Gestational diabetes mellitus diagnosed at 24 to 28 weeks of gestation in older and obese Women: Is it too late?

Autoři: Wonjin Kim aff001;  Soo Kyung Park aff003;  Yoo Lee Kim aff001
Působiště autorů: Department of Internal Medicine, Division of Endocrinology and Metabolism, CHA Gangnam Medical Center, CHA University School of Medicine, Seoul, Korea aff001;  Yonsei University College of Medicine, Seoul, Korea aff002;  Departmentof Epidemiology and Biostatistics, School of Public Health, University of Maryland, College Park, Maryland, United States of America aff003
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0225955



The prevalence of elderly pregnancy and maternal obesity is increasing worldwide. In old and obese women, metabolic derangement affecting fetal growth might be present earlier than the diagnosis of gestational diabetes mellitus (GDM) or even before pregnancy. We thus investigated whether GDM diagnosed at 24–28 weeks of gestation had already affected fetal abdominal growth and, if so, whether elderly pregnancy and/or maternal obesity aggravate fetal abdominal obesity.


We retrospectively reviewed the medical records of 7820 singleton pregnant women who had been universally screened using a 50-g glucose challenge test (GCT) at 24–28 weeks of gestation, and underwent a 3-h 100-g oral glucose tolerance test (OGTT) if GCT were ≥140mg/dl. GDM and normal glucose tolerance (NGT) were diagnosed using the Carpenter-Coustan criteria. Fetal abdominal obesity was investigated by assessing the fetal abdominal overgrowth ratios (FAORs) of the ultrasonographically estimated gestational age (GA) of abdominal circumference per actual GA by the last menstruation period, biparietal diameter or femur length, respectively. Fetal abdominal overgrowth was defined as FAOR ≥ 90th percentile. The subjects were divided into four study groups: group 1 (age < 35 years and pre-pregnancy body mass index [BMI] < 25 kg/m2), group 2 (age < 35 years and ≥ 25), group 3 (age ≥ 35 years and BMI < 25), and group 4 (age ≥ 35 years and ≥ 25).


The overall prevalence of GDM was 5.1%, with old and obese group 4 exhibiting the highest prevalence (22.4%). FAORs were significantly higher in the fetus of those with GDM than in the NGT subjects. But, in the subgroup analysis, only old and nonobese group 3 and old and obese group 4 with GDM exhibited significantly higher FAORs than the NGT subjects. Also, risk of fetal abdominal overgrowth was increased in group 3 and 4 subjects with GDM but not in young and nonobese group 1 GDM. The risk of fetal abdominal overgrowth significantly increased with maternal age >35 years, pre-pregnancy BMI >20kg/m2, and HbA1c >37.7 mmol/mol (5.6%). In multivariate analyses, maternal age and HbA1c were significantly associated with FAORs.


GDM diagnosed at 24–28 weeks of gestation already affected fetal abdominal obesity in older and/or obese women, but not in younger and nonobese women. Our data suggest that selective screening and appropriate intervention of GDM earlier than 24–28 weeks of gestation might be necessary for high-risk old and/or obese women.

Klíčová slova:

Biostatistics – Body Mass Index – Management of high-risk pregnancies – Obesity – Pregnancy


1. American Diabetes A. 2. Classification and Diagnosis of Diabetes: Standards of Medical Care in Diabetes-2019. Diabetes Care. 2019;42: S13–S28. doi: 10.2337/dc19-S002 30559228

2. Zhu Y, Zhang C. Prevalence of Gestational Diabetes and Risk of Progression to Type 2 Diabetes: a Global Perspective. Curr Diab Rep. 2016;16: 7. doi: 10.1007/s11892-015-0699-x 26742932

3. Saccone G, Caissutti C, Khalifeh A, Meltzer S, Scifres C, Simhan HN, et al. One step versus two step approach for gestational diabetes screening: systematic review and meta-analysis of the randomized trials. J Matern Fetal Neonatal Med. 2019;32: 1547–1555. doi: 10.1080/14767058.2017.1408068 29157030

4. Committee on Practice B-O. ACOG Practice Bulletin No. 190: Gestational Diabetes Mellitus. Obstet Gynecol. 2018;131: e49–e64. doi: 10.1097/AOG.0000000000002501 29370047

5. Moyer VA, Force USPST. Screening for gestational diabetes mellitus: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med. 2014;160: 414–420. doi: 10.7326/M13-2905 24424622

6. Blumer I, Hadar E, Hadden DR, Jovanovic L, Mestman JH, Murad MH, et al. Diabetes and pregnancy: an endocrine society clinical practice guideline. J Clin Endocrinol Metab. 2013;98: 4227–4249. doi: 10.1210/jc.2013-2465 24194617

7. Sweeting AN, Ross GP, Hyett J, Molyneaux L, Constantino M, Harding AJ, et al. Gestational Diabetes Mellitus in Early Pregnancy: Evidence for Poor Pregnancy Outcomes Despite Treatment. Diabetes Care. 2016;39: 75–81. doi: 10.2337/dc15-0433 26645084

8. Lawrence JM, Contreras R, Chen W, Sacks DA. Trends in the prevalence of preexisting diabetes and gestational diabetes mellitus among a racially/ethnically diverse population of pregnant women, 1999–2005. Diabetes Care. 2008;31: 899–904. doi: 10.2337/dc07-2345 18223030

9. Menke A, Casagrande S, Geiss L, Cowie CC. Prevalence of and Trends in Diabetes Among Adults in the United States, 1988–2012. JAMA. 2015;314: 1021–1029. doi: 10.1001/jama.2015.10029 26348752

10. Feig DS, Razzaq A, Sykora K, Hux JE, Anderson GM. Trends in deliveries, prenatal care, and obstetrical complications in women with pregestational diabetes: a population-based study in Ontario, Canada, 1996–2001. Diabetes Care. 2006;29: 232–235. doi: 10.2337/diacare.29.02.06.dc05-1482 16443865

11. Organization WH. Diagnostic Criteria and Classification of Hyperglycaemia First Detected in Pregnancy. World Health Organization; 2013. pp. 63.

12. International Association of D, Pregnancy Study Groups Consensus P, Metzger BE, Gabbe SG, Persson B, Buchanan TA, et al. International association of diabetes and pregnancy study groups recommendations on the diagnosis and classification of hyperglycemia in pregnancy. Diabetes Care. 2010;33: 676–682. doi: 10.2337/dc09-1848 20190296

13. Group HSCR, Metzger BE, Lowe LP, Dyer AR, Trimble ER, Chaovarindr U, et al. Hyperglycemia and adverse pregnancy outcomes. N Engl J Med. 2008;358: 1991–2002. doi: 10.1056/NEJMoa0707943 18463375

14. American Diabetes A. Standards of medical care in diabetes-2014. Diabetes Care. 2014;37 Suppl 1: S14–80. doi: 10.2337/dc14-S014 24357209

15. Committee of Clinical Practice Guidelines KDA. 2019 Clinical Practice Guidelines for Gestational Diabetes Mellitus in Korea; 2019.

16. Crowther CA, Hiller JE, Moss JR, McPhee AJ, Jeffries WS, Robinson JS, et al. Effect of treatment of gestational diabetes mellitus on pregnancy outcomes. N Engl J Med. 2005;352: 2477–2486. doi: 10.1056/NEJMoa042973 15951574

17. Landon MB, Spong CY, Thom E, Carpenter MW, Ramin SM, Casey B, et al. A multicenter, randomized trial of treatment for mild gestational diabetes. N Engl J Med. 2009;361: 1339–1348. doi: 10.1056/NEJMoa0902430 19797280

18. Tantanasis T, Daniilidis A, Giannoulis C, Tzafettas M, Dinas K, Loufopoulos A, et al. Sonographic assessment of fetal subcutaneous fat tissue thickness as an indicator of gestational diabetes. Eur J Obstet Gynecol Reprod Biol. 2010;152: 157–162. doi: 10.1016/j.ejogrb.2010.05.035 20609509

19. de Santis MS, Taricco E, Radaelli T, Spada E, Rigano S, Ferrazzi E, et al. Growth of fetal lean mass and fetal fat mass in gestational diabetes. Ultrasound Obstet Gynecol. 2010;36: 328–337. doi: 10.1002/uog.7575 20131333

20. Larciprete G, Valensise H, Vasapollo B, Novelli GP, Parretti E, Altomare F, et al. Fetal subcutaneous tissue thickness (SCTT) in healthy and gestational diabetic pregnancies. Ultrasound Obstet Gynecol. 2003;22: 591–597. doi: 10.1002/uog.926 14689531

21. Aksoy H, Aksoy U, Yucel B, Saygi Ozyurt S, Aydin T, Alparslan Babayigit M. Fetal anterior abdominal wall thickness may be an early ultrasonographic sign of gestational diabetes mellitus. J Matern Fetal Neonatal Med. 2016;29: 2028–2032. doi: 10.3109/14767058.2015.1072164 26333303

22. Catalano PM, Thomas A, Huston-Presley L, Amini SB. Increased fetal adiposity: a very sensitive marker of abnormal in utero development. Am J Obstet Gynecol. 2003;189: 1698–1704. doi: 10.1016/s0002-9378(03)00828-7 14710101

23. Enzi G, Inelmen EM, Caretta F, Villani F, Zanardo V, DeBiasi F. Development of adipose tissue in newborns of gestational-diabetic and insulin-dependent diabetic mothers. Diabetes. 1980;29: 100–104. doi: 10.2337/diab.29.2.100 6986294

24. Nasrat H, Abalkhail B, Fageeh W, Shabat A, el Zahrany F. Anthropometric measurement of newborns of gestational diabetic mothers: does it indicate disproportionate fetal growth? J Matern Fetal Med. 1997;6: 291–295. doi: 10.1002/(SICI)1520-6661(199709/10)6:5<291::AID-MFM10>3.0.CO;2-O 9360189

25. Venkataraman H, Ram U, Craik S, Arungunasekaran A, Seshadri S, Saravanan P. Increased fetal adiposity prior to diagnosis of gestational diabetes in South Asians: more evidence for the 'thin-fat' baby. Diabetologia. 2017;60: 399–405. doi: 10.1007/s00125-016-4166-2 27913848

26. Sovio U, Murphy HR, Smith GC. Accelerated Fetal Growth Prior to Diagnosis of Gestational Diabetes Mellitus: A Prospective Cohort Study of Nulliparous Women. Diabetes Care. 2016;39: 982–987. doi: 10.2337/dc16-0160 27208333

27. Shinozuka N MH, Kagawa H, Taketani Y. Standard values of ultrasonographic fetal biometry. Jpn J Med Ultrasonics. 1996;23: 877–888

28. Shinozuka N AN, Sato S, Kanzaki T, Takeuch H, Natori M, Chiba Y, Okai T. Ellipse Tracing Fetal Growth Assessment Using Abdominal Circumference. J Med Ultrasound. 2000;8: 87–94

29. Shinozuka N, Okai T, Kohzuma S, Mukubo M, Shih CT, Maeda T, et al. Formulas for fetal weight estimation by ultrasound measurements based on neonatal specific gravities and volumes. Am J Obstet Gynecol. 1987;157: 1140–1145. doi: 10.1016/s0002-9378(87)80278-8 3318464

30. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28: 412–419. doi: 10.1007/bf00280883 3899825

31. O'Sullivan JB, Mahan CM. Criteria for the Oral Glucose Tolerance Test in Pregnancy. Diabetes. 1964;13: 278–285 14166677

32. Avalos GE, Owens LA, Dunne F, Collaborators AD. Applying current screening tools for gestational diabetes mellitus to a European population: is it time for change? Diabetes Care. 2013;36: 3040–3044. doi: 10.2337/dc12-2669 23757431

33. Duran A, Saenz S, Torrejon MJ, Bordiu E, Del Valle L, Galindo M, et al. Introduction of IADPSG criteria for the screening and diagnosis of gestational diabetes mellitus results in improved pregnancy outcomes at a lower cost in a large cohort of pregnant women: the St. Carlos Gestational Diabetes Study. Diabetes Care. 2014;37: 2442–2450. doi: 10.2337/dc14-0179 24947793

34. Miailhe G, Kayem G, Girard G, Legardeur H, Mandelbrot L. Selective rather than universal screening for gestational diabetes mellitus? Eur J Obstet Gynecol Reprod Biol. 2015;191: 95–100. doi: 10.1016/j.ejogrb.2015.05.003 26112365

35. Benhalima K, Van Crombrugge P, Moyson C, Verhaeghe J, Vandeginste S, Verlaenen H, et al. Risk factor screening for gestational diabetes mellitus based on the 2013 WHO criteria. Eur J Endocrinol. 2019;180: 353–363. doi: 10.1530/EJE-19-0117 31120231

36. Shah BR, Sharifi F. Perinatal outcomes for untreated women with gestational diabetes by IADPSG criteria: a population-based study. BJOG. 2019. doi: 10.1111/1471-0528.15964 31553136

37. Shindo R, Aoki S, Kasai J, Saigusa Y, Nakanishi S, Miyagi E. Impact of introducing the International Association of Diabetes and Pregnancy Study Groups (IADPSG) criteria on pregnancy outcomes in Japan. Endocr J. 2019. doi: 10.1507/endocrj.EJ19-0279 31511438

38. Costa E, Kirckpartick C, Gerday C, De Kempeneer A, Derisbourg S, Vercoutere A, et al. Change in prevalence of gestational diabetes and obstetric complications when applying IADPSG screening criteria in a Belgian French speaking University Hospital. A retrospective cohort study. BMC Pregnancy Childbirth. 2019;19: 249. doi: 10.1186/s12884-019-2406-4 31311547

39. Feldman RK, Tieu RS, Yasumura L. Gestational Diabetes Screening: The International Association of the Diabetes and Pregnancy Study Groups Compared With Carpenter-Coustan Screening. Obstet Gynecol. 2016;127: 10–17. doi: 10.1097/AOG.0000000000001132 26646142

40. Jacklin PB, Maresh MJ, Patterson CC, Stanley KP, Dornhorst A, Burman-Roy S, et al. A cost-effectiveness comparison of the NICE 2015 and WHO 2013 diagnostic criteria for women with gestational diabetes with and without risk factors. BMJ Open. 2017;7: e016621. doi: 10.1136/bmjopen-2017-016621 28801424

41. Bianchi C, de Gennaro G, Romano M, Battini L, Aragona M, Corfini M, et al. Italian national guidelines for the screening of gestational diabetes: Time for a critical appraisal? Nutr Metab Cardiovasc Dis. 2017;27: 717–722. doi: 10.1016/j.numecd.2017.06.010 28755805

42. Nankervis A, McIntyre HD, Moses RG, Ross GP, Callaway LK. Testing for gestational diabetes mellitus in Australia. Diabetes Care. 2013;36: e64. doi: 10.2337/dc12-2345 23613605

43. Diabetes in Pregnancy: Management of Diabetes and Its Complications from Pre-Conception to the Postnatal Period. Available: Accessed 16 July 2016.

44. American Diabetes A. 2. Classification and Diagnosis of Diabetes. Diabetes Care. 2016;39 Suppl 1: S13–22. doi: 10.2337/dc16-S005 26696675

45. Handelsman Y, Mechanick JI, Blonde L, Grunberger G, Bloomgarden ZT, Bray GA, et al. American Association of Clinical Endocrinologists Medical Guidelines for Clinical Practice for developing a diabetes mellitus comprehensive care plan. Endocr Pract. 2011;17 Suppl 2: 1–53 doi: 10.4158/ep.17.s2.1 21474420

46. Hod M, Kapur A, Sacks DA, Hadar E, Agarwal M, Di Renzo GC, et al. The International Federation of Gynecology and Obstetrics (FIGO) Initiative on gestational diabetes mellitus: A pragmatic guide for diagnosis, management, and care(). Int J Gynaecol Obstet. 2015;131 Suppl 3: S173–S211. doi: 10.1016/S0020-7292(15)30033-3 29644654

47. Hod M, Pretty M, Mahmood T, Figo E, Ebcog. Joint position statement on universal screening for GDM in Europe by FIGO, EBCOG and EAPM. Eur J Obstet Gynecol Reprod Biol. 2018;228: 329–330. doi: 10.1016/j.ejogrb.2018.05.037 29895471

48. Metzger BE. Summary and recommendations of the Third International Workshop-Conference on Gestational Diabetes Mellitus. Diabetes. 1991;40 Suppl 2: 197–201. doi: 10.2337/diab.40.2.s197 1748259

49. Jang HC, Cho NH, Jung KB, Oh KS, Dooley SL, Metzger BE. Screening for gestational diabetes mellitus in Korea. Int J Gynaecol Obstet. 1995;51: 115–122. doi: 10.1016/0020-7292(95)02524-g 8635631

50. Kim MH, Kwak SH, Kim SH, Hong JS, Chung HR, Choi SH, et al. Pregnancy Outcomes of Women Additionally Diagnosed as Gestational Diabetes by the International Association of the Diabetes and Pregnancy Study Groups Criteria. Diabetes Metab J. 2019. doi: 10.4093/dmj.2018.0192 30877713

51. Ehrlich S, Lambers D, Baccarelli A, Khoury J, Macaluso M, Ho SM. Endocrine Disruptors: A Potential Risk Factor for Gestational Diabetes Mellitus. Am J Perinatol. 2016;33: 1313–1318. doi: 10.1055/s-0036-1586500 27490770

52. Lean SC, Derricott H, Jones RL, Heazell AEP. Advanced maternal age and adverse pregnancy outcomes: A systematic review and meta-analysis. PLoS One. 2017;12: e0186287. doi: 10.1371/journal.pone.0186287 29040334

53. Melchior H, Kurch-Bek D, Mund M. The Prevalence of Gestational Diabetes. Dtsch Arztebl Int. 2017;114: 412–418. doi: 10.3238/arztebl.2017.0412 28669379

54. Egan AM, Vellinga A, Harreiter J, Simmons D, Desoye G, Corcoy R, et al. Epidemiology of gestational diabetes mellitus according to IADPSG/WHO 2013 criteria among obese pregnant women in Europe. Diabetologia. 2017;60: 1913–1921. doi: 10.1007/s00125-017-4353-9 28702810

55. Laine MK, Kautiainen H, Gissler M, Raina M, Aahos I, Jarvinen K, et al. Gestational diabetes in primiparous women-impact of age and adiposity: a register-based cohort study. Acta Obstet Gynecol Scand. 2018;97: 187–194. doi: 10.1111/aogs.13271 29194561

56. Group HSCR. Hyperglycemia and Adverse Pregnancy Outcome (HAPO) Study: associations with neonatal anthropometrics. Diabetes. 2009;58: 453–459. doi: 10.2337/db08-1112 19011170

57. Lowe LP, Metzger BE, Dyer AR, Lowe J, McCance DR, Lappin TR, et al. Hyperglycemia and Adverse Pregnancy Outcome (HAPO) Study: associations of maternal A1C and glucose with pregnancy outcomes. Diabetes Care. 2012;35: 574–580. doi: 10.2337/dc11-1687 22301123

58. Khalafallah A, Phuah E, Al-Barazan AM, Nikakis I, Radford A, Clarkson W, et al. Glycosylated haemoglobin for screening and diagnosis of gestational diabetes mellitus. BMJ Open. 2016;6: e011059. doi: 10.1136/bmjopen-2016-011059 27044587

59. Rey E, Attie C, Bonin A. The effects of first-trimester diabetes control on the incidence of macrosomia. Am J Obstet Gynecol. 1999;181: 202–206. doi: 10.1016/s0002-9378(99)70460-6 10411820

60. Sweeting AN, Ross GP, Hyett J, Molyneaux L, Tan K, Constantino M, et al. Baseline HbA1c to Identify High-Risk Gestational Diabetes: Utility in Early vs Standard Gestational Diabetes. J Clin Endocrinol Metab. 2017;102: 150–156. doi: 10.1210/jc.2016-2951 27797673

61. Desoye G, Nolan CJ. The fetal glucose steal: an underappreciated phenomenon in diabetic pregnancy. Diabetologia. 2016;59: 1089–1094. doi: 10.1007/s00125-016-3931-6 26995651

62. American Diabetes A. 14. Management of Diabetes in Pregnancy: Standards of Medical Care in Diabetes-2019. Diabetes Care. 2019;42: S165–S172. doi: 10.2337/dc19-S014 30559240

63. McIntyre HD, Sacks DA, Barbour LA, Feig DS, Catalano PM, Damm P, et al. Issues With the Diagnosis and Classification of Hyperglycemia in Early Pregnancy. Diabetes Care. 2016;39: 53–54. doi: 10.2337/dc15-1887 26519336

64. Zhu WW, Yang HX, Wei YM, Yan J, Wang ZL, Li XL, et al. Evaluation of the value of fasting plasma glucose in the first prenatal visit to diagnose gestational diabetes mellitus in china. Diabetes Care. 2013;36: 586–590. doi: 10.2337/dc12-1157 23193214

65. Simmons D, Devers MC, Wolmarans L, Johnson E. Difficulties in the use of risk factors to screen for gestational diabetes mellitus. Diabetes Care. 2009;32: e8. doi: 10.2337/dc08-1313 19114625

66. Poissonnet CM, Burdi AR, Bookstein FL. Growth and development of human adipose tissue during early gestation. Early Hum Dev. 1983;8: 1–11. doi: 10.1016/0378-3782(83)90028-2 6851910

67. Riskin-Mashiah S, Younes G, Damti A, Auslender R. First-trimester fasting hyperglycemia and adverse pregnancy outcomes. Diabetes Care. 2009;32: 1639–1643. doi: 10.2337/dc09-0688 19549728

68. Colstrup M, Mathiesen ER, Damm P, Jensen DM, Ringholm L. Pregnancy in women with type 1 diabetes: have the goals of St. Vincent declaration been met concerning foetal and neonatal complications? J Matern Fetal Neonatal Med. 2013;26: 1682–1686. doi: 10.3109/14767058.2013.794214 23570252

69. Ryan DK, Haddow L, Ramaesh A, Kelly R, Johns EC, Denison FC, et al. Early screening and treatment of gestational diabetes in high-risk women improves maternal and neonatal outcomes: A retrospective clinical audit. Diabetes Res Clin Pract. 2018;144: 294–301. doi: 10.1016/j.diabres.2018.09.013 30244050

70. Feghali MN, Abebe KZ, Comer DM, Caritis S, Catov JM, Scifres CM. Pregnancy outcomes in women with an early diagnosis of gestational diabetes mellitus. Diabetes Res Clin Pract. 2018;138: 177–186. doi: 10.1016/j.diabres.2018.02.004 29427694

Článek vyšel v časopise


2019 Číslo 12