factor-I is a marker for nutritional state, Pediatrics Endocrinology Review, vol. 13, no. 2, p. 499-511. https://doi.org/26841638
Hefferman, M., Summers, R. J., Thorburn, A., Ogru, E., Gianello, R., Jiang, W.-J., Frank M. Ng. 2001. The effects of human GH and its lipolytic fragment (AOD9604) on lipid metabolism following chronic treatment in obese mice and beta3-AR knock-Out Mice, Endocrinology, vol. 142, no. 12, p. 5182-5189. https://doi.org/10.1210/endo.142.12.8522 DOI: https://doi.org/10.1210/endo.142.12.8522
Hintz, R. L., Suskind, R., Amatayakul, K., Thanangkul, O., Olson, R. 1978. Plasma Somatomedin and growth hormone values in childrean with protein-calorie malnutrition, The Journal of Pediatrics, vol. 92, no. 1, p. 153–156. https://doi.org/10.1016/S0022-3476(78)80099-7 DOI: https://doi.org/10.1016/S0022-3476(78)80099-7
Hoppe, C., Molgard, C., Juul, A., Michaelsen, K. F. 2004. High intakes of skimmed milk, but not meat, increase serum IGF-I and IGFBP-3 in eight-year-old boys, European Journal of Clinical Nutrition, original communication, vol. 58, p. 1211-1216. https://doi.org/10.1038/sj.ejcn.1601948 DOI: https://doi.org/10.1038/sj.ejcn.1601948
Jenkins, P. J., Frajese, V., Jones, A. M., Camacho-Hubner, C., Lowe, D. G., Fairclough, P. D., Chew, S. L., Grossman, A. B., Monson, J. P., Besser, G. M. 2000. Insulin-like growth factor I and the development of colorectal neoplasia in acromegaly, Journal of Endocrinology and Metabolism, vol. 85, no. 9, p. 3218-3221. https://doi.org/10.1210/jcem.85.9.6806 DOI: https://doi.org/10.1210/jcem.85.9.6806
Kamycheva, E., Berg, V., Jorde, R. 2012. Insulin-like growth factor I, growth hormone, and insulin sensitivity: the efeects of a one year cholecalsiferol supplementation in middle-aged overweight and obese subjects, Endocrine, vol. 42, p. 412-418. https://doi.org/10.1007/s12020-012-9825-6 DOI: https://doi.org/10.1007/s12020-012-9825-6
Kartini, A., Subagio, H. W., Hadisaputro, S., Kartasurya, M. I., Suhartono, S., Budiyono, B. 2019. Pesticide Exposure and Stunting among Children in Agricultural Areas, The International Journal of Occupational and Environtmental Medicine, vol. 10, no. 1, p. 17-29. https://doi.org/10.15171/ijoem.2019.1428 DOI: https://doi.org/10.15171/ijoem.2019.1428
Khovidhunkit, W., Kim, M.-S., Memon, R. A., Shigenaga, J. K., Moser, A. H., Feingold, K. R., Grunfeld, C. 2004. Effects of infection and inflammation on lipid and lipoprotein metabolism: mechanisms and consequences to the host, Journal of Lipid Research, The Patogenesis of Atherosclerosis, vol. 45, p. 1169-1196. https://doi.org/DOI 10.1194/jlr.R300019-JLR200 DOI: https://doi.org/10.1194/jlr.R300019-JLR200
Kundam, D. N., Acham, I. O., Girgih, A. T. 2018. Bioactive Compounds in Fish and Their Health Benefits, Asian Food Science Journal, vol. 4, no. 4, p. 1-14. https://doi.org/10.9734/AFSJ/2018/41803 DOI: https://doi.org/10.9734/AFSJ/2018/41803
Lann, D., LeRoith, D. 2008. The role of endocrine insulin-like growth factor-I and insulin in breast cancer, Journal Of Mammary Gland Biology Neoplasia, vol. 13, p. 371-379. https://doi.org/10.1007/s10911-008-9100-x DOI: https://doi.org/10.1007/s10911-008-9100-x
Laron, Z. 2001. Insulin-like growth factor 1 (IGF-1): a growth hormone. Journal of Clinical Pathology, vol. 54, no. 5, p. 311-316. https://doi.org/10.1136/mp.54.5.311 DOI: https://doi.org/10.1136/mp.54.5.311
Liu, J.-L., Coschigano, K. T., Robertson, K., Lipsett, M., Guo, Y., Kopchick, J. J., Kumar, U., Liu, Y. L. 2004. Disruption of growth hormone receptor gene causes diminished pancreatic islet size and increased insulin sensitivity in mice, American Journal of Physiology and Metabolism, vol. 287, no. 3, p. 405-413. https://doi.org/10.1152/ajpendo.00423.2003 DOI: https://doi.org/10.1152/ajpendo.00423.2003
Lunn, P. G. 2007. The impact of infection and butrition on gut function and growth in childhood, Proceeding of Nutrition Society, vol. 59, no. 1, p. 147-154. https://doi.org/10.1017/S0029665100000173 DOI: https://doi.org/10.1017/S0029665100000173
Martins, V. J. B., de Alberqueuque, M. P., Sawaya, A. L. 2017. Endocrine changes in undernutrition metabolic programming, and nutritional recovery, Handbook of Famine, Starvation and Nutrient Deprivation https://doi.org/DOI 10.1007/978-3-319-40007-5_41-1 DOI: https://doi.org/10.1007/978-3-319-40007-5_41-1
McDonald, T. J., Nijland, M. J., Nathanielsz, P. W. 2007. The insulin-like growth factor syste and the fetal brain: Effects of poor maternal nutrition, Reviews in Endocrinology and Metabolic Disorders, vol. 8, p. 71-84. https://doi.org/DOI 10.1007/s11154-007-9044-2 DOI: https://doi.org/10.1007/s11154-007-9044-2
Misra, M., Miller, K. K., Bjornson, J., Hackman, A., Aggarwal, A., Chung, J., Ott, M., Herzog, D. B., Johnson, M. L., Klibanski, A. 2003. Alterations in growth hormon secretory dynamics in adolecent girls with anorexia nervosa and effects on bone metabolism, The Journal of Clinical Endocrinology & Metabolism, vol. 88, no. 12, p. 5615-5623. https://doi.org/10.1210/jc.2003-030532 DOI: https://doi.org/10.1210/jc.2003-030532
Nobile, V., Duclos, E., Michelotti, A., Bizzaro, G., Negro, M., Soisson, F. 2016. Supplementation with a fish protein hydrolysate (Micromesistius poutassou): effects on body weight, body composition, and CCK/GLP-1 secretion, Food and Nutrition Research, vol. 60, no. 1, p. 1-10. https://doi.org/10.3402/fnr.v60.29857 DOI: https://doi.org/10.3402/fnr.v60.29857
Pratama, R. I., Rostini, R., Rochima, E. 2018. Amino acids profile and volatile flavour compound of raw and steamed Patin catfish (Pangasius hypophthalmus) and narrow-barred Spanish Mackerel (Scomberomorus commerson), IOP Conference Series: Earth and Environtmental Science, vol. 116, p. 1-17. https://doi.org/10.1088/1755-1315/116/1/012056 DOI: https://doi.org/10.1088/1755-1315/116/1/012056
Pucilowska, J. B., Davenport, M. L., Kabir, I., Underwood, L. E. 1993. The effect of dietary protein supplementation on insulin-like growth factors (IGFs) and IGF-binding proteins in children with shigellosis, The Journal of Clinical Endocrinology and Metabolism, vol. 77, no. 1, p. 1516-1521. https://doi.org/10.1210/jcem.77.6.7505287 DOI: https://doi.org/10.1210/jc.77.6.1516
Rinderknecht, E., Humbel, R. E. 1978. The amino acid sequence of human insulin-like growth factor I its structural homology with pro-insulin, The Journal of Biology Chemistry, vol. 253, no. 8, p. 2769-2776. DOI: https://doi.org/10.1016/S0021-9258(17)40889-1
Rogers, Q. R., Harper, A. E. 1965. Amino acids diet and maximal growth in the rat, The Journal of Nutrition, vol. 87, no. 3, p. 267-273. https://doi.org/10.1093/jn/87.3.267 DOI: https://doi.org/10.1093/jn/87.3.267
Rosen, C., Yakar, S. 2020. Growth hormone, insulin-like growth factor, and IGF binding proteins, Principle of Bone Biology, no. 42, p. 985-1015. https://doi.org/10.1016/B978-0-12-814841-9.00042-7 DOI: https://doi.org/10.1016/B978-0-12-814841-9.00042-7
Saunders, J., Smith, T., Stroud, M. 2011. Malnutrition and Undernutrition, ELSEVIER, Undernutrition and Clinical Nutrition, vol. 39, no. 1, p. 45-50. https://doi.org/10.1016/j.mpmed.2018.12.012 DOI: https://doi.org/10.1016/j.mpmed.2010.10.007
Skottner, A. 2012. Biosynthesis of Growth Hormone and Insulin-Like Growth Factor-I and the Regulation of their Secretion., The Open Endocrinology Journal, vol. 6, p. 3-12. https://doi.org/10.2174/1874216501206010003 DOI: https://doi.org/10.2174/1874216501206010003
Smith, I. F., Latham, M. C, Azubuike, J. A., Butler, W. R., Phillips, L. S., Pond, W. G., Enwonwu, C. O. 1981. Blood plasma levels of cortisol, insulin, growth hormone and somatomedin in children with marasmus, kwashiorkor, and intermediate forms of protein energy malnutrition, Experimental Biology and Medicine, vol. 167, p. 607-611. https://doi.org/10.3181/00379727-167-41222 DOI: https://doi.org/10.3181/00379727-167-41222
Smith, W. J., Underwood, L. E., Keyes, L., Clemmon, D. R. 1997. Use of Insulin-Like Growth Factor I (IGF-I) and IGF Binding Protein Measurements to Monitor Feeding of Premature Infants, Journal of Clinical Endocrinology and Metabolic, vol. 82, no. 12, p. 3982-3988. https://doi.org/10.1210/jcem.82.12.4452 DOI: https://doi.org/10.1210/jc.82.12.3982
Soliman, A. T., Hassan, A. E. H., Aref, M. K., Hintz, R. L., Rosenfeld, R. G., Rogol, A. D. 1986. Serum insulin-like growth factors I and II concentrations and growth hormone and insulin responses to arginine infusion in children with protein-energy malnutrition before and after nutritional rehabilitation, Pediatrics Researchs, vol. 20, p. 1122-1130. https://doi.org/10.1203/00006450-198611000-00012 DOI: https://doi.org/10.1203/00006450-198611000-00012
Turner, M. R., Reed, P. J., Munday, K. A. 1976. Action of growth hormone in vitro on the net uptake and incorporation into protein of amino acids in muscle from intact rabbits given protein-deficient diets, British Journal of Nutrition, vol. 35, no. 1, p. 1-10. https://doi.org/10.1079/BJN19760003 DOI: https://doi.org/10.1079/BJN19760003
Underwood, L. E., Thissen, J. P., Lemozy, S., Ketelslegers, J. M., Clemmons, D. R. 1994. Hormonal and nutritional regulation of IGF-1 and Its Binding Proteins, Hormonal Research in Pediatrics, Session 1 Basic Aspects and Clinical Relevance of Binding Protein in the Action of GH and IGF-1, vol. 42, p. 145-151. https://doi.org/10.1159/000184187 DOI: https://doi.org/10.1159/000184187
UNICEF, WHO, World Bank Group 2018. Levels and trends in child malnutrition., UNICEF/WHO/World Bank Joint Child Malnutrition Estimatetes, Key Findings of the 2018 Edition, UNICEF, WHO, World Bank Group. Available at https://www.who.int/nutgrowthdb/2018-jme-brochure.pdf
Van Norren, K., Kegler, D., Argiles, J., Luiking, Y., Gorselink, M., Laviano, A., Arts, K., Faber, J., Jansen, H., van der Beek, E., van Helvoort, A. 2009. Dietary supplementation with a specific combination of high protein, leucine, and fish oil improves muscle function and daily activity in tumour-bearing cachectic mice, Nature, vol. 100, p. 713-722. https://doi.org/10.1038/sj.bjc.6604905 DOI: https://doi.org/10.1038/sj.bjc.6604905
Vorwerk, P., Yamanaka, Y., Spagnolli, A., Oh, Y., Rosenfeld, R. G. 1998. Insulin IGF binding by IGFBP-3 fragments derived from proteolysis, baculovirus expression and normal urine, Journal of Endocrinology and Metabolism, vol. 83, no. 4, p. 1392-1395. https://doi.org/10.1210/jcem.83.4.4858 DOI: https://doi.org/10.1210/jcem.83.4.4858
Windsor, M., Barlow, S. 1981. Introduction on fishery by-products, Farnham, Surrey, England, Fishing News Book Ltd, Mollecular Nutrition Food Research, vol 26, no.6, p. 558. https://doi.org/10.1002/food.19820260619 DOI: https://doi.org/10.1002/food.19820260619
Wong, C. P, Bray, T. M., Khanna, S. K. 2019. Growth, Bone Health, and Cognition: Nutritional Evaluation of a Sustainable Ocean-Based Advance Protein Powder (APP), Ecology Food and Nutrition, vol. 58, no. 2, p. 80-92. https://doi.org/10.1080/03670244.2019.1565759 DOI: https://doi.org/10.1080/03670244.2019.1565759
Zamboni, G., Dufillot, D., Antoniazzi, F., Valentini, R., Gendrel, D., Tato, L. 1996. Growth Hormone-Binding Proteins and Insulin-Like Growth Factor-Binding Proteins in Protein-Energy Malnutrition, before and after Nutritional Rehabilitation, Pediatrics Researchs, vol. 39, p. 410-414. https://doi.org/10.1203/00006450-199603000-00006 DOI: https://doi.org/10.1203/00006450-199603000-00006
Zambrano, E., Rodriguez-Gonzales, G., Guzman, C., Garcia-Becerra, R., Boeck, L., Diaz, L., Menjivar, M., Larrea, F., Nathanielsz, P. 2005. A maternal low protein diet during pregnancy and lactation in the rat impairs male reproductive development, The Physiological Society, vol. 563, no. 1, p. 265-284. https://doi.org/10.1113/jphysiol.2004.078543 DOI: https://doi.org/10.1113/jphysiol.2004.078543
Zhang, T., Chen, J., Tang, X., Luo, Q., Xu, D., Yu, B. 2019. Interaction between adipocytes and high-density lipoprotein: new insights into the mechanism of obesity-induced dyslipidemia and atherosclerosis, Lipid in Health and Disease, vol. 18, no. 223, p. 1170-1179. https://doi.org/10.1186/s12944-019-1170-9 DOI: https://doi.org/10.1186/s12944-019-1170-9
Zhang, Y., McGillicuddy, F. C., Hinkle, C. C., ONeill, S., Glick, J. M., Rothblat, G. H., Reilly, M. P. 2010. Adipocyte Modulation of High-Density Lipoprotein Cholesterol, Circulation, vol. 121, no. 11, p. 1347-1355. https://doi.org/10.1161/CIRCULATIONAHA.109.897330 DOI: https://doi.org/10.1161/CIRCULATIONAHA.109.897330
Published
How to Cite
Issue
Section
License
This license permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited, and is not altered, transformed, or built upon in any way.
