Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-28T12:10:02.378Z Has data issue: false hasContentIssue false

Can measurement of the foetal renal parenchymal thickness with ultrasound be used as an indirect measure of nephron number?

Published online by Cambridge University Press:  15 April 2020

Sonja Brennan*
Affiliation:
Ultrasound Department, The Townsville Hospital, Douglas, Townsville, Australia College of Public Health, Medical and Veterinary Sciences, James Cook University, Townsville, Australia
David Watson
Affiliation:
Maternal Fetal Medicine Unit, Department of Obstetrics and Gynaecology, The Townsville Hospital, Townsville, Australia
Michal Schneider
Affiliation:
Department of Medical Imaging & Radiation Sciences, Monash University, Melbourne, Australia
Donna Rudd
Affiliation:
College of Public Health, Medical and Veterinary Sciences, James Cook University, Townsville, Australia
Yogavijayan Kandasamy
Affiliation:
College of Public Health, Medical and Veterinary Sciences, James Cook University, Townsville, Australia Department of Neonatology, The Townsville Hospital, Townsville, Australia Mothers and Babies Research Centre, Hunter Medical Research Institute, John Hunter Hospital, The University of Newcastle, Newcastle, Australia
*
Address for correspondence: Sonja Brennan, Ultrasound Department, The Townsville Hospital, IMB 47, P.O. Box 670, Douglas, Townsville, QLD4810, Australia. Email: [email protected]; [email protected]

Abstract

Chronic kidney disease continues to be under recognised and is associated with a significant global health burden and costs. An adverse intrauterine environment may result in a depleted nephron number and an increased risk of chronic kidney disease. Antenatal ultrasound was used to measure the foetal renal parenchymal thickness (RPT), as a novel method to estimate nephron number. Foetal renal artery blood flow was also assessed. This prospective, longitudinal study evaluated the foetal kidneys of 102 appropriately grown and 30 foetal growth-restricted foetuses between 20 and 37 weeks gestational age (GA) to provide vital knowledge on the influences foetal growth restriction has on the developing kidneys. The foetal RPT and renal artery blood flow were measured at least every 4 weeks using ultrasound. The RPT was found to be significantly thinner in growth-restricted foetuses compared to appropriately grown foetuses [likelihood ratio (LR) = 21.06, P ≤ 0.0001] and the difference increases with GA. In foetuses with the same head circumference, a growth-restricted foetus was more likely to have a thinner parenchyma than an appropriately grown foetus (LR = 8.9, P = 0.0028), supporting the principle that growth-restricted foetuses preferentially shunt blood towards the brain. No significant difference was seen in the renal arteries between appropriately grown and growth-restricted foetuses. Measurement of the RPT appears to be a more sensitive measure than current methods. It has the potential to identify infants with a possible reduced nephron endowment allowing for monitoring and interventions to be focused on individuals at a higher risk of developing future hypertension and chronic kidney disease.

Type
Original Article
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Luyckx, VA, Tonelli, M, Stanifer, JW. The global burden of kidney disease and the sustainable development goals. Bull World Health Organ. 2018; 96(6), 41422D.CrossRefGoogle ScholarPubMed
Couser, WG, Remuzzi, G, Mendis, S, Tonelli, M. The contribution of chronic kidney disease to the global burden of major noncommunicable diseases. Kidney Int. 2011; 80(12), 12581270.CrossRefGoogle ScholarPubMed
Levey, AS, Atkins, R, Coresh, J, et al. Chronic kidney disease as a global public health problem: Approaches and initiatives - a position statement from Kidney Disease Improving Global Outcomes. Kidney Int. 2007; 72(3), 247259.CrossRefGoogle ScholarPubMed
Brenner, BM, Garcia, DL, Anderson, S. Glomeruli and blood pressure. Less of one, more the other? Am J Hypertens. 1988; 1(4 Pt 1), 335347.CrossRefGoogle ScholarPubMed
Luyckx, VA, Brenner, BM. Birth weight, malnutrition and kidney-associated outcomes--a global concern. Nat Rev Nephrol. 2015; 11(3), 135149.CrossRefGoogle ScholarPubMed
Zohdi, V, Sutherland, MR, Lim, K, Gubhaju, L, Zimanyi, MA, Black, MJ. Low birth weight due to intrauterine growth restriction and/or preterm birth: effects on nephron number and long-term renal health. Int J Nephrol. 2012; 2012, 13.CrossRefGoogle ScholarPubMed
Bagby, SP. Developmental origins of renal disease: should nephron protection begin at birth? Clin J Am Soc Nephrol. 2009; 4(1), 1013.CrossRefGoogle ScholarPubMed
Hinchliffe, SA, Lynch, MRJ, Sargent, PH, Howard, CV, Van Velzen, D. The effect of intrauterine growth retardation on the development of renal nephrons. BJOG. 1992; 99(4), 296301.CrossRefGoogle ScholarPubMed
White, SL, Perkovic, V, Cass, A, et al. Is low birth weight an antecedent of CKD in later life? A systematic review of observational studies. Am J Kidney Dis. 2009; 54(2), 248261.CrossRefGoogle ScholarPubMed
Smith, GCS. Universal screening for foetal growth restriction. Best Pract Res Clin Obstet Gynaecol. 2018; 49, 1628.CrossRefGoogle ScholarPubMed
Resnik, RMD. Intrauterine growth restriction. Obstet Gynecol. 2002; 99(3), 490496.Google ScholarPubMed
Barker, DJ, Osmond, C, Law, CM. The intrauterine and early postnatal origins of cardiovascular disease and chronic bronchitis. J Epidemiol Community Health. 1989; 43(3), 237240.CrossRefGoogle ScholarPubMed
Gordijn, SJ, Beune, IM, Thilaganathan, B, et al. Consensus definition of fetal growth restriction: a Delphi procedure. Ultrasound Obstet Gynecol. 2016; 48(3), 333339.CrossRefGoogle ScholarPubMed
Hoy, WE, Bertram, JF, Denton, RD, Zimanyi, M, Samuel, T, Hughson, MD. Nephron number, glomerular volume, renal disease and hypertension. Curr Opin Nephrol Hypertens. 2008; 17(3), 258265.CrossRefGoogle ScholarPubMed
Luyckx, VA, Bertram, JF, Brenner, BM, et al. Effect of fetal and child health on kidney development and long-term risk of hypertension and kidney disease. The Lancet. 2013; 382(9888), 273283.CrossRefGoogle ScholarPubMed
Brennan, S, Watson, D, Rudd, D, Schneider, M, Kandasamy, Y. Evaluation of fetal kidney growth using ultrasound: a systematic review. Eur J Radiol. 2017; 96, 5564.CrossRefGoogle ScholarPubMed
Ismaili, K, Schurmans, T, Wissing, KM, Hall, M, Van Aelst, C, Janssen, F. Early prognostic factors of infants with chronic renal failure caused by renal dysplasia. Pediatr Nephrol. 2001; 16(3), 260264.CrossRefGoogle ScholarPubMed
Baschat, AA, Hecher, K. Fetal growth restriction due to placental disease. Semin Perinatol. 2004; 28(1), 6780.CrossRefGoogle ScholarPubMed
Townsville Hospital and Health Service Annual Report 2017-2018. Townsville Hospital and Health Service; 2018.Google Scholar
Brennan, S, Kandasamy, Y. Renal parenchymal thickness as a measure of renal growth in low-birth-weight infants versus normal-birth-weight infants. Ultrasound Med Biol. 2013; 39(12), 23152320.CrossRefGoogle ScholarPubMed
Hadlock, FP, Harrist, RB, Sharman, RS, Deter, RL, Park, SK. Estimation of fetal weight with the use of head, body, and femur measurements—a prospective study. Am J Obstet Gynecol. 1985; 151(3), 333337.CrossRefGoogle ScholarPubMed
Nicolaides, KH, Wright, D, Syngelaki, A, Wright, A, Akolekar, R. Fetal medicine foundation fetal and neonatal population weight charts. Ultrasound Obstet Gynecol. 2018; 52(1), 4451.CrossRefGoogle ScholarPubMed
Core Team, R. R: A language and environment for statistical computing. R Foundation for Statistical Computing. 2019. Available from: URL https://www.R-project.org/.Google Scholar
RStudio Team. RStudio: Integrated Development Environment for R. RStudio, Inc. 2018. Available from: http://www.rstudio.com/.Google Scholar
Pinheiro, J, Bates, D, DebRoy, S, Sarkar, D, R Core Team. nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1-139. 2019. Available from: https://CRAN.R-project.org/package=nlme.Google Scholar
Wickham, H. ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag. 2016. Available from: https://ggplot2.tidyverse.org.CrossRefGoogle Scholar
Silver, LE, Decamps, PJ, Korst, LM, Platt, LD, Castro, L. Intrauterine growth restriction is accompanied by decreased renal volume in the human fetus.[Erratum appears in Am J Obstet Gynecol. 2004 Mar; 27(3):1062]. Am J Obstet Gynecol. 2003; 188(5), 13201350.CrossRefGoogle Scholar
Chang, CH, Tsai, PY, Yu, CH, Ko, HC, Chang, FM. Predicting fetal growth restriction with renal volume using 3-D ultrasound: efficacy evaluation. Ultrasound Med Biol. 2008; 34(4), 533537.CrossRefGoogle ScholarPubMed
Drougia, A, Giapros, V, Hotoura, E, Papadopoulou, F, Argyropoulou, M, Andronikou, S. The effects of gestational age and growth restriction on compensatory kidney growth. Nephrol Dial Transplant. 2009; 24(1), 142148.CrossRefGoogle ScholarPubMed
Figueras, F, Gratacos, E. An integrated approach to fetal growth restriction. Best Pract Res Clin Obstet Gynaecol. 2017; 38, 4858.CrossRefGoogle ScholarPubMed
Baayen, RH, Davidson, DJ, Bates, DM. Mixed-effects modeling with crossed random effects for subjects and items. J Mem and Lang. 2008; 59(4), 390412.CrossRefGoogle Scholar
Hinchliffe, SA, Sargent, PH, Howard, CV, Chan, YF, van Velzen, D. Human intrauterine renal growth expressed in absolute number of glomeruli assessed by the disector method and Cavalieri principle. Lab Invest. 1991; 64(6), 777784.Google ScholarPubMed
Verburg, BO, Geelhoed, JJM, Steegers, EAP, et al. Fetal kidney volume and its association with growth and blood flow in fetal life: the Generation R study. Kidney Int. 2007; 72(6), 754761.CrossRefGoogle ScholarPubMed
Konje, JC, Bell, SC, Morton, JJ, de Chazal, R, Taylor, DJ. Human fetal kidney morphometry during gestation and the relationship between weight, kidney morphometry and plasma active renin concentration at birth. Clin Sci. 1996; 91(2), 169175.CrossRefGoogle ScholarPubMed
Sharma, D, Shastri, S, Farahbakhsh, N, Sharma, P. Intrauterine growth restriction – part 1. J Matern Fetal Neonatal Med. 2016; 29(24), 39773987.CrossRefGoogle ScholarPubMed
Kandasamy, Y, Smith, R, Wright, IMR, Lumbers, ER. Relationships between glomerular filtration rate and kidney volume in low-birth-weight neonates. J Nephrol. 2013; 26(5), 894898.CrossRefGoogle ScholarPubMed
Kandasamy, Y, Smith, R, Wright, IMR, Lumbers, ER. Reduced nephron endowment in the neonates of Indigenous Australian peoples. J Dev Orig Health Dis. 2014; 5(1), 3135.CrossRefGoogle ScholarPubMed
Kooijman, MN, Bakker, H, van der Heijden, AJ, et al. Childhood kidney outcomes in relation to fetal blood flow and kidney size. J Am Soc Nephrol. 2014; 25(11), 26162624.CrossRefGoogle ScholarPubMed
Roderick, PJ, Jeffrey, RF, Yuen, HM, Godfrey, KM, West, J, Wright, J. Smaller kidney size at birth in South Asians: findings from the Born in Bradford birth cohort study. Nephrol Dial Transplant. 2016; 31(3), 455465.CrossRefGoogle ScholarPubMed
Bakker, J, Olree, M, Kaatee, R, de Lange, EE, Beek, FJ. In vitro measurement of kidney size: comparison of ultrasonography and MRI. Ultrasound Med Biol. 1998; 24(5), 683.CrossRefGoogle ScholarPubMed
Cheong, B, Muthupillai, R, Rubin, MF, Flamm, SD. Normal values for renal length and volume as measured by magnetic resonance imaging. Clin J Am Soc Nephrol. 2007; 2(1), 3845.CrossRefGoogle ScholarPubMed
Kadioglu, A. Renal measurements, including length, parenchymal thickness, and medullary pyramid thickness, in healthy children: What are the normative ultrasound values? AJR. 2010; 194(2), 509515.CrossRefGoogle ScholarPubMed
Brennan, S, Kandasamy, Y. Ultrasound imaging of the renal parenchyma of premature neonates for the assessment of renal growth and glomerulomegaly. Ultrasound Med Biol. 2017; 43(11), 25462549.CrossRefGoogle ScholarPubMed
Kelley, JC, White, JT, Goetz, JT, Romero, E, Leslie, JA, Prieto, JC. Sonographic renal parenchymal measurements for the evaluation and management of ureteropelvic junction obstruction in children. Front Pediatr. 2016; 4, 42.CrossRefGoogle ScholarPubMed
Eze, CU, Akpan, VP, Nwadike, IU. Sonographic assessment of normal renal parenchymal and medullary pyramid thicknesses among children in Enugu, Southeast, Nigeria. Radiography. 2016; 22(1), 2531.CrossRefGoogle Scholar
Hadar, E, Davidovits, M, Mashiach, R, et al. Sonographic evaluation of kidney parenchymal growth in the fetus. Arch Gynecol Obstet. 2012; 286(4), 867872.CrossRefGoogle ScholarPubMed
Stigter, RH, Mulder, EJ, Bruinse, HW, Visser, GH. Doppler studies on the fetal renal artery in the severely growth-restricted fetus. Ultrasound Obstet Gynecol. 2001; 18(2), 141145.CrossRefGoogle ScholarPubMed
Blackburn, S. Maternal, Fetal, & Neonatal Physiology. 5th ed, 2018; 720 p. Elsevier, St Louis, Mo, USA.Google Scholar
Luyckx, VA, Perico, N, Somaschini, M, et al. A developmental approach to the prevention of hypertension and kidney disease: a report from the Low Birth Weight and Nephron Number Working Group. Lancet. 2017; 390(10092), 424428.CrossRefGoogle ScholarPubMed
Supplementary material: File

Brennan et al. supplementary material

Tables S1-S7

Download Brennan et al. supplementary material(File)
File 28.7 KB