{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,17]],"date-time":"2026-08-17T21:38:16Z","timestamp":1787002696470,"version":"build-2736575974"},"reference-count":38,"publisher":"Springer Science and Business Media LLC","issue":"2","license":[{"start":{"date-parts":[[2017,5,31]],"date-time":"2017-05-31T00:00:00Z","timestamp":1496188800000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/www.springer.com\/tdm"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Pediatr Res"],"published-print":{"date-parts":[[2017,8]]},"DOI":"10.1038\/pr.2017.53","type":"journal-article","created":{"date-parts":[[2017,4,18]],"date-time":"2017-04-18T12:04:41Z","timestamp":1492517081000},"page":"340-348","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":26,"title":["Low birth weight is associated with impaired murine kidney development and function"],"prefix":"10.1038","volume":"82","author":[{"given":"Christina","family":"Barnett","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Oluwadara","family":"Nnoli","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wasan","family":"Abdulmahdi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lauren","family":"Nesi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael","family":"Shen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joseph A","family":"Zullo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David L","family":"Payne","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tala","family":"Azar","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Parth","family":"Dwivedi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kunzah","family":"Syed","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jonathan","family":"Gromis","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mark","family":"Lipphardt","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Edson","family":"Jules","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eric L","family":"Maranda","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Amy","family":"Patel","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"May M","family":"Rabadi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Brian B","family":"Ratliff","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2017,5,31]]},"reference":[{"key":"BFpr201753_CR1","first-page":"1","volume":"64","author":"BE Hamilton","year":"2015","unstructured":"Hamilton BE, Martin JA, Osterman MJ, Curtin SC, Matthews TJ . Births final data for 2014. Natl Vital Stat Rep 2015;64:1\u201364.","journal-title":"Natl Vital Stat Rep"},{"key":"BFpr201753_CR2","doi-asserted-by":"publisher","first-page":"1848","DOI":"10.1056\/NEJMe058187","volume":"353","author":"MW Gillman","year":"2005","unstructured":"Gillman MW . Developmental origins of health and disease. N Engl J Med 2005;353:1848\u201350.","journal-title":"N Engl J Med"},{"key":"BFpr201753_CR3","doi-asserted-by":"publisher","first-page":"1344S","DOI":"10.1093\/ajcn\/71.5.1344s","volume":"71","author":"KM Godfrey","year":"2000","unstructured":"Godfrey KM, Barker DJ . Fetal nutrition and adult disease. Am J Clin Nutr 2000;71:1344S\u20131352S.","journal-title":"Am J Clin Nutr"},{"key":"BFpr201753_CR4","doi-asserted-by":"publisher","first-page":"151","DOI":"10.1681\/ASN.2007020252","volume":"19","author":"BE Vikse","year":"2008","unstructured":"Vikse BE, Irgens LM, Leivestad T, Hallan S, Iversen BM . Low birth weight increases risk for end-stage renal disease. J Am Soc Nephrol 2008;19:151\u20137.","journal-title":"J Am Soc Nephrol"},{"key":"BFpr201753_CR5","doi-asserted-by":"publisher","first-page":"1509","DOI":"10.1007\/s00467-016-3384-7","volume":"31","author":"DD Khalsa","year":"2016","unstructured":"Khalsa DD, Beydoun HA, Carmody JB . Prevalence of chronic kidney disease risk factors among low birth weight adolescents. Pediatr Nephrol 2016;31:1509\u201316.","journal-title":"Pediatr Nephrol"},{"key":"BFpr201753_CR6","doi-asserted-by":"publisher","first-page":"135","DOI":"10.1038\/nrneph.2014.251","volume":"11","author":"VA Luyckx","year":"2015","unstructured":"Luyckx VA, Brenner BM . Birth weight, malnutrition and kidney-associated outcomes\u2014a global concern. Nat Rev Nephrol 2015;11:135\u201349.","journal-title":"Nat Rev Nephrol"},{"key":"BFpr201753_CR7","doi-asserted-by":"publisher","first-page":"71","DOI":"10.2215\/CJN.01700408","volume":"4","author":"JB Hodgin","year":"2009","unstructured":"Hodgin JB, Rasoulpour M, Markowitz GS, D'Agati VD . Very low birth weight is a risk factor for secondary focal segmental glomerulosclerosis. Clin J Am Soc Nephrol 2009;4:71\u20136.","journal-title":"Clin J Am Soc Nephrol"},{"key":"BFpr201753_CR8","doi-asserted-by":"publisher","first-page":"127","DOI":"10.1016\/j.celrep.2014.02.033","volume":"7","author":"C Cebrian","year":"2014","unstructured":"Cebrian C, Asai N, D'Agati V, Costantini F . The number of fetal nephron progenitor cells limits ureteric branching and adult nephron endowment. Cell Rep 2014;7:127\u201337.","journal-title":"Cell Rep"},{"key":"BFpr201753_CR9","doi-asserted-by":"publisher","first-page":"100","DOI":"10.1186\/s12882-016-0314-7","volume":"17","author":"A Iyengar","year":"2016","unstructured":"Iyengar A, Nesargi S, George A, Sinha N, Selvam S, Luyckx VA . Are low birth weight neonates at risk for suboptimal renal growth and function during infancy? BMC Nephrol 2016;17:100.","journal-title":"BMC Nephrol"},{"key":"BFpr201753_CR10","doi-asserted-by":"publisher","first-page":"333","DOI":"10.1007\/978-1-61779-851-1_30","volume":"886","author":"LA Cullen-McEwen","year":"2012","unstructured":"Cullen-McEwen LA, Douglas-Denton RN, Bertram JF . Estimating total nephron number in the adult kidney using the physical disector\/fractionator combination. Methods Mol Biol 2012;886:333\u201350.","journal-title":"Methods Mol Biol"},{"key":"BFpr201753_CR11","doi-asserted-by":"publisher","first-page":"F1448","DOI":"10.1152\/ajprenal.00055.2011","volume":"300","author":"LA Cullen-McEwen","year":"2011","unstructured":"Cullen-McEwen LA, Armitage JA, Nyengaard JR, Moritz KM, Bertram JF . A design-based method for estimating glomerular number in the developing kidney. Am J Physiol Renal Physiol 2011;300:F1448\u201353.","journal-title":"Am J Physiol Renal Physiol"},{"key":"BFpr201753_CR12","doi-asserted-by":"publisher","first-page":"F783","DOI":"10.1152\/ajprenal.00279.2012","volume":"303","author":"A Schreiber","year":"2012","unstructured":"Schreiber A, Shulhevich Y, Geraci S et al, Transcutaneous measurement of renal function in conscious mice. Am J Physiol Renal Physiol 2012;303:F783\u20138.","journal-title":"Am J Physiol Renal Physiol"},{"key":"BFpr201753_CR13","doi-asserted-by":"publisher","first-page":"2997","DOI":"10.1093\/ndt\/gfp225","volume":"24","author":"D Schock-Kusch","year":"2009","unstructured":"Schock-Kusch D, Sadick M, Henninger N et al, Transcutaneous measurement of glomerular filtration rate using FITC-sinistrin in rats. Nephrol Dial Transplant 2009;24:2997\u20133001.","journal-title":"Nephrol Dial Transplant"},{"issue":"1","key":"BFpr201753_CR14","doi-asserted-by":"publisher","first-page":"pdb.prot5558-pd","DOI":"10.1101\/pdb.prot5558","volume":"2011","author":"H. Barak","year":"2011","unstructured":"Barak H, Boyle SC . Organ culture and immunostaining of mouse embryonic kidneys. Cold Spring Harb Protoc 2011;2011: pdb prot5558.","journal-title":"Cold Spring Harbor Protocols"},{"key":"BFpr201753_CR15","doi-asserted-by":"publisher","first-page":"894","DOI":"10.5301\/jn.5000220","volume":"26","author":"Y Kandasamy","year":"2013","unstructured":"Kandasamy Y, Smith R, Wright IM, Lumbers ER . Relationships between glomerular filtration rate and kidney volume in low-birth-weight neonates. J Nephrol 2013;26:894\u201388.","journal-title":"J Nephrol"},{"key":"BFpr201753_CR16","doi-asserted-by":"publisher","first-page":"R197","DOI":"10.1152\/ajpregu.00741.2007","volume":"295","author":"KA Brennan","year":"2008","unstructured":"Brennan KA, Kaufman S, Reynolds SW et al, Differential effects of maternal nutrient restriction through pregnancy on kidney development and later blood pressure control in the resulting offspring. Am J Physiol Regul Integr Comp Physiol 2008;295:R197\u2013205.","journal-title":"Am J Physiol Regul Integr Comp Physiol"},{"key":"BFpr201753_CR17","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1076\/apab.111.1.8.15136","volume":"111","author":"SC Langley-Evans","year":"2003","unstructured":"Langley-Evans SC, Langley-Evans AJ, Marchand MC . Nutritional programming of blood pressure and renal morphology. Arch Physiol Biochem 2003;111:8\u201316.","journal-title":"Arch Physiol Biochem"},{"key":"BFpr201753_CR18","doi-asserted-by":"publisher","first-page":"965","DOI":"10.1016\/S0024-3205(99)00022-3","volume":"64","author":"SC Langley-Evans","year":"1999","unstructured":"Langley-Evans SC, Welham SJ, Jackson AA . Fetal exposure to a maternal low protein diet impairs nephrogenesis and promotes hypertension in the rat. Life Sci 1999;64:965\u201374.","journal-title":"Life Sci"},{"key":"BFpr201753_CR19","doi-asserted-by":"publisher","first-page":"188","DOI":"10.1016\/j.devcel.2014.02.017","volume":"29","author":"KM Short","year":"2014","unstructured":"Short KM, Combes AN, Lefevre J et al, Global quantification of tissue dynamics in the developing mouse kidney. Dev Cell 2014;29:188\u2013202.","journal-title":"Dev Cell"},{"key":"BFpr201753_CR20","doi-asserted-by":"publisher","first-page":"906","DOI":"10.2174\/138945007781386875","volume":"8","author":"LL Woods","year":"2007","unstructured":"Woods LL . Maternal nutrition and predisposition to later kidney disease. Curr Drug Targets 2007;8:906\u201313.","journal-title":"Curr Drug Targets"},{"key":"BFpr201753_CR21","doi-asserted-by":"publisher","first-page":"1231","DOI":"10.1046\/j.1523-1755.2002.00264.x","volume":"61","author":"SJ Welham","year":"2002","unstructured":"Welham SJ, Wade A, Woolf AS . Protein restriction in pregnancy is associated with increased apoptosis of mesenchymal cells at the start of rat metanephrogenesis. Kidney Int 2002;61:1231\u201342.","journal-title":"Kidney Int"},{"key":"BFpr201753_CR22","doi-asserted-by":"publisher","first-page":"588S","DOI":"10.1080\/07315724.2004.10719428","volume":"23","author":"DJ Barker","year":"2004","unstructured":"Barker DJ . The developmental origins of adult disease. J Am Coll Nutr 2004;23:588S\u201395.","journal-title":"J Am Coll Nutr"},{"key":"BFpr201753_CR23","doi-asserted-by":"publisher","first-page":"2111","DOI":"10.1097\/HJH.0000000000001051","volume":"34","author":"J Li","year":"2016","unstructured":"Li J, Tsuprykov O, Yang X, Hocher B . Paternal programming of offspring cardiometabolic diseases in later life. J Hypertens 2016;34:2111\u201326.","journal-title":"J Hypertens"},{"key":"BFpr201753_CR24","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1016\/j.ijgo.2004.09.017","volume":"88","author":"XM Xiao","year":"2005","unstructured":"Xiao XM, Li LP . L-Arginine treatment for asymmetric fetal growth restriction. Int J Gynaecol Obstet 2005;88:15\u20138.","journal-title":"Int J Gynaecol Obstet"},{"key":"BFpr201753_CR25","doi-asserted-by":"publisher","first-page":"499","DOI":"10.1258\/0007142991902574","volume":"55","author":"HJ McArdle","year":"1999","unstructured":"McArdle HJ, Ashworth CJ . Micronutrients in fetal growth and development. Br Med Bull 1999;55:499\u2013510.","journal-title":"Br Med Bull"},{"key":"BFpr201753_CR26","doi-asserted-by":"publisher","first-page":"75","DOI":"10.1017\/S0029665111003302","volume":"71","author":"LK Park","year":"2012","unstructured":"Park LK, Friso S, Choi SW . Nutritional influences on epigenetics and age-related disease. Proc Nutr Soc 2012;71:75\u201383.","journal-title":"Proc Nutr Soc"},{"key":"BFpr201753_CR27","doi-asserted-by":"publisher","first-page":"894","DOI":"10.1093\/jn\/128.5.894","volume":"128","author":"G Wu","year":"1998","unstructured":"Wu G, Pond WG, Ott T, Bazer FW . Maternal dietary protein deficiency decreases amino acid concentrations in fetal plasma and allantoic fluid of pigs. J Nutr 1998;128:894\u2013902.","journal-title":"J Nutr"},{"key":"BFpr201753_CR28","doi-asserted-by":"publisher","first-page":"R955","DOI":"10.1152\/ajpregu.00455.2004","volume":"289","author":"LL Woods","year":"2005","unstructured":"Woods LL, Weeks DA . Prenatal programming of adult blood pressure: role of maternal corticosteroids. Am J Physiol Regul Integr Comp Physiol 2005;289:R955\u2013R962.","journal-title":"Am J Physiol Regul Integr Comp Physiol"},{"key":"BFpr201753_CR29","doi-asserted-by":"publisher","first-page":"1339","DOI":"10.1111\/j.1523-1755.2004.00511.x","volume":"65","author":"LL Woods","year":"2004","unstructured":"Woods LL, Weeks DA, Rasch R . Programming of adult blood pressure by maternal protein restriction: role of nephrogenesis. Kidney Int 2004;65:1339\u201348.","journal-title":"Kidney Int"},{"key":"BFpr201753_CR30","doi-asserted-by":"publisher","first-page":"238","DOI":"10.1046\/j.1523-1755.2001.00484.x","volume":"59","author":"VM Vehaskari","year":"2001","unstructured":"Vehaskari VM, Aviles DH, Manning J . Prenatal programming of adult hypertension in the rat. Kidney Int 2001;59:238\u201345.","journal-title":"Kidney Int"},{"key":"BFpr201753_CR31","doi-asserted-by":"publisher","first-page":"607","DOI":"10.1042\/cs0910607","volume":"91","author":"SC Langley-Evans","year":"1996","unstructured":"Langley-Evans SC, Welham SJ, Sherman RC, Jackson AA . Weanling rats exposed to maternal low-protein diets during discrete periods of gestation exhibit differing severity of hypertension. Clin Sci 1996;91:607\u201315.","journal-title":"Clin Sci"},{"key":"BFpr201753_CR32","doi-asserted-by":"publisher","first-page":"919","DOI":"10.1159\/000447801","volume":"39","author":"C Reichetzeder","year":"2016","unstructured":"Reichetzeder C, Dwi Putra SE, Li J, Hocher B . Developmental origins of disease - crisis precipitates change. Cell Physiol Biochem 2016;39:919\u201338.","journal-title":"Cell Physiol Biochem"},{"key":"BFpr201753_CR33","doi-asserted-by":"publisher","first-page":"1010","DOI":"10.1590\/S0100-879X2010007500113","volume":"43","author":"FF Mesquita","year":"2010","unstructured":"Mesquita FF, Gontijo JA, Boer PA . Maternal undernutrition and the offspring kidney: from fetal to adult life. Braz J Med Biol Res 2010;43:1010\u20138.","journal-title":"Braz J Med Biol Res"},{"key":"BFpr201753_CR34","doi-asserted-by":"publisher","first-page":"1247","DOI":"10.1242\/dev.057646","volume":"138","author":"CM Karner","year":"2011","unstructured":"Karner CM, Das A, Ma Z et al, Canonical Wnt9b signaling balances progenitor cell expansion and differentiation during kidney development. Development 2011;138:1247\u201357.","journal-title":"Development"},{"key":"BFpr201753_CR35","doi-asserted-by":"publisher","first-page":"3847","DOI":"10.1242\/dev.01944","volume":"132","author":"U Grieshammer","year":"2005","unstructured":"Grieshammer U, Cebrian C, Ilagan R, Meyers E, Herzlinger D, Martin GR . FGF8 is required for cell survival at distinct stages of nephrogenesis and for regulation of gene expression in nascent nephrons. Development 2005;132:3847\u201357.","journal-title":"Development"},{"key":"BFpr201753_CR36","doi-asserted-by":"publisher","first-page":"3859","DOI":"10.1242\/dev.01945","volume":"132","author":"AO Perantoni","year":"2005","unstructured":"Perantoni AO, Timofeeva O, Naillat F et al, Inactivation of FGF8 in early mesoderm reveals an essential role in kidney development. Development 2005;132:3859\u201371.","journal-title":"Development"},{"key":"BFpr201753_CR37","doi-asserted-by":"publisher","first-page":"e52748","DOI":"10.1371\/journal.pone.0052748","volume":"7","author":"E Kanitz","year":"2012","unstructured":"Kanitz E, Otten W, Tuchscherer M et al, High and low proteinratio carbohydrate dietary ratios during gestation alter maternal-fetal cortisol regulation in pigs. PLoS ONE 2012;7:e52748.","journal-title":"PLoS ONE"},{"issue":"Suppl","key":"BFpr201753_CR38","doi-asserted-by":"publisher","first-page":"S54","DOI":"10.1016\/j.placenta.2010.01.002","volume":"31","author":"KL Thornburg","year":"2010","unstructured":"Thornburg KL, O'Tierney PF, Louey S . Review: the placenta is a programming agent for cardiovascular disease. Placenta 2010;31 (Suppl): S54\u20139.","journal-title":"Placenta"}],"container-title":["Pediatric Research"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/www.nature.com\/articles\/pr201753.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/www.nature.com\/articles\/pr201753","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/www.nature.com\/doifinder\/10.1038\/pr.2017.53","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"},{"URL":"http:\/\/www.nature.com\/articles\/pr201753.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,5,20]],"date-time":"2023-05-20T17:04:36Z","timestamp":1684602276000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/pr201753"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,5,31]]},"references-count":38,"journal-issue":{"issue":"2","published-print":{"date-parts":[[2017,8]]}},"alternative-id":["BFpr201753"],"URL":"https:\/\/doi.org\/10.1038\/pr.2017.53","relation":{},"ISSN":["0031-3998","1530-0447"],"issn-type":[{"value":"0031-3998","type":"print"},{"value":"1530-0447","type":"electronic"}],"subject":[],"published":{"date-parts":[[2017,5,31]]},"assertion":[{"value":"24 October 2016","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"19 February 2017","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"31 May 2017","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no conflict of interest.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}]}}