Experimentally induced intrauterine growth restriction in rabbits leads to differential remodelling of left versus right ventricular myocardial microstructure

Histochemistry and Cell Biology

Volumn 148, Issue 5, 2017, Pages 557-567

  Schipke, Julia ^a,b,f   Gonzalez Tendero, Anna ^c   Cornejo, Lidia ^c   Willführ, Alper ^a   Bijnens, Bart ^d,e   Crispi, Fatima ^c   Mühlfeld, Christian ^a,b,f   Gratacós, Eduard ^c  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b Cluster of Excellence REBIRTH (From Regenerative Biology to Reconstructive Therapy)   (Germany)

^c UNIVERSITY OF BARCELONA   (Spain)

^d INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^e UNIVERSITAT POMPEU FABRA   (Spain)

^f Biomedical Research in Endstage and Obstructive Lung Disease Hannover (BREATH)   (Germany)

Author keywords

Cardiomyocyte number; IUGR; Microvascularization; Ventricle related

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; CARDIAC MUSCLE CELL; CARDIOVASCULAR RISK; COMPARATIVE STUDY; CONTROLLED STUDY; DIASTOLIC DYSFUNCTION; DISEASE ASSOCIATION; ECHOCARDIOGRAPHY; GESTATIONAL AGE; HEART LEFT VENTRICLE; HEART MUSCLE CAPILLARY; HEART OUTPUT; HEART RIGHT VENTRICLE; HEART VENTRICLE REMODELING; HEART WEIGHT; INTRAUTERINE GROWTH RETARDATION; MICROVASCULARIZATION; NEW ZEALAND WHITE (RABBIT); NONHUMAN; PRIORITY JOURNAL; PULSATILITY INDEX; STEREOLOGY; ANIMAL; CARDIAC MUSCLE; DISEASE MODEL; FEMALE; HEART LEFT VENTRICLE FUNCTION; HEART RIGHT VENTRICLE FUNCTION; LEPORIDAE; LIGATION; PATHOLOGY; PLACENTA; PREGNANCY; UTERUS; VASCULARIZATION;

ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; FETAL GROWTH RETARDATION; LIGATION; MYOCARDIUM; PLACENTA; PREGNANCY; RABBITS; UTERUS; VENTRICULAR DYSFUNCTION, LEFT; VENTRICULAR DYSFUNCTION, RIGHT;

EID: 85022229264     PISSN: 09486143     EISSN: 1432119X     Source Type: Journal    
DOI: 10.1007/s00418-017-1587-z     Document Type: Article

References (43)

1. Alberry M, Soothill P (2007) Management of fetal growth restriction. Arch Dis Child Fetal Neonatal Ed 92:F62–F67. doi:10.1136/adc.2005.082297
2. Bae S, Xiao Y, Li G, Casiano CA, Zhang L (2003) Effect of maternal chronic hypoxic exposure during gestation on apoptosis in fetal rat heart. Am J Physiol Heart Circ Physiol 285:H983–H990. doi:10.1152/ajpheart.00005.2003
3. Barker DJ, Osmond C, Golding J, Kuh D, Wadsworth ME (1989) Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. BMJ 298:564–567
4. Baschat AA, Gembruch U (2002) Evaluation of the fetal coronary circulation. Ultrasound Obstet Gynecol 20:405–412. doi:10.1046/j.1469-0705.2002.00798.x
5. Baschat AA, Gembruch U, Reiss I, Gortner L, Diedrich K (1997) Demonstration of fetal coronary blood flow by Doppler ultrasound in relation to arterial and venous flow velocity waveforms and perinatal outcome—the ‘heart-sparing effect’. Ultrasound Obstet Gynecol 9:162–172. doi:10.1046/j.1469-0705.1997.09030162.x
6. Bernstein IM, Horbar JD, Badger GJ, Ohlsson A, Golan A (2000) Morbidity and mortality among very-low-birth-weight neonates with intrauterine growth restriction. The Vermont Oxford Network. Am J Obstet Gynecol 182:198–206
7. Botting KJ, McMillen IC, Forbes H, Nyengaard JR, Morrison JL (2014) Chronic hypoxemia in late gestation decreases cardiomyocyte number but does not change expression of hypoxia-responsive genes. J Am Heart Assoc. doi:10.1161/JAHA.113.000531
8. Breisch EA, Houser SR, Carey RA, Spann JF, Bove AA (1980) Myocardial blood flow and capillary density in chronic pressure overload of the feline left ventricle. Cardiovasc Res 14:469–475
9. Bruel A, Nyengaard JR (2005) Design-based stereological estimation of the total number of cardiac myocytes in histological sections. Basic Res Cardiol 100:311–319. doi:10.1007/s00395-005-0524-9
10. Bubb KJ, Cock ML, Black MJ, Dodic M, Boon WM, Parkington HC, Harding R, Tare M (2007) Intrauterine growth restriction delays cardiomyocyte maturation and alters coronary artery function in the fetal sheep. J Physiol 578:871–881. doi:10.1113/jphysiol.2006.121160
11. Buckingham M, Meilhac S, Zaffran S (2005) Building the mammalian heart from two sources of myocardial cells. Nat Rev Genet 6:826–835. doi:10.1038/nrg1710
12. Chaoui R (2004) Coronary arteries in fetal life: physiology, malformations and the “heart-sparing effect”. Acta Paediatr Suppl 93:6–12
13. Chen J, Yaniz-Galende E, Kagan HJ, Liang L, Hekmaty S, Giannarelli C, Hajjar R (2015) Abnormalities of capillary microarchitecture in a rat model of coronary ischemic congestive heart failure. Am J Physiol Heart Circ Physiol 308:H830–H840. doi:10.1152/ajpheart.00583.2014
14. Comas M, Crispi F, Cruz-Martinez R, Martinez JM, Figueras F, Gratacos E (2010) Usefulness of myocardial tissue Doppler vs conventional echocardiography in the evaluation of cardiac dysfunction in early-onset intrauterine growth restriction. Am J Obstet Gynecol 203:45–47. doi:10.1016/j.ajog.2010.02.044
15. Corstius HB, Zimanyi MA, Maka N, Herath T, Thomas W, van der Laarse A, Wreford NG, Black MJ (2005) Effect of intrauterine growth restriction on the number of cardiomyocytes in rat hearts. Pediatr Res 57:796–800. doi:10.1203/01.PDR.0000157726.65492.CD
16. Crispi F, Bijnens B, Figueras F, Bartrons J, Eixarch E, Le NF, Ahmed A, Gratacos E (2010) Fetal growth restriction results in remodeled and less efficient hearts in children. Circulation 121:2427–2436. doi:10.1161/CIRCULATIONAHA.110.937995
17. Crispi F, Bijnens B, Sepulveda-Swatson E, Cruz-Lemini M, Rojas-Benavente J, Gonzalez-Tendero A, Garcia-Posada R, Rodriguez-Lopez M, Demicheva E, Sitges M, Gratacos E (2014) Postsystolic shortening by myocardial deformation imaging as a sign of cardiac adaptation to pressure overload in fetal growth restriction. Circ Cardiovasc Imaging 7:781–787. doi:10.1161/CIRCIMAGING.113.001490
18. Eixarch E, Figueras F, Hernandez-Andrade E, Crispi F, Nadal A, Torre I, Oliveira S, Gratacos E (2009) An experimental model of fetal growth restriction based on selective ligature of uteroplacental vessels in the pregnant rabbit. Fetal Diagn Ther 26:203–211. doi:10.1159/000264063
19. Eixarch E, Hernandez-Andrade E, Crispi F, Illa M, Torre I, Figueras F, Gratacos E (2011) Impact on fetal mortality and cardiovascular Doppler of selective ligature of uteroplacental vessels compared with undernutrition in a rabbit model of intrauterine growth restriction. Placenta 32:304–309. doi:10.1016/j.placenta.2011.01.014
20. Figueras F, Gratacos E (2014) Update on the diagnosis and classification of fetal growth restriction and proposal of a stage-based management protocol. Fetal Diagn Ther 36:86–98. doi:10.1159/000357592
21. Hauton D, Ousley V (2009) Prenatal hypoxia induces increased cardiac contractility on a background of decreased capillary density. BMC Cardiovasc Disord 9:1. doi:10.1186/1471-2261-9-1
22. Hecher K, Snijders R, Campbell S, Nicolaides K (1995) Fetal venous, intracardiac, and arterial blood flow measurements in intrauterine growth retardation: relationship with fetal blood gases. Am J Obstet Gynecol 173:10–15
23. Iruretagoyena JI, Gonzalez-Tendero A, Garcia-Canadilla P, Amat-Roldan I, Torre I, Nadal A, Crispi F, Gratacos E (2014) Cardiac dysfunction is associated with altered sarcomere ultrastructure in intrauterine growth restriction. Am J Obstet Gynecol 210:550–557. doi:10.1016/j.ajog.2014.01.023
24. Kiserud T, Acharya G (2004) The fetal circulation. Prenat Diagn 24:1049–1059. doi:10.1002/pd.1062
25. Lim K, Zimanyi MA, Black MJ (2006) Effect of maternal protein restriction in rats on cardiac fibrosis and capillarization in adulthood. Pediatr Res 60:83–87. doi:10.1203/01.pdr.0000220361.08181.c3
26. Louey S, Jonker SS, Giraud GD, Thornburg KL (2007) Placental insufficiency decreases cell cycle activity and terminal maturation in fetal sheep cardiomyocytes. J Physiol 580:639–648. doi:10.1113/jphysiol.2006.122200
27. Master JS, Zimanyi MA, Yin KV, Moritz KM, Gallo LA, Tran M, Wlodek ME, Black MJ (2014) Transgenerational left ventricular hypertrophy and hypertension in offspring after uteroplacental insufficiency in male rats. Clin Exp Pharmacol Physiol 41:884–890. doi:10.1111/1440-1681.12303
28. Mayhew TM, Charnock-Jones DS, Kaufmann P (2004a) Aspects of human fetoplacental vasculogenesis and angiogenesis. III. Changes in complicated pregnancies. Placenta 25:127–139. doi:10.1016/j.placenta.2003.10.010
29. Mayhew TM, Wijesekara J, Baker PN, Ong SS (2004b) Morphometric evidence that villous development and fetoplacental angiogenesis are compromised by intrauterine growth restriction but not by pre-eclampsia. Placenta 25:829–833. doi:10.1016/j.placenta.2004.04.011
30. Mendez J, Keys A (1960) Density and composition of mammalian muscle. Metabolism 9:184–188
31. Morrison JL, Botting KJ, Dyer JL, Williams SJ, Thornburg KL, McMillen IC (2007) Restriction of placental function alters heart development in the sheep fetus. Am J Physiol Regul Integr Comp Physiol 293:R306–R313. doi:10.1152/ajpregu.00798.2006
32. Mühlfeld C (2014) Quantitative morphology of the vascularisation of organs: a stereological approach illustrated using the cardiac circulation. Ann Anat 196:12–19. doi:10.1016/j.aanat.2012.10.010
33. Mühlfeld C, Nyengaard JR, Mayhew TM (2010) A review of state-of-the-art stereology for better quantitative 3D morphology in cardiac research. Cardiovasc Pathol 19:65–82. doi:10.1016/j.carpath.2008.10.015
34. Olson EN (2006) Gene regulatory networks in the evolution and development of the heart. Science 313:1922–1927. doi:10.1126/science.1132292
35. Porrello ER, Widdop RE, Delbridge LM (2008) Early origins of cardiac hypertrophy: does cardiomyocyte attrition programme for pathological ‘catch-up’ growth of the heart? Clin Exp Pharmacol Physiol 35:1358–1364. doi:10.1111/j.1440-1681.2008.05036.x
36. Rudolph AM (1970) The changes in the circulation after birth. Their importance in congenital heart disease. Circulation 41:343–359
37. Schipke J, Banmann E, Nikam S, Voswinckel R, Kohlstedt K, Loot AE, Fleming I, Muhlfeld C (2014) The number of cardiac myocytes in the hypertrophic and hypotrophic left ventricle of the obese and calorie-restricted mouse heart. J Anat 225:539–547. doi:10.1111/joa.12236
38. Schipke J, Roloff K, Kuhn M, Muhlfeld C (2015) Systemic, but not cardiomyocyte-specific, deletion of the natriuretic peptide receptor guanylyl cyclase A increases cardiomyocyte number in neonatal mice. Histochem Cell Biol 144:365–375. doi:10.1007/s00418-015-1337-z
39. Sterio DC (1984) The unbiased estimation of number and sizes of arbitrary particles using the disector. J Microsc 134:127–136
40. Thornburg KL, Reller MD (1999) Coronary flow regulation in the fetal sheep. Am J Physiol 277:R1249–R1260
41. Thornburg K, Jonker S, O’Tierney P, Chattergoon N, Louey S, Faber J, Giraud G (2011) Regulation of the cardiomyocyte population in the developing heart. Prog Biophys Mol Biol 106:289–299. doi:10.1016/j.pbiomolbio.2010.11.010
42. Wang KC, Brooks DA, Summers-Pearce B, Bobrovskaya L, Tosh DN, Duffield JA, Botting KJ, Zhang S, Caroline MI, Morrison JL (2015) Low birth weight activates the renin-angiotensin system, but limits cardiac angiogenesis in early postnatal life. Physiol Rep. doi:10.14814/phy2.12270
43. Weibel ER (1979) Stereological methods. Practical methods for biological morphometry, vol 1. Academic Press, New York