Intrauterine growth restriction: screening and diagnosis using animal models
Fernando Felicioni, Thaís Garcia Santos, Thaís de Mérici Domingues e Paula, Hélio Chiarini-Garcia, Fernanda Radicchi Campos Lobato de Almeida
Intrauterine growth restriction (IUGR) is a serious condition of multifactorial origin, mainly caused by maternal malnutrition, multiple gestation associated with nutrient competition, abuse of nocive substances and infections. The diagnosis of such syndrome is complex, as its own manifestations can mask its occurrence, requiring a thorough assessment of body weight and size. Moreover, it is not responsive to any kind of treatment. There is evidence that IUGR may predispose the individual to several pathologies, such as diabetes, hypertension and metabolic syndrome in adulthood, and it has also been linked to thrifty phenotype hypothesis. Thus, a healthy lifestyle is needed to better prevent those pathologies. Given the world high prevalence and importance of IUGR, mainly in developing countries, this review is focused on discussing how different animal models contribute to the biological screening and diagnosis of this condition.
Almeida FRCL, Silva GAB, Fiúza ATL, Chiana DA, Ferreira AJ, Chiarini-Garcia H. 2012. Gestational and postnatal protein deficiency affects postnatal development and histomorphometry of liver, kidneys, and ovaries of female rats’ offspring. Appl Physiol Nutr Metab, 37:293-300.
Alvarenga ALN, Chiarini-Garcia H, Cardeal PC, Moreira LP, Foxcroft GR, Fontes DO, Almeida FRCL. 2013. Intra-uterine growth retardation affects birthweight and postnatal development in pigs, impairing muscle accretion, duodenal mucosa morphology and carcass traits. Reprod Fertil Dev, 25:387-395.
Armitage JA, Khan IY, Taylor PD, Nathanielsz PW, Poston L. 2004. Developmental programming of the metabolic syndrome by maternal nutritional imbalance: how strong is the evidence from experimental models in mammals? J Physiol, 561(Pt2):355-377.
Ashworth CJ. 2013. Late pregnancy: The effects of intra-uterine life on production traits in offspring. Anim Frontiers, 3:62-67.
Bada HS, Das A, Bauer CR, Shankaran S, Lester BM, Gard CC, Wright LL, LaGasse L, Higgins R. 2005. Low birth weight and preterm births: etiologic fraction attributable to prenatal drug exposure. J Perinatol, 25:631-637.
Barbero A, Porcu C, Spezzigu A, Succu S, Dattena M, Gallus M, molle G, Naitana S, Gonzalez-Bulnes A, Berlinguer F. 2018. Changes in renal hemodynamics of undernourished fetuses appear earlier than IUGR evidences. J Dev Orig Health Dis, 9:338-343.
Briana DD, Boutsikou M, Marmarinos A, Gourgiotis D, Malamitsi-Puchner A. 2018. Perinatal sclerostin concentrations in abnormal fetal growth: the impact of gestational diabetes. J Matern Fetal Neonatal Med, 31:1-5.
Butt, MS., Sultan, MT. 2011. Coffee and its consumption: Beneﬁts and risks. Crit Rev Food Sci Nutr, 51:363-73.
Christian MS, Brent RL. 2001. Teratogen update: evaluation of the reproductive and developmental risks of caffeine. Teratology, 64:51-78.
Díaz P, Powell TL, Jansson T. 2014. The role of placental nutrient sensing in maternal-fetal resource allocation. Biol Reprod, 91:1-10.
Etuk EU. 2010. Animals models for studying diabetes mellitus. Agric Biol J N Am, 1:130-134.
European Food Standards Agency (EFSA). 2015. Scientific opinion on the safety of caffeine. Panel on dietetic products, nutrition and allergies (NDA). EFSA J, 13:4102.
Ferenc K, Pietrzak P, Podlewski MM, Piwowarski J, Jkiliańczyk R, Guilloteau P, Zabielski R. 2014. Intrauterine growth retarded piglet as a model for humans-studies on the perinatal development of the gut structure and function. Reprod Biol, 14:51-60.
Ferenc K, Pilzys T, Skrzypek T, Garbicz D, Marcinkowski M, Dylewska M, Gladysz P, Skorobogatov O, Gajewski Z, Gzesiuk E, Zabielski R. 2017. Structure and function of enterocyte in intrauterine growth retarded pig neonates. Dis Markers, 2017:1-9.
Food and Drug Administration (FDA). 2012. Center for science and public interest publisher of nutrition action health letter. Available on: http://www.fda.gov/OHRMS/DOCKETS/dailys/02/Apr02/042902/97p0329let6.pdf Accessed on October 19, 20018.
Gao H, Yallampalli U, Yallampalli C. 2013. Gestational protein restriction affects trophoblast differentiation. Front. Biosci, 5:591-601.
Gheorghe CP, Holweger JD, Longo LD. 2009. Placental gene expression responses to maternal protein restriction in the mouse. Placenta, 30:411-417.
Giabicani EA, Pham A. 2018. Diagnosis and management of postnatal fetal growth restriction. Best Pract Res Clin Endocrinol Metab, 32:523-534.
Gonzalez PN, Gasperowicz M, Barbelto-Andrés NK, Cross JC, Benedikt H. 2016. Chronic protein restriction in mice impacts placental function and maternal body weight before fetal growth. PLoS One, 11:1-18.
Hales CN, Barker DJP. 1992. Type 2 (non-insuline-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia, 35:595-601.
Hales CN, Barker DJP. 2001. The thrifty phenotype hypothesis. Br Med Bull, 60:5-20.
Hennington BS, Alexander BT. 2013. Linking IUGR and blood pressure: insight into the human origins of cardiovascular disease. Circulation, 125:2179-2180. Huang J, Zhou S, Ping J, Pan X, Liang G, Xu D, Kou
H, Bao C, Wang H. 2012. Role of P53-dependent placental apoptosis in the reproductive and developmental toxicities of caffeine in rodents. Clin Exp Pharmacol Physiol, 39: 357-63.
Isaac SM, Langford MB, Simmons DG, Adamson SL. 2014. Anatomy of the mouse placenta throughout gestation. In: Croy BA, Yamada AT, DeMayo FJ, Adamson SL. The Guide to Investigation of Mouse Pregnancy. Elsevier, 69-73.
Ito T, Hoshiai K, Tanabe K, Nakamura A, Funamoto K, Aoyagi A, Chisaka H, Okamura K, Yaegashi N, Kimura Y. 2011. Maternal undernutrition with vaginal inflammation impairs the neonatal oligodendrogenesis in mice. Tohoku J Exp Med, 223:215-222.
Jahanfar S, Jaafar SH. 2015. Effects of restricted caffeine intake by mother on fetal, neonatal and pregnancy outcomes. Cochrane Database Syst Rev, 6:CD006965.
Jahan-Mihan A, Rodriguez J, Christie C, Sadeghi M, Zerbe T. 2015. The role of maternal dietary proteins in development of metabolic syndrome in offspring. Nutrients, 7:9185-9217.
King JC. 2000. Physiology of pregnancy and nutrient metabolism. Am J Clin Nutr, 71:1218S-25S.
Klebanoff M, Levine RJ, Clemens JD, Wilkins DG. 2002. Maternal serum caffeine metabolites and small-for-gestational age birth. Am J Epidemiol, 155:32-37.
Kurjak A, Latin V, Polak J. 1978. Ultrasonic recognition of two types of growth retardation by measurement of four fetal dimensions. J Perinat Med, 6:102-108.
Liu X, Lin Y, Tian B, Miao J, Xi C, Liu C. 2014. Maternal protein restriction alters VEGF signaling and decreases pulmonary alveolar in fetal rats. Int J Clin Exp Pathol, 7:3101-3111.
Lundsberg LS, Bracken MB, Saftlas AF. 1997. Low-to-Moderate gestational alcohol use and intrauterine growth retardation, low birthweight, and preterm delivery. Ann Epidemiol, 7:498-508.
Ma ZL, Wan G, Lu W, Cheng X, Chuai M, Lee KK, Yang X. 2015. Investigating the effect of excess caffeine exposure on placental angiogenesis using chicken ‘functional’ placental blood vessel network. J Appl Toxicol, 36:285-95.
Martin-Gronert MS, Ozanne SE. 2006. Maternal nutrition during pregnancy and health of the offspring. Biochem Soc Trans, 34:779-782.
Momoi N, Tinney JP, Liu LJ, Elshershari H, Hoffmann PJ, Ralphe JC, Keller BB, Tobita K. 2008. Modest maternal caffeine exposure affects developing embryonic cardiovascular function and growth. Am J Physiol Heart Circ Physiol, 294:2248-2256.
Mose T, Kjaerstad MB, Mathiesen L, Nielsen JB, Edelfors S, Knudsen LE. 2008. Placental passage of benzoic acid, caffeine, and glyphosate in an ex vivo human perfusion system. J Toxicol Environ Health, 71:984-91.
Muñoz G, Biogiorni-Malavé I. 1979. Influence of dietary protein restriction on ovulation, fertilization rates and pre-implantation embryonic development in mice. J Exp Zool, 210:253-258.
Óvilo C, González-Bulnes A, Benítez R, Ayuso M, Barbero A, Pérez-Solana ML, Barragán C, Astiz S, Fernandez A, López-Bote C. 2014. Prenatal programming in an obese swine model: Sex-related effects of maternal energy restriction on morphology, metabolism and hypothalamic gene expression. Br J Nutr, 111: 735-746.
Paula TMD, Shang FLT, Chiarini-Garcia H, Almeida FRCL. 2017. Caffeine Intake during Pregnancy: What Are the Real Evidences? J Pharm Pharmacol, 5:249-260.
Puccio G, Giuffré M, Piccione M, Piro E, Malerba V, Corsello G. 2014. Intrauterine growth pattern and birthweight discordance in twin pregnancies: a retrospective study. Ital J Pediatr, 40:43.
Rutland CS, Latunde-Dada AO, Thorpe A, Plant R, Langley-Evans S, Leach L. 2007. Effect of gestational nutrition on vascular integrity in the murine placenta. Placenta, 28:734-742.
Salan RA, Das JK, Bhutta ZA. 2014. Impact of intrauterine growth restriction on long-term health. Curr Opin Clin Nutr Metab Care, 17:249-25.
Sharma D, Shastru S, Farahbakhsh N, Sharma P. 2016. Intrauterine growth restriction - part 1. J Matern Fetal Neonatal Med, 24:3977-3987.
Shi Y, Li S, Wu Q, Sun L, Zhang J, Pan N, Wang Q, Bi Y, An J, Lu X, Gao GF, Wang X. 2018. Vertical transmission of the zika virus causes neurological disorders in mouse offspring. Sci Rep, 8:3541.
Skrzypek T, Szymańczyk S, Ferenc K, Kazimierczak W, Szczepaniak K, Zabielski R. 2018. The contribution of vacuolated foetal-type enterocytes in the process of maturation of the small intestine in piglets. J Anim Feed Sci, 27:187-201.
Swanson AM, David AL. 2015. Animal models of fetal growth restriction: Considerations for translational medicine. Placenta, 36:623-630.
Wainwright P, Stefanescu R. 1983. Prenatal protein deprivation increases defects of the corpus callosum in BALB/c laboratory mice. Exp Neurol, 81:694-702.
Wang Y. 2005. Basic knowledge of functional experiment. In: Medical Functional Experimental Tutoria, H. Z. Hu, Ed., chapter 2, Science Press, Beijing, China.
Wu G, Bazer FM, Wallace JM, Spencer TE. 2006. Intrauterine growth retardation: Implications for the animal sciences. J Anim Sci, 84:2316-2337.
Yadegari M, Khazaei M, Anvari M, Eskandari M. 2016. Prenatal Caffeine Exposure Impairs Pregnancy in Rats. Int J Fertil Steril, 9:558-562.
Zabielski R, Godlewski MM, Guilloteau P. 2008. Control of development o gastrointestinal system in neonates. J Physiol Pharmacol, 59:35-54.