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Renal morphology and glomerular capillarisation in young adult sheep born moderately preterm

Published online by Cambridge University Press:  10 December 2020

Megan R. Sutherland Open the ORCID record for Megan R. Sutherland [Opens in a new window] ,
Waleed Malik ,
Vivian B. Nguyen ,
Vivian Tran ,
Graeme R. Polglase  and
Mary Jane Black
Megan R. Sutherland*
Affiliation:
Department of Anatomy and Developmental Biology and the Monash Biomedicine Discovery Institute, Monash University, Clayton, Victoria, Australia
Waleed Malik
Affiliation:
Department of Anatomy and Developmental Biology and the Monash Biomedicine Discovery Institute, Monash University, Clayton, Victoria, Australia
Vivian B. Nguyen
Affiliation:
Department of Anatomy and Developmental Biology and the Monash Biomedicine Discovery Institute, Monash University, Clayton, Victoria, Australia
Vivian Tran
Affiliation:
Department of Anatomy and Developmental Biology and the Monash Biomedicine Discovery Institute, Monash University, Clayton, Victoria, Australia
Graeme R. Polglase
Affiliation:
The Ritchie Centre, Department of Obstetrics and Gynaecology, Monash University and the Hudson Institute of Medical Research, Clayton, Victoria, Australia
Mary Jane Black
Affiliation:
Department of Anatomy and Developmental Biology and the Monash Biomedicine Discovery Institute, Monash University, Clayton, Victoria, Australia
*
Address for correspondence: Megan Sutherland, Department of Anatomy & Developmental Biology, 19 Innovation Walk, Building 76, Monash University, Clayton, Victoria, 3800, Australia. Email: megan.sutherland@monash.edu
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Abstract

Preterm birth (delivery <37 weeks of gestation) is associated with impaired glomerular capillary growth in neonates; if this persists, it may be a contributing factor in the increased risk of hypertension and chronic kidney disease in people born preterm. Therefore, in this study, we aimed to determine the long-term impact of preterm birth on renal morphology, in adult sheep. Singleton male sheep were delivered moderately preterm at 132 days (~0.9) of gestation (n = 6) or at term (147 days gestation; n = 6) and euthanised at 14.5 months of age (early adulthood). Stereological methods were used to determine mean renal corpuscle and glomerular volumes, and glomerular capillary length and surface area, in the outer, mid and inner regions of the renal cortex. Glomerulosclerosis and interstitial collagen levels were assessed histologically. By 14.5 months of age, there was no difference between the term and preterm sheep in body or kidney weight. Renal corpuscle volume was significantly larger in the preterm sheep than the term sheep, with the preterm sheep exhibiting enlarged Bowman’s spaces; however, there was no difference in glomerular volume between groups, with no impact of preterm birth on capillary length or surface area per glomerulus. There was also no difference in interstitial collagen levels or glomerulosclerosis index between groups. Findings suggest that moderate preterm birth does not adversely affect glomerular structure in early adulthood. The enlarged Bowman’s space in the renal corpuscles of the preterm sheep kidneys, however, is of concern and merits further research into its cause and functional consequences.

Keywords

Preterm birthkidney developmentkidney diseaseglomerulusBowman’s space
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 12 , Issue 6 , December 2021 , pp. 975 - 981
Copyright
© The Author(s), 2020. Published by Cambridge University Press in association with International Society for Developmental Origins of Health and Disease

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References

Chawanpaiboon, S, Vogel, JP, Moller, AB, et al. Global, regional, and national estimates of levels of preterm birth in 2014: a systematic review and modelling analysis. Lancet Glob Health. 2019; 7(1), e37–e46.CrossRefGoogle ScholarPubMed
Goldenberg, RL, Culhane, JF, Iams, JD, Romero, R. Epidemiology and causes of preterm birth. Lancet. 2008; 371(9606), 75–84.CrossRefGoogle ScholarPubMed
Australian Institute of Health and Welfare. Australia’s mothers and babies 2017—in brief. Canberra: AIHW, 2019.Google Scholar
Luu, TM, Katz, SL, Leeson, P, Thebaud, B, Nuyt, AM. Preterm birth: risk factor for early-onset chronic diseases. CMAJ. 2016; 188(10), 736–746.CrossRefGoogle ScholarPubMed
de Jong, F, Monuteaux, MC, van Elburg, RM, Gillman, MW, Belfort, MB. Systematic review and meta-analysis of preterm birth and later systolic blood pressure. Hypertension. 2012; 59(2), 226–234.CrossRefGoogle ScholarPubMed
Hovi, P, Vohr, B, Ment, LR, et al. Blood pressure in young adults born at very low birth weight: adults born preterm international collaboration. Hypertension. 2016; 68(4), 880–887.CrossRefGoogle ScholarPubMed
Parkinson, JR, Hyde, MJ, Gale, C, Santhakumaran, S, Modi, N. Preterm birth and the metabolic syndrome in adult life: a systematic review and meta-analysis. Pediatrics. 2013; 131(4), e1240–e1263.CrossRefGoogle ScholarPubMed
Edwards, MO, Watkins, WJ, Kotecha, SJ, et al. Higher systolic blood pressure with normal vascular function measurements in preterm-born children. Acta Paediatr. 2014; 103(9), 904–912.CrossRefGoogle ScholarPubMed
Carmody, JB, Charlton, JR. Short-term gestation, long-term risk: prematurity and chronic kidney disease. Pediatrics. 2013; 131(6), 1168–1179.CrossRefGoogle ScholarPubMed
Sutherland, M, Ryan, D, Black, MJ, Kent, AL. Long-term renal consequences of preterm birth. Clin Perinatol. 2014; 41(3), 561–573.CrossRefGoogle ScholarPubMed
Ikezumi, Y, Suzuki, T, Karasawa, T, et al. Low birthweight and premature birth are risk factors for podocytopenia and focal segmental glomerulosclerosis. Am J Nephrol. 2013; 38(2), 149–157.CrossRefGoogle ScholarPubMed
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(1), 71–76.CrossRefGoogle ScholarPubMed
Koike, K, Ikezumi, Y, Tsuboi, N, et al. Glomerular density and volume in renal biopsy specimens of children with proteinuria relative to preterm birth and gestational age. Clin J Am Soc Nephrol. 2017; 12(4), 585–590.CrossRefGoogle ScholarPubMed
Hirano, D, Ishikura, K, Uemura, O, et al. Association between low birth weight and childhood-onset chronic kidney disease in Japan: a combined analysis of a nationwide survey for paediatric chronic kidney disease and the National Vital Statistics Report. Nephrol Dial Transplant. 2016; 31(11), 1895–1900.CrossRefGoogle ScholarPubMed
Crump, C, Sundquist, J, Winkleby, MA, Sundquist, K. Preterm birth and risk of chronic kidney disease from childhood into mid-adulthood: national cohort study. BMJ. 2019; 365, l1346.CrossRefGoogle ScholarPubMed
Ryan, D, Sutherland, MR, Flores, TJ, et al. Development of the human fetal kidney from mid to late gestation in male and female infants. EBioMedicine. 2018; 27, 275–283.CrossRefGoogle ScholarPubMed
Moore, L, Williams, R, Staples, A. Glomerular dimensions in children under 16 years of age. J Pathol. 1993; 171(2), 145–150.CrossRefGoogle ScholarPubMed
Thony, HC, Luethy, CM, Zimmermann, A, Laux-End, R, Oetliker, OH, Bianchetti, MG. Histological features of glomerular immaturity in infants and small children with normal or altered tubular function. Eur J Pediatr. 1995; 154(9 Suppl 4), S65–S68.CrossRefGoogle ScholarPubMed
Sutherland, MR, Gubhaju, L, Moore, L, et al. Accelerated maturation and abnormal morphology in the preterm neonatal kidney. J Am Soc Nephrol. 2011; 22(7), 1365–1374.CrossRefGoogle ScholarPubMed
Rodriguez, MM, Gomez, AH, Abitbol, CL, Chandar, JJ, Duara, S, Zilleruelo, GE. Histomorphometric analysis of postnatal glomerulogenesis in extremely preterm infants. Pediatr Dev Pathol. 2004; 7(1), 17–25.CrossRefGoogle ScholarPubMed
Gubhaju, L, Sutherland, MR, Yoder, BA, Zulli, A, Bertram, JF, Black, MJ. Is nephrogenesis affected by preterm birth? Studies in a non-human primate model. Am J Physiol Renal Physiol. 2009; 297(6), F1668–F1677.CrossRefGoogle Scholar
Sutherland, MR, Gubhaju, L, Yoder, BA, Stahlman, MT, Black, MJ. The effects of postnatal retinoic acid administration on nephron endowment in the preterm baboon kidney. Pediatr Res. 2009; 65(4), 397–402.CrossRefGoogle ScholarPubMed
Sutherland, MR, Ryan, D, Dahl, MJ, Albertine, KH, Black, MJ. Effects of preterm birth and ventilation on glomerular capillary growth in the neonatal lamb kidney. J Hypertens. 2016; 34(10), 1988–1997.CrossRefGoogle ScholarPubMed
Staub, E, Dahl, MJ, Yost, C, et al. Preterm birth and ventilation decrease surface density of glomerular capillaries in lambs, regardless of postnatal respiratory support mode. Pediatr Res. 2017; 82(1), 93–100.CrossRefGoogle ScholarPubMed
Fong, D, Denton, KM, Moritz, KM, Evans, R, Singh, RR. Compensatory responses to nephron deficiency: adaptive or maladaptive? Nephrology (Carlton). 2014; 19(3), 119–128.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), 335–347.CrossRefGoogle ScholarPubMed
De Matteo, R, Ishak, N, Hanita, T, Harding, R, Sozo, F. Respiratory adaptation and surfactant composition of unanesthetized male and female lambs differ for up to 8 h after preterm birth. Pediatr Res. 2016; 79(1), 13–21.CrossRefGoogle ScholarPubMed
Ishak, N, Hanita, T, Sozo, F, Maritz, G, Harding, R, De Matteo, R. Sex differences in cardiorespiratory transition and surfactant composition following preterm birth in sheep. Am J Physiol Regul Integr Comp Physiol 2012; 303(7), R778–R789.CrossRefGoogle ScholarPubMed
Peacock, JL, Marston, L, Marlow, N, Calvert, SA, Greenough, A. Neonatal and infant outcome in boys and girls born very prematurely. Pediatr Res. 2012; 71(3), 305–310.CrossRefGoogle ScholarPubMed
Ingemarsson, I. Gender aspects of preterm birth. BJOG. 2003; 110(Suppl 20), 34–38.CrossRefGoogle ScholarPubMed
Evans, M, Fryzek, JP, Elinder, CG, et al. The natural history of chronic renal failure: results from an unselected, population-based, inception cohort in Sweden. Am J Kidney Dis. 2005; 46(5), 863–870.CrossRefGoogle ScholarPubMed
Eriksen, BO, Ingebretsen, OC. The progression of chronic kidney disease: a 10-year population-based study of the effects of gender and age. Kidney Int. 2006; 69(2), 375–382.CrossRefGoogle ScholarPubMed
Neugarten, J, Golestaneh, L. Gender and the prevalence and progression of renal disease. Adv Chronic Kidney Dis. 2013; 20(5), 390–395.CrossRefGoogle ScholarPubMed
Nguyen, VB, De Matteo, R, Harding, R, Stefanidis, A, Polglase, GR, Black, MJ. Experimentally induced preterm birth in sheep following a clinical course of antenatal betamethasone: effects on growth and long-term survival. Reprod Sci. 2017; 24(8), 1203–1213.CrossRefGoogle ScholarPubMed
Gundersen, HJ. The smooth fractionator. J Microsc. 2002; 207(Pt 3), 191–210.CrossRefGoogle ScholarPubMed
Sutherland, MR, Vojisavljevic, D, Black, MJ. A practical guide to the stereological assessment of glomerular number, size, and cellular composition. Anat Rec. 2020; 303, 2679–2692.CrossRefGoogle Scholar
Sutherland, MR, O’Reilly, M, Kenna, K, et al. Neonatal hyperoxia: effects on nephrogenesis and long-term glomerular structure. Am J Physiol Renal Physiol. 2013; 304(10), F1308–F1316.CrossRefGoogle ScholarPubMed
Sutherland, MR, Beland, C, Lukaszewski, MA, Cloutier, A, Bertagnolli, M, Nuyt, AM. Age- and sex-related changes in rat renal function and pathology following neonatal hyperoxia exposure. Physiol Rep. 2016; 4(15), e12887.CrossRefGoogle ScholarPubMed
Weibel, ER, Gomez, DM. A principle for counting tissue structures on random sections. J Appl Physiol. 1962; 17, 343–348.CrossRefGoogle ScholarPubMed
Barros, FC, Papageorghiou, AT, Victora, CG, et al. The distribution of clinical phenotypes of preterm birth syndrome: implications for prevention. JAMA Pediatr. 2015; 169(3), 220–229.CrossRefGoogle ScholarPubMed
Dusick, AM, Poindexter, BB, Ehrenkranz, RA, Lemons, JA. Growth failure in the preterm infant: can we catch up? Semin Perinatol. 2003; 27(4), 302–310.CrossRefGoogle ScholarPubMed
Johnson, MJ, Wootton, SA, Leaf, AA, Jackson, AA. Preterm birth and body composition at term equivalent age: a systematic review and meta-analysis. Pediatrics. 2012; 130(3), e640–e649.CrossRefGoogle ScholarPubMed
Batista, RF, Silva, AA, Barbieri, MA, Simoes, VM, Bettiol, H. Factors associated with height catch-up and catch-down growth among schoolchildren. PLoS One. 2012; 7(3), e32903.CrossRefGoogle ScholarPubMed
Roberts, G, Cheong, J, Opie, G, et al. Growth of extremely preterm survivors from birth to 18 years of age compared with term controls. Pediatrics. 2013; 131(2), e439–e445.CrossRefGoogle ScholarPubMed
Clark, RH, Thomas, P, Peabody, J. Extrauterine growth restriction remains a serious problem in prematurely born neonates. Pediatrics. 2003; 111(5 Pt 1), 986–990.CrossRefGoogle ScholarPubMed
Kwinta, P, Klimek, M, Drozdz, D, et al. Assessment of long-term renal complications in extremely low birth weight children. Pediatr Nephrol. 2011; 26(7), 1095–1103.CrossRefGoogle ScholarPubMed
Rakow, A, Johansson, S, Legnevall, L, et al. Renal volume and function in school-age children born preterm or small for gestational age. Pediatr Nephrol. 2008; 23(8), 1309–1315.CrossRefGoogle ScholarPubMed
Keijzer-Veen, MG, Devos, AS, Meradji, M, Dekker, FW, Nauta, J, van der Heijden, BJ. Reduced renal length and volume 20 years after very preterm birth. Pediatr Nephrol. 2010; 25(3), 499–507.CrossRefGoogle ScholarPubMed
Rakow, A, Laestadius, A, Liliemark, U, et al. Kidney volume, kidney function, and ambulatory blood pressure in children born extremely preterm with and without nephrocalcinosis. Pediatr Nephrol. 2019; 34(10), 1765–1776.CrossRefGoogle ScholarPubMed
Starzec, K, Klimek, M, Grudzien, A, Jagla, M, Kwinta, P. Longitudinal assessment of renal size and function in extremely low birth weight children at 7 and 11 years of age. Pediatr Nephrol. 2016; 31(11), 2119–2126.CrossRefGoogle ScholarPubMed
Zaffanello, M, Brugnara, M, Bruno, C, et al. Renal function and volume of infants born with a very low birth-weight: a preliminary cross-sectional study. Acta Paediatr. 2010; 99(8), 1192–1198.CrossRefGoogle ScholarPubMed
Sasaki, T, Tsuboi, N, Haruhara, K, et al. Bowman capsule volume and related factors in adults with normal renal function. Kidney Int Rep. 2018; 3(2), 314–320.CrossRefGoogle ScholarPubMed
Tobar, A, Ori, Y, Benchetrit, S, et al. Proximal tubular hypertrophy and enlarged glomerular and proximal tubular urinary space in obese subjects with proteinuria. PLoS One 2013; 8(9), e75547.CrossRefGoogle ScholarPubMed
Mrocki, MM, Nguyen, VB, Lombardo, P, et al. Moderate preterm birth affects right ventricular structure and function and pulmonary artery blood flow in adult sheep. J Physiol. 2018; 596(23), 5965–5975.CrossRefGoogle ScholarPubMed
Osathanondh, V, Potter, EL. Development of human kidney as shown by microdissection. III. Formation and interrelationship of collecting tubules and nephrons. Arch Pathol. 1963; 76, 290–302.Google ScholarPubMed
Puelles, VG, Zimanyi, MA, Samuel, T, et al. Estimating individual glomerular volume in the human kidney: clinical perspectives. Nephrol Dial Transplant. 2011; 27(5), 1880–1888.CrossRefGoogle ScholarPubMed
Gimonet, V, Bussieres, L, Medjebeur, AA, Gasser, B, Lelongt, B, Laborde, K. Nephrogenesis and angiotensin II receptor subtypes gene expression in the fetal lamb. Am J Physiol. 1998; 274(6), F1062–F1069.Google ScholarPubMed