Original Article
Effect of Treatment of Gestational Diabetes Mellitus on Pregnancy Outcomes
N Engl J Med 2005; 352:2477-2486June 16, 2005DOI: 10.1056/NEJMoa042973
- Abstract
Background
We conducted a randomized clinical trial to determine whether treatment of women with gestational diabetes mellitus reduced the risk of perinatal complications.
Methods
We randomly assigned women between 24 and 34 weeks' gestation who had gestational diabetes to receive dietary advice, blood glucose monitoring, and insulin therapy as needed (the intervention group) or routine care. Primary outcomes included serious perinatal complications (defined as death, shoulder dystocia, bone fracture, and nerve palsy), admission to the neonatal nursery, jaundice requiring phototherapy, induction of labor, cesarean birth, and maternal anxiety, depression, and health status.
Results
The rate of serious perinatal complications was significantly lower among the infants of the 490 women in the intervention group than among the infants of the 510 women in the routine-care group (1 percent vs. 4 percent; relative risk adjusted for maternal age, race or ethnic group, and parity, 0.33; 95 percent confidence interval, 0.14 to 0.75; P=0.01). However, more infants of women in the intervention group were admitted to the neonatal nursery (71 percent vs. 61 percent; adjusted relative risk, 1.13; 95 percent confidence interval, 1.03 to 1.23; P=0.01). Women in the intervention group had a higher rate of induction of labor than the women in the routine-care group (39 percent vs. 29 percent; adjusted relative risk, 1.36; 95 percent confidence interval, 1.15 to 1.62; P<0.001), although the rates of cesarean delivery were similar (31 percent and 32 percent, respectively; adjusted relative risk, 0.97; 95 percent confidence interval, 0.81 to 1.16; P=0.73). At three months post partum, data on the women's mood and quality of life, available for 573 women, revealed lower rates of depression and higher scores, consistent with improved health status, in the intervention group.
Conclusions
Treatment of gestational diabetes reduces serious perinatal morbidity and may also improve the woman's health-related quality of life.
Media in This Article
Figure 1
Enrollment and Outcomes.Table 1
Baseline Characteristics of the Women.Article Activity
- Article
Gestational diabetes mellitus occurs in 2 to 9 percent of all pregnancies1,2 and is associated with substantial rates of maternal and perinatal complications. The risk of perinatal mortality is not increased,3 but the risk of macrosomia is. Other perinatal risks include shoulder dystocia, birth injuries such as bone fractures and nerve palsies, and hypoglycemia. Long-term adverse health outcomes reported among infants born to mothers with gestational diabetes include sustained impairment of glucose tolerance,4 subsequent obesity5 (although not when adjusted for size6), and impaired intellectual achievement.7 For women, gestational diabetes is a strong risk factor for diabetes.8
Although the risks associated with gestational diabetes are well recognized, it remains uncertain whether screening and treatment to reduce maternal glucose levels reduce these risks. Given this uncertainty, professional groups disagree on whether to recommend routine screening, selective screening based on risk factors for gestational diabetes, or no screening; some recommend screening,1,2,9,10 whereas others do not.11-14 There have been repeated calls for well-designed, randomized trials to determine the efficacy of screening, diagnosis, and management of gestational diabetes.1,3,15-18 We designed the Australian Carbohydrate Intolerance Study in Pregnant Women (ACHOIS) trial to assess whether the treatment of gestational diabetes would reduce perinatal complications and to assess the effects of treatment on maternal outcome, mood, and quality of life.
Methods
Design and Study Population
Eligible women had a singleton or twin pregnancy between 16 and 30 weeks' gestation, attended antenatal clinics at the collaborating hospitals, had one or more risk factors for gestational diabetes on selective screening or a positive 50-g oral glucose-challenge test (glucose level one hour after glucose challenge at least 7.8 mmol per liter [140 mg per deciliter]), and had a 75-g oral glucose-tolerance test at 24 to 34 weeks' gestation in which the venous plasma glucose level was less than 7.8 mmol per liter after an overnight fast and was 7.8 to 11.0 mmol per liter (198 mg per deciliter) at two hours.19 When the study was initiated, women meeting these criteria were classified as having glucose intolerance of pregnancy, on the basis of the World Health Organization (WHO) definition: a glycemic response to a standard oral glucose-tolerance test that was intermediate between the normal and diabetic response, with an onset or recognition of the condition during the present pregnancy.19 From 1998 onward, the WHO classified any glucose levels above normal as indicative of gestational diabetes.20 Women with more severe glucose impairment were not eligible for this trial.
Women were advised to follow a normal diet 48 hours before the oral glucose-tolerance test and to fast for 8 hours the night before the test. Blood samples were obtained after the overnight fast and one and two hours after the receipt of the 75-g oral glucose load. Women with previously treated gestational diabetes or active chronic systemic disease (except essential hypertension) were excluded.
The protocol was approved by the ethics committee at each of the 18 collaborating centers (14 in Australia and 4 in the United Kingdom). All women provided written informed consent. None of the funding bodies were involved in the trial design or conduct; collection, analysis, or interpretation of the data; or preparation, review, or approval of the manuscript.
Women were provided with written information about the study, and this information was reviewed with them orally before their oral glucose-tolerance test. They were informed that they would be eligible for randomization only if their results were in the range specified above. If they were assigned to the intervention group, they received a slip indicating a diagnosis of glucose intolerance of pregnancy and the plan for intervention, whereas if they were assigned to routine care, they received a slip indicating that they did not have gestational diabetes. This approach was continued throughout the trial, because there remained uncertainty as to the level of glucose impairment associated with adverse perinatal outcomes21; there was wide variation in the glucose levels used to define the need for treatment22; some committees,1,20 but not others,9 made changes in the nomenclature; and there was still no clear evidence of the benefits and harms of treatment.17,18 After consent had been obtained, a proportion of the women (not fewer than one in five) who had normal oral glucose-tolerance test results were assigned to the routine-care group to help maintain blinding. Women whose glucose levels exceeded cutoff values for eligibility were informed that they had gestational diabetes.
Interventions
Stratification was according to center and singleton or twin gestation. Randomization was performed centrally with the use of numbers generated by computer with variable block sizes of 6, 8, and 10. The full numerical results of the oral glucose-tolerance test were not released to the women or their providers until after birth, before discharge from the hospital.
Women who were randomly assigned to the intervention group received ongoing care by the attending obstetrical team with a physician's support. Interventions included individualized dietary advice from a qualified dietitian, which took into consideration a woman's prepregnancy weight, activity level, dietary intake, and weight gain; instructions on how to self-monitor glucose levels, which the woman was then asked to do four times daily until the levels had been in the recommended range for 2 weeks (fasting glucose levels of at least 3.5 mmol per liter [63 mg per deciliter] and no more than 5.5 mmol per liter [99 mg per deciliter], preprandial levels of no more than 5.5 mmol per liter, and levels two hours postprandially that were no more than 7.0 mmol per liter [126 mg per deciliter]), followed by daily monitoring at rotating times during the day; and insulin therapy, with the dose adjusted on the basis of glucose levels, if there were two capillary-blood glucose results during the 2-week period in which the fasting level was at least 5.5 mmol per liter or the postprandial level was at least 7.0 mmol per liter at 35 weeks' gestation or less, if the postprandial level was at least 8.0 mmol per liter (144 mg per deciliter) at more than 35 weeks' gestation, or if one capillary-blood glucose result during the 2-week period was at least 9.0 mmol per liter (162 mg per deciliter).
The care of the women in the intervention group replicated clinical care in which universal screening and treatment for gestational diabetes are available. Women in the routine-care group and their caregivers were unaware of the diagnosis of glucose intolerance of pregnancy. At the discretion of the attending clinician, if indications arose that were suggestive of diabetes, further assessment for gestational diabetes was permitted, with treatment as considered appropriate. The care of the women in the routine-care group replicated clinical care in which screening for gestational diabetes is not available. The care women and infants received was otherwise according to standard practice at each center. A research assistant extracted data on treatment from the medical records of the woman and her infant to the time of hospital discharge as well as on antenatal, birth, or postnatal complications.
Outcome Variables
Primary outcomes among the infants were a composite measure of serious perinatal complications (defined as one or more of the following: death, shoulder dystocia, bone fracture, and nerve palsy), admission to the neonatal nursery, and jaundice requiring phototherapy. The presence and severity of shoulder dystocia were assessed by means of a standardized checklist completed by the caregiver present at the birth.
Primary clinical outcomes among the women were the need for induction of labor and cesarean section. Maternal health status was assessed by means of the Medical Outcomes Study 36-Item Short-Form General Health Survey (SF-36), which assesses eight aspects of health status: general and mental health, physical and social functioning, physical and emotional role, pain, and vitality; scores on each scale can range from 0 (worst) to 100 (best).23 Maternal psychological outcomes included measures of anxiety, depression, and health-related quality of life. Anxiety was assessed with the use of the short form of the Spielberger State–Trait Anxiety Inventory,24 a self-rating scale consisting of 6 items (scores below 15 are considered normal). The presence of depression was reflected by a score of more than 12 on the Edinburgh Postnatal Depression Scale.25 Questionnaires were mailed six weeks after study entry and at three months post partum to 916 women (92 percent of the total) recruited to the study after funding for this assessment became available.
Secondary outcomes among the infants included components of the composite primary outcome, gestational age at birth, birth weight, and other measures of health. Secondary outcomes among the women included the number of prenatal visits to a health professional, the mode of birth, weight gain during pregnancy, the number of antenatal admissions, and the presence or absence of pregnancy-induced hypertension (defined as a blood pressure of at least 140/90 mm Hg on two occasions four or more hours apart) and other complications.
Statistical Analysis
Statistical analyses were based on the intention to treat and used SAS software, version 8.2 (SAS Institute). Analyses were adjusted for maternal age, race or ethnic group, and parity. Binary outcomes are presented as relative risks, with 95 percent confidence intervals; the number needed to treat to benefit (i.e., the number of patients who would need to be treated for a benefit in one patient) and the number needed to treat to harm (i.e., the number of patients who would need to be treated for harm to occur in one patient), with their 95 percent confidence intervals,26 are presented for primary clinical outcomes. Relative risks were calculated with the use of log binomial regression. Continuous variables were analyzed by means of analysis of variance if they were normally distributed and by means of nonparametric tests if their distribution was not normal. The health state utility was calculated from the SF-36 according to the method of Brazier et al.27 With no evidence of increased variance owing to the small number of twins in the study, no adjustment was made for clustering of babies with the same mothers. A P value of 0.05 was considered to indicate statistical significance; all P values were two-sided. A step-down Sidak adjustment was made for analyses involving multiple primary clinical end points.28
We estimated that we would need to enroll 1000 women for the study to have a statistical power of 80 percent (two-sided alpha value of 0.05) to detect a reduction in the risk of a serious perinatal outcome from 5.2 percent to 2.0 percent, using outcomes reported for all South Australian births29 and data from Women's and Children's Hospital in Adelaide. Data were reviewed once in January 1999 by our independent data-monitoring committee, whose members were unaware of the treatment assignments, after the enrollment of 460 women. The study protocol included a prespecified stopping rule for a difference in a major end point of at least 3 SD between the groups.
Results
Of the 1000 women enrolled in the study, 490 were assigned to the intervention group and 510 to the routine-care group (Figure 1Figure 1
Enrollment and Outcomes.). Recruitment started in September 1993 and stopped in June 2003, after 1000 women had been enrolled. Clinical outcomes were obtained up to the time of hospital discharge for all women and their 1030 infants.On the whole, the two groups were similar at entry. As compared with the women in the routine-care group, women in the intervention group were older and were less likely to be white or primiparous (Table 1Table 1
Baseline Characteristics of the Women.). Ninety-three percent of the women had been found to be at risk for gestational diabetes on the basis of the oral glucose-challenge test, and the remainder on the basis of risk factors.Primary Outcomes
The rate of serious perinatal outcomes among the infants (defined by one or more of the following: death, shoulder dystocia, bone fracture, and nerve palsy) was significantly lower in the intervention group than the routine-care group (1 percent vs. 4 percent; P=0.01, adjusted for maternal age, race or ethnic group, and parity (Table 2Table 2
Primary Clinical Outcomes among the Infants and Their Mothers.). Thus, the number needed to treat to prevent a serious outcome in an infant was 34 (95 percent confidence interval, 20 to 103). A higher percentage of infants born to women in the intervention group than of infants born to women in the routine-care group were admitted to the neonatal nursery (71 percent vs. 61 percent, adjusted P=0.01). The length of stay in the neonatal nursery among the infants who were admitted did not differ significantly between groups (median of 1 day for both groups; interquartile range, 1 to 2 days in the intervention group and 1 to 3 days in the routine-care group; adjusted P=0.81). There was no significant difference in the percentage of infants who had jaundice requiring phototherapy in the two groups (adjusted P=0.72) (Table 2).The induction of labor was significantly more common in the intervention group than in the routine-care group (39 percent vs. 29 percent; adjusted P<0.001) (Table 2). The rates of cesarean delivery were similar in the two groups (adjusted P=0.73) (Table 2), as were the reasons for cesarean delivery.
Step-down Sidak adjustments were made to correct for the analyses of multiple primary clinical end points (Table 2). The results remained consistent across these analyses, with the intervention group having a reduced risk of serious perinatal outcomes (corrected P=0.04) and an increased likelihood of admission to the neonatal nursery for the infant (corrected P=0.04) and use of induction of labor for the mother (corrected P=0.003).
Maternal health status was measured in 682 women (68 percent) who completed the questionnaires six weeks after enrollment and 573 women (57 percent) who completed them three months post partum. Women who completed assessments were slightly older than, but otherwise similar to, women who did not.
All measures on the SF-3623 showed trends in favor of the intervention group, although not all were significant (Table 3Table 3
Quality of Life during Pregnancy and Three Months after Giving Birth.). At three months post partum, fewer women in the intervention group than in the routine-care group had a score on the Edinburgh Postnatal Depression Scale25 suggestive of depression (23 vs. 50 [8 percent vs. 17 percent]). The level of anxiety was similar in the two groups (Table 3).Secondary Outcomes
No perinatal deaths occurred among the infants of mothers in the intervention group, but there were five perinatal deaths (three stillbirths and two neonatal deaths) among infants born to women in the routine-care group (Figure 1 and Table 2). Two stillbirths were unexplained intrauterine deaths at term of appropriately grown infants, and the other, at 35 weeks' gestation, was associated with preeclampsia and intrauterine growth restriction. One infant had a lethal congenital anomaly, and one infant died after an asphyxial condition during labor without antepartum hemorrhage.
There was no significant difference in the rates of shoulder dystocia between the intervention and routine-care groups (1 percent and 3 percent, respectively) (Table 2). No infant in the intervention group had a bone fracture or nerve palsy, whereas in the routine-care group, one infant had both a fractured humerus that was not related to a difficult birth and a radial-nerve palsy, one infant had Erb's palsy related to shoulder dystocia, and one infant had Erb's palsy alone (Table 2).
Infants born to women in the intervention group had significantly lower mean birth weights than infants born to women in the routine-care group (P<0.001) (Table 4Table 4
Secondary Outcomes among the Infants.), and they were also born at an earlier gestational age, in keeping with the higher incidence of induction of labor in their mothers (Table 5Table 5
Secondary Clinical Outcomes among the Women.). Significantly fewer infants in the intervention group were large for gestational age at birth, and significantly fewer had macrosomia (defined by a birth weight of 4 kg or greater) (Table 4). There was no significant difference between groups in the proportion of infants who were small for gestational age.Women in the intervention group had fewer antenatal clinic visits after enrollment than did women in the routine-care group, but they had more visits to the physician and were significantly more likely to see a dietitian and a diabetes educator (Table 5). One hundred women in the intervention group (20 percent) received insulin therapy, as compared with 17 in the routine-care group (3 percent). Weight gain from the booking appointment to the last antenatal visit was less in the intervention group than in the routine-care group (Table 5). The rates of antenatal hospital admissions were similar in the two groups. Fewer women in the intervention group than in the routine-care group received a diagnosis of preeclampsia during the antenatal period (Table 5).
Discussion
In this randomized clinical trial, treatment of women with gestational diabetes — including dietary advice, blood glucose monitoring, and insulin therapy — reduced the rate of serious perinatal outcomes (defined as death, shoulder dystocia, bone fracture, and nerve palsy) from 4 percent to 1 percent. These benefits were associated with an increased use of induction of labor for the mother and an increased rate of admission to the neonatal nursery for the infant, both of which may be related to the knowledge of the diagnosis by the attending physician. The earlier gestational age at birth as a consequence of the induction of labor may have contributed to the reduction in serious perinatal outcomes. Others have reported an increased rate of cesarean delivery associated with the diagnosis and treatment of gestational diabetes.12 In our study, the rate of cesarean delivery was similar in the two groups.
We chose primary clinical outcomes to assess the effects of treatment for gestational diabetes on both the mothers and the infants. Differences between groups remained significant after adjustment for known confounders (maternal age, race or ethnic group, and parity) and for analyses involving multiple primary end points.
Infants born to mothers receiving intensive therapy had lower birth weights than those born to women receiving routine care, an observation that may be explained at least in part by the earlier gestational age at birth in this group, related to the increased use of induction of labor. Infants in this group were no more likely to be small for gestational age, but they were significantly less likely to be large for gestational age and to have macrosomia. Infants who are large for gestational age are prone to impaired glucose tolerance or diabetes in later life, and girls4 have an increased risk of gestational diabetes.6 Long-term follow-up is needed to assess whether the lower birth weights among the infants in the intervention group will translate into reduced rates of these later complications.
Despite the increased rate of admission to the neonatal nursery in the intervention group, there were no significant differences between the groups of infants in secondary clinical outcomes, such as hypoglycemia requiring intravenous therapy. As compared with the women in the routine-care group, the women in the intervention group made more visits to the medical clinic and were more likely to see a dietitian and diabetes educator. However, they made fewer antenatal clinic visits, a difference that was most likely related to their increased likelihood of induction and their infants' earlier gestational age at birth. The reduction in the risk of preeclampsia in the intervention group may be related to the earlier gestational age at birth.
A potentially controversial aspect of our study design from an ethical standpoint was the fact that women were not informed of their diagnosis of “gestational diabetes” during the course of the study, after the change in the WHO criteria. However, despite changes in the nomenclature for gestational diabetes,1,19,20 there continued to be no conclusive evidence regarding the effects of treatment of gestational diabetes17,18 and there were wide variations in clinical practice during the time of this study.22 Women in the study received standard pregnancy care consistent with care in which screening for gestational diabetes is not routine.
Our trial also revealed an improved health-related quality of life among women in the intervention group, both during the antenatal period and three months after birth, together with a reduction in the incidence of depression after birth. These findings are contrary to reports suggesting a decline in women's perception of their own health after they receive a diagnosis of gestational diabetes.31,32 However, results for these outcomes should be interpreted with caution, since the analysis included only a subgroup of the women.
There has been a lack of data from large randomized clinical trials on the effects of screening and treatment of women with gestational diabetes mellitus. An observational study is currently in progress to assess associations between maternal glucose levels and perinatal outcomes,20 and an ongoing randomized trial in the United States is addressing the effect of therapy for mild gestational diabetes, as did our study.33 Our results indicate that treatment of gestational diabetes in the form of dietary advice, blood glucose monitoring, and insulin therapy as required for glycemic control reduces the rate of serious perinatal complications, without increasing the rate of cesarean delivery.
Funded by two three-year project grants from the National Health and Medical Research Council Australia, the Queen Victoria Hospital Research Foundation, Adelaide, and supported by the Department of Obstetrics and Gynaecology at the University of Adelaide, South Australia.
We are indebted to the women and their children who participated in this study.
Source Information
From the Departments of Obstetrics and Gynaecology (C.A.C., J.S.R.) and Public Health (J.E.H., J.R.M.), University of Adelaide; the Department of Perinatal Medicine, Women's and Children's Hospital (A.J.M.); and the Department of Medicine, Lyell McEwin Health Service (W.S.J.) — all in Adelaide, Australia.
Members of the ACHOIS Trial Group are listed in the Appendix.
Appendix
The following persons and institutions participated in the ACHOIS Trial Group: Coordinating Team: C. Crowther, J. Hiller, J. Moss, A. McPhee, W. Jeffries, J. Robinson, A. Thomas, S. Alton, I. Flight, J. Hayton, A. Deussen, E. Griffith, S. Russell, S. Gibbons, C. Holst, K. Robinson; Steering Group: C. Crowther, J. Hiller, J. Moss, A. McPhee, W. Jeffries, J. Robinson; Statistical Support: K. Willson; Data-Monitoring Committee: J. Lumley (chair), L. Watson; Writing Group: C. Crowther, J. Hiller, J. Moss, A. McPhee, W. Jeffries, J. Robinson; Data Support: S. Brown, K. Bruggemann, P. Moore; Hospitals (total number of women recruited at each hospital is given in parentheses): Blacktown District Hospital, New South Wales (79): D. Chipps, R. Myszka, S. Hendon, M. McLean, H. Merker, J. Bradford; Bradford Royal Infirmary Maternity Unit, United Kingdom (0): D. Tuffnell, J. West; Caboolture Hospital, Queensland (28): M. Ratnapala, R. Hinton, D. Woodford, D. Cave, C. Armstrong, A. Vacca, P. Joubert, S. Mego, V. Heazelwood; Campbelltown Hospital, Sydney, New South Wales (1): H. Grunstein, S. Fleming, B. Marney; Flinders Medical Center, Adelaide, South Australia (43): K. Harris, J. Ebert, R. Bryce, S. Judd, M. Keirse, C. Verco; General Infirmary, Leeds, United Kingdom (3): E. Ferriman, G. Mason, C. Lidelle-Johnson, J. Pearce; Hammersmith Hospital, London (2): M. de Swiet, A. McCarthy; Hervey Bay Hospital, Queensland (24): A. Lindberg, D. Ludwig, K. Wickremachandran; Lyell McEwin Hospital, Adelaide, South Australia (125): G. Dekker, P. Duggan, I. Hocking, W. Jeffries, S. Kennedy-Andrews, N. Kretschmer, H. Millar, J. Mowbray; Modbury Hospital, Adelaide, South Australia (68): C. Archer, C. Hughes, G. Matthews, M. Morton, N. Price, L. Purins, N. Tamlin, J. Sieben; Nambour General Hospital, Queensland (37): C. Cocks, M. Gregora, S. Hamwood, G. Pinn, C. Rutherford, C. Sheehan, T. Stubbs, V. Smith-Orr; Northern General Hospital, Sheffield, United Kingdom (41): S. Rutter, C. Bruce, R. Fraser; Queen Elizabeth Hospital, Adelaide, South Australia (29): B. Pridmore (deceased), W. Hague, P. Phillips, M. Sladek, S. Torr; Royal North Shore Hospital, Sydney (198): G. Burton, R. Hitchman, I. Kelso, A. McElduff, J. Morris; St. George Hospital, Sydney (1): C. Homer, G. Davis; Toowoomba Base Hospital, Queensland (11): P. Bridger, Y. Chadha, D. Gibson, M. Ratnapala; Townsville Hospital, Queensland (48): D. Watson, A. Rane, A. Robinson, J. Whitehall, S. Dunstone, R. Chadwick, A. Dederer, A. Lawrence; Women's and Children's Hospital, South Australia (261): C. Crowther, R. Burnet, A. McPhee, J. Robinson, A. Thomas, S. Alton, J. Hayton, J. Paynter, A. Deussen, J. Avery, S. Agett, D. Morris, B. Peat, C. Wilkinson, V. Coppinger, J. Dodd.
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Nilmini Wickramasinghe, Indrit Troshani, Sally Rao Hill, William Hague, Steve Goldberg. (2013) A Transaction Cost Assessment of a Pervasive Technology Solution for Gestational Diabetes. International Journal of Healthcare Information Systems and Informatics 6:4, 60-76
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Shirlee Jaffe, Georgios Doulaveris, Theofano Orfanelli, Mariana Arantes, Débora Damasceno, Iracema Calderon, Marilza V. C. Rudge, Steven S. Witkin. (2013) Induction of the 72 kDa heat shock protein by glucose ingestion in black pregnant women. Cell Stress and Chaperones 18:4, 527-530
3
Azadeh Houshmand, Dorte Møller Jensen, Elisabeth R. Mathiesen, Peter Damm. (2013) Evolution of diagnostic criteria for gestational diabetes mellitus. Acta Obstetricia et Gynecologica Scandinavica 92:7, 739-745
4
R. Helseth, E. Vanky, O. Salvesen, S. M. Carlsen. (2013) Gestational diabetes mellitus among Norwegian women with polycystic ovary syndrome: prevalence and risk factors according to the WHO and the modified IADPSG criteria. European Journal of Endocrinology 169:1, 65-72
5
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