Original Article
Correlations between Antepartum Maternal Metabolism and Intelligence of Offspring
N Engl J Med 1991; 325:911-916September 26, 1991
- Abstract
- Abstract
Background
It is not clear to what extent maternal metabolism during pregnancy affects the cognitive and behavioral function of the offspring by altering brain development in utero. To investigate this question, we correlated measures of metabolism in pregnant diabetic and nondiabetic women with the intellectual development of their offspring.
Methods
The study included 223 pregnant women and their singleton offspring: 89 women had diabetes before pregnancy (pregestational diabetes mellitus), 99 had the onset of diabetes during pregnancy (gestational diabetes mellitus), and 35 had normal carbohydrate metabolism during their pregnancy. We correlated measures of maternal glucose and lipid metabolism (fasting plasma glucose levels, hemoglobin A1c levels, episodes of hypoglycemia, episodes of acetonuria, and plasma β-hydroxybutyrate and free fatty acid levels) with two measures of intellectual development in the offspring — the mental-development index of the Bayley Scales of Infant Development, given at the age of two years, and the Stanford–Binet Intelligence Scale, given at the ages of three, four, and five years and expressed as an average of the three scores.
Results
After correction for socioeconomic status, race or ethnic origin, and patient group, the children's mental-development-index scores at the age of two years correlated inversely with the mothers' third-trimester plasma β-hydroxybutyrate levels (r = —0.21, P<0.01); the average Stanford–Binet scores correlated inversely with third-trimester plasma β-hydroxybutyrate (r = —0.20, P<0.02) and free fatty acid (r = —0.27, P<0.002) levels. No other correlations were significant. Including various perinatal events (e.g., prematurity and acidemia) in the analyses did not alter the results.
Conclusions
Maternal diabetes during pregnancy may affect behavioral and intellectual development in the offspring. The associations between gestational ketonemia in the mother and a lower IQ in the child warrant continued efforts to avoid ketoacidosis and accelerated starvation in all pregnant women. (N Engl J Med 1991; 325:911–6.)
Media in This Article
Table 1
Indexes of Metabolic Control in the Mothers Studied.*Table 2
Characteristics of the Neonates Born to Women with Pregestational Diabetes, Women with Gestational Diabetes, or Nondiabetic Women.*Article Activity
- Article
DURING pregnancy, most maternal fuels gain access to the developing conceptus in a concentration-dependent fashion.1 Circulating maternal fuels may affect the quantitative and qualitative characteristics of the nutrient mixture in which organogenesis and cellular replication, differentiation, and functional maturation occur.1 , 2 Alterations in maternal fuels may have long-range effects on the offspring by modifying terminally differentiating, poorly replicating cells during critical phases of embryonic or fetal life3 , 4; in this context maternal fuels may have actions above and beyond their simple nutrient functions. Fuel disturbances early in gestation may influence organogenesis in a classic teratogenic fashion, whereas disturbances occurring later in gestation may produce more subtle, although perhaps no less profound, teratogenesis.
This report summarizes the relations between the metabolic status of pregnant women, as reflected by the presence of hypoglycemia and measurements of urinary acetone, hemoglobin A1c, and fasting plasma glucose, β-hydroxybutyrate, and free fatty acids, during the second and third trimesters of pregnancy and the intellectual growth of their offspring in early childhood, as assessed by the mental-development index of the Bayley Scales of Infant Development5 at the age of two years and their average score on the Stanford–Binet Intelligence Scale6 at the ages of three, four, and five years.
Methods
Subjects
We studied 223 pregnant women and their singleton offspring. Eighty-nine of the women had known diabetes mellitus that predated the pregnancy (pregestational diabetes mellitus); 99 had gestational diabetes mellitus7; and 35 had normal glucose metabolism, as documented by oral glucose tolerance defined according to the criteria of O'Sullivan and Mahan.8 Women with pregestational diabetes were referred to our program for prenatal care from throughout metropolitan Chicago. The women with gestational diabetes included those referred to evaluate the need for insulin treatment, women screened for gestational diabetes relatively early in gestation because of classic risk factors, and women from the general prenatal clinics at our hospital who were screened for glucose intolerance routinely at 24 to 28 weeks of gestation.
We excluded all women who required medication on a long-term basis for the treatment of medical or psychiatric problems. Five women (four with diabetes and one with normal glucose metabolism) were excluded from the study because they repeatedly failed to complete scheduled tests, keep clinic appointments, and maintain records of home measurements of levels of urinary glucose and acetone or capillary blood glucose (as these results became available). Five women voluntarily withdrew from the study during gestation: two moved from the city, and three sought medical care elsewhere. Finally, we excluded from the analyses six pairs of twins and one child who had severe intrauterine growth retardation (birth weight, 590 g) and prematurity (gestational age at delivery, <28 weeks), among other complications. The mother of this child had one of the most poorly controlled cases of diabetes in our study population, and the child was of subnormal intelligence (mental-development index at two years of age, 50); including him in the analyses would have disproportionately influenced the results in favor of the hypothesis. All participating women gave informed written consent, and detailed demographic and socioeconomic data were collected through interviews conducted by our staff. The Wechsler Adult Intelligence Scale9 was also administered to the mothers.
Antepartum Care
Antepartum care was provided according to a detailed protocol, by a team of diabetologists, obstetricians, neonatologists, nurse educators, dietitians, and social workers. Women with diabetes were given care consistent with prevailing practice, which included multiple insulin injections each day, and the goal of obstetrical management was vaginal delivery at term. All women were seen at least biweekly before 30 weeks of gestation, and weekly thereafter. Women with insulin-dependent diabetes were hospitalized for one week immediately after enrollment to assess metabolic status and receive information about diabetes. Women who enrolled before the 24th week of pregnancy were hospitalized a second time at 28 weeks of pregnancy to regulate the disease more closely.
At each outpatient visit and twice weekly during the hospitalizations, blood samples were drawn after an overnight fast for measurements of plasma glucose,10 β-hydroxybutyrate,11 and free fatty acids.10 Glycosylated hemoglobin was measured initially as hemoglobin A1c by column chromatography with macrocolumns,12 and in the last two years of the study as total glycosylated hemoglobin by gel electrophoresis.13 Values obtained by the two methods in 35 samples were highly correlated (r = 0.88, P<0.001), and a conversion formula was derived to express all results as hemoglobin A1c so that they could be pooled for statistical analysis. The mean concentrations of hemoglobin A1c and fasting plasma glucose, β-hydroxybutyrate, and free fatty acids measured during the second and third trimesters were calculated for individual women by averaging all measurements obtained during those periods. Finally, all the women with diabetes were asked to record the results of urine tests for acetonuria (Acetest) performed four times daily as outpatients and on each voided specimen during hospitalizations. The percentage of days on which one or more urine specimens tested positive for acetone ("moderate" or "large") was calculated to provide an index of acetonuria in diabetic women who reported results for at least 14 days per trimester. Episodes of symptomatic hypoglycemia and recorded measurements of plasma glucose that were less than 2.8 mmol per liter (50 mg per deciliter) were also tabulated in the women treated with insulin. The percentage of days on which an insulin reaction occurred was calculated to provide an index of hypoglycemia in the pregnant women who had recorded such information for a minimum of 14 days per trimester.
Entry into the program was sufficiently early (see below) to allow estimates of metabolic control during the second trimester in 92 percent of the women with pregestational diabetes, 46 percent of the women with gestational diabetes, and 80 percent of the women with normal glucose metabolism.
Neonatal Care
The newborn infants were immediately transferred to radiant bed warmers, and Apgar scores were recorded at one and five minutes. Fetal blood gas tension and pH at delivery were measured in blood drawn from doubly clamped segments of umbilical cord. Plasma glucose was measured in cord blood at delivery and in blood samples obtained by heel stick at hourly intervals for the first four hours thereafter. The initial feeding was given four hours after birth unless hypoglycemia (plasma glucose, ≤1.7 mmol per liter [30 mg per deciliter]) was present. In that case, the infants were fed immediately, intravenous glucose was administered, or both. Plasma glucose, calcium, and bilirubin were measured, and vital signs were monitored. Neonatologists estimated gestational age according to the method of Dubowitz et al.14 and performed complete physical examinations as described by Lubchenco et al.15 When there were discrepancies between these calculations and the due dates estimated on the basis of maternal reports, the gestational age established by physical examination was used.
Measures of Intelligence
We evaluated the children at the age of two years with the Bayley Scales of Infant Development5 and at least once at the ages of three, four, and five years with the Stanford–Binet Intelligence Scale.6 All tests were performed without knowledge of the mother's antepartum metabolic status or the child's previous test scores.
The correlations among the Stanford–Binet scores were 0.82 between years 3 and 4, 0.65 between years 4 and 5, and 0.72 between years 3 and 5 (P<0.001 for all comparisons). We therefore calculated the average IQ score for the three years to obtain an improved estimate of the children's true intelligence and reduce the number of redundant analyses. The correlation between the average Stanford–Binet IQ score and the mental-development-index score at the age of two years was 0.72 (n = 149, P<0.001).
Socioeconomic Status
Previous studies have shown that the IQ of the mother, her level of education, the father's level of education, and family income are highly intercorrelated.16 Furthermore, each of these variables correlates, although not independently, with the IQ of the child during early childhood and later.17 In line with these well-established findings, we computed a single composite index of socioeconomic status by calculating the z score for each variable (mother's IQ, mother's level of education, father's level of education, and family income) and then taking the average of these z scores as the socioeconomic-status score. Thus, our socioeconomic-status index reflected each variable equally and was scaled such that a score of 0 represented the average home environment in our sample, a score of 1 represented a home environment that was 1 SD above the average, and so forth.
Statistical Analysis
The results were analyzed with the partial-correlation, one-way analysis of variance, and multivariate analysis of variance programs provided in the SPSS/PC+ base18 and advanced19 statistics packages for the IBM PC and with chi-square analyses and Fisher's exact test. Specific group comparisons were made by partitioning three-by-two contingency tables according to the method of Castellan20 within the chi-square analyses and with Tukey's multiple-range test within the analyses of variance and multivariate analyses of variance. Comparisons of the results of partial correlations were performed according to the procedure of McNemar.21 Results are given as means ±SD.
Results
Maternal Metabolism during Pregnancy
On average, the women with pregestational diabetes were enrolled at 11.9±7.5 weeks of gestation, the women with gestational diabetes at 24.0±9.0 weeks, and the nondiabetic women at 18.5±5.3 weeks. The maternal concentrations of hemoglobin A1c, fasting plasma glucose, β-hydroxybutyrate, and free fatty acids and the frequency of hypoglycemia and acetonuria during the second and third trimesters in each group are summarized in Table 1Table 1
Indexes of Metabolic Control in the Mothers Studied.*. The mean values for fasting plasma glucose during the second trimester and for fasting plasma glucose and hemoglobin A1c during the third trimester were significantly higher in the women with pregestational diabetes than in those with gestational diabetes (P<0.05 for all comparisons); the women with gestational diabetes in turn had significantly higher values than the nondiabetic women (P<0.05 for all comparisons). Concentrations of hemoglobin A1c during the second trimester were higher in the women with pregestational diabetes than in those with gestational diabetes (P<0.05) or the nondiabetic women (P<0.05). Hypoglycemia, measured as the percentage of days on which an insulin reaction occurred, was more common in the women with pregestational diabetes (occurring approximately once weekly on average) than in those with gestational diabetes (occurring rarely) in both trimesters (P<0.001 for both comparisons). The mean plasma β-hydroxybutyrate values in the second trimester were significantly higher in the women with pregestational diabetes than in the nondiabetic women (P<0.05). The mean frequency of acetonuria was significantly higher in the women with gestational diabetes than in those with pregestational diabetes in the second (P<0.05) and third (P<0.001) trimesters. The mean fasting plasma glucose level was significantly higher in the second trimester than in the third trimester in both groups with diabetes (P<0.001), but not in the nondiabetic women. The frequency of hypoglycemia was greater in the third than in the second trimester in both groups of diabetic women (P<0.05).Physical Findings in Newborns
Pertinent delivery and neonatal information is summarized in Table 2Table 2
Characteristics of the Neonates Born to Women with Pregestational Diabetes, Women with Gestational Diabetes, or Nondiabetic Women.*. The mean gestational age at delivery was significantly lower in the infants of mothers with diabetes than in the infants of the nondiabetic mothers (P<0.05). However, the incidence of preterm deliveries did not differ significantly among the three groups. Birth weight was significantly higher in the offspring of mothers with pregestational diabetes than in the offspring of mothers with gestational diabetes (P<0.05) or nondiabetic mothers (P<0.05). The incidence of macrosomia was significantly higher in the infants of mothers with pregestational diabetes than in the infants of mothers with gestational diabetes (P<0.01) or nondiabetic mothers (P<0.01). Intrauterine growth retardation occurred infrequently, and its incidence did not differ among the three groups. The mean plasma glucose level in cord blood did not differ significantly among the three groups, nor did the incidence of acidemia. The incidence of neonatal hypoglycemia was significantly higher in the infants of mothers with pregestational diabetes than in the infants of mothers with gestational diabetes (P<0.001). In turn the incidence was higher in the infants of mothers with gestational diabetes than in the infants of nondiabetic mothers (P<0.05). Finally, there were no significant differences among the groups in the incidence of hypocalcemia (serum calcium, ≤1.88 mmol per liter) or hyperbilirubinemia (serum bilirubin, ≥206 μmol per liter in term infants and ≥20 μmol per liter in preterm infants). More offspring of mothers with pregestational diabetes (8 percent) had five-minute Apgar scores of less than 7 than did offspring of mothers with gestational diabetes (0 percent, P<0.001) or of nondiabetic mothers (0 percent, P<0.10).Child Intelligence
Mental-development-index scores were obtained at two years of age for 186 of the 223 children (83 percent); 186 children (83 percent) were given the Stanford–Binet test at least once at the ages of three, four, and five years; and 149 children (67 percent) had both assessments. The mean values in each group, corrected for socioeconomic status and race or ethnicity, are shown in Table 3Table 3
Scores for the Mental-Development Index and Stanford–Binet Test.*.To examine the relation between the antepartum metabolism of the mother and the IQ of her child, partial correlations were performed between the indexes of maternal glucose metabolism (expressed as the fasting plasma glucose level, hemoglobin A1c level, and frequency of maternal hypoglycemia) and lipid metabolism (expressed as the plasma levels of β-hydroxybutyrate and free fatty acids, and the percentage of days on which acetonuria was present) in the second and third trimesters and the children's scores on the mental-development index at the age of two years and average score on the Stanford–Binet test at the ages of three, four, and five years after a correction was made for socioeconomic status, race or ethnic origin, and patient group. Partial-correlation analyses were done because socioeconomic and cultural factors are known to influence performance on intelligence tests,16 as well as to control for any potential influences of diabetes type that are not indexed by maternal metabolism, such as genetic factors.
No significant correlations were found between intelligence scores and the indexes of glycemic control (fasting plasma glucose, hemoglobin A1c, and hypoglycemia) during the second and third trimesters. As shown in Table 4Table 4
Partial Correlations between Indexes of the Mothers' Antepartum Lipid Metabolism and Children's Intelligence at Two and Three to Five Years.*, however, three of six correlations involving indexes of third-trimester maternal lipid metabolism were significant. The children's mental-development-index scores at two years of age correlated inversely with the mothers' third-trimester plasma β-hydroxybutyrate values (r = —0.21, P<0.01), and the average Stanford–Binet scores correlated inversely with the third-trimester values for plasma β-hydroxybutyrate (r = —0.20, P<0.02) and free fatty acids (r = —0.27, P<0.002). In addition, the correlation between the mental-development-index scores and second-trimester plasma β-hydroxybutyrate values was marginally significant (r = —0.17, n = 112, P = 0.08). In each case, with more aberrant metabolism in the mother, the child's intellectual development was poorer. No other correlations were significant (P>0.10).To evaluate the effects of various perinatal factors on the correlations of the mother's metabolism with the child's IQ, the partial-correlation analyses were repeated with the following variables included as covariates: gestational age at delivery, macrosomia, intrauterine growth retardation, cord-blood pH, neonatal hypoglycemia, hyperbilirubinemia, and five-minute Apgar score. The r values from these analyses, as well as those reported in Table 4, were converted into z scores and compared.21 In no instances were the previously reported correlations with metabolic indexes altered significantly by any of the perinatal factors we examined (P>0.3 for all comparisons).
Discussion
This study describes the relation between the mother's antepartum metabolic status and the intellectual growth of her offspring. The mental-development index and Stanford–Binet test are widely regarded as the premier instruments for assessing intellectual performance in early childhood. Such characterizations are of particular interest for correlations with antepartum metabolic events, since plasticity in the central nervous system22 and intellectual performance17 are greatly diminished by two to five years of age.
We found significant correlations between the lipid metabolism of the mother in the third trimester and the child's intelligence at two and at three to five years of age. The children's mental-development-index scores at the age of two years were negatively correlated with third-trimester maternal plasma β-hydroxybutyrate values, and the children's average Stanford–Binet scores at three to five years of age were negatively correlated with third-trimester maternal plasma β-hydroxybutyrate and free fatty acid values. In each case, poorer metabolic regulation in the mother was attended by her child's poorer performance on standard IQ tests. It should be emphasized that the correlations were established within groups of pregnant women whose metabolic status and obstetrical course ranged from nearly normal to moderately impaired. Acetonuria was infrequent, and although hypoglycemia occurred approximately once weekly in women with insulin-dependent diabetes mellitus, only seven cases required medical treatment. In our study, among pregnant women with diabetes (pregestational and gestational diabetes), the incidence of essential hypertension and preeclampsia was 6 percent and 8 percent, respectively. Moreover, the correlations were established in a fairly representative sample of healthy children. Although macrosomia and hypoglycemia were more frequent among the offspring of diabetic mothers than among the offspring of nondiabetic mothers, the two groups of infants did not differ significantly with regard to the incidence of prematurity, intrauterine growth retardation, hypocalcemia, or hyperbilirubinemia. Among the offspring of diabetic mothers, the uncorrected mean (±SD) for the average Stanford–Binet score at three to five years was 98±16, as compared with 100±16 nationally, and only six children (3.8 percent) had uncorrected Stanford–Binet scores of 69 or below (i.e., subnormal intellect), as compared with 2.6 percent nationally.6 Indeed, from this perspective our study constitutes an impressive demonstration of the health benefits afforded mother and child by vigilant antepartum and obstetrical management of maternal diabetes.
The correlations between the mother's lipid metabolism and her child's intelligence were found after any potential effects of patient group (pregestational diabetes, gestational diabetes, or normal glucose metabolism) on the child's IQ were taken into account. Thus, insofar as most of the women with pregestational diabetes had Type I diabetes, whereas women with gestational diabetes are at high risk for Type II diabetes, the correlations appeared to be determined by phenotypic factors (i.e., the degree of disturbance in the mother's metabolism during pregnancy) rather than genotypic considerations (i.e., the nature of the mother's diabetes). Finally, the correlations are independent of the effects of numerous neonatal complications, including prematurity, acidemia, and hypoglycemia. In this regard we suggest that maternal metabolic control and prematurity may have been significant confounders in earlier studies that linked adverse neurologic sequelae and developmental impairment in the offspring of diabetic mothers with neonatal complications such as hypoglycemia.23 , 24
Three additional factors should be considered. First, these findings are consistent with earlier reports that diabetes in the mother may affect behavioral and intellectual development in the offspring.25 26 27 28 29 30 31 32 The previously reported relation between the child's IQ and acetonuria in the mother29 30 31 was not found in this study, however, probably because acetonuria was relatively infrequent and, when it did occur, was mild. Only 47 percent of the women with diabetes, who on average performed more than 260 tests for acetonuria on 53 days during the third trimester, had a positive test during that time. In this 47 percent, the mean percentage of days on which tests were positive was 7.6 (i.e., <1 day per week), and only 2.5 percent of the tests were positive. By comparison, Stehbens et al.30 reported a 48 percent incidence of third-trimester acetonuria in patients tested four times daily only during hospitalization; however, 39 percent of the acetone tests were positive. Our finding that maternal hypoglycemia and child intelligence were not significantly related is consistent with the findings that hypoglycemic coma, in contrast to hyperglycemic or ketoacidotic coma, is not associated with adverse neonatal outcome.23 , 29
Second, since metabolic control across trimesters may be interrelated, we cannot exclude an influence of first- or second-trimester control in our population. Indeed, the correlation between second-trimester plasma β-hydroxybutyrate levels and two-year mental-development-index scores was marginally significant (P = 0.08). Petersen and colleagues25 also suggest that a delay in intrauterine growth during the first trimester in the presence of maternal diabetes is associated with psychomotor deficits in the progeny at the age of four to five years. Such delays presumably derive from poor diabetic control, as judged by higher initial hemoglobin A1c values.33
Finally, these results extend our earlier observations of the same group of children at birth. We found that the ratings on three of four dimensions of the Neonatal Behavioral Assessment Scale34 — the interactive, motor, and physiologic-control dimensions —correlated significantly with maternal hemoglobin A1c and fasting plasma glucose levels during the second and third trimesters.35 Thus, in these tests of neurobehavioral integration at birth — that is, before socioeconomic and cultural factors intrude — the same relations were found: poorer performance on the part of the child was correlated with poorer regulation of maternal diabetes during pregnancy.
On the basis of these data on intellectual performance in early childhood and our earlier observations of neurobehavioral integration in the newborn,35 we think that intrauterine metabolic experiences continue to affect the behavioral and intellectual function of offspring in early childhood. The demonstration of these relations in diabetic women with good-to-excellent metabolic regulation in the second and third trimesters of gestation and their offspring attests to the exquisite sensitivity of developmental events to fuel-mediated teratogenesis. The associations between ketonemia in mothers with diabetes during pregnancy and lower IQ in their children speak for the need for continued efforts to avoid ketoacidosis and accelerated starvation in all pregnant women.
Supported in part by grants (DK10699, DK07169, HD11021, HD19070, HD62903, and RR48) from the National Institutes of Health.
We are indebted to Dr. Norbert Freinkel, who until his untimely death on September 5, 1989, had the central role in the conceptual development of the research and management programs at the Northwestern University Diabetes in Pregnancy Center; to senior collaborators, such as Dr. R.L. Phelps (Department of Medicine), Drs. R. Depp, S. Dooley, R. Sabbagha, J. Sciarra, M. Socol, and R. Tamura (Department of Obstetrics), and Drs. J. Boehm and E. Ogata (Department of Neonatology), who made important contributions to the design and implementation of the antepartum and peripartum management procedures; to the nursing staff of the Clinical Research Unit at Northwestern Memorial Hospital for help in the care of our patients; and to Dr. Nam Cho, Mr. Geoff Page, Mr. Ed Murillo, and past members of the Biometry Section of the Diabetes in Pregnancy Center for help in data management and analysis.
Source Information
From the Departments of Medicine (B.E.M.) and Psychiatry (T.R., W.J.B., K.B.) and the Center for Endocrinology, Metabolism, and Nutrition (T.R., B.E.M., W.J.B., K.B.), Northwestern University Medical School and Northwestern Memorial Hospital (Prentice Women's Hospital), Chicago. Address reprint requests to Dr. Rizzo at Northwestern University, Searle Bldg. 10–526, 303 E. Chicago Ave., Chicago, IL 60611.
- References
References
1
Freinkel 2
Freinkel N, Phelps RL, Metzger BE. Intermediary metabolism during normal pregnancy. In: Sutherland HW, Stowers JM, eds. Carbohydrate metabolism in pregnancy and the newborn. New York: Springer-Verlag, 1979:1–31.
3
Freinkel
CrossRef | Web of Science | Medline4
Freinkel N, Metzger BE, Ogata ES, et al. More concerning pregnancy as a "tissue-culture experience." In: Waldhausl WK, ed. Proceedings of the 10th Congress of the International Diabetes Federation. Amsterdam: Excerpta Medica, 1979:731–4.
5
Bayley N. Manual for the Bayley Scales of Infant Development. New York: Psychological Corporation, 1969.
6
Terman LM, Merrill MA. Stanford–Binet Intelligence Scale. Chicago: Riverside Publishing, 1973.
7
Freinkel 8
O'Sullivan
Web of Science | Medline9
Wechsler D. WAIS-R manual: Wechsler Adult Intelligence Scale — Revised. New York: Psychological Corporation, 1981.
10
Metzger
Web of Science | Medline11
Li
Web of Science | Medline12
Trivelli
Full Text | Web of Science | Medline13
Menard
Web of Science | Medline14
Dubowitz
CrossRef | Web of Science | Medline15
Lubchenco
Web of Science | Medline16
Scarr S. Race, social class, and individual differences in I.Q. Hillside, N.J.: Lawrence Erlbaum, 1981.
17
McCall
CrossRef | Web of Science | Medline18
SPSS Inc. SPSS/PC+ V2.0 base manual. Chicago: SPSS, 1988:B153–B163, B220–B223.
19
Idem. SPSS/PC+ advanced statistics V2.0. Chicago: SPSS, 1988:103–51.
20
Castellan
CrossRef | Medline21
McNemar Q. Psychological statistics. 3rd ed. New York: John Wiley, 1962:139–40.
22
Dobbing J. The later development of the brain and its vulnerability. In: Davis JA, Dobbing J, eds. Scientific foundations of paediatrics. 2nd ed. Baltimore: University Park Press, 1981:744–59.
23
Pedersen J. The pregnant diabetic and her newborn. 2nd ed. Baltimore: Williams & Wilkins, 1977.
24
Cornblath M, Schwartz R. Disorders of carbohydrate metabolism in infancy. Philadelphia: W.B. Saunders, 1976.
25
Petersen
CrossRef | Web of Science | Medline26
Morris
CrossRef | Web of Science27
Yssing M. Long-term prognosis of children born to mothers diabetic when pregnant. In: Camerini-Davis RA, Cole HS, eds. Early diabetes in early life. New York: Academic Press, 1975:575–86.
28
Bibergeil H, Godel E, Amendt P. Diabetes and pregnancy: early and late prognosis of children of diabetic mothers. In: Camerini-Davis RA, Cole HS, eds. Early diabetes in early life. New York: Academic Press, 1975:427–34.
29
Churchill
Web of Science | Medline30
Stehbens
Web of Science | Medline31
Berendes HW. Effect of maternal acetonuria on I.Q. of offspring. In: Camerini-Davis RA, Cole HS, eds. Early diabetes in early life. New York: Academic Press, 1975:135–40.
32
Naeye 33
Pedersen
Web of Science | Medline34
Brazelton TB. Neonatal behavioral assessment scale. Clinics in developmental medicine. No. 50. Philadelphia: J.B. Lippincott, 1973.
35
Rizzo
Web of Science | Medline
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Raul Artal, Charles J. Lockwood, Haywood L. Brown. (2010) Weight Gain Recommendations in Pregnancy and the Obesity Epidemic. Obstetrics & Gynecology 115:1, 152-155
CrossRef27
Tracy Riggins, Neely C. Miller, Patricia J. Bauer, Michael K. Georgieff, Charles A. Nelson. (2009) Consequences of Low Neonatal Iron Status Due to Maternal Diabetes Mellitus on Explicit Memory Performance in Childhood. Developmental Neuropsychology 34:6, 762-779
CrossRef28
N.L. Gonzalez-Gonzalez, V. Medina, E. Padron, E. Domenech, N.M. Diaz Gomez, H. Armas, J.L. Bartha. (2009) Fetal and Neonatal Habituation in Infants of Diabetic Mothers. The Journal of Pediatrics 154:4, 492-497
CrossRef29
M. Brinciotti, M. Matricardi, A. Colatrella, F. Torcia, F. Fallucca, A. Napoli. (2009) Visual evoked potentials in infants of diabetic mothers: Relations to clinical and metabolic status during pregnancy and delivery. Clinical Neurophysiology 120:3, 563-568
CrossRef30
SCOTT M NELSON, ROBERT S LINDSAY. (2009) TYPE 1 DIABETES IN PREGNANCY; INFLUENCES ON MOTHER AND FETUS. Fetal and Maternal Medicine Review 20:01, 17
CrossRef31
Boran Jiang, S. Dinesh Kumar, Wan Ting Loh, J. Manikandan, Eng-Ang Ling, Samuel S. W. Tay, S. Thameem Dheen. (2008) Global gene expression analysis of cranial neural tubes in embryos of diabetic mice. Journal of Neuroscience Research 86:16, 3481-3493
CrossRef32
S.K. Singh, Amit Rastogi. (2008) Gestational diabetes mellitus. Diabetes and Metabolic Syndrome: Clinical Research and Reviews 2:3, 227-234
CrossRef33
Oded Langer. 2008. Gestational diabetes: The consequences of not-treating. , 107-117.
CrossRef34
Emily Albertson, Lois Jovanovic. 2008. Medical nutritional therapy for gestational diabetes mellitus. , 196-204.
CrossRef35
A. Lapolla, M.G. Dalfrà, C. Lencioni, G. Di Cianni. 2008. Hypoglycemia in diabetic pregnancy. , 246-252.
CrossRef36
Dana Dabelea, David J. Pettitt. 2008. Long-term implications: Child and adult. , 362-370.
CrossRef37
Asher Ornoy. 2008. Growth and neuro-development of children born to diabetic mothers and to mothers with gestational diabetes. , 371-378.
CrossRef38
Boyd E. Metzger. 2008. The Freinkel legacy. , 19-24.
CrossRef39
Guido Menato, Simona Bo, Anna Signorile, Marie-Laure Gallo, Ilenia Cotrino, Chiara Botto Poala, Marco Massobrio. (2008) Current management of gestational diabetes mellitus. Expert Review of Obstetrics & Gynecology 3:1, 73-91
CrossRef40
Jason A. Parker, Deborah L. Conway. (2007) Diabetic Ketoacidosis in Pregnancy. Obstetrics and Gynecology Clinics of North America 34:3, 533-543
CrossRef41
G. Dahlquist, B. Källén. (2007) School marks for Swedish children whose mothers had diabetes during pregnancy: a population-based study. Diabetologia 50:9, 1826-1831
CrossRef42
Martine H. Hollander, K Marieke Paarlberg, Anjoke J. M. Huisjes. (2007) Gestational Diabetes: A Review of the Current Literature and Guidelines. Obstetrical & Gynecological Survey 62:2, 125-136
CrossRef43
I. Jordan, P. Audra, G. Putet. (2007) Reci??n nacidos de madre diab??tica. EMC - Pediatr??a 42:3, 1-20
CrossRef44
H Gin, A Vambergue, C Vasseur, V Rigalleau, P Dufour, A Roques, M Romon, D Millet, P Hincker, P Fontaine. (2006) Blood ketone monitoring: a comparison between gestational diabetes and non-diabetic pregnant women. Diabetes & Metabolism 32:6, 592-597
CrossRef45
Elke Rodekamp, Thomas Harder, Rainer Kohlhoff, Joachim W. Dudenhausen, Andreas Plagemann. (2006) Impact of breast-feeding on psychomotor and neuropsychological development in children of diabetic mothers: role of the late neonatal period. Journal of Perinatal Medicine 34:6, 490-496
CrossRef46
Diane Reader, Patricia Splett, Erica P. Gunderson. (2006) Impact of Gestational Diabetes Mellitus Nutrition Practice Guidelines Implemented by Registered Dietitians on Pregnancy Outcomes. Journal of the American Dietetic Association 106:9, 1426-1433
CrossRef47
Lois Jovanovic. (2006) The importance of postprandial glucose concentration: lessons learned from diabetes and pregnancy. Drug Development Research 67:7, 591-594
CrossRef48
Helen Leonard, Nick de Klerk, Jenny Bourke, Carol Bower. (2006) Maternal Health in Pregnancy and Intellectual Disability in the Offspring: A Population-Based Study. Annals of Epidemiology 16:6, 448-454
CrossRef49
Beverley Thomas, Kebreab Ghebremeskel, Clara Lowy, Michael Crawford, Bridget Offley-Shore. (2006) Nutrient intake of women with and without gestational diabetes with a specific focus on fatty acids. Nutrition 22:3, 230-236
CrossRef50
Natan Patlas, Meytal Avgil, Ehud Ziv, Asher Ornoy, Eleazar Shafrir. (2006) Pregnancy Outcome in the <i>Psammomys obesus</i> Gerbil on Low- and High-Energy Diets. Biology of the Neonate 90:1, 58-65
CrossRef51
Oded Langer, Yariv Yogev, Orli Most, Elly M.J. Xenakis. (2006) Reply. American Journal of Obstetrics and Gynecology 194:1, 299-300
CrossRef52
B Guerci, N Tubiana-Rufi, B Bauduceau, R Bresson, A Cuperlier, C Delcroix, D Durain, C Fermon, JP Le Floch, C Le Devehat, V Melki, L Monnier, H Mosnier-Pudar, P Taboulet, H Hanaire-Broutin. (2005) Advantages to using capillary blood ɛ-hydroxybutyrate determination for the detection and treatment of diabetic ketosis. Diabetes & Metabolism 31:4, 401-406
CrossRef53
Lois Jovanovic. (2005) Turning the Tide: Type 2 Diabetes Trends in Offspring of Mothers with Gestational Diabetes Mellitus. Metabolic Syndrome and Related Disorders 3:3, 233-243
CrossRef54
B.A. Thomas, Kebreab Ghebremeskel, Clara Lowy, Brigid Offley-Shore, Michael A. Crawford. (2005) Plasma fatty acids of neonates born to mothers with and without gestational diabetes. Prostaglandins, Leukotrienes and Essential Fatty Acids 72:5, 335-341
CrossRef55
Marie A. Luerssen, Anne L. Winsch. (2005) Identifying and Treating Gestational Diabetes Mellitus. AJN, American Journal of Nursing 105:4, 65-71
CrossRef56
Lois Jovanovic. (2004) Nutrition and pregnancy: The link between dietary intake and diabetes. Current Diabetes Reports 4:4, 266-272
CrossRef57
ASHAJYOTHI M. SIDDAPPA, MICHAEL K. GEORGIEFF, SANDI WEWERKA, CATHY WORWA, CHARLES A. NELSON, RAYE-ANN DEREGNIER. (2004) Iron Deficiency Alters Auditory Recognition Memory in Newborn Infants of Diabetic Mothers. Pediatric Research 55:6, 1034-1041
CrossRef58
Kebreab Ghebremeskel, Beverley Thomas, Clara Lowy, Yoeju Min, Michael A. Crawford. (2004) Type 1 diabetes compromises plasma arachidonic and docosahexaenoic acids in newborn babies. Lipids 39:4, 335-342
CrossRef59
Lois Jovanovic. 2003. Diabetes Mellitus, Pregnancy, and Gestational Diabetes. .
CrossRef60
Davida F. Kruger, Karen White, Aimee Galpern, Kelly Mann, Ann Massirio, Melinda McLellan, Jeanne Stevenson. (2003) Effect of Modem Transmission of Blood Glucose Data on Telephone Consultation Time, Clinic Work Flow, and Patient Satisfaction for Patients With Gestational Diabetes Mellitus. Journal of the American Academy of Nurse Practitioners 15:8, 371-375
CrossRef61
S Ohgi. (2003) Neonatal behavioral assessment scale as a predictor of later developmental disabilities of low birth-weight and/or premature infants. Brain and Development 25:5, 313-321
CrossRef62
G. Di Cianni, R. Miccoli, L. Volpe, C. Lencioni, S. Del Prato. (2003) Intermediate metabolism in normal pregnancy and in gestational diabetes. Diabetes/Metabolism Research and Reviews 19:4, 259-270
CrossRef63
A Ornoy. (2003) The impact of intrauterine exposure versus postnatal environment in neurodevelopmental toxicity: long-term neurobehavioral studies in children at risk for developmental disorders. Toxicology Letters 140-141, 171-181
CrossRef64
HIROSHI YAMASHITA, JIANHUA SHAO, LIPING QIAO, MICHAEL PAGLIASSOTTI, JACOB E. FRIEDMAN. (2003) Effect of Spontaneous Gestational Diabetes on Fetal and Postnatal Hepatic Insulin Resistance in Leprdb/+ Mice. Pediatric Research 53:3, 411-418
CrossRef65
Steven S. Robertson, LeRoy J. Dierker. (2003) Fetal cyclic motor activity in diabetic pregnancies: Sensitivity to maternal blood glucose. Developmental Psychobiology 42:1, 9-16
CrossRef66
Arthur I. Eidelman, Arnon Samueloff. (2002) The pathophysiology of the fetus of the diabetic mother. Seminars in Perinatology 26:3, 232-236
CrossRef67
Edith W. M. T. ter Braak, Inge M. Evers, D. Willem Erkelens, Gerard H. A. Visser. (2002) Maternal hypoglycemia during pregnancy in type 1 diabetes: maternal and fetal consequences. Diabetes/Metabolism Research and Reviews 18:2, 96-105
CrossRef68
MONIQUE ROMON, MARIE-CHRISTINE NUTTENS, ANNE VAMBERGUE, ODILE VÉRIER-MINE, SERGE BIAUSQUE, CHRISTINE LEMAIRE, PIERRE FONTAINE, JEAN-LOUIS SALOMEZ, RÉGIS BEUSCART. (2001) Higher Carbohydrate Intake is Associated with Decreased Incidence of Newborn Macrosomia in Women with Gestational Diabetes. Journal of the American Dietetic Association 101:8, 897-902
CrossRef69
A Åberg, L Westbom. (2001) Association between maternal pre-existing or gestational diabetes and health problems in children. Acta Paediatrica 90:7, 746-750
CrossRef70
Anne Rae, Dianne Bond, Sharon Evans, Felicity North, Brian Roberman, Barry Walters. (2000) A randomised controlled trial of dietary energy restriction in the management of obese women with gestational diabetes. The Australian and New Zealand Journal of Obstetrics and Gynaecology 40:4, 416-422
CrossRef71
N.Nicola Doherty, Peter G Hepper. (2000) Habituation in fetuses of diabetic mothers. Early Human Development 59:2, 85-93
CrossRef72
LOIS JOVANOVIC. (2000) Role of Diet and Insulin Treatment of Diabetes in Pregnancy. Clinical Obstetrics and Gynecology 43:1, 46-55
CrossRef73
D. K. James, Florence M. Telfer, Nicol. (2000) Reduced fetal movements and maternal medication - new pregnancy risk factors for neurodevelopmental disability in childhood. Journal of Obstetrics & Gynaecology 20:3, 226-234
CrossRef74
Lois Jovanovic. (2000) Medical nutritional therapy in pregnant women with pregestational diabetes mellitus. The Journal of Maternal-Fetal Medicine 9:1, 21-28
CrossRef75
Charles A. Nelson, Sandi Wewerka, Kathleen M. Thomas, Raye-ann deRegnier, Stephanie Tribbey-Walbridge, Michael Georgieff. (2000) Neurocognitive sequelae of infants of diabetic mothers.. Behavioral Neuroscience 114:5, 950-956
CrossRef76
Lori Laffel. (1999) Ketone bodies: a review of physiology, pathophysiology and application of monitoring to diabetes. Diabetes/Metabolism Research and Reviews 15:6, 412-426
CrossRef77
(1999) Gestational diabetes mellitus and its complications. Asia Pacific Journal of Clinical Nutrition 8:1, 82-89
CrossRef78
Edmond A. Ryan. (1998) PREGNANCY IN DIABETES. Medical Clinics of North America 82:4, 823-845
CrossRef79
TA Rizzo, BL Silverman, BE Metzger, NH Cho. (1997) Behavioral adjustment in children of diabetic mothers. Acta Paediatrica 86:9, 969-974
CrossRef80
Robert Fraser, Janet Cresswell. (1997) What should obstetricians be doing about the Barker hypothesis?. BJOG: An International Journal of Obstetrics and Gynaecology 104:6, 645-647
CrossRef81
Thomas A. Rizzo, Boyd E. Metzger, Sharon L. Dooley, Nam H. Cho. (1997) Early Malnutrition and Child Neurobehavioral Development: Insights from the Study of Children of Diabetic Mothers. Child Development 68:1, 26-38
CrossRef82
Lois Jovanovic-Peterson, Charles M. Peterson. (1996) Review of Gestational Diabetes Mellitus and Low-calorie Diet and Physical Exercise as Therapy. Diabetes/Metabolism Reviews 12:4, 287-308
CrossRef83
Holly L. Casele, Sharon L. Dooley, Boyd E. Metzger. (1996) Metabolic response to meal eating and extended overnight fast in twin gestation. American Journal of Obstetrics and Gynecology 175:4, 917-921
CrossRef84
Y. Yamashita, Y. Kawano, N. Kuriya, Y. Murakami, T. Matsuishi, K. Yoshimatsu, H. Kato. (1996) Intellectual development of offspring of diabetic mothers. Acta Paediatrica 85:10, 1192-1196
CrossRef85
Naomi Weintrob, Moshe Karp, Moshe Hod. (1996) Short- and long-range complications in offspring of diabetic mothers. Journal of Diabetes and its Complications 10:5, 294-301
CrossRef86
Phillip J. Shubert, Michael C. Gordon, Mark B. Landon, Steven G. Gabbe, Douglas A. Kniss. (1996) Ketoacids attenuate glucose uptake in human trophoblasts isolated from first-trimester chorionic villi. American Journal of Obstetrics and Gynecology 175:1, 56-62
CrossRef87
L JOVANOVICPETERSON, C PETERSON. (1996) EXERCISE AND THE NUTRITIONAL MANAGEMENT OF DIABETES DURING PREGNANCY. Obstetrics and Gynecology Clinics of North America 23:1, 75-86
CrossRef88
V WHITEMAN, C HOMKO, E REECE. (1996) MANAGEMENT OF HYPOGLYCEMIA AND DIABETIC KETOACIDOSIS IN PREGNANCY. Obstetrics and Gynecology Clinics of North America 23:1, 87-107
CrossRef89
Thomas A Rizzo, Sharon L Dooley, Boyd E Metzger, Nam H Cho, Edward S Ogata, Bernard L Silverman. (1995) Prenatal and perinatal influences on long-term psychomotor development in offspring of diabetic mothers. American Journal of Obstetrics and Gynecology 173:6, 1753-1758
CrossRef90
B. M. Byrne, M. D. Gillmer, R.C. Turner, A. Aynsley-Green. (1995) Glucose homeostasis in adulthood and in pregnancy in a patient with hepatic glycogen synthetase deficiency. BJOG: An International Journal of Obstetrics and Gynaecology 102:11, 931-933
CrossRef91
Pierre Decouflé, Coleen A. Boyle. (1995) The Relationship between maternal education and mental retardation in 10-year-old children. Annals of Epidemiology 5:5, 347-353
CrossRef92
Ulf J. Eriksson. (1995) The pathogenesis of congenital malformations in diabetic pregnancy. Diabetes / Metabolism Reviews 11:1, 63-82
CrossRef93
CATHY FAGEN, JACQUELINE D KING, MIRIAM ERICK. (1995) Nutrition Management in Women with Gestational Diabetes Mellitus. Journal of the American Dietetic Association 95:4, 460-467
CrossRef94
Robert Fraser. (1995) Diabetic control in pregnancy and intrauterine growth of the fetus. BJOG: An International Journal of Obstetrics and Gynaecology 102:4, 275-277
CrossRef95
Erma Jean Lawson, Shireen Rajaram. (1994) A transformed pregnancy: the psychosocial consequences of gestational diabetes.. Sociology of Health and Illness 16:4, 536-562
CrossRef96
Clifford J. Sells, Nancy M. Robinson, Zane Brown, Robert H. Knopp. (1994) Long-term developmental follow-up of infants of diabetic mothers. The Journal of Pediatrics 125:1, S9-S17
CrossRef97
R. G. Moses. (1994) The Medical Management of Gestational Diabetes in Australia within a Solo Private Practice. Diabetic Medicine 11:6, 597-600
CrossRef98
Thomas A. Buchanan, M.D, John L. Kitzmiller, M.D. (1994) METABOLIC INTERACTIONS OF DIABETES AND PREGNANCY. Annual Review of Medicine 45:1, 245-260
CrossRef99
Richard E Gilbert, Con Tsalamandris, Leon A Bach, Sianna Panagiotopoulos, Richard C O'Brien, Terri J Allen, Ian Goodall, Val Young, Ego Seeman, Robin M L Murray, Mark E Cooper, George Jerums. (1993) Long-term glycemic control and the rate of progression of early diabetic kidney disease. Kidney International 44:4, 855-859
CrossRef100
R.N. Roberts, J.M. Moohan, R.L.K. Foo, J.M.G. Harley, A.I. Traub, D.R. Hadden. (1993) Fetal Outcome in Mothers with Impaired Glucose Tolerance in Pregnancy. Diabetic Medicine 10:5, 438-443
CrossRef101
K. Huddle, M. England, A. Nagar. (1993) Outcome of Pregnancy in Diabetic Women in Soweto, South Africa 1983-1992. Diabetic Medicine 10:3, 290-294
CrossRef102
Sandra C. Van Calcar, Cary O. Harding, Susan R. Davidson, Lewis A. Barness, Jon A. Wolff. (1992) Case reports of successful pregnancy in women with maple syrup urine disease and propionic acidemia. American Journal of Medical Genetics 44:5, 641-646
CrossRef103
(1992) Review article. Journal of Perinatal Medicine 20:4, 253-266
CrossRef104
Jovanovic-Peterson, Lois, Peterson, Charles M., . (1991) Sweet Success, but an Acid Aftertaste?. New England Journal of Medicine 325:13, 959-960
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