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Changes in renal hemodynamics of undernourished fetuses appear earlier than IUGR evidences

Published online by Cambridge University Press:  28 January 2018

A. Barbero
Affiliation:
Diagnostic Imaging Service, Universidad Alfonso X El Sabio, Spain
C. Porcu
Affiliation:
Department of Veterinary Medicine, University of Sassari, Sassari, Italy
A. Spezzigu
Affiliation:
Embryo Sardegna, Technology, Reproduction and Fertility, Perfugas, Sardegna, Italy
S. Succu
Affiliation:
Department of Veterinary Medicine, University of Sassari, Sassari, Italy
M. Dattena
Affiliation:
Department of Animal Production, AGRIS Sardegna, Italy
M. Gallus
Affiliation:
Department of Animal Production, AGRIS Sardegna, Italy
G. Molle
Affiliation:
Department of Animal Production, AGRIS Sardegna, Italy
S. Naitana
Affiliation:
Department of Veterinary Medicine, University of Sassari, Sassari, Italy
A. Gonzalez-Bulnes
Affiliation:
Comparative Physiology Group, SGIT-INIA, Spain
F. Berlinguer*
Affiliation:
Department of Veterinary Medicine, University of Sassari, Sassari, Italy
*
Author for correspondence: F. Berlinguer, Department of Veterinary Medicine, University of Sassari, Via Vienna 2, 07100 Sassari, Italy. E-mail: [email protected]

Abstract

The present study used a sheep model of intrauterine growth restriction, combining maternal undernutrition and twinning, to determine possible markers of early damage to the fetal kidney. The occurrence of early deviations in fetal hemodynamics which may be indicative of changes in blood perfusion was assessed by Doppler ultrasonography. A total of 24 sheep divided in two groups were fed with the same standard grain-based diet but fulfilling either their daily maintenance requirements for pregnancy (control group; n=12, six singleton and six twin pregnancies) or only the 50% of such quantity (food-restricted group; n=12; four singleton and eight twin pregnancies). All the fetuses were assessed by both B-mode and Doppler ultrasonography at Day 115 of pregnancy. Fetal blood supply was affected by maternal undernutrition, although there were still no evidences of brain-sparing excepting in fetuses at greatest challenge (twins in underfed pregnancies). However, there were early changes in the blood supply to the kidneys of underfed fetuses and underfed twins evidenced decreases in kidney size.

Type
Original Article
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2018 

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Footnotes

These authors contributed equally to this work.

References

1. Brodsky, D, Christou, H. Current concepts in intrauterine growth restriction. J Intens Care Med. 2004; 19, 307319.Google Scholar
2. Nardozza, LM, Araujo Júnior, E, Barbosa, MM, et al. Fetal growth restriction: current knowledge to the general Obs/Gyn. Arch Gynecol Obstet. 2012; 286, 113.Google Scholar
3. Cetin, I, Mando, C, Calabrese, S. Maternal predictors of intrauterine growth restriction. Curr Opin Clin Nutr Metab Care. 2013; 16, 310319.Google Scholar
4. Baschat, AA. Fetal responses to placental insufficiency: an update. BJOG. 2004; 111, 10311041.Google Scholar
5. Ghidini, A. Idiopathic fetal growth restriction: a pathophysiologic approach. Obstet Gynecol Surv. 1996; 51, 376382.Google Scholar
6. Moore, LG, Niermeyer, S, Zamudio, S. Human adaptation to high altitude: regional and life-cycle perspectives. Am J Phys Anthropol. 1998; (Suppl. 27), 2564.Google Scholar
7. Jensen, GM, Moore, LG. The effect of high altitude and other risk factors on birthweight: independent or interactive effects? Am J Public Health. 1997; 87, 10031007.Google Scholar
8. Mortola, JP, Frappell, PB, Aguero, L, Armstrong, K. Birth weight and altitude: a study in Peruvian communities. J Pediatr. 2000; 136, 324329.CrossRefGoogle ScholarPubMed
9. Giussani, DA, Niu, Y, Herrera, EA, et al. Heart disease link to fetal hypoxia and oxidative stress. Adv Exp Med Biol. 2014; 814, 7787.Google Scholar
10. Ismail, H, Chang, YL. Sequelae of fetal growth restriction. J Med Ultrasound. 2012; 20, 191200.Google Scholar
11. Saffery, R. Epigenetic change as the major mediator of fetal programming in humans: are we there yet? Ann Nutr Metab. 2014; 64, 203207.Google Scholar
12. Puddu, M, Fanos, V, Podda, F, Zaffanello, M. The kidney from prenatal to adult life: perinatal programming and reduction of number of nephrons during development. Am J Nephrol. 2009; 30, 162170.Google Scholar
13. Ritz, E, Amann, K, Koleganova, N, Benz, K. Prenatal programming-effects on blood pressure and renal function. Nat Rev Nephrol. 2011; 7, 137144.Google Scholar
14. Dötsch, J, Alejandre-Alcazar, M, Janoschek, R, et al. Perinatal programming of renal function. Curr Opin Pediatr. 2016; 28, 188194.Google Scholar
15. Miller, J, Turan, S, Baschat, AA. Fetal growth restriction. Semin Perinatol. 2008; 32, 274280.Google Scholar
16. Rizzo, G, Arduini, D. Intrauterine growth restriction: diagnosis and management. A review. Minerva Ginecol. 2009; 61, 411420.Google Scholar
17. Kouskouti, C, Regner, K, Knabl, J, Kainer, F. Cardiotocography and the evolution into computerised cardiotocography in the management of intrauterine growth restriction. Arch Gynecol Obstet. 2017; 295, 811816.Google Scholar
18. Gonzalez-Bulnes, A, Astiz, S, Parraguez, VH, Garcia-Contreras, C, Vazquez-Gomez, M. Empowering translational research in fetal growth restriction: sheep and swine animal models. Curr Pharm Biotechnol. 2016; 17, 848855.Google Scholar
19. Armitage, JA, Taylor, PD, Poston, L. Experimental models of developmental programming: consequences of exposure to an energy rich diet during development. J Physiol. 2005; 565, 38.Google Scholar
20. Schroeder, M, Shbiro, L, Zagoory-Sharon, O, Moran, TH, Weller, A. Toward an animal model of childhood-onset obesity: follow-up of OLETF rats during pregnancy and lactation. Am J Physiol Regul Integr Comp Physiol. 2009; 296, R224R232.Google Scholar
21. Rosenfeld, CS. Animal models to study environmental epigenetics. Biol Reprod. 2010; 82, 473488.Google Scholar
22. Neitzke, U, Harder, T, Schellong, K, et al. Intrauterine growth restriction in a rodent model and developmental programming of the metabolic syndrome: a critical appraisal of the experimental evidence. Placenta. 2008; 29, 246254.Google Scholar
23. Neitzke, U, Harder, T, Plagemann, A. Intrauterine growth restriction and developmental programming of the metabolic syndrome: a critical appraisal. Microcirculation. 2011; 18, 304311.Google Scholar
24. Charlton, V, Johengen, M. Effects of intrauterine nutritional supplementation on fetal growth retardation. Biol Neonate. 1985; 48, 125142.Google Scholar
25. Symonds, ME, Budge, H, Stephenson, T, McMillen, IC. Fetal endocrinology and development-manipulation and adaptation to long-term nutritional and environmental challenges. Reproduction. 2001; 121, 853862.Google Scholar
26. Wallace, JM, Aitken, RP, Milne, JS, Hay, WW. Nutritionally mediated placental growth restriction in the growing adolescent: consequences for the fetus. Biol Reprod. 2004; 71, 10551062.Google Scholar
27. Morel, O, Pachy, F, Chavatte-Palmer, P, et al. Correlation between utero-placental three-dimensional power Doppler indices and the uterine real blood flow: evaluation in a pregnant sheep experimental model. Ultrasound Obstet Gynecol. 2010; 36, 635640.Google Scholar
28. Vonnahme, KA, Lemley, CO. Programming the offspring through altered uteroplacental hemodynamics: how maternal environment impacts uterine and umbilical blood flow in cattle, sheep and pigs. Reprod Fertil Develop. 2012; 24, 97104.Google Scholar
29. Scherjon, SA, Smolders-DeHaas, H, Kok, JH, Zondervan, HA. The “brain-sparing” effect: antenatal cerebral Doppler findings in relation to neurologic outcome in very preterm infants. Am J Obstet Gynecol. 1993; 169, 169175.Google Scholar
30. Osgerby, JC, Wathes, DC, Howard, D, Gadd, TS. The effect of maternal undernutrition on the placental growth trajectory and the uterine insulin-like growth factor axis in the pregnant ewe. J Endocrinol. 2004; 182, 89103.Google Scholar
31. Zywicki, M, Blohowiak, SE, Magness, RR, Segar, JL, Kling, PJ. Increasing fetal ovine number per gestation alters fetal plasma clinical chemistry values. Physiol Rep. 2016; 4, e12905.Google Scholar
32. Unterscheider, J, Daly, S, Geary, MP, et al. Optimizing the definition of intrauterine growth restriction: the multicenter prospective PORTO study. Am J Obstet Gynecol. 2013; 208, 290.e1–6.Google Scholar
33. Mureşan, D, Rotar, IC, Stamatian, F. The usefulness of fetal Doppler evaluation in early versus late onset intrauterine growth restriction. Review of the literature. Med Ultrason. 2016; 18, 103109.Google Scholar
34. Shahinaj, R, Manoku, N, Kroi, E, Tasha, I. The value of the middle cerebral to umbilical artery Doppler ratio in the prediction of neonatal outcome in patient with preeclampsia and gestational hypertension. J Prenat Med. 2010; 4, 1721.Google Scholar
35. DeVore, GR. The importance of the cerebroplacental ratio in the evaluation of fetal well-being in SGA and AGA fetuses. Am J Obstet Gynecol. 2015; 213, 515.Google Scholar
36. Nassr, AA, Abdelmagied, AM, Shazly, SA. Fetal cerebro-placental ratio and adverse perinatal outcome: systematic review and meta-analysis of the association and diagnostic performance. J Perinat Med. 2016; 44, 249256.Google Scholar
37. Albu, AR, Anca, AF, Horhoianu, VV, Horhoianu, IA. Predictive factors for intrauterine growth restriction. J Med Life. 2014; 7, 165171.Google Scholar
38. Devoe, LD, Gardner, P, Dear, C, Faircloth, D. The significance of increasing umbilical artery systolic-diastolic ratios in third-trimester pregnancy. Obstet Gynecol. 1992; 80, 684687.Google Scholar
39. Mensah, GA, Croft, JB, Giles, WH. The heart, kidney, and brain as target organs in hypertension. Cardiol Clin. 2002; 20, 225247.Google Scholar
40. Vyas, S, Nicolaides, KH, Campbell, S. Renal artery flow-velocity waveforms in normal and hypoxemic fetuses. Am J Obstet Gynecol. 1989; 161, 168172.Google Scholar
41. Arduini, D, Rizzo, G. Fetal renal artery velocity waveforms and amniotic fluid volume in growth-retarded and post-term fetuses. Obstet Gynecol. 1991; 77, 370373.Google Scholar
42. Yoshimura, S, Masuzaki, H, Gotoh, H, Ishimaru, T. Fetal redistribution of blood flow and amniotic fluid volume in growth-retarded fetuses. Early Hum Dev. 1997; 47, 297304.Google Scholar
43. Surányi, A, Streitman, K, Pál, A, et al. Fetal renal artery flow and renal echogenicity in the chronically hypoxic state. Pediatr Nephrol. 2000; 14, 393399.Google Scholar
44. Stigter, RH, Mulder, EJH, Bruinse, HW, Visser, GHA. Doppler studies on the fetal renal artery in the severely growth-restricted fetus. Ultrasound Obstet Gynecol. 2001; 18, 141145.Google Scholar
45. Arbeille, P. Fetal arterial Doppler-IUGR and hypoxia. Eur J Obstet Gynecol Reprod Biol. 1997; 75, 5153.Google Scholar
46. Peeters, LLH, Sheldon, RE, Douglas-Jones, M, Makowski, EL, Meschia, G. Blood flow to fetal organs as a function of arterial oxygen content. Am J Obstet Gynecol. 1979; 135, 637646.Google Scholar
47. Shepherdj, T, Abboudf, M. The renal circulation. In Handbook of Physiology (eds. Knox FG, Spielman WS), Section 2, vol. 3, 1983; pp. 205–209. American Physiological Society: Washington, DC.Google Scholar
48. Tanabe, R. Doppler ultrasonographic assessment of fetal renal artery blood flow velocity waveforms in intrauterine growth retarded fetuses. Kurume Med J. 1992; 39, 203208.Google Scholar