Skip to main content
Top
Published in: Diabetology & Metabolic Syndrome 1/2010

Open Access 01-12-2010 | Research

Evaluation of neonatally-induced mild diabetes in rats: Maternal and fetal repercussions

Authors: Isabela L Iessi, Aline Bueno, Yuri K Sinzato, Kristin N Taylor, Marilza VC Rudge, Débora C Damasceno

Published in: Diabetology & Metabolic Syndrome | Issue 1/2010

Login to get access

Abstract

Many experimental studies have been performed to evaluate mild diabetes effects. However, results are divergent regarding glycemia and insulin measurement, fetal macrossomia, and placental weights. The aim was to investigate repercussions of neonatally-induced mild diabetes on the maternal organism and presence of congenital defects in their offspring in other mild diabetes model. On the day of birth, female offspring were distributed into two groups: Group streptozotocin (STZ): received 100 mg STZ/kg body weight, and Control Group: received vehicle in a similar time period. Maternal weights and glycemias were determined at days 0, 7, 14 and 21 of pregnancy. At day 21 of pregnancy, the rats were anesthetized and a laparotomy was performed to weigh and analyze living fetuses and placentas. The fetuses were classified as small (SPA), appropriate (APA) and large (LPA) for pregnancy age. Fetuses were also analyzed for the presence of external anomalies and processed for skeletal anomaly and ossification sites analysis. Statistical significance was considered as p < 0.05. In STZ group, there was increased glycemia at 0 and 14 days of pregnancy, lower weights throughout pregnancy, higher placental weight and index, an increased proportion of fetuses classified as SPA and LPA, and their fetuses presented with an increased frequency of abnormal sternebra, and absent cervical nuclei, which were not enough to cause the emergence of skeletal anomalies. Thus, this study shows that mild diabetes altered fetal development, characterized by intrauterine growth restriction. Further, the reached glycemia does not lead to any major congenital defects in the fetuses of streptozotocin-induced mild diabetic rats.
Appendix
Available only for authorised users
Literature
1.
go back to reference Rolo AP, Palmeira CM: Diabetes and mitochondrial function: Role of hyperglycemia and oxidative stress. Toxicol Appl Pharmacol. 2006, 212 (2): 167-178. 10.1016/j.taap.2006.01.003.CrossRefPubMed Rolo AP, Palmeira CM: Diabetes and mitochondrial function: Role of hyperglycemia and oxidative stress. Toxicol Appl Pharmacol. 2006, 212 (2): 167-178. 10.1016/j.taap.2006.01.003.CrossRefPubMed
2.
go back to reference Metzger BE: The hyperglycemia and adverse pregnancy outcome (HAPO) study. International Journal Gynecology Obstetrics. 2002, 78: 69-77. 10.1016/S0020-7292(02)00092-9.CrossRef Metzger BE: The hyperglycemia and adverse pregnancy outcome (HAPO) study. International Journal Gynecology Obstetrics. 2002, 78: 69-77. 10.1016/S0020-7292(02)00092-9.CrossRef
3.
go back to reference Merzouk H, Bouchenak M, Loukidi B, Madani S, Prost J, Belleville J: Fetal macrosomia related to maternal poorly controlles type 1 diabetes strongly impairs serum lipoprotein concentrations and composition. Journal Clinical Pathology. 2000, 53: 917-923. 10.1136/jcp.53.12.917.CrossRef Merzouk H, Bouchenak M, Loukidi B, Madani S, Prost J, Belleville J: Fetal macrosomia related to maternal poorly controlles type 1 diabetes strongly impairs serum lipoprotein concentrations and composition. Journal Clinical Pathology. 2000, 53: 917-923. 10.1136/jcp.53.12.917.CrossRef
4.
go back to reference Eriksson UJ: Congenital anomalies in diabetic pregnancy. Seminars in Fetal & Neonatal Medicine. 2008, 1-9. Eriksson UJ: Congenital anomalies in diabetic pregnancy. Seminars in Fetal & Neonatal Medicine. 2008, 1-9.
5.
go back to reference Reece AE, Homko CJ: Pregnancy Care and the Prevention of Fetal Malformations in the Pregnancy Complicated by Diabetes. Clinical Obstetrics and Gynecology. 2007, 50 (4): 990-997. 10.1097/GRF.0b013e31815a634b.CrossRefPubMed Reece AE, Homko CJ: Pregnancy Care and the Prevention of Fetal Malformations in the Pregnancy Complicated by Diabetes. Clinical Obstetrics and Gynecology. 2007, 50 (4): 990-997. 10.1097/GRF.0b013e31815a634b.CrossRefPubMed
6.
go back to reference Ray JG, O'Brien TE, Chan WS: Preconception care and the risk of congenital anomalies in the offspring of women with diabetes mellitus: a meta-analysis. QJM. 2001, 94: 435-444. 10.1093/qjmed/94.8.435.CrossRefPubMed Ray JG, O'Brien TE, Chan WS: Preconception care and the risk of congenital anomalies in the offspring of women with diabetes mellitus: a meta-analysis. QJM. 2001, 94: 435-444. 10.1093/qjmed/94.8.435.CrossRefPubMed
7.
go back to reference Platt MJ, Stanisstreet M, Casson IF, et al: St Vincent's declaration 10 years on: outcomes of diabetic pregnancies. Diabet Med. 2002, 19: 216-220. 10.1046/j.1464-5491.2002.00665.x.CrossRefPubMed Platt MJ, Stanisstreet M, Casson IF, et al: St Vincent's declaration 10 years on: outcomes of diabetic pregnancies. Diabet Med. 2002, 19: 216-220. 10.1046/j.1464-5491.2002.00665.x.CrossRefPubMed
8.
go back to reference Evers IM, de Valk HW, Visser GH: Risk of complications of pregnancy in women with type 1 diabetes: nationwide prospective study in the Netherlands. Br Med J. 2004, 328: 915-924. 10.1136/bmj.38043.583160.EE.CrossRef Evers IM, de Valk HW, Visser GH: Risk of complications of pregnancy in women with type 1 diabetes: nationwide prospective study in the Netherlands. Br Med J. 2004, 328: 915-924. 10.1136/bmj.38043.583160.EE.CrossRef
9.
go back to reference Verheijen EC, Critchley JA, Whitelaw DC, Tuffnell DJ: Outcomes of pregnancies in women with pre-existing type 1 or type 2 diabetes, in an ethnically mixed population. Br J Obstet Gynaecol. 2005, 112: 1500-1503.CrossRef Verheijen EC, Critchley JA, Whitelaw DC, Tuffnell DJ: Outcomes of pregnancies in women with pre-existing type 1 or type 2 diabetes, in an ethnically mixed population. Br J Obstet Gynaecol. 2005, 112: 1500-1503.CrossRef
10.
go back to reference Schaefer-Graf UM, Buchanan TA, Xiang A, Songster G, Montoro M, Kjos SL: Patterns of congenital anomalies and relationship to initial maternal fasting glucose levels in pregnancies complicated by type 2 and gestational diabetes. Am J Obstet Gynecol. 2000, 182: 313-320. 10.1016/S0002-9378(00)70217-1.CrossRefPubMed Schaefer-Graf UM, Buchanan TA, Xiang A, Songster G, Montoro M, Kjos SL: Patterns of congenital anomalies and relationship to initial maternal fasting glucose levels in pregnancies complicated by type 2 and gestational diabetes. Am J Obstet Gynecol. 2000, 182: 313-320. 10.1016/S0002-9378(00)70217-1.CrossRefPubMed
11.
go back to reference Brydon P, Smith T, Proffitt M, Gee H, Holder R, Dunne F: Pregnancy outcome in women with type 2 diabetes mellitus needs to be addressed. Int J Clin Pract. 2000, 54: 418-419.PubMed Brydon P, Smith T, Proffitt M, Gee H, Holder R, Dunne F: Pregnancy outcome in women with type 2 diabetes mellitus needs to be addressed. Int J Clin Pract. 2000, 54: 418-419.PubMed
12.
go back to reference Dunne F, Brydon P, Smith K, Gee H: Pregnancy in women with Type 2 diabetes: 12 years outcome data 1990-2002. Diabet Med. 2003, 20: 734-738. 10.1046/j.1464-5491.2003.01017.x.CrossRefPubMed Dunne F, Brydon P, Smith K, Gee H: Pregnancy in women with Type 2 diabetes: 12 years outcome data 1990-2002. Diabet Med. 2003, 20: 734-738. 10.1046/j.1464-5491.2003.01017.x.CrossRefPubMed
13.
go back to reference Garcia-Patterson A, Erdozain L, Ginovart G, et al: In human gestational diabetes mellitus congenital malformations are related to pre-pregnancy body mass index and to severity of diabetes. Diabetologia. 2004, 47: 509-514. 10.1007/s00125-004-1337-3.CrossRefPubMed Garcia-Patterson A, Erdozain L, Ginovart G, et al: In human gestational diabetes mellitus congenital malformations are related to pre-pregnancy body mass index and to severity of diabetes. Diabetologia. 2004, 47: 509-514. 10.1007/s00125-004-1337-3.CrossRefPubMed
14.
go back to reference Kucera J: Rate and type of congenital anomalies among offspring of diabetic women. J Reprod Med. 1971, 7: 61-70. Kucera J: Rate and type of congenital anomalies among offspring of diabetic women. J Reprod Med. 1971, 7: 61-70.
15.
go back to reference Towner D, Kjos S, Leung B, et al: Congenital malformations in pregnancies complicated by NIDDM. Diabetes Care. 1995, 18: 1446-1451. 10.2337/diacare.18.11.1446.CrossRefPubMed Towner D, Kjos S, Leung B, et al: Congenital malformations in pregnancies complicated by NIDDM. Diabetes Care. 1995, 18: 1446-1451. 10.2337/diacare.18.11.1446.CrossRefPubMed
16.
go back to reference Von Kries R, Kimmerle R, Schmidt JE, Hachmeister A, Bohm O, Wolf HG: Pregnancy outcomes in mothers with pregestational diabetes: a populationbased study in North Rhine (Germany) from 1988 to 1993. Eur J Pediatr. 1997, 156: 963-967. 10.1007/s004310050752.CrossRefPubMed Von Kries R, Kimmerle R, Schmidt JE, Hachmeister A, Bohm O, Wolf HG: Pregnancy outcomes in mothers with pregestational diabetes: a populationbased study in North Rhine (Germany) from 1988 to 1993. Eur J Pediatr. 1997, 156: 963-967. 10.1007/s004310050752.CrossRefPubMed
17.
go back to reference Aberg A, Westbom L, Kallen B: Congenital malformations among infants whose mothers had gestational diabetes or preexisting diabetes. Early Hum Dev. 2001, 61: 85-95. 10.1016/S0378-3782(00)00125-0.CrossRefPubMed Aberg A, Westbom L, Kallen B: Congenital malformations among infants whose mothers had gestational diabetes or preexisting diabetes. Early Hum Dev. 2001, 61: 85-95. 10.1016/S0378-3782(00)00125-0.CrossRefPubMed
18.
go back to reference Hawthorne G, Robson S, Ryall EA, Sen D, Roberts SH, Ward Platt MP: Prospective population based survey of outcome of pregnancy in diabetic women: results of the Northern Diabetic Pregnancy Audit, 1994. Br Med J. 1997, 315: 279-281.CrossRef Hawthorne G, Robson S, Ryall EA, Sen D, Roberts SH, Ward Platt MP: Prospective population based survey of outcome of pregnancy in diabetic women: results of the Northern Diabetic Pregnancy Audit, 1994. Br Med J. 1997, 315: 279-281.CrossRef
19.
go back to reference Casson IF, Clarke CA, Howard CV, et al: Outcomes of pregnancy in insulin dependent diabetic women: results of a five year population cohort study. Br Med J. 1997, 315: 275-278.CrossRef Casson IF, Clarke CA, Howard CV, et al: Outcomes of pregnancy in insulin dependent diabetic women: results of a five year population cohort study. Br Med J. 1997, 315: 275-278.CrossRef
20.
go back to reference Martínez-Frias ML: Epidemiological analysis of outcomes of pregnancy in diabetic mothers: identification of the most characteristic and most frequent congenital anomalies. Am J Med Genet. 1994, 51: 108-13. 10.1002/ajmg.1320510206.CrossRefPubMed Martínez-Frias ML: Epidemiological analysis of outcomes of pregnancy in diabetic mothers: identification of the most characteristic and most frequent congenital anomalies. Am J Med Genet. 1994, 51: 108-13. 10.1002/ajmg.1320510206.CrossRefPubMed
21.
go back to reference Mills JL: Malformations in infants of diabetic mothers. Teratology. 1982, 25: 385-94. 10.1002/tera.1420250316.CrossRefPubMed Mills JL: Malformations in infants of diabetic mothers. Teratology. 1982, 25: 385-94. 10.1002/tera.1420250316.CrossRefPubMed
22.
go back to reference Lopez-Soldado I, Herrera E: Different diabetogenic response to moderat doses of streptozotocin in pregnant rats, and its long-term consequences in the offspring. Exp Diabesity Res. 2003, 4: 107-118.PubMedCentralCrossRefPubMed Lopez-Soldado I, Herrera E: Different diabetogenic response to moderat doses of streptozotocin in pregnant rats, and its long-term consequences in the offspring. Exp Diabesity Res. 2003, 4: 107-118.PubMedCentralCrossRefPubMed
23.
go back to reference Damasceno DC, Volpato GT, Calderon IMP, et al: Oxidative stress and diabetes in pregnant rats. Anim Reprod Sci. 2002, 235-244. 10.1016/S0378-4320(02)00094-5. Damasceno DC, Volpato GT, Calderon IMP, et al: Oxidative stress and diabetes in pregnant rats. Anim Reprod Sci. 2002, 235-244. 10.1016/S0378-4320(02)00094-5.
24.
go back to reference Eriksson UJ, Cederberg J, Wentzel P: Congenital malformations in offspring of diabetic mothers--animal and human studies. Rev Endocr Metab Disord. 2003, 4 (1): 79-93. 10.1023/A:1021879504372.CrossRefPubMed Eriksson UJ, Cederberg J, Wentzel P: Congenital malformations in offspring of diabetic mothers--animal and human studies. Rev Endocr Metab Disord. 2003, 4 (1): 79-93. 10.1023/A:1021879504372.CrossRefPubMed
25.
go back to reference Souza MSS, Lima PHO, Sinzato YK, Rudge MVC, Pereira OCM, Damasceno DC: Effects of cigarette smoke expose on pregnancy outcome of diabetic rats and on their offspring. Reproductive Bio Medicine Online. 2009, 18 (4): 562-567. 10.1016/S1472-6483(10)60135-6.CrossRef Souza MSS, Lima PHO, Sinzato YK, Rudge MVC, Pereira OCM, Damasceno DC: Effects of cigarette smoke expose on pregnancy outcome of diabetic rats and on their offspring. Reproductive Bio Medicine Online. 2009, 18 (4): 562-567. 10.1016/S1472-6483(10)60135-6.CrossRef
26.
go back to reference Portha B, Levacher C, Picon L, Rosselin G: Diabetogenic effect of streptozotocinin on the rat during the perinatal period. Diabetes. 1974, 23 (11): 888-895.CrossRef Portha B, Levacher C, Picon L, Rosselin G: Diabetogenic effect of streptozotocinin on the rat during the perinatal period. Diabetes. 1974, 23 (11): 888-895.CrossRef
27.
go back to reference Tsuji K, Taminato T, Usami M, Ishida H, Kitano N, Fukumoto H, Koh G, Kurose T, Yamada Y, Yano H, et al: Characteristic features of insulin secretion in the streptozotocin-induced NIDDM rat model. Metabolism. 1988, 37: 1040-1044. 10.1016/0026-0495(88)90064-9.CrossRefPubMed Tsuji K, Taminato T, Usami M, Ishida H, Kitano N, Fukumoto H, Koh G, Kurose T, Yamada Y, Yano H, et al: Characteristic features of insulin secretion in the streptozotocin-induced NIDDM rat model. Metabolism. 1988, 37: 1040-1044. 10.1016/0026-0495(88)90064-9.CrossRefPubMed
28.
go back to reference Merzouk H, Madane S, Boualga A, Prost J, Bouchenak M, Belleville J: Age-related changes in cholesterol metabolism in macrosomic offspring of rats with streptozotocin-induced diabetes. J Lipid Res. 2001, 42: 1152-1159.PubMed Merzouk H, Madane S, Boualga A, Prost J, Bouchenak M, Belleville J: Age-related changes in cholesterol metabolism in macrosomic offspring of rats with streptozotocin-induced diabetes. J Lipid Res. 2001, 42: 1152-1159.PubMed
29.
go back to reference Merzouk H, Madani S, Hichami A, Prost J, Moutairou K, Belleville J, et al: Impaired lipoprotein metabolism in obese offspring of streptozotocin-induced diabetic rats. Lipids. 2002, 37 (8): 773-781. 10.1007/s11745-002-0960-9.CrossRefPubMed Merzouk H, Madani S, Hichami A, Prost J, Moutairou K, Belleville J, et al: Impaired lipoprotein metabolism in obese offspring of streptozotocin-induced diabetic rats. Lipids. 2002, 37 (8): 773-781. 10.1007/s11745-002-0960-9.CrossRefPubMed
30.
go back to reference Soulimane-Mokhtari NA, Guermouche B, Yessoufou A, Saker M, Moutairou K, Hichami A, Merzouk H, Khan NA: Modulation of lipid metabolism by n-3 polyunsaturated fatty acids in gestational diabetic rats and their macrosomic offspring. Clin Sci. 2005, 109: 287-295. 10.1042/CS20050028.CrossRefPubMed Soulimane-Mokhtari NA, Guermouche B, Yessoufou A, Saker M, Moutairou K, Hichami A, Merzouk H, Khan NA: Modulation of lipid metabolism by n-3 polyunsaturated fatty acids in gestational diabetic rats and their macrosomic offspring. Clin Sci. 2005, 109: 287-295. 10.1042/CS20050028.CrossRefPubMed
31.
go back to reference Merzouk H, Kahn NA: Implication of lipids in macrosomia of diabetic pregnancy: can n-3 polynsaturated fatty acids exert beneficial effects?. Clin Sci. 2003, 105: 519-529. 10.1042/CS20030143.CrossRefPubMed Merzouk H, Kahn NA: Implication of lipids in macrosomia of diabetic pregnancy: can n-3 polynsaturated fatty acids exert beneficial effects?. Clin Sci. 2003, 105: 519-529. 10.1042/CS20030143.CrossRefPubMed
32.
go back to reference Staples RE, Schnell VL: Refinements in rapid clearing technic in the KOH-alizarin red S method for fetal bone. Stain Technol. 1964, 39: 61-63.PubMed Staples RE, Schnell VL: Refinements in rapid clearing technic in the KOH-alizarin red S method for fetal bone. Stain Technol. 1964, 39: 61-63.PubMed
33.
go back to reference Aliverti V, Bonanomi L, Giavini E, et al: The extent of fetal ossification as an index of delayed development in teratogenic studies on the rats. Teratology. 1979, 20: 237-242. 10.1002/tera.1420200208.CrossRefPubMed Aliverti V, Bonanomi L, Giavini E, et al: The extent of fetal ossification as an index of delayed development in teratogenic studies on the rats. Teratology. 1979, 20: 237-242. 10.1002/tera.1420200208.CrossRefPubMed
34.
go back to reference Vieira S: Estatística Experimental. Ed Atlas SA São Paulo. 1999, 313- Vieira S: Estatística Experimental. Ed Atlas SA São Paulo. 1999, 313-
35.
go back to reference Zar JH: Biostatistical analysis. 1999, New Jersey: Pretence Hall Zar JH: Biostatistical analysis. 1999, New Jersey: Pretence Hall
36.
go back to reference Diamant YZ, Metzger BE, Freikel N, Shafir E: Placental lipid and glycogen content in human and experimental diabetes mellitus. Am J Obstet Gynecol. 1982, 144: 5-11.PubMed Diamant YZ, Metzger BE, Freikel N, Shafir E: Placental lipid and glycogen content in human and experimental diabetes mellitus. Am J Obstet Gynecol. 1982, 144: 5-11.PubMed
37.
go back to reference Desoye G, Hauguel-de Mouzon S: The human placenta in gestational diabetes mellitus. The insulin and cytokine network. Diabetes Care. 2007, 30: 120-126. 10.2337/dc07-s203.CrossRef Desoye G, Hauguel-de Mouzon S: The human placenta in gestational diabetes mellitus. The insulin and cytokine network. Diabetes Care. 2007, 30: 120-126. 10.2337/dc07-s203.CrossRef
38.
go back to reference Bonner-Weir S, Trent DF, Honey RN, Weir GC: Responses of neonatal rat islets to streptozotocin. Diabetes. 1981, 30: 64-69. 10.2337/diabetes.30.1.64.CrossRefPubMed Bonner-Weir S, Trent DF, Honey RN, Weir GC: Responses of neonatal rat islets to streptozotocin. Diabetes. 1981, 30: 64-69. 10.2337/diabetes.30.1.64.CrossRefPubMed
39.
go back to reference Portha B, Kergoat M: Dynamics of glucose-induced insulin release during the spontaneous remission of streptozotocin diabetes induced in the newborn rat. Diabetes. 1985, 34 (6): 574-579. 10.2337/diabetes.34.6.574.CrossRefPubMed Portha B, Kergoat M: Dynamics of glucose-induced insulin release during the spontaneous remission of streptozotocin diabetes induced in the newborn rat. Diabetes. 1985, 34 (6): 574-579. 10.2337/diabetes.34.6.574.CrossRefPubMed
40.
go back to reference Rudge MVC, Borges VTM, Calderon IMP: Adaptação do organismo materno à gravidez. Obstetrícia básica. Edited by: Neme B. 2000, São Paulo: Sarvier, 42-51. Rudge MVC, Borges VTM, Calderon IMP: Adaptação do organismo materno à gravidez. Obstetrícia básica. Edited by: Neme B. 2000, São Paulo: Sarvier, 42-51.
41.
go back to reference Volpato GT, Damasceno DC, Campos KE, Rocha R, Rudge MVC, Calderon IMP: Avaliação do efeito do exercício físico no metabolismo de ratas diabéticas prenhes. Rev Bras Med Esporte. 2006, 12: 229-233. 10.1590/S1517-86922006000500001.CrossRef Volpato GT, Damasceno DC, Campos KE, Rocha R, Rudge MVC, Calderon IMP: Avaliação do efeito do exercício físico no metabolismo de ratas diabéticas prenhes. Rev Bras Med Esporte. 2006, 12: 229-233. 10.1590/S1517-86922006000500001.CrossRef
42.
go back to reference Kim E, Sohn S, Lee M, Jung J, Kineman RD, Park S: Differential responses of the growth hormone axis in two rat models of streptozotocin-induced insulinopenic diabetes. J Endocrinol. 2006, 188: 263-270. 10.1677/joe.1.06501.CrossRefPubMed Kim E, Sohn S, Lee M, Jung J, Kineman RD, Park S: Differential responses of the growth hormone axis in two rat models of streptozotocin-induced insulinopenic diabetes. J Endocrinol. 2006, 188: 263-270. 10.1677/joe.1.06501.CrossRefPubMed
44.
go back to reference Becerra JE, Khoury MJ, Cordero JF, Erickson JD: Diabetes mellitus during pregnancy and the risks for specific birth defects: a population-based case-control study. Pediatrics. 1990, 851: 1-9. Becerra JE, Khoury MJ, Cordero JF, Erickson JD: Diabetes mellitus during pregnancy and the risks for specific birth defects: a population-based case-control study. Pediatrics. 1990, 851: 1-9.
45.
go back to reference Kervran A, Guillaume M, Jost A: The endocrine pancreas of the fetus from diabetics pregnant rats. Diabetologia. 1978, 15: 387-393. 10.1007/BF01219648.CrossRefPubMed Kervran A, Guillaume M, Jost A: The endocrine pancreas of the fetus from diabetics pregnant rats. Diabetologia. 1978, 15: 387-393. 10.1007/BF01219648.CrossRefPubMed
46.
go back to reference Aerts L, Van Assche FA: Animal evidence for the transgenerational development of diabetes mellitus. Int J Biochem Cell Biol. 2006, 38: 894-903. 10.1016/j.biocel.2005.07.006.CrossRefPubMed Aerts L, Van Assche FA: Animal evidence for the transgenerational development of diabetes mellitus. Int J Biochem Cell Biol. 2006, 38: 894-903. 10.1016/j.biocel.2005.07.006.CrossRefPubMed
47.
go back to reference Holemans K, Aerts L, Van Assche FA: Fetal growth restriction and consequences for the offspring in animal models. J Soc Gynecol Investg. 2003, 10: 392-399. 10.1016/S1071-5576(03)00134-5.CrossRef Holemans K, Aerts L, Van Assche FA: Fetal growth restriction and consequences for the offspring in animal models. J Soc Gynecol Investg. 2003, 10: 392-399. 10.1016/S1071-5576(03)00134-5.CrossRef
48.
go back to reference Hales CN, Barker DJ, Clark PM, Cox LJ, Fall C, Osmond C, Winter PD: Fetal and infant growth and impaired glucose tolerance at age 64. Br Med J. 1991, 303: 1019-1022. 10.1136/bmj.303.6809.1019.CrossRef Hales CN, Barker DJ, Clark PM, Cox LJ, Fall C, Osmond C, Winter PD: Fetal and infant growth and impaired glucose tolerance at age 64. Br Med J. 1991, 303: 1019-1022. 10.1136/bmj.303.6809.1019.CrossRef
49.
go back to reference McKeigue PM, Lithell HO, Leon DA: Glucose tolerance and resistance to insulin-stimulated glucose uptake in men aged 70 years in relation to size at birth. Diabetologia. 1998, 41: 1133-1138. 10.1007/s001250051042.CrossRefPubMed McKeigue PM, Lithell HO, Leon DA: Glucose tolerance and resistance to insulin-stimulated glucose uptake in men aged 70 years in relation to size at birth. Diabetologia. 1998, 41: 1133-1138. 10.1007/s001250051042.CrossRefPubMed
50.
go back to reference Robinson S, Walton RJ, Clark PM, Barker DJ, Hales CN, Osmond C: The relation of fetal growth to plasma glucose in young men. Diabetologia. 1992, 35: 444-446. 10.1007/BF02342441.CrossRefPubMed Robinson S, Walton RJ, Clark PM, Barker DJ, Hales CN, Osmond C: The relation of fetal growth to plasma glucose in young men. Diabetologia. 1992, 35: 444-446. 10.1007/BF02342441.CrossRefPubMed
51.
go back to reference Cook JT, Levy JC, Page RC, Shaw JA, Hattersley AT, Turner RC: Association of low birth weight with b cell function in the adult first-degree relatives of non-insulin dependent subjects. Br Med J. 1993, 306: 302-306. 10.1136/bmj.306.6873.302.CrossRef Cook JT, Levy JC, Page RC, Shaw JA, Hattersley AT, Turner RC: Association of low birth weight with b cell function in the adult first-degree relatives of non-insulin dependent subjects. Br Med J. 1993, 306: 302-306. 10.1136/bmj.306.6873.302.CrossRef
52.
go back to reference Phillips DI, Barker DJ, Hales CN, Hirst S, Osmond C: Thinness at birth an insulin resistance in adult life. Diabetologia. 1994, 37: 150-154. 10.1007/s001250050086.CrossRefPubMed Phillips DI, Barker DJ, Hales CN, Hirst S, Osmond C: Thinness at birth an insulin resistance in adult life. Diabetologia. 1994, 37: 150-154. 10.1007/s001250050086.CrossRefPubMed
53.
go back to reference Economides DL, Proudler A, Nicolaides KH: Plasma insulin in appropriate- and small-for-gestacional-age fetuses. Am J Obstet Gynecol. 1989, 160: 1091-1094.CrossRefPubMed Economides DL, Proudler A, Nicolaides KH: Plasma insulin in appropriate- and small-for-gestacional-age fetuses. Am J Obstet Gynecol. 1989, 160: 1091-1094.CrossRefPubMed
54.
go back to reference Hubinont C, Nicolini U, Fisk NM, Tannirandorn Y, Rodeck CH: Endocrine pancreatic function in growth-retarded fetuses. Obstet Gynecol. 1991, 77: 541-544.PubMed Hubinont C, Nicolini U, Fisk NM, Tannirandorn Y, Rodeck CH: Endocrine pancreatic function in growth-retarded fetuses. Obstet Gynecol. 1991, 77: 541-544.PubMed
55.
go back to reference Nicolini U, Hubinont C, Santolaya J, Fisk NM, Rodeck CH: Effects of fetal intravenous glucose challenge in normal and growth-retarded fetuses. Horm Metab Res. 1990, 22: 426-430. 10.1055/s-2007-1004939.CrossRefPubMed Nicolini U, Hubinont C, Santolaya J, Fisk NM, Rodeck CH: Effects of fetal intravenous glucose challenge in normal and growth-retarded fetuses. Horm Metab Res. 1990, 22: 426-430. 10.1055/s-2007-1004939.CrossRefPubMed
56.
go back to reference Colle E, Shiff D, Andrew G, Bauer CB, Fitzhardinge P: Insulin responses during catch-up growth of infants who were small for gestacional age. Pediatrics. 1976, 57: 363-371.PubMed Colle E, Shiff D, Andrew G, Bauer CB, Fitzhardinge P: Insulin responses during catch-up growth of infants who were small for gestacional age. Pediatrics. 1976, 57: 363-371.PubMed
57.
go back to reference Salle B, Ruitton-Uglienco A: Glucose disappearance rate, insulin response and growth hormone response in the small for gestacional age and premature infant of very low birth weight. Biol Neonate. 1976, 29: 1-17. 10.1159/000240843.CrossRefPubMed Salle B, Ruitton-Uglienco A: Glucose disappearance rate, insulin response and growth hormone response in the small for gestacional age and premature infant of very low birth weight. Biol Neonate. 1976, 29: 1-17. 10.1159/000240843.CrossRefPubMed
58.
go back to reference Van Assche FA, De Prins F, Aerts L, Verjans M: The endocrine pancreas in small-for-dates infants. Br J Obstet Gynaecol. 1977, 84: 751-753.CrossRefPubMed Van Assche FA, De Prins F, Aerts L, Verjans M: The endocrine pancreas in small-for-dates infants. Br J Obstet Gynaecol. 1977, 84: 751-753.CrossRefPubMed
59.
go back to reference Alsat E, Marcotty C, Gabriel R, Igout A, Frankenne F, Hennen G, Evian-Brion D: Molecular approach to intrauterine growth retardation: An overview of recent data. Reprod Fertil. 1995, 7: 1457-1464. 10.1071/RD9951457.CrossRef Alsat E, Marcotty C, Gabriel R, Igout A, Frankenne F, Hennen G, Evian-Brion D: Molecular approach to intrauterine growth retardation: An overview of recent data. Reprod Fertil. 1995, 7: 1457-1464. 10.1071/RD9951457.CrossRef
60.
go back to reference Setia S, Sridhar MG: Changes in GH/IGF-1 axis in intrauterine growth retardation: consequences of fetal programming?. Horm Metab Res. 2009, 41 (11): 791-198. 10.1055/s-0029-1231026.CrossRefPubMed Setia S, Sridhar MG: Changes in GH/IGF-1 axis in intrauterine growth retardation: consequences of fetal programming?. Horm Metab Res. 2009, 41 (11): 791-198. 10.1055/s-0029-1231026.CrossRefPubMed
61.
go back to reference Kouseff BG: Diabetic embryopathy. Curr Opin Pediatr. 1999, 11l: 348-352. 10.1097/00008480-199908000-00014.CrossRef Kouseff BG: Diabetic embryopathy. Curr Opin Pediatr. 1999, 11l: 348-352. 10.1097/00008480-199908000-00014.CrossRef
62.
go back to reference Suhonen L, Hiilesmaa V, Teramo K: Glycaemic control during early pregnancy and fetal malformations in women with type 1 diabetes mellitus. Diabetologia. 2000, 43l: 79-82. 10.1007/s001250050010.CrossRef Suhonen L, Hiilesmaa V, Teramo K: Glycaemic control during early pregnancy and fetal malformations in women with type 1 diabetes mellitus. Diabetologia. 2000, 43l: 79-82. 10.1007/s001250050010.CrossRef
Metadata
Title
Evaluation of neonatally-induced mild diabetes in rats: Maternal and fetal repercussions
Authors
Isabela L Iessi
Aline Bueno
Yuri K Sinzato
Kristin N Taylor
Marilza VC Rudge
Débora C Damasceno
Publication date
01-12-2010
Publisher
BioMed Central
Published in
Diabetology & Metabolic Syndrome / Issue 1/2010
Electronic ISSN: 1758-5996
DOI
https://doi.org/10.1186/1758-5996-2-37

Other articles of this Issue 1/2010

Diabetology & Metabolic Syndrome 1/2010 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.