{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,16]],"date-time":"2026-04-16T10:38:53Z","timestamp":1776335933058,"version":"3.51.2"},"reference-count":32,"publisher":"Springer Science and Business Media LLC","issue":"7","license":[{"start":{"date-parts":[[2021,3,10]],"date-time":"2021-03-10T00:00:00Z","timestamp":1615334400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2021,3,10]],"date-time":"2021-03-10T00:00:00Z","timestamp":1615334400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100006390","name":"Universit\u00e9 de Lausanne","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100006390","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Eur J Pediatr"],"published-print":{"date-parts":[[2021,7]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Glomerular filtration rate (GFR) is difficult to measure, and estimating formulas are notorious for lacking precision. This study aims to assess if the inclusion of additional biomarkers improves the performance of eGFR formulas. A hundred and sixteen children with renal diseases were enrolled. Data for age, weight, height, inulin clearance (iGFR), serum creatinine, cystatin C, neutrophil gelatinase-associated lipocalin (NGAL), parathyroid hormone (PTH), albumin, and brain natriuretic peptide (BNP) were collected. These variables were added to the revised and combined (serum creatinine and cystatin C) Schwartz formulas, and the quadratic and combined quadratic formulas. We calculated the adjusted <jats:italic>r<\/jats:italic>-square (<jats:italic>r<\/jats:italic><jats:sup>2<\/jats:sup>) in relation to iGFR and tested the improvement in variance explained by means of the likelihood ratio test. The combined Schwartz and the combined quadratic formulas yielded best results with an <jats:italic>r<\/jats:italic><jats:sup>2<\/jats:sup> of 0.676 and 0.730, respectively. The addition of BNP and PTH to the combined Schwartz and quadratic formulas improved the variance slightly. NGAL and albumin failed to improve the prediction of GFR further. These study results also confirm that the addition of cystatin C improves the performance of estimating GFR formulas, in particular the Schwartz formula.<\/jats:p><jats:p><jats:italic>Conclusion<\/jats:italic>: The addition of serum NGAL, BNP, PTH, and albumin to the combined Schwartz and quadratic formulas for estimating GFR did not improve GFR prediction in our population.<jats:table-wrap><jats:table><jats:tbody>\n                    <jats:tr>\n                      <jats:td colspan=\"2\"><jats:bold>What is Known:<\/jats:bold><jats:italic>\u2022 Estimating glomerular filtration rate (GFR) formulas include serum creatinine and\/or cystatin C but lack precision when compared to measured GFR.<\/jats:italic><jats:italic>\u2022 The serum concentrations of some biological parameters such as neutrophil gelatinase-associated lipocalin (NGAL), parathyroid hormone (PTH), albumin, and brain natriuretic peptide (BNP) vary with the level of renal function.<\/jats:italic><\/jats:td>\n                    <\/jats:tr>\n                    <jats:tr>\n                      <jats:td colspan=\"2\"><jats:bold>What is New:<\/jats:bold><jats:italic>\u2022 The addition of BNP and PTH to the combined quadratic formula improved its performance only slightly. NGAL and albumin failed to improve the prediction of GFR further.<\/jats:italic><\/jats:td>\n                    <\/jats:tr>\n                  <\/jats:tbody><\/jats:table><\/jats:table-wrap><\/jats:p>","DOI":"10.1007\/s00431-021-04019-w","type":"journal-article","created":{"date-parts":[[2021,3,10]],"date-time":"2021-03-10T22:02:48Z","timestamp":1615413768000},"page":"2223-2228","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["Serum NGAL, BNP, PTH, and albumin do not improve glomerular filtration rate estimating formulas in children"],"prefix":"10.1007","volume":"180","author":[{"given":"Julie","family":"Mouron-Hryciuk","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Fran\u00e7ois","family":"Cachat","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Paloma","family":"Parvex","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Thomas","family":"Perneger","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hassib","family":"Chehade","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2021,3,10]]},"reference":[{"key":"4019_CR1","unstructured":"National Kidney Foundation (2002) K\/DOQI clinical practice guidelines for chronic kidney disease: evaluation, classification, and stratification. Am J Kidney Dis 39(2 Suppl 1):S1\u2013S266"},{"issue":"12","key":"4019_CR2","first-page":"625","volume":"122","author":"A Pr\u00e9vot","year":"2002","unstructured":"Pr\u00e9vot A, Martini S, Guignard J-P (2002) Glomerular filtration markers in pediatrics. Rev Med Suisse Romande 122(12):625\u2013630","journal-title":"Rev Med Suisse Romande"},{"key":"4019_CR3","doi-asserted-by":"publisher","first-page":"1195","DOI":"10.1093\/ndt\/gft509","volume":"29","author":"L Fan","year":"2014","unstructured":"Fan L, Inker LA, Rossert J, Froissart M, Rossing P, Mauer M, Levey AS (2014) Glomerular filtration rate estimation using cystatin C alone or combined with creatinine as a confirmatory test. Nephrol Dial Transplant 29:1195\u20131203","journal-title":"Nephrol Dial Transplant"},{"issue":"3","key":"4019_CR4","doi-asserted-by":"publisher","first-page":"395","DOI":"10.1053\/j.ajkd.2007.11.018","volume":"51","author":"LA Stevens","year":"2008","unstructured":"Stevens LA, Coresh J, Schmid CH, Feldman HI, Froissart M, Kusek J, Rossert J, van Lente F, Bruce RD III, Zhang Y(L), Greene T, Levey AS (2008) Estimating GFR using serum cystatin C alone and in combination with serum creatinine: a pooled analysis of 3,418 individuals with CKD. Am J Kidney Dis 51(3):395\u2013406","journal-title":"Am J Kidney Dis"},{"key":"4019_CR5","doi-asserted-by":"publisher","first-page":"929","DOI":"10.1007\/s00467-008-0991-y","volume":"24","author":"TB Andersen","year":"2009","unstructured":"Andersen TB, Eskild-Jensen A, Fr\u00f8kiaer J et al (2009) Measuring glomerular filtration rate in children; can cystatin C replace established methods? A review. Pediatr Nephrol 24:929\u2013941","journal-title":"Pediatr Nephrol"},{"key":"4019_CR6","doi-asserted-by":"publisher","first-page":"383","DOI":"10.1016\/j.clinbiochem.2006.10.026","volume":"40","author":"JF Roos","year":"2007","unstructured":"Roos JF, Doust J, Tett SE, Kirkpatrick CMJ (2007) Diagnostic accuracy of cystatin C compared to serum creatinine for the estimation of renal dysfunction in adults and children-a meta-analysis. Clin Biochem 40:383\u2013391","journal-title":"Clin Biochem"},{"key":"4019_CR7","doi-asserted-by":"publisher","first-page":"345","DOI":"10.5527\/wjn.v4.i3.345","volume":"4","author":"J Santos","year":"2015","unstructured":"Santos J, Martins LS (2015) Estimating glomerular filtration rate in kidney transplantation: Still searching for the best marker. World J Nephrol 4:345\u2013353","journal-title":"World J Nephrol"},{"key":"4019_CR8","doi-asserted-by":"publisher","first-page":"31","DOI":"10.1159\/000180580","volume":"16","author":"DW Cockcroft","year":"1976","unstructured":"Cockcroft DW, Gault MH (1976) Prediction of creatinine clearance from serum creatinine. Nephron 16:31\u201341","journal-title":"Nephron"},{"key":"4019_CR9","doi-asserted-by":"publisher","first-page":"461","DOI":"10.7326\/0003-4819-130-6-199903160-00002","volume":"130","author":"AS Levey","year":"1999","unstructured":"Levey AS, Bosch JP, Lewis JB, Greene T, Rogers N, Roth D (1999) A more accurate method to estimate glomerular filtration rate from serum creatinine: a new prediction equation. Modification of diet in renal disease study group. Ann Intern Med 130:461\u2013470","journal-title":"Ann Intern Med"},{"key":"4019_CR10","doi-asserted-by":"publisher","first-page":"571","DOI":"10.1016\/S0031-3955(16)36251-4","volume":"34","author":"GJ Schwartz","year":"1987","unstructured":"Schwartz GJ, Brion LP, Spitzer A (1987) The use of plasma creatinine concentration for estimating glomerular filtration rate in infants, children, and adolescents. Pediatr Clin N Am 34:571\u2013590","journal-title":"Pediatr Clin N Am"},{"key":"4019_CR11","doi-asserted-by":"publisher","first-page":"629","DOI":"10.1681\/ASN.2008030287","volume":"20","author":"GJ Schwartz","year":"2009","unstructured":"Schwartz GJ, Mu\u00f1oz A, Schneider MF, Mak RH, Kaskel F, Warady BA, Furth SL (2009) New equations to estimate GFR in children with CKD. J Am Soc Nephrol 20:629\u2013637","journal-title":"J Am Soc Nephrol"},{"key":"4019_CR12","doi-asserted-by":"publisher","first-page":"445","DOI":"10.1038\/ki.2012.169","volume":"82","author":"GJ Schwartz","year":"2012","unstructured":"Schwartz GJ, Schneider MF, Maier PS, Moxey-Mims M, Dharnidharka VR, Warady B et al (2012) Improved equations estimating GFR in children with chronic kidney disease using an immunonephelometric determination of cystatin C. Kidney Int 82:445\u2013453","journal-title":"Kidney Int"},{"key":"4019_CR13","doi-asserted-by":"publisher","first-page":"524","DOI":"10.1038\/ki.2012.388","volume":"83","author":"A Gao","year":"2013","unstructured":"Gao A, Cachat F, Faouzi M, Bardy D, Mosig D, Meyrat B-J, Girardin E, Chehade H (2013) Comparison of the glomerular filtration rate in children by the new revised Schwartz formula and a new generalized formula. Kidney Int 83:524\u2013530","journal-title":"Kidney Int"},{"key":"4019_CR14","doi-asserted-by":"publisher","first-page":"54","DOI":"10.2215\/CJN.00940113","volume":"9","author":"H Chehade","year":"2014","unstructured":"Chehade H, Cachat F, Jannot A-S, Meyrat B-J, Mosig D, Bardy D, Parvex P, Girardin E (2014) New combined serum creatinine and cystatin C quadratic formula for GFR assessment in children. Clin J Am Soc Nephrol 9:54\u201363","journal-title":"Clin J Am Soc Nephrol"},{"key":"4019_CR15","doi-asserted-by":"publisher","first-page":"101","DOI":"10.1007\/s00467-006-0244-x","volume":"22","author":"MM Mitsnefes","year":"2007","unstructured":"Mitsnefes MM, Kathman TS, Mishra J, Kartal J, Khoury PR, Nickolas TL, Barasch J, Devarajan P (2007) Serum neutrophil gelatinase-associated lipocalin as a marker of renal function in children with chronic kidney disease. Pediatr Nephrol 22:101\u2013108","journal-title":"Pediatr Nephrol"},{"key":"4019_CR16","doi-asserted-by":"publisher","first-page":"120","DOI":"10.3389\/fmed.2020.00120","volume":"7","author":"S Fu","year":"2020","unstructured":"Fu S, Yu H, Li Y, Lv F, Deng J, Zhang F, Luan F, Zhao Y, Yao Y (2020) Multiple measures of mineral metabolism were associated with renal function in Chinese centenarians: a cross-sectional study. Front Med 7:120","journal-title":"Front Med"},{"key":"4019_CR17","doi-asserted-by":"publisher","first-page":"795","DOI":"10.1007\/s40620-019-00690-3","volume":"33","author":"K Okamoto","year":"2020","unstructured":"Okamoto K, Fujii H, Goto S, Kono K, Watanabe K, Nishi S (2020) Changes in the whole\/intact parathyroid hormone ratio and their clinical implications in patients with chronic kidney disease. J Nephrol 33:795\u2013802","journal-title":"J Nephrol"},{"key":"4019_CR18","first-page":"563","volume":"151","author":"N Cano","year":"2000","unstructured":"Cano N (2000) Malnutrition and chronic renal failure. Ann Med Interne (Paris) 151:563\u2013574","journal-title":"Ann Med Interne (Paris)"},{"key":"4019_CR19","doi-asserted-by":"publisher","first-page":"7","DOI":"10.3121\/cmr.2009.867","volume":"8","author":"CL Wiley","year":"2010","unstructured":"Wiley CL, Switzer SP, Berg RL, Glurich I, Dart RA (2010) Association of B-type natriuretic peptide levels with estimated glomerular filtration rate and congestive heart failure. Clin Med Res 8:7\u201312","journal-title":"Clin Med Res"},{"key":"4019_CR20","doi-asserted-by":"publisher","first-page":"303","DOI":"10.1111\/eci.12234","volume":"44","author":"H Takase","year":"2014","unstructured":"Takase H, Dohi Y (2014) Kidney function crucially affects B-type natriuretic peptide (BNP), N-terminal proBNP and their relationship. Eur J Clin Investig 44:303\u2013308","journal-title":"Eur J Clin Investig"},{"key":"4019_CR21","first-page":"15","volume":"20","author":"NK Yuen","year":"2016","unstructured":"Yuen NK, Ananthakrishnan S, Campbell MJ (2016) Hyperparathyroidism of renal disease. Perm J 20:15\u2013127","journal-title":"Perm J"},{"key":"4019_CR22","doi-asserted-by":"publisher","first-page":"18","DOI":"10.3177\/jnsv.64.18","volume":"64","author":"S-W Choi","year":"2018","unstructured":"Choi S-W, Kweon S-S, Lee Y-H, Ryu S-Y, Choi J-S, Nam H-S et al (2018) Parathyroid hormone levels are independently associated with eGFR and albuminuria: the Dong-gu study. J Nutr Sci Vitaminol 64:18\u201325","journal-title":"J Nutr Sci Vitaminol"},{"key":"4019_CR23","doi-asserted-by":"publisher","first-page":"629","DOI":"10.4158\/EP14537.OR","volume":"21","author":"F Tassone","year":"2015","unstructured":"Tassone F, Gianotti L, Baffoni C, Pellegrino M, Castellano E, Borretta G (2015) KDIGO categories of glomerular filtration rate and parathyroid hormone secretion in primary hyperparathyroidism. Endocr Pract 21:629\u2013633","journal-title":"Endocr Pract"},{"key":"4019_CR24","doi-asserted-by":"crossref","unstructured":"Bolignano D, Lacquaniti A, Coppolino G, Donato V, Campo S, Fazio MR et al (2009) Neutrophil gelatinase-associated lipocalin (NGAL) and progression of chronic kidney disease. Clin J Am Soc Nephrol 337-344","DOI":"10.2215\/CJN.03530708"},{"key":"4019_CR25","doi-asserted-by":"publisher","first-page":"1012","DOI":"10.1053\/j.ajkd.2009.07.020","volume":"54","author":"M Haase","year":"2009","unstructured":"Haase M, Bellomo R, Devarajan P, Schlattmann P, Haase-Fielitz A, NGAL Meta-analysis Investigator Group (2009) Accuracy of neutrophil gelatinase-associated lipocalin (NGAL) in diagnosis and prognosis in acute kidney injury: a systematic review and meta-analysis. Am J Kidney Dis 54:1012\u20131024","journal-title":"Am J Kidney Dis"},{"key":"4019_CR26","doi-asserted-by":"publisher","first-page":"1009","DOI":"10.1016\/j.jpeds.2010.12.057","volume":"158","author":"CD Krawczeski","year":"2011","unstructured":"Krawczeski CD, Woo JG, Wang Y, Bennett MR, Ma Q, Devarajan P (2011) Neutrophil gelatinase-associated lipocalin concentrations predict development of acute kidney injury in neonates and children after cardiopulmonary bypass. J Pediatr 158:1009\u20131015.e1","journal-title":"J Pediatr"},{"key":"4019_CR27","doi-asserted-by":"publisher","first-page":"401","DOI":"10.2215\/CJN.04860514","volume":"B10","author":"SH Witzel","year":"2015","unstructured":"Witzel SH, Huang S-HS, Braam B, Filler G (2015) Estimation of GFR using \u03b2-trace protein in children. Clin J Am Soc Nephrol B10:401\u2013409","journal-title":"Clin J Am Soc Nephrol"},{"key":"4019_CR28","doi-asserted-by":"publisher","first-page":"786","DOI":"10.1016\/j.ekir.2019.02.010","volume":"4","author":"D Scarr","year":"2019","unstructured":"Scarr D, Bjornstad P, Lovblom LE, Lovshin JA, Boulet G, Lytvyn Y, Farooqi MA, Lai V, Orszag A, Weisman A, Keenan HA, Brent MH, Paul N, Bril V, Cherney DZI, Perkins BA (2019) Estimating GFR by serum creatinine, cystatin C, and \u03b22-microglobulin in older adults: results from the Canadian study of longevity in type 1 diabetes. Kidney Int Rep 4:786\u2013796","journal-title":"Kidney Int Rep"},{"key":"4019_CR29","first-page":"S0272-6386(20)3","volume":"4","author":"LA Inker","year":"2020","unstructured":"Inker LA, Couture SJ, Tighiouart H, Abraham AG, Beck GJ, Feldman HI et al (2020) A new panel estimated GFR, including \u03b22-microglobulin and \u03b2-trace protein and not including race, developed in a diverse population. Am J Kidney Dis 4:S0272-6386(20)31126-4","journal-title":"Am J Kidney Dis"},{"key":"4019_CR30","doi-asserted-by":"publisher","first-page":"172","DOI":"10.1016\/j.xkme.2019.11.004","volume":"2","author":"N Chen","year":"2020","unstructured":"Chen N, Shi H, Zhang L, Zuo L, Xie J, Xie D, Karger AB, Miao S, Ren H, Zhang W, Wang W, Pan Y, Minji W, Sui Z, Okparavero A, Simon A, Chaudhari J, Eckfeldt JH, Inker LA, Levey AS (2020) GFR estimation using a panel of filtration markers in Shanghai and Beijing. Kidney Med 2:172\u2013180","journal-title":"Kidney Med"},{"key":"4019_CR31","doi-asserted-by":"publisher","first-page":"1553","DOI":"10.1007\/s00467-018-3973-8","volume":"33","author":"E den Bakker","year":"2018","unstructured":"den Bakker E, Gemke R, van Wijk JAE, Hubeek I, Stoffel-Wagner B, B\u00f6kenkamp A (2018) Combining GFR estimates from cystatin C and creatinine-what is the optimal mix? Pediatr Nephrol 33:1553\u20131563","journal-title":"Pediatr Nephrol"},{"key":"4019_CR32","first-page":"437","volume":"165","author":"F Deng","year":"2015","unstructured":"Deng F, Finer G, Haymond S, Brooks E, Langman CB (2015) Applicability of estimating glomerular filtration rate equations in pediatric patients: comparison with a measured glomerular filtration rate by iohexol clearance. Transl Res J Lab Clin Med 165:437\u2013445","journal-title":"Transl Res J Lab Clin Med"}],"container-title":["European Journal of Pediatrics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00431-021-04019-w.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s00431-021-04019-w\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00431-021-04019-w.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,6,11]],"date-time":"2021-06-11T14:11:07Z","timestamp":1623420667000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s00431-021-04019-w"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,3,10]]},"references-count":32,"journal-issue":{"issue":"7","published-print":{"date-parts":[[2021,7]]}},"alternative-id":["4019"],"URL":"https:\/\/doi.org\/10.1007\/s00431-021-04019-w","relation":{},"ISSN":["0340-6199","1432-1076"],"issn-type":[{"value":"0340-6199","type":"print"},{"value":"1432-1076","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,3,10]]},"assertion":[{"value":"18 August 2020","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"2 March 2021","order":2,"name":"revised","label":"Revised","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"4 March 2021","order":3,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"10 March 2021","order":4,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The study has been approved by the local Ethic Committee (Lausanne Ethic Research Committee Protocol number 345\/12).","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval"}},{"value":"The study has been approved by the Research Ethic Committee of Lausanne.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent to participate and for publication"}},{"value":"The authors declare no competing interests.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}]}}