Download PDF
Am J Perinatol
DOI: 10.1055/a-2490-3118
Review Article

A Queen City Legacy: 45 Years of Research in Pregnant Women with Insulin-Dependent Diabetes Mellitus, The Diabetes in Pregnancy Program Project Grant

Jane C. Khoury   *
1   Division of Biostatistics and Epidemiology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio
2   Department of Pediatrics, University of Cincinnati, College of Medicine, Cincinnati, Ohio
3   Division of Endocrinology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio
,
Menachem Miodovnik   *
4   Division of Maternal-Fetal Medicine, Department of Obstetrics and Gynecology, Inova Health System, Fairfax, Virginia
,
Francis B. Mimouni
5   Department of Pediatrics and Research Institute, Leumit Health Services, and the Sackler School of Medicine, Tel Aviv University, Tel Aviv, Israel
,
Shelley Ehrlich
1   Division of Biostatistics and Epidemiology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio
2   Department of Pediatrics, University of Cincinnati, College of Medicine, Cincinnati, Ohio
6   Department of Environmental and Public Health Sciences, University of Cincinnati, College of Medicine, Cincinnati, Ohio
,
Rhonda Szcznesiak
1   Division of Biostatistics and Epidemiology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio
2   Department of Pediatrics, University of Cincinnati, College of Medicine, Cincinnati, Ohio
,
Barak Rosenn
7   Department of Obstetrics and Gynecology, Jersey City Medical Center, West New York, New Jersey
› Author Affiliations Funding The studies described were supported in part by the Diabetes in Pregnancy Program Project Grant (HD11725) funded from 1978 to 1993 by the U.S. Department of Health and Human Services, National Institutes of Health, National Institute of Child Health and Human Development, and in part by The TEAM Study funded from 2016 to 2022 by National Institute of Diabetes and Digestive and Kidney Diseases (R01 DK109956).
› Further Information
Also available at
    Permissions and Reprints

Abstract

The Diabetes in Pregnancy Program Project Grant (PPG) was a 15-year program focused on enhancing the care for women with insulin-dependent diabetes mellitus (IDDM) during pregnancy and improving the well-being of their offspring. Launched in July 1978 at the University of Cincinnati, the PPG pursued a multifaceted research agenda encompassing basic science, animal and placental studies, and maternal and neonatal clinical trials to understand the physiological and pathophysiological aspects of IDDM during pregnancy. A total of 402 singleton pregnancies in 259 women with IDDM were enrolled prior to 10 weeks gestation over the 15-year period. Of the 402 pregnancies, there were 295 live births, 1 stillbirth, 4 neonatal deaths, and 15 infants were born with major congenital malformations. Central to the program's methodology was the management of diabetes during pregnancy, involving intensive insulin therapy and meticulous monitoring using the cutting-edge technology of the time to achieve glycemic control. The extensive research of the PPG yielded profound insights into the effects of maternal diabetes on embryonic and fetal development and neonatal health. Through animal studies, notably using pregnant sheep, the program clarified the mechanisms of fetal hypoxia and metabolic disorders. Clinical trials underscored the significance of early glycemic control in mitigating the risks of spontaneous abortions, congenital malformations, and neonatal complications. The program also examined the influence of pregnancy on the progression of microvascular diseases, the role of maternal weight and weight gain in pregnancy outcomes, and the distinctive growth patterns of fetuses in IDDM pregnancies. Furthermore, the PPG probed the incidence and underlying mechanisms of hypoglycemia during pregnancy and the heightened risk of obstetric complications in IDDM patients. Our findings established a foundation of knowledge to aid clinicians, researchers, and health care providers in best practices and ensure a lasting impact on the care of pregnant women with pregestational diabetes.

Key Points

  • Prepregnancy management reduces maternal, fetal, and neonatal complications in IDDM.

  • Strict glycemic control improves many pregnancy outcomes in IDDM.

  • Fetal glycemic exposure may have lifelong effects.

Keywords

diabetes in pregnancy - Program Project Grant - insulin-dependent diabetes mellitus - glycemic control - maternal complications - neonatal complications

Ethical Approval

All studies were approved by the Investigational Review Board at the University of Cincinnati, and where applicable, by the Investigational Review Board at Cincinnati Children's Hospital Medical Center.


* These are co-first authors.




Publication History

Received: 24 July 2024

Accepted: 26 November 2024

Article published online:
24 December 2024

© 2024. Thieme. All rights reserved.

Thieme Medical Publishers, Inc.
333 Seventh Avenue, 18th Floor, New York, NY 10001, USA

 

  • References

  • 1 Ballard JL, Holroyde J, Tsang RC, Chan G, Sutherland JM, Knowles HC. High malformation rates and decreased mortality in infants of diabetic mothers managed after the first trimester of pregnancy (1956-1978). Am J Obstet Gynecol 1984; 148 (08) 1111-1118
    CrossrefPubMedSearch in Google Scholar
  • 2 McElvy SS, Miodovnik M, Rosenn B. et al. A focused preconceptional and early pregnancy program in women with type 1 diabetes reduces perinatal mortality and malformation rates to general population levels. J Matern Fetal Med 2000; 9 (01) 14-20
    PubMedSearch in Google Scholar
  • 3 Cole RA, Soeldner JS, Dunn PJ, Bunn HF. A rapid method for the determination of glycosylated hemoglobins using high pressure liquid chromatography. Metabolism 1978; 27 (03) 289-301
    CrossrefPubMedSearch in Google Scholar
  • 4 Kaplan LA, Cline D, Gartside P, Burstein S, Sperling M, Stein EA. Hemoglobin A1 in hemolysates from healthy and insulin-dependent diabetic children, as determined with a temperature-controlled minicolumn assay. Clin Chem 1982; 28 (01) 13-18
    CrossrefPubMedSearch in Google Scholar
  • 5 Ballard JL, Novak KK, Driver M. A simplified score for assessment of fetal maturation of newly born infants. J Pediatr 1979; 95 (5 Pt 1): 769-774
    CrossrefPubMedSearch in Google Scholar
  • 6 Miodovnik M, Lavin JP, Harrington DJ, Leung LS, Seeds AE, Clark KE. Effect of maternal ketoacidemia on the pregnant ewe and the fetus. Am J Obstet Gynecol 1982; 144 (05) 585-593
    CrossrefPubMedSearch in Google Scholar
  • 7 Clark KE, Miodovnik M, Skillman CA, Mimouni F. Review of fetal cardiovascular and metabolic responses to diabetic insults in the pregnant ewe. Am J Perinatol 1988; 5 (04) 312-318
    Thieme ConnectPubMedSearch in Google Scholar
  • 8 Miodovnik M, Skillman CA, Hertzberg V, Harrington DJ, Clark KE. Effect of maternal hyperketonemia in hyperglycemic pregnant ewes and their fetuses. Am J Obstet Gynecol 1986; 154 (02) 394-401
    CrossrefPubMedSearch in Google Scholar
  • 9 Miodovnik M, Lavin JP, Harrington DJ, Leung L, Seeds AE, Clark KE. Cardiovascular and biochemical effects of infusion of beta hydroxybutyrate into the fetal lamb. Am J Obstet Gynecol 1982; 144 (05) 594-600
    CrossrefPubMedSearch in Google Scholar
  • 10 Skillman CA, Plessinger MA, Woods JR, Clark KE. Effect of graded reductions in uteroplacental blood flow on the fetal lamb. Am J Physiol 1985; 249 (6 Pt 2): H1098-H1105
    PubMedSearch in Google Scholar
  • 11 Miodovnik M, Mimouni F, Berk M, Clark KE. Alloxan-induced diabetes mellitus in the pregnant ewe: metabolic and cardiovascular effects on the mother and her fetus. Am J Obstet Gynecol 1989; 160 (5 Pt 1): 1239-1244
    CrossrefPubMedSearch in Google Scholar
  • 12 Coetzee A, Hall DR, Langenegger EJ, van de Vyver M, Conradie M. Pregnancy and diabetic ketoacidosis: fetal jeopardy and windows of opportunity. Front Clin Diabetes Healthc 2023; 4 (04) 1266017
    CrossrefPubMedSearch in Google Scholar
  • 13 Cetin H, Yalaz M, Akisu M, Kultursay N. Polycythaemia in infants of diabetic mothers: β-hydroxybutyrate stimulates erythropoietic activity. J Int Med Res 2011; 39 (03) 815-821
    CrossrefPubMedSearch in Google Scholar
  • 14 Philipps AF, Porte PJ, Stabinsky S, Rosenkrantz TS, Raye JR. Effects of chronic fetal hyperglycemia upon oxygen consumption in the ovine uterus and conceptus. J Clin Invest 1984; 74 (01) 279-286
    CrossrefPubMedSearch in Google Scholar
  • 15 Green DW, Mimouni F. Nucleated erythrocytes in healthy infants and in infants of diabetic mothers. J Pediatr 1990; 116 (01) 129-131
    CrossrefPubMedSearch in Google Scholar
  • 16 Green DW, Khoury J, Mimouni F. Neonatal hematocrit and maternal glycemic control in insulin-dependent diabetes. J Pediatr 1992; 120 (2 Pt 1): 302-305
    CrossrefPubMedSearch in Google Scholar
  • 17 Mimouni F, Miodovnik M, Siddiqi TA, Butler JB, Holroyde J, Tsang RC. Neonatal polycythemia in infants of insulin-dependent diabetic mothers. Obstet Gynecol 1986; 68 (03) 370-372
    CrossrefPubMedSearch in Google Scholar
  • 18 Miodovnik M, Mimouni F, Tsang RC. et al. Management of the insulin-dependent diabetic during labor and delivery. Influences on neonatal outcome. Am J Perinatol 1987; 4 (02) 106-114
    Thieme ConnectPubMedSearch in Google Scholar
  • 19 Mimouni F, Miodovnik M, Siddiqi TA, Khoury J, Tsang RC. Perinatal asphyxia in infants of insulin-dependent diabetic mothers. J Pediatr 1988; 113 (02) 345-353
    CrossrefPubMedSearch in Google Scholar
  • 20 Rosenn B, Miodovnik M, Kranias G. et al. Progression of diabetic retinopathy in pregnancy: association with hypertension in pregnancy. Am J Obstet Gynecol 1992; 166 (04) 1214-1218
    CrossrefPubMedSearch in Google Scholar
  • 21 Miodovnik M, Rosenn BM, Khoury JC, Grigsby JL, Siddiqi TA. Does pregnancy increase the risk for development and progression of diabetic nephropathy?. Am J Obstet Gynecol 1996; 174 (04) 1180-1189 , discussion 1189–1191
    CrossrefPubMedSearch in Google Scholar
  • 22 Mimouni F, Khoury JC, Ehrlich S, Sheffer-Mimouni G, Rosenn B, Miodovnik M. Is pregnancy a risk factor for progression of diabetic retinopathy and nephropathy? A matched cohort study. Am J Perinatol 2024
    PubMedSearch in Google Scholar
  • 23 Feghali M, Khoury JC, Shveiky D, Miodovnik M. Association of vaginal delivery efforts with retinal disease in women with type I diabetes. J Matern Fetal Neonatal Med 2012; 25 (01) 27-31
    CrossrefPubMedSearch in Google Scholar
  • 24 Khoury JC, Miodovnik M, LeMasters G, Sibai B. Pregnancy outcome and progression of diabetic nephropathy. What's next?. J Matern Fetal Neonatal Med 2002; 11 (04) 238-244
    CrossrefPubMedSearch in Google Scholar
  • 25 Haeri S, Khoury J, Kovilam O, Miodovnik M. The association of intrauterine growth abnormalities in women with type 1 diabetes mellitus complicated by vasculopathy. Am J Obstet Gynecol 2008; 199 (03) 278.e1-278.e5
    CrossrefPubMedSearch in Google Scholar
  • 26 McElvy SS, Demarini S, Miodovnik M, Khoury JC, Rosenn B, Tsang RC. Fetal weight and progression of diabetic retinopathy. Obstet Gynecol 2001; 97 (04) 587-592
    PubMedSearch in Google Scholar
  • 27 Klein BE, Moss SE, Klein R. Effect of pregnancy on progression of diabetic retinopathy. Diabetes Care 1990; 13 (01) 34-40
    CrossrefPubMedSearch in Google Scholar
  • 28 Diabetes Control and Complications Trial Research Group. Effect of pregnancy on microvascular complications in the diabetes control and complications trial. Diabetes Care 2000; 23 (08) 1084-1091
    CrossrefPubMedSearch in Google Scholar
  • 29 Kawakita T, Bowers K, Coviello E. et al. Prepregnancy weight in women with type i diabetes mellitus: Effect on pregnancy outcomes. Am J Perinatol 2016; 33 (13) 1300-1305
    Thieme ConnectPubMedSearch in Google Scholar
  • 30 Kawakita T, Bowers K, McWhorter K. et al. Characterizing gestational weight gain according to institute of medicine guidelines in women with type 1 diabetes mellitus: Association with maternal and perinatal outcome. Am J Perinatol 2016; 33 (13) 1266-1272
    Thieme ConnectPubMedSearch in Google Scholar
  • 31 McWhorter KL, Bowers K, Dolan L, Deka R, Jackson CL, Khoury JC. Assessing the impact of excessive gestational weight gain among women with type 1 diabetes on overweight/obesity in their adolescent and young adult offspring: a pilot study. Front Endocrinol (Lausanne) 2018; 9: 713-718
    CrossrefPubMedSearch in Google Scholar
  • 32 Feghali MN, Khoury JC, Timofeev J, Shveiky D, Driggers RW, Miodovnik M. Asymmetric large for gestational age newborns in pregnancies complicated by diabetes mellitus: is maternal obesity a culprit?. J Matern Fetal Neonatal Med 2012; 25 (01) 32-35
    CrossrefPubMedSearch in Google Scholar
  • 33 Leddy MA, Power ML, Schulkin J. The impact of maternal obesity on maternal and fetal health. Rev Obstet Gynecol 2008; 1 (04) 170-178
    PubMedSearch in Google Scholar
  • 34 Kalkwarf HJ, Bell RC, Khoury JC, Gouge AL, Miodovnik M. Dietary fiber intakes and insulin requirements in pregnant women with type 1 diabetes. J Am Diet Assoc 2001; 101 (03) 305-310
    CrossrefPubMedSearch in Google Scholar
  • 35 Morales M, López-Delgado MI, Alcántara A. et al. Preserved GLP-I effects on glycogen synthase a activity and glucose metabolism in isolated hepatocytes and skeletal muscle from diabetic rats. Diabetes 1997; 46 (08) 1264-1269
    CrossrefPubMedSearch in Google Scholar
  • 36 D'Alessio DA, Prigeon RL, Ensinck JW. Enteral enhancement of glucose disposition by both insulin-dependent and insulin-independent processes. A physiological role of glucagon-like peptide I. Diabetes 1995; 44 (12) 1433-1437
    CrossrefPubMedSearch in Google Scholar
  • 37 Holst JJ. Enteroglucagon. Annu Rev Physiol 1997; 59: 257-271
    CrossrefPubMedSearch in Google Scholar
  • 38 Hvidberg A, Nielson MT, Hillsted J, Orskov C, Hoist JJ. Effect of glucagon-like peptide 1 (proglucagon 78–107 amide) on hepatic glucose production in healthy man. Metabolism 1994; 43 (01) 104-108
    CrossrefPubMedSearch in Google Scholar
  • 39 Khoury JC, Miodovnik M, Buncher CR. et al. Consequences of smoking and caffeine consumption during pregnancy in women with type 1 diabetes. J Matern Fetal Neonatal Med 2004; 15 (01) 44-50
    CrossrefPubMedSearch in Google Scholar
  • 40 Miodovnik M, Lavin JP, Knowles HC, Holroyde J, Stys SJ. Spontaneous abortion among insulin-dependent diabetic women. Am J Obstet Gynecol 1984; 150 (04) 372-376
    CrossrefPubMedSearch in Google Scholar
  • 41 Miodovnik M, Skillman C, Holroyde JC, Butler JB, Wendel JS, Siddiqi TA. Elevated maternal glycohemoglobin in early pregnancy and spontaneous abortion among insulin-dependent diabetic women. Am J Obstet Gynecol 1985; 153 (04) 439-442
    CrossrefPubMedSearch in Google Scholar
  • 42 Miodovnik M, Mimouni F, Siddiqi TA, Khoury J, Berk MA. Spontaneous abortions in repeat diabetic pregnancies: a relationship with glycemic control. Obstet Gynecol 1990; 75 (01) 75-78
    PubMedSearch in Google Scholar
  • 43 Bendon RW, Mimouni F, Khoury J, Miodovnik M. Histopathology of spontaneous abortion in diabetic pregnancies. Am J Perinatol 1990; 7 (03) 207-210
    Thieme ConnectPubMedSearch in Google Scholar
  • 44 Miodovnik M, Mimouni F, Dignan PS. et al. Major malformations in infants of IDDM women. Vasculopathy and early first-trimester poor glycemic control. Diabetes Care 1988; 11 (09) 713-718
    CrossrefPubMedSearch in Google Scholar
  • 45 Rosenn B, Miodovnik M, Dignan PS, Siddiqi TA, Khoury J, Mimouni F. Minor congenital malformations in infants of insulin-dependent diabetic women: association with poor glycemic control. Obstet Gynecol 1990; 76 (5 Pt 1): 745-749
    CrossrefPubMedSearch in Google Scholar
  • 46 Rosenn B, Miodovnik M, Combs CA, Khoury J, Siddiqi TA. Glycemic thresholds for spontaneous abortion and congenital malformations in insulin-dependent diabetes mellitus. Obstet Gynecol 1994; 84 (04) 515-520
    PubMedSearch in Google Scholar
  • 47 Rosenn B, Miodovnik M, Combs CA, Khoury J, Siddiqi TA. Pre-conception management of insulin-dependent diabetes: improvement of pregnancy outcome. Obstet Gynecol 1991; 77 (06) 846-849
    PubMedSearch in Google Scholar
  • 48 Rosenn B, Miodovnik M, Mimouni F, Khoury JC, Siddiqi TA. Patient experience in a diabetic program project improves subsequent pregnancy outcome. Obstet Gynecol 1991; 77 (01) 87-91
    PubMedSearch in Google Scholar
  • 49 Mills JL, Simpson JL, Driscoll SG. et al. Incidence of spontaneous abortion among normal women and insulin-dependent diabetic women whose pregnancies were identified within 21 days of conception. N Engl J Med 1988; 319 (25) 1617-1623
    CrossrefPubMedSearch in Google Scholar
  • 50 Jensen DM, Damm P, Moelsted-Pedersen L. et al. Outcomes in type 1 diabetic pregnancies: a nationwide, population-based study. Diabetes Care 2004; 27 (12) 2819-2823
    CrossrefPubMedSearch in Google Scholar
  • 51 Platt MJ, Stanisstreet M, Casson IF. et al. St Vincent's Declaration 10 years on: outcomes of diabetic pregnancies. Diabet Med 2002; 19 (03) 216-220
    CrossrefPubMedSearch in Google Scholar
  • 52 Key TC, Giuffrida R, Moore TR. Predictive value of early pregnancy glycohemoglobin in the insulin-treated diabetic patient. Am J Obstet Gynecol 1987; 156 (05) 1096-1100
    CrossrefPubMedSearch in Google Scholar
  • 53 Greene MF, Hare JW, Cloherty JP, Benacerraf BR, Soeldner JS. First-trimester hemoglobin A1 and risk for major malformation and spontaneous abortion in diabetic pregnancy. Teratology 1989; 39 (03) 225-231
    CrossrefPubMedSearch in Google Scholar
  • 54 Kitzmiller JL, Buchanan TA, Kjos S, Combs CA, Ratner RE. Pre-conception care of diabetes, congenital malformations, and spontaneous abortions. Diabetes Care 1996; 19 (05) 514-541
    CrossrefPubMedSearch in Google Scholar
  • 55 Siddiqi TA, Miodovnik M, Mimouni F, Clark EA, Khoury JC, Tsang RC. Biphasic intrauterine growth in insulin-dependent diabetic pregnancies. J Am Coll Nutr 1989; 8 (03) 225-234
    CrossrefPubMedSearch in Google Scholar
  • 56 Ballard JL, Rosenn B, Khoury JC, Miodovnik M. Diabetic fetal macrosomia: significance of disproportionate growth. J Pediatr 1993; 122 (01) 115-119
    CrossrefPubMedSearch in Google Scholar
  • 57 Bollepalli S, Dolan LM, Miodovnik M, Feghali M, Khoury JC. Asymmetric large-for-gestational-age infants of type 1 diabetic women: morbidity and abdominal growth. Am J Perinatol 2010; 27 (08) 603-610
    Thieme ConnectPubMedSearch in Google Scholar
  • 58 Rosenn BM, Miodovnik M, Khoury JC, Siddiqi TA. Deficient counterregulation: a possible risk factor for excessive fetal growth in IDDM pregnancies. Diabetes Care 1997; 20 (05) 872-874
    CrossrefPubMedSearch in Google Scholar
  • 59 Mimouni F, Miodovnik M, Rosenn B, Khoury J, Siddiqi TA. Birth trauma in insulin-dependent diabetic pregnancies. Am J Perinatol 1992; 9 (03) 205-208
    Thieme ConnectPubMedSearch in Google Scholar
  • 60 Mehta S, Khoury J, Miodovnik M, Kawakita T, Ehrlich S, Bowers K. Placental weight in pregnant women with type 1 diabetes mellitus: the association with fetal growth. Am J Perinatol 2016; 33 (13) 1255-1261
    Thieme ConnectPubMedSearch in Google Scholar
  • 61 Menon RK, Cohen RM, Sperling MA, Cutfield WS, Mimouni F, Khoury JC. Transplacental passage of insulin in pregnant women with insulin-dependent diabetes mellitus. Its role in fetal macrosomia. N Engl J Med 1990; 323 (05) 309-315
    CrossrefPubMedSearch in Google Scholar
  • 62 Rosenn B, Miodovnik M, Combs CA, Williams T, Wittekind C, Siddiqi TA. Human versus animal insulin in the management of insulin-dependent diabetes: lack of effect on fetal growth. Obstet Gynecol 1991; 78 (04) 590-593
    PubMedSearch in Google Scholar
  • 63 Rosenn B, Miodovnik M, Holcberg G, Jaekle RK, Khoury J, Siddiqi TA. Hypoglycemia: the price of intensive insulin therapy for pregnant women with insulin-dependent diabetes mellitus pregnancies. Obstet Gynecol 1995; 85 (03) 417-422
    CrossrefPubMedSearch in Google Scholar
  • 64 Rosenn BM, Miodovnik M, Khoury JC, Siddiqi TA. Counterregulatory hormonal responses to hypoglycemia during pregnancy. Obstet Gynecol 1996; 87 (04) 568-574
    CrossrefPubMedSearch in Google Scholar
  • 65 Rosenn B, Miodovnik M, Combs CA, Khoury J, Siddiqi TA. Poor glycemic control and antepartum obstetric complications in women with insulin-dependent diabetes. Int J Gynaecol Obstet 1993; 43 (01) 21-28
    CrossrefPubMedSearch in Google Scholar
  • 66 Kovilam O, Khoury J, Miodovnik M, Chames M, Spinnoto J, Sibai B. Spontaneous preterm delivery in the type 1 diabetic pregnancy: the role of glycemic control. J Matern Fetal Neonatal Med 2002; 11 (04) 245-248
    CrossrefPubMedSearch in Google Scholar
  • 67 Miodovnik M, Peros N, Holroyde JC, Siddiqi TA. Treatment of premature labor in insulin-dependent diabetic women. Obstet Gynecol 1985; 65 (05) 621-627
    PubMedSearch in Google Scholar
  • 68 Mimouni F, Miodovnik M, Siddiqi TA, Berk MA, Wittekind C, Tsang RC. High spontaneous premature labor rate in insulin-dependent diabetic pregnant women: an association with poor glycemic control and urogenital infection. Obstet Gynecol 1988; 72 (02) 175-180
    PubMedSearch in Google Scholar
  • 69 Siddiqi T, Rosenn B, Mimouni F, Khoury J, Miodovnik M. Hypertension during pregnancy in insulin-dependent diabetic women. Obstet Gynecol 1991; 77 (04) 514-519
    PubMedSearch in Google Scholar
  • 70 Stamler EF, Cruz ML, Mimouni F. et al. High infectious morbidity in pregnant women with insulin-dependent diabetes: an understated complication. Am J Obstet Gynecol 1990; 163 (4 Pt 1): 1217-1221
    CrossrefPubMedSearch in Google Scholar
  • 71 Combs CA, Rosenn B, Kitzmiller JL, Khoury JC, Wheeler BC, Miodovnik M. Early-pregnancy proteinuria in diabetes related to preeclampsia. Obstet Gynecol 1993; 82 (05) 802-807
    PubMedSearch in Google Scholar
  • 72 Tsang RC, Oh W. Neonatal hypocalcemia in low birth weight infants. Pediatrics 1970; 45 (05) 773-781
    CrossrefPubMedSearch in Google Scholar
  • 73 Tsang RC, Kleinman LI, Sutherland JM, Light IJ. Hypocalcemia in infants of diabetic mothers. Studies in calcium, phosphorus, and magnesium metabolism and parathormone responsiveness. J Pediatr 1972; 80 (03) 384-395
    PubMedSearch in Google Scholar
  • 74 Tsang RC. Neonatal magnesium disturbances. Am J Dis Child 1972; 124 (02) 282-293
    PubMedSearch in Google Scholar
  • 75 Levine BS, Coburn JW. Magnesium, the mimic/antagonist of calcium. N Engl J Med 1984; 310 (19) 1253-1255
    CrossrefPubMedSearch in Google Scholar
  • 76 Tsang RC, Chen I, Friedman MA. et al. Parathyroid function in infants of diabetic mothers. J Pediatr 1975; 86 (03) 399-404
    CrossrefPubMedSearch in Google Scholar
  • 77 Tsang RC, Strub R, Brown DR, Steichen J, Hartman C, Chen IW. Hypomagnesemia in infants of diabetic mothers: perinatal studies. J Pediatr 1976; l 89 (01) 115-119
    CrossrefPubMedSearch in Google Scholar
  • 78 Mimouni F, Miodovnik M, Tsang RC, Callahan J, Shaul P. Decreased amniotic fluid magnesium concentration in diabetic pregnancy. Obstet Gynecol 1987; 69 (01) 12-14
    PubMedSearch in Google Scholar
  • 79 Mimouni F, Loughead JL, Tsang RC, Khoury J. Postnatal surge in serum calcitonin concentrations: no contribution to neonatal hypocalcemia in infants of diabetic mothers. Pediatr Res 1990; 28 (05) 493-495
    CrossrefPubMedSearch in Google Scholar
  • 80 Demarini S, Mimouni F, Tsang RC, Khoury J, Hertzberg V. Impact of metabolic control of diabetes during pregnancy on neonatal hypocalcemia: a randomized study. Obstet Gynecol 1994; 83 (06) 918-922
    CrossrefPubMedSearch in Google Scholar
  • 81 Mehta KC, Kalkwarf HJ, Mimouni F, Khoury J, Tsang RC. Randomized trial of magnesium administration to prevent hypocalcemia in infants of diabetic mothers. J Perinatol 1998; 18 (05) 352-356
    PubMedSearch in Google Scholar
  • 82 Mimouni F, Steichen JJ, Tsang RC, Hertzberg V, Miodovnik M. Decreased bone mineral content in infants of diabetic mothers. Am J Perinatol 1988; 5 (04) 339-343
    Thieme ConnectPubMedSearch in Google Scholar
  • 83 Demarini S, Specker BL, Sierra RI, Miodovnik M, Tsang RC. Evidence of increased intrauterine bone resorption in term infants of mothers with insulin-dependent diabetes. J Pediatr 1995; 126 (5 Pt 1): 796-798
    CrossrefPubMedSearch in Google Scholar
  • 84 Szczesniak RD, Li D, Duan LL, Altaye M, Miodovnik M, Khoury JC. Longitudinal patterns of glycemic control and blood pressure in pregnant women with type 1 diabetes mellitus: Phenotypes from functional data analysis. Am J Perinatol 2016; 33 (13) 1282-1290
    Thieme ConnectPubMedSearch in Google Scholar
  • 85 Gupta R, Khoury J, Altaye M, Dolan L, Szczesniak RD. Glycemic excursions in type 1 diabetes in pregnancy: a semiparametric statistical approach to identify sensitive time points during gestation. J Diabetes Res 2017; 2017: 2852913
    CrossrefPubMedSearch in Google Scholar
  • 86 Gupta R, Khoury JC, Altaye M, Jandarov R, Szczesniak RD. Assessing the relationship between gestational glycemic control and risk of preterm birth in women with type 1 diabetes: a joint modeling approach. J Diabetes Res 2020; 2020: 3074532
    CrossrefPubMedSearch in Google Scholar
  • 87 Gupta R, Khoury JC, Altaye M, Jandarov R, Szczesniak RD. Flexible multivariate joint model of longitudinal intensity and binary process for medical monitoring of frequently collected data. Stat Med 2021; 40 (07) 1845-1858
    CrossrefPubMedSearch in Google Scholar
  • 88 Vandyke R, Ren Y, Sucharew HJ, Miodovnik M, Rosenn B, Khoury JC. Characterizing maternal glycemic control: a more informative approach using semiparametric regression. J Matern Fetal Neonatal Med 2012; 25 (01) 15-19
    CrossrefPubMedSearch in Google Scholar
  • 89 Scott EM, Feig DS, Murphy HR, Law GR. CONCEPTT Collaborative Group. Continuous glucose monitoring in pregnancy: importance of analyzing temporal profiles to understand clinical outcomes. Diabetes Care 2020; 43 (06) 1178-1184
    CrossrefPubMedSearch in Google Scholar
  • 90 Sweeting MJ, Barrett JK, Thompson SG, Wood AM. The use of repeated blood pressure measures for cardiovascular risk prediction: a comparison of statistical models in the ARIC study. Stat Med 2017; 36 (28) 4514-4528
    CrossrefPubMedSearch in Google Scholar
  • 91 Khoury JC, Altaye M, Ehrlich S. et al. Does birthweight represent imprinting for life? preliminary findings from the Level and Timing of Diabetic Hyperglycemia in Utero: Transgenerational Effect on Adult Morbidity (TEAM) Study. Reports 2020; 3 (04) 36
    CrossrefPubMedSearch in Google Scholar
  • 92 Bowers K, Ehrlich S, Dolan LM. et al. Elevated Anthropometric and Metabolic Indicators among Young Adult Offspring of Mothers with Pregestational Diabetes: Early Results from the Transgenerational Effect on Adult Morbidity Study (the TEAM Study). J Diabetes Res 2021; 2021: 6590431
    CrossrefPubMedSearch in Google Scholar