Journal of Obstetrics and Gynaecology, November 2014; 34: 666–668 © 2014 Informa UK, Ltd. ISSN 0144-3615 print/ISSN 1364-6893 online DOI: 10.3109/01443615.2014.920788

OBSTETRICS

Perinatal outcomes of borderline diabetic pregnant women E. Yesildager1, G. Koken1, A. N. C. Gungor2, R. Demirel3, D. Arioz1, F. Celik1 & M. Yilmazer1

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Departments of 1Obstetrics and Gynecology, 3Public Health, Medicine Faculty, Afyon Kocatepe University, Afyonkarahisar and 2Obstetrics and Gynecology, Medicine Faculty, Canakkale Onsekiz Mart University, Canakkale, Turkey

We examined the perinatal outcomes of borderline diabetic pregnant women who had impaired 50 g oral glucose challenge test (OGCT) results, but normal 100 g oral glucose tolerance test (OGTT) results. Our study group included 70 pregnant women who had increased 50 g OGCT results, but normal 100 g OGTT results, and a control group of 122 pregnant women with normal 50 g OGCT results. Polyhydramnios, macrosomia and neonatal birth weight were significantly higher in the study group. After adjusting the results for possibly affecting variables, the risk of polyhydramnios remained significant, while the risk of macrosomia and neonatal birth weight was not significant between the groups. The results from the study group were similar to the control group, when adjusted for other risk factors. Increased 50 g OGCT results in pregnant women can be accepted as a benign state if the 100 g OGTT results are normal. Keywords: Borderline diabetic, oral glucose tolerance test, perinatal outcome, pregnancy

Introduction Gestational diabetes mellitus (GDM) is defined as the presence of different degrees of carbohydrate intolerance that begins or is first diagnosed during pregnancy. This definition does not consider insulin use, diet regulation or the continuation of the intolerance after pregnancy. Nearly 7% of all pregnancies are complicated by gestatational diabetes, and, in regard to the test and the population characteristics, its frequency varies between 1% and 14% (Coustan 2000; American Diabetes Association 2005; Wolf et al. 2004). The clinical importance of GDM is based on its strong relationship to maternal and fetal morbidity involving issues such as pre-eclampsia, polyhydramnios, macrosomia, delivery trauma, operative delivery, neonatal metabolic complications and perinatal mortality (Soheilykhah et al. 2010). A widely used method for diagnosing GDM is a two-step process, consisting of a 50 g oral glucose challenge test (OGCT) screening between the 24th and 28th weeks of gestation and a 100 g oral glucose tolerance test (OGTT) for selected patients, according to the results of the initial screening test (American Diabetes Association 2004). Impaired 50 g OGCT results but normal 100 g OGTT results are defined as ‘glucose intolerance’ or ‘borderline diabetes’ by some authors (Stamilio et al. 2004). Although the risks of GDM

are known, maternal and fetal complications among borderline patients have not yet been clarified (Ju et al. 2008). We examine the perinatal outcomes of these patients in the current study.

Materials and methods This prospective controlled study was conducted between 11 January 2010 and 11 January 2011, at the Afyon Kocatepe University Obstetrics and Gynaecology Department. Ethical committee approval and written consent of the participating patients were obtained. Patients who met the inclusion criteria and were called for a 50 g OGCT between the 24th and 28th weeks of gestation during the first 8 months of the study, and who gave consent to take part in the study, were included. Overall, 192 pregnant women were included. They were regularly monitored until the end of their pregnancies. All delivered in our clinic. Because there were no changes in the follow-up protocol and no known increased risks for patients, clinicians were not advised of the patients’ OGTT status. Group 1, the study group, included 70 patients who had high levels in the 50 g OGCT, but normal levels in the 100 g OGTT. Group 2, the control group, included 122 pregnant women who had normal levels in the 50 g OGCT. Women with multiple pregnancies, pre-gestational diabetes and pregnant women with fetal abnormalities were excluded from the study. All patients were monitored until delivery, and the groups were compared according to perinatal outcomes. We performed 50 g OGCT in patients who applied to our clinic between the 24th and 28th weeks of gestation. After 8–14 h of fasting, patients consumed a 50 g glucose solution. After an hour, a venous blood sample was taken. Plasma glucose levels were measured using a Cobas 501-C device made by Roche Diagnostics and using the hexokinase method spectrophotometrically. Patients with blood glucose levels ⬍ 140 mg/dl were defined as ‘normal’, those with ⬎ 200 mg/dl were defined as ‘GDM’ and those ⱖ 140 mg were defined as ‘impaired glucose tolerance’. The latter group subsequently had a 100 g OGTT after 8–14 h of fasting. Then, 1-h, 2-h and 3-h venous glucose levels were measured. Determined values were estimated according to Carpenter and Coustan’s criteria, and two or more elevated levels were described as ‘GDM’. One level elevation was described as ‘impaired glucose tolerance’. Patients with all normal levels were termed ‘normoglycaemic’. Patients were evaluated for: blood pressure; fasting glucose levels; family history; prior GDM history; parity; age; pregestational BMI; weight gain during the pregnancy; obstetric

Correspondence: A. N. C. Gungor, Department of Obstetrics and Gynecology, Medicine Faculty, Canakkale Onsekiz Mart University, Canakkale, Turkey. E-mail: [email protected]

Perinatal outcomes of borderline diabetic pregnant women 667 complications; macrosomia (birth weight above 4,000 g); polyhydramnios (deepest pool of amniotic fluid ⱖ 8 cm for at least one visit); pre-eclampsia; intrauterine growth retardation (IUGR); preterm rupture of membranes (PROM); gestational week of delivery; delivery type; delivery complications; caesarean indications; postpartum complications and hospitalisation duration. The newborns were evaluated in terms of APGAR scores, birth weight, gender, need for neonatal intensive care unit (NICU) services and antenatal and neonatal mortality. Data estimation was done using the SPSS (Statistical Package for Social Sciences) for Windows 11.5. All results were indicated as mean (⫾ SD). Measurable variables were compared with independent t-tests, and qualitative variables were compared with a χ2-test. Regression analyses were conducted to adjust the results. A value of p ⬍ 0.05 was accepted for statistical significance.

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Results The demographic characteristics of the groups are described in Table I. Polyhydramnios and macrosomia were significantly more prevalent in Group 1 (p ⬍ 0.05) (Table II). After adjusting the results for possibly affecting variables, the risk of polyhydramnios remained significant, while the risk of macrosomia and neonatal birth weight lost its significance between groups. The following were not significantly different between groups (p ⬎ 0.05) (Table II): PROM; preterm labour (PL); pregnancyinduced hypertension (PIH); pre-eclampsia; IUGR; oligohydramnios; antenatal hospitalisation duration; delivery before the 37th week of gestation; delivery type; fetal distress-indicated caesarean section (CS); gestational week at delivery; labour duration; shoulder dystocia; vaginal lacerations; extension of episiotomy; uterine atonia; blood transfusion; postpartum fever; endometritis and hospitalisation duration for delivery. Neonatal birth weights were significantly higher in Group 1. APGAR scores, the need for the NICU, antenatal and neonatal mortality did not differ significantly between the groups (p ⬎ 0.05) (Table III).

Discussion GDM has been extensively reported in the literature since it was first defined. Specifically, the clinical importance of the mild form of the disease is controversial. There is no consensus in the literature about screening techniques, diagnostic criteria, insulin requirement circumstances or oral antidiabetic use (Landon et al. 2007). Screening using a 50 g OGCT can be conducted between the 24th and 28th weeks of gestation, with the patient fasting or not

Table II. Maternal outcomes of the groups. Group 1 (n ⫽ 70) n Polyhydramnios EMR PL PIH Pre-eclampsia IUGR Oligohydramnios Macrosomia Antenatal hospitalisation Delivery before 37 weeks Vaginal birth CS CS caused by fetal distress Delivery (week) (mean ⫾ SD) Labour duration (h) (mean ⫾ SD) Shoulder dystocia Vaginal laceration Extended episiotomy Uterine atonia Blood transfusion Postpartum fever Endometritis Hospitalisation duration (day) (mean ⫾ SD)

Group 2 (n ⫽ 122)

(%)

n

16 22.9 3 4.3 8 11.4 1 1.4 2 2.9 4 5.7 0 0 9 12.9 14 20 3 4.3 28 40 42 60 7 16.7 38.75 ⫾ 2.04 3.54 ⫾ 3.75 2 7.1 11 39.3 7 25 2 2.9 2 2.9 4 5.7 1 1.4 1.63 ⫾ 0.65

(%)

3 2.5 1 8 8 6.6 2 1.6 2 1.6 9 7.4 2 1.6 6 4.9 14 11.5 6 4.9 62 50.8 60 49.2 7 11.7 38.69 ⫾ 1.41 4.63 ⫾ 4.28 1 1.6 17 27.4 9 14.5 2 1.6 2 1.6 7 5.7 0 0 1.60 ⫾ 0.58

p value 0.000† 0.138† 0.24† 1† 0.623† 0.772† 0.534† 0.048† 0.107† 1† 0.148† 0.148† 0.47† 0.808∗ 0.078∗ 0.227† 0.26† 0.246† 0.623† 0.623† 1† 0.365† 0.716∗

∗Independent t-test, †χ2-test.

fasting. If it is done while the patient is fasting, the test is more sensitive (Sermer et al. 1994). The American Diabetes Association (ADA) has stated that a threshold level can be accepted at 130 mg/ dl or 140 mg/dl. If the threshold level is accepted as 140 mg/dl, it will identify 80% of all cases; if the threshold level is accepted as 130 mg/dl, 90% of all cases can be detected (Kjos and Buchanan 1999). There is a large group of patients that have high levels in the 50 g OGCT, but normal levels in the 100 g OGTT. In a study conducted in Turkey, in which 807 pregnant women were screened, 59 (7.3%) of them had impaired 50 g OGCT results, but only 10 of them met the GDM criteria (Erem et al. 2003). The followup strategies and perinatal outcomes of those ‘borderline GDM’ patients are not clearly known. Stamilio et al. (2004) showed that those patients had more perinatal complications, so they must be followed cautiously and might benefit from a diabetic diet. Unlike previous reports (Stamilio et al. 2004; Gumus and Turhan 2008; Table III. Neonatal outcomes of the groups.

Table I. Demographic data of groups (mean ⫾ SD).

Age (years) Gravida Parity Pre-gestational BMI Postpartum BMI Gestational weight gain (kg) Family history of DM (n, %) GDM history (n, %) SBP (mmHg) DBP (mmHg) Fasting blood glucose (mg/dl) ∗Independent t-test, †χ2-test.

Group 1 (n ⫽ 70)

Group 1 (n ⫽ 70)

Group 2 (n ⫽ 122)

p value

29.41 ⫾ 5.24 2.7 ⫾ 1.5 2.3 ⫾ 0.119 24.86 ⫾ 4.74 30.57 ⫾ 4.94 14.5 ⫾ 3.16 22 (31.4%) 8 (11.4%) 107.71 ⫾ 15.52 64.1 ⫾ 10.96 85.94 ⫾ 14.55

25.77 ⫾ 5.20 2.1 ⫾ 1.06 1.8 ⫾ 0.81 23.17 ⫾ 3.29 27.32 ⫾ 3.29 10.8 ⫾ 3.22 7 (5.7%) 0 (0%) 107.90 ⫾ 12.67 65.98 ⫾ 10.41 83.22 ⫾ 10.01

0.000∗ 0.008∗ 0.001∗ 0.01∗ 0.000∗ 0.000∗ 0.000† 0.000† 0.190∗ 0.256∗ 0.129∗

n Gender Male Female Neonatal birth weight (kg) (mean ⫾ SD) APGAR score (mean ⫾ SD) 1 min 5 min Need to NCU Antenatal mortality Neonatal mortality ∗Independent t-test, †χ2-test.

(%)

Group 2 (n ⫽ 122) n

(%)

p value

39 55.7 31 44.3 3,338.2 ⫾ 606.8

57 46.7 65 53.3 3,169.4 ⫾ 456.8

0.23∗

8.72 ⫾ 1.22 9.52 ⫾ 1.27 4 5.7 1 1.4 1 1.4

8.72 ⫾ 0.77 9.76 ⫾ 0.76 5 4.1 0 0 1 0.8

0.995∗ 0.164∗ 0.726† 0.365† 1.000†

0.03∗

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668

E. Yesildager et al.

Gezer et al. 2002; Dudhbhai et al. 2006), we found similar obstetric outcomes for those borderline GDM patients, as compared with the normal control group. Advanced age, increased BMI, parity, family history and fetal macrosomia are more prevalent in GDM patients (Berkus and Langer 1993; Owen et al. 1995). Similarly, we found that the age, gravidity, pre-gestational BMI, gestational weight gain, family history of DM, prior GDM history and fetal macrosomia were higher in the study group. The neonatal birth weights were significantly higher in the study group. This can be explained either because of maternal obesity and gestational weight gain in the study group or because of impaired glucose intolerance. After adjusting the results for the parameters that were significantly different between groups, the relationship between macrosomia and borderline diabetes was not significant. Fetal macrosomia is a risk factor for shoulder dystocia. While Dudhbhai et al. (2006) and Pugh et al. (2010) found similar rates for shoulder dystocia in borderline patients and the control group, Stamilio et al.’s (2004) study results showed an increased risk for shoulder dystocia in borderline GDM patients. We, too, failed to find an increased risk for shoulder dystocia. Polyhydramnios and increased amniotic fluid indexes over the 95th or 97.5th percentiles have been shown to be more prevalent in borderline GDM patients (Golan et al. 1994; Gumus and Turhan 2008). The current study also demonstrated a significant increase in the study group for other factors of concern. Insulin resistance is known to be related to pre-eclampsia formation (Wolf et al. 2002; HAPO Study Cooperative Research Group 2008). In our study, although not at a significant threshold, increased risk for PIH and pre-eclampsia was demonstrated in the study group. This might be because of the small sample size. While Stamilio et al.’s (2004) results showed increased CS delivery rates in borderline patients, Dudhbhai et al. (2006) found similar CS rates for those patients in comparison with the control group. We found increased but non-significant rates of CS for borderline GDM patients, which also might be because of the sample size or the high caesarean rates in the study population. Ju et al. (2008) argue that there is an increased risk for fetal distress, indicated by CS delivery, in borderline GDM patients. We found similar CS rates for fetal distress indication in both the study and the control groups. Macrosomia might cause an extended episiotomy, vaginal lacerations and uterine atonia. We did not find an increased risk for those complications in the study group, probably because of the CS delivery of macrosomic fetuses. Unlike the outcomes in the newborns of diabetic mothers, we found no increased risk for low APGAR scores and NICU admission in the study group. One of the most frightening complications of diabetic pregnancies is unexplained fetal demise. Beyond the 36th week of gestation, this complication is seen more often in pregnant women with poor glycaemic control, vascular disease, fetal macrosomia or pre-eclampsia (Landon et al. 2007). Stamilio et al.’s (2004) results showed an increased risk for antenatal fetal death in borderline GDM patients. However, we did not find an increased risk for this complication in the study group. While Stamilio et al.’s (2004) and Gumus and Turhan’s (2008) results showed increased adverse perinatal outcomes for borderline GDM patients, Dudhbhai et al. (2006) stated that this group of patients can be followed-up as low-risk patients. The current study also demonstrates similar perinatal outcomes for those borderline GDM patients with normal controls. One limitation of our study is using 50 g OGCT for screening GDM. By screening glucose tolerance with 50 g OGCT, there is a high risk of false negativity.

In conclusion, some characteristics of borderline GDM patients are similar to normal control patients. There is a need for new, well-designed prospective studies, with large sample sizes for borderline GDM patients to clarify the effects of the problem on perinatal outcomes. Declaration of interest: The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.

References American Diabetes Association. 2004. Diagnosis and classification of diabetes mellitus. Diabetes Care 27(Suppl 1):S5–S10. American Diabetes Association. 2005. Diagnosis and classification of diabetes mellitus. Diabetes Care 28(Suppl 1):S37–S42. Berkus MD, Langer O. 1993. Glucose tolerance test: Degree of glucose abnormality correlates with neonatal outcome. Obstetrics and Gynecology 81:344–348. Coustan DR. 2000. Making the diagnosis of gestational diabetes mellitus. Clinical Obstetrics and Gynecology 43:99–105. Dudhbhai M, Limb L, Bombard A, Juliard K, Meenakshi B, Trachlenberg Y et al. 2006. Characteristics of patients with abnormal glucose challenge test and normal oral glucose tolerance test results: Comparison with normal and gestational diabetic patients. American Journal of Obstetrics and Gynecology 194:e42–e45. Erem C, Cihanyurdu N, Deger O, Karahan C, Can G, Telatar M. 2003. Screening for gestational diabetes mellitus in northeastern Turkey (Trabzon City). European Journal of Epidemiology 18:39–43. Gezer A, Esen F, Mutlu H , Öztürk E, Ocak V. 2002. Prognosis of patients with positive screening but negative diagnostic test for gestational diabetes. Archives of Gynecology and Obstetrics 266:201–204. Golan A, Wolman I, Sagi J, Yovel I, David MP. 1994. Persistence of polyhydramnios during pregnancy-its significance and correlation with maternal and fetal complications. Gynecologic and Obstetric Investigations 37:18–20. Gumus II, Turhan NO. 2008. Are patients with positive screening but negative diagnostic test for gestational diabetes under risk for adverse pregnancy outcome? Journal of Obstetrics and Gynaecology Research 34:359–363. HAPO Study Cooperative Research Group. 2008. Hyperglycemia and adverse pregnancy outcomes. New England Journal of Medicine 358:1991–2002. Ju H, Rumbold RA, Wilson JK, Crowther CA. 2008. Borderline gestational diabetes mellitus and pregnancy outcomes. British Medical Council. Pregnancy and Childbirth 8:31. Kjos SL, Buchanan TA. 1999. Gestational diabetes mellitus. New England Journal of Medicine 341:1749–1756. Landon MB, Catalano PM, Gabbe SG. 2007. Diabetes mellitus complicating pregnancy. In: Gabbe SG, Niebyl JR, Simpson JL et al. editors. Obstetrics: Normal and problem pregnancies. New York: Churchill Livingstone Elsevier Press. p 976–1010. Owen J, Phelan ST, Landon MB, Gabbe SG. 1995. Gestational diabetes survey. American Journal of Obstetrics and Gynecology 172:615–620. Pugh SK, Poole AT, Hill JB, Magann HF, Chauhan SF, Morrison JC. 2010. Abnormal 1 h glucose challenge test followed by a normal 3 h glucose challenge test: Does it identify adverse pregnancy outcome? Journal of Mississippi State Medical Association 51:3–6. Sermer M, Naylor CD, Gare DJ, Kenshole AB, Ritchie JW, Farine D et al. 1994. Impact of time since last meal on the gestational glucose challenge test. American Journal of Obstetrics and Gynecology 171: 607–616. Soheilykhah S, Mogibian M, Rahimi-Saghand S, Rashidi M, Soheilykhah S, Piroz M et al. 2010. Incidence of gestational diabetes mellitus in pregnant women. Iranian Journal of Reproductive Medicine 8:24–28. Stamilio DM, Olsen T, Ratcliffe S, Sehdev HM, Macones GA. 2004. False-positive 1-hour glucose challenge test and adverse perinatal outcomes. Obstetrics and Gynecology 103:148–156. Wolf M, Sandler L, Munoz K, Hsu K, Ecker JL, Thadhani R. 2002. First trimester insulin resistance and subsequent preeclampsia: a prospective study. Journal of Clinical Endocrinology and Metabolism 87:1563–1568. Wolf M, Sauk J, Shah A, Smirnakis KV, Kimble RJ, Ecker JL et al. 2004. Inflammation and glucose intolerance: a prospective study of gestational diabetes mellitus. Diabetes Care 27:21–27.

Perinatal outcomes of borderline diabetic pregnant women.

We examined the perinatal outcomes of borderline diabetic pregnant women who had impaired 50 g oral glucose challenge test (OGCT) results, but normal ...
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